Paper - The microscopic structure of the yolk-sac of the pig embryo (1916)

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Jordan HE. The microscopic structure of the yolk-sac of the pig embryo, with special reference to the origin of the erythrocytes. (1919) Amer. J Anat. 19(2): 277-302.

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This 1916 paper by Jordan describes the histology of the yolk-sac of the pig.

Also by this author: Jordan HE. The histology of the umbilical cord of the pig, with special reference to the vasculogenic and hemopoietic activity of its extensively vascularized connective tissue. (1919) Amer. J Anat. 26(1): 1-28.

Modern Notes: yolk sac | pig

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The Microscopic Structure of the Yolk-sac of the Pig Embryo

With Special Reference to the Origin of the Erythrocytes

H. E. Jordan

Department of Anatomy, University of Virginia

Thirty-Five Figures (Two Plates)

I. Introduction

The chief purpose in view in this study of the Template:Yolk-sac of the pig embryo was the acquisition of further data regarding the earliest stages in blood cell origin and development in mammals. The yolk-sac was believed to be the most favorable material for the search for evidence concerning the disputed relationship between mesenchyma, primitive endothelium and haemoblasts. The pig embryo was selected for study on account of its ready availability. It was hoped that information could be contributed to the following debated questions in haemopoiesis: 1) Does the angioblast bear any direct genetic relationship to the entoderm? 2) Does the yolk-sac mesothelium produce haemoblasts? 3) Does the mesenchyma differentiate in part into endothelium? 4) Do haemoblasts arise directly from mesenchyma? 5) Do haemoblasts differentiate from endothelium? 6) What is the origin and function of the giant cells of the yolksac? The first question involves a careful consideration of the structure of the entoderm; which in turn raises the question: 7) What is the function of the entoderm in yolk-sacs which contain little or no yolk?

A preliminary report of this study appeared in the Proceedings of the thirty-first session of the American Association of Anatomists (Anat. Rec, 9:1, '15, pp. 92-97). In the present paper more extensive observations, with illustrations, are recorded. Moreover, a further study of the entoderm compels a reinterpretation of the cytoplasmic filaments of these cells; my earlier conclusion that they are mitochondrial in nature no longer seems warranted.

A portion of this investigation was done at the Marine Biological Laboratory, Woods Hole, Massachusetts during the summer of '14. I take this opportunity to gratefully acknowledge my indebtedness to the institution for the privileges of a research room.

II. Material and Methods

The material consists of pig embryos ranging in length from 5 to 25 mm. Zenker's and Helly's fluids were used for fixation. The stains employed were the Giemsa blood stain, and the haematoxylin and eosin combination. Sacs of stages within the limits specified differ essentially only with respect of relative abundance of the various types of early blood cells. The 10 to 15 mm. stages were soon discovered to be most favorable for this study, since here was included in the same sections both earliest and later stages in haemopoiesis. Haemopoietic phenomena seem to be at their height in the yolk-sac of the pig embryo at about the 10 mm. stage of development.

III. Descriptive

a. The entoderm

It seems preferable to begin the description of the histology of the yolk-sac with the entodermal constituent of its wall.

In the 5 mm. stage the entodermal cells are cuboidal, and arranged in a single layer; there is as yet no trace either of solid or tubular evaginations into the enveloping mesenchyma.

In the 10 mm. stage of development the lining cells are columnar, the taller being about twice the length of the tallest cells in the earlier stage ; they are still arranged in a single layer. However, there is great variation in the form of the cells; the predominating type of entodermal cell is columnar, but all transitional forms appear from very low cuboidal to tall columnar cells. At certain points the entoderm invaginates the mesenchyma in the form of short cords and tubules. The 'tubules' are scarcely more than shallow folds, but recall the larger branched tubules of the yolk-sac of human embryos of this length (Meyer (18) ; Jordan (10).) The condition is probably to be interpreted in terms of a mechanical adjustment on the part of the entoderm to the exiguous confines delimited by the enveloping mesenchyma, or it may perhaps be merely a shrinkage phenomenon.

At the 25 mm. stage of developnient the entodermal cells appear shorter columnar but are still almost invariably arranged in only a single layer. Occasional small stratified areas occur similar to those characteristic of the human yolk-sac of even much earlier stages, but they are perhaps most correctly interpreted as short .stout entodermal buds or cords. At this stage the very sparse enveloping mesenchyma is extensively invaded by very numerous robust solid cords and irregular tubules of entodermal cells. In tangential sections the yolk-sac wall of this stage looks strikingly like reptilian liver tissue.

The cytology of the entoderm is essentially identical for the 5 to 25 mm. stages (figs. 2 and 31). The vesicular nucleus is relatively large and spherical, and is generally placed nearer the basal pole. It contains one or several large, spheroidal chromatic nucleoli (fig. 2) and a delicate wide-meshed granular reticulum. Many of the cells are undergoing mitosis. The cell wall appears distinct. But there is no indication of terminal bars nor brush borders, such as have been described for the entodermal cells of the human yolk-sac by Branca (2). In Giemsastained preparations the cytoplasm is colored dark blue, the nuclei light blue, and the nucleoli bluish orange or lilac.

The most striking feature of these cells is the presence of a generous amount of delicate filaments (basal filaments; ergastoplasmic filaments) scattered throughout the finely granular basophilic cytoplasm. They are oriented in general parallel to the long axis of the cell. They may be coarser or finer, in length equal to that of the entire cell or much shorter; and they may be apparently homogeneous or segmented (fig. 31). The latter condition would seem to indicate the possibility that they may fragment into secretion granules, but the evidence for this conclusion is not wholly satisfactory. Their probable significance and nature will be discussed in a later section. It may suffice here to state that the cells of the liver (fig. 32) and those of the mesonephric tubules contain apparently identical cytoplasmic threads; and that in no case do they bear any direct relationship to mitochondria, which must have been dissolved by the fixing fluids used.

b. The mesothelium

The outer surface of the yolk-sac wall, like the homologous layer of the splanchnopleure generally, is characterized by a layer of greatly flattened cells each bulging more or less at the point where the nucleus is located. The cytoplasm is delicately reticular like that of the underlying mesenchyma, with which the mesothelial cells are apparently in syncytial continuity (figs. 2 and 4). The nuclei are generally relatively large, oval, vesicular structures, with one or several small irregular net-knots, and a delicate wide-meshed nuclear reticulum (figs. 9 and 20). In their general form, structure and light staining capacity they are practically identical with the nuclei of the mesenchyma and the endothelium (figs. 13 to 18). In the Giemsa stain the nuclei of these three tissues are similarly colored bluish orange, while the cytoplasm stains a lighter blue. Occasional cells may be seen in mitosis, but there is no clear evidence to indicate that their prohferation products may differentiate into haemoblasts. The proliferation is most probably related only to the extension of the mesothelial covering. Certain cells, however, are more or less rounded, simulating early stages in the formation of haemoblasts from endothelium (fig. 20) .

c. The mesenchyma

The mesenchyma is of very variable amount in different portions of the wall (figs. 2, 4, 29 and 30) ; in certain regions it is so sparse as to be barely discernible between the entoderm and the mesothelium ; in other regions it may greatly exceed in width that of the tallest portions of the entoderm. It is a loose-meshed syncytium containing numerous spaces and occasional small blood islands, and larger and smaller blood vessels or sinusoids (figs. 29 and 30). Around certain spaces the mesenchymal cells may become arranged so as to very closely simulate endothelial cells. Indeed it seems impossible to differentiate between such a cell and certain endothelial cells from blood-cell-containing channels. It seems difficult to avoid the conclusion that endothelium is thus differentiated from the mesenchyma, the differentiation depending here as in the case of the structurally apparently identical mesothelium, upon the mechanical factor of pressure (fig. 29). Many of the mesenchymal nuclei are in some phase of mitosis, and occasional nuclei appear to be dividing amitotically.

d. The endothelium

The cells lining blood-cell-containing channels are flattened elements, of fusiform shape in sections. The commonest type of cell contains a vesicular oval nucleus, practically identical with that of the mesenchyma and the mesothelium (figs. 4, 13 and 29) ; and also the delicate reticular cytoplasmic structure of the endothelial cells is like that of these cells. Moreover, the endothelial cells appear to be in direct syncytial continuity with the mesenchyma. Many are in mitosis, and occasional nuclei appear to be dividing amitotically. It seems most probable that they are actually mesenchymal cells modified in shape by the pressure of the confined blood stream. Endothelial cells which lie next the entoderm are sharply separated therefrom (figs. 29 and 30). The entodermal cells rest upon a delicate but distinct basement membrane, with which the endothelium is not in structural continuity (fig. 2). The vascular anlages (angioblast) are at certain points in direct continuity with the mesenchyme, but are sharply demarked from the entoderm (fig. 29). There is no evidence here that the angioblast has any direct genetic relationship to the entoderm; all the available morphologic data are opposed to the idea of such a relationship. The endothelium includes, however, numerous cells which may be arranged into a complete series connecting the above described endothelial cell with a haemoblast (figs. 4, 13, 14, 15 and 16). The transition steps consist of a progressive rounding up of the nucleus and a gathering of the cytoplasm around it. At the same time the nucleus enlarges and the cytoplasm appears to increase in amount. Moreover the cytoplasm becomes more highly basophilic and appears finely granular. The cell as a whole, of fusiform shape, becomes progressively shorter and finally separates from the endothelial wall either as a short fusiform cell, or frequently as a spherical cell flattened at its proximal pole and drawn out laterally into delicate processes which gradually separate from the vessel wall (figs. 5 and 6). Such cells may even become multinucleated before separation (figs. 8 and 9), and undergo cytoplasmic differentiation, even elaborating haemoglobin, as will be described below. The multinuclear condition appears to be the result of amitotic nuclear division (figs. 9 and 35). The observation of the differentiation of endothelial cells into haemoblasts is of cardinal importance, and will be more fully discussed in a later section.

e. The blood cells

1) Terminology. Four distinct types of cells may be recognized: 1) The haemoblasts, or blood mother-cells. These correspond with the priinitive 'lymphocytes' of Maximow (16), and the 'mesamoeboid cells' of Minot (19). 2) The erythroblasts, corresponding with the 'ichthyoid' blood cell of Minot, and in part with the 'megaloblast' of Maximow. 3) The normoblasts, corresponding with the 'sauroid' cell of Minot. The last two may be designated inclusively as erythrocytes. 4) The giant cells, both megakaryocytes and polykaryocytes.

The majority of the blood cells can be classified under one or the other of the above heads. However, between typical primitive haemoblasts and erj^throblasts, and between the latter and normoblasts, as also between haemoblasts and giant cells, complete series of transition forms occur.

Up to the 15 mm. stage no cell is present that can be certainly identified as a leucocyte. The haemoblasts are structurally very similar to the lymphocytes of the adult, and if they are indeed in part at least, functionally identical, as claimed by Maximow in support of the monophyletic theory of haemopoiesis, they may be properly designated 'lymphocytes.'

2) Haemoblasts. This terminology implies that the cell designated 'haemoblast' is the common mother-cell of both leucocytes and erythrocytes. No evidence, besides its very close similarity to a lymphocyte, accrues from this study to indicate that the cell in question is also a leucocyte progenitor. It may be noted, however, that this cell would apparently have to undergo less differentiation in becoming a mononuclear, or even a polymorphonuclear, leucocyte, than in becoming an erythroplastid. Moreover, there is now a very considerable body of embryologic data to show that this cell in certain mammals (rabbit, Maximow (16); birds, Dantschakoff (5); reptiles, Dantschakoff (6), and Jordan and Flippin (14); and selachii and amphibia, Maximow (17)) is indeed the parent cell of both red and white blood corpuscles. Thus while the haemogenic process here to be described is purely erythropoietic, the primitive cell is nevertheless properly termed 'haemoblast.'

The haemoblast is in its youngest form a relatively small cell, ranging from about half to approximately the full size of the definitive normoblast, with a larger nucleus and much less cytoplasm (figs. 1, 2 and 3). It has a relatively enormous nucleus, which is enveloped by a narrow shell of cytoplasm generally wider at one point over an area of from less than a quarter to more than a half of the surface (fig. 1 a). The cytoplasm is finely granular and deeply basophilic. The nucleus is vesicular with one or several spheroidal chromatic masses (nucleoli), scattered irregularly through a wide-meshed, delicate, frequently granular reticulum containing larger chromatin granules peripherally on the nuclear membrane. In Giemsa-stained preparations the nucleoli are colored lilac, the nuclear sap bluish pink, the cytoplasm deep blue. The haemoblast may show several blunt pseudopods indicating amoeboid capacity (figs. 2 and 27). The young haemoblasts are more generally peripherally placed in the blood vessels, the later differentiation stages more centrally.

The haemoblasts show a very wide range of size variations and nuclear forms, while at the same time adhering to a very close structural similarity both nuclear and cytoplasmic (figs. 1, 2, 3 and 7). By growth the primitive haemoblast may become very large; this growth may be chiefly nuclear (fig. 34) or chiefly cytoplasmic (fig. 7). It does not seem possible to draw a sharp line between large haemoblasts and certain so-called 'giant cells,' to be described below. Their essential nuclear and cytoplasmic features are very similar.

By division a larger haemoblast gives rise to smaller, structurally identical, haemoblasts. The mode of division may be mitotic, and apparently also amitotic (figs. 3, c, d, and e, and 22). Cytoplasmic division frequently does not directly follow nuclear division, thus giving rise to binucleated cells (fig. 3 d and e). Similarly, tripolar spindles may produce trinucleated cells (fig. 21), or the same may be probably produced also by direct division (figs. 11 and 12). Multinuclear cells are probably similarly formed (figs. 25 and 35). The bi- and multinucleated types will be further described under 'giant cells.'

Haemoblasts have a double source of origin: 1) from the mesenchyma (fig. 30) ; 2) from the endothelium of the earliest blood vessels (fig. 4). Since this endothelium, however, also originally arose from mesenchyme, the primary, in part indirect source, is the same, namely the original mesenchyma.

The endothelial origin of haemoblasts has already been partially described above under 'endothelium.' It need merely be emphasized here that the evidence on this point seems unequivocal; transition stages are practically innumerable; their abundance is so great as to make it difficult to adhere to a reasonable limit in the selection of illustrations. Possible objections to the interpretation here given to the observations will be considered below. The above description pertains only to intravascular haemopoiesis; the endothelium contributes also, but apparently much more rarely (except in the mesonephric glomeruli of the body of the embryo) , extra vascular haemoblasts. The continuity of such with the endothelial wall countervails the possible objection that these are migrants (fig. 4).

The direct mesenchymal origin of haemoblasts concerns itself with the blood-islands and certain isolated cells separating from the mesenchymal syncytium. Peripherally the bloodislands are in continuity with the mesenchyma, where endothelial cells are differentiated; centrally the cells are haemoblasts in various earlier stages of metamorphosis into erythroblasts ; some of these may be binucleated (fig. 29).

The unique and crucial evidence for mesenchymal origin of haemoblasts pertains to certain isolated cells caught in the actual process of differentiation and separation from the syncytium. These are admittedly rare, but the evidence they furnish is of prime importance. It supplies the link in the monophyletic theory of haemogenesis concerning which there has been the greatest scepticism. Figure 30 is an illustration of the clearest case of the condition referred to. Here is shown an area of mesenchyma in which two of the nuclei, as well as their enveloping cytoplasm, have mesenchymal features; the third nucleus (//) and its enveloping cytoplasm are of typically haemoblast character. A delicate chromatic nuclear bridge still connects the haemoblast nucleus with the mesenchyma nucleus. The significance of this nuclear bridge is uncertain, but it plainly reveals genetic relationship whatever its meaning in terms of type of cell division. Such instances should definitely dispose of the objection that all mesenchymal haemoblasts are migrants from adjacent blood vessels. Haemoblasts are very variable in form, due to the variable number and form of their pseudopods (fig. 27). They must be regarded as capable of extensive amoeboid motility.

It is a matter of sufficient importance to warrant special emphasis at this point, that between typical haemoblasts and typical erythroblasts, next to be described, transition forms exist abundantly (fig. 1 b) . The marks of transition pertain both to the nucleus and the cytoplasm. The change is perhaps most marked in the staining capacity of the cytoplasm. This loses its intense basophily, and in Giemsa preparations becomes a much lighter pink or grayish blue. This chemical alteration inheres principally in the elaboration of a small amount of haemoglobin. The cytoplasm shows also faintly a coarse widemeshed reticulum. And a distinct cell wall is now evident (fig. 1 b), whereas the haemoblast is apparently a naked cell. The nucleus becomes relatively smaller and more chromatic; the nucleoli tend to disappear, and the nuclear reticulum becomes coarser, more granular and more chromatic.

3) Erythroblasts. These cells are characterized by their slightly smaller spherical nuclei and an acidophil cytoplasm generous in amount (fig. 1 c). The nuclei generally lack distinct nucleoli but contain a coarsely granular, intensely chromatic, nuclear reticulum. The cytoplasm has frequently a finely granular appearance (fig. 3 f). In Giemsa preparations the nucleus stains blue, the cytoplasm a faint brownish pink. These cells are much more uniform in size than the haemoblasts and are generally mononuclear. They undergo very extensive mitotic proliferation. The transition stages (figs. 1 b and 3 f) between the haemoblast and the erythroblast, characterized by a bluish pink color in Giemsa preparation, correspond to the 'megaloblast' described by Maximow in the rabbit.

Occasionally a disintegrating erythroblast may be seen ingested by an endothelial cell (fig. 28). This observation indicates a phagocytic function on the part of the endothehiim of the yolk-sac vessels. An alternative interpretation will be discussed below.

4) Normoblasts. The normoblasts differ from the erythroblasts in that they have a smaller more compact and chromatic nucleus, and a more acidophilic cytoplasm (figs. 1 d, 2 e and 3 g). These cells are very uniform in size. In this character of size uniformity they differ markedly from the similar cells in certain lower forms, for example, in turtles. They multiply extensively by the indirect method of cell division. In Giemsa preparations the cytoplasm stains a brilliant red, the coarsely granular nucleus a deep blue. The nucleus frequently has an irregular lobed contour. The chromatin is frequently gathered into several large and many smaller clumps, the reticulum being delicate and only slightly chromatic. In preparations fixed in Zenker's fluid, the haemoglobin content has become dissolved, and the cytoplasmic area reveals a coarse wide-meshed reticulum, bounded peripherally by a coarse cell membrane (fig. 3 g). By abstriction of the portion of the cytoplasm containing the excentric nucleus, in the manner described by Emmel (7), the erythrocyte becomes an erythroplastid. These stages in plastid formation are still extremely rare in 10 mm. embryos.

5) Giant cells. These cells include a great variety of different forms and sizes. The extremes include: 1) An enormous cell consisting almost wholly of nucleus, the naked cytoplasm constituting a mere shell (figs. 33 and 34). The cytoplasm is basophilic. The vesicular nucleus is generally extensively lobed and contains many large spheroidal and irregular chromatic masses; its nuclear reticulum is wide-meshed, granular, and intensely chromatic. 2) A cell of similarly large size with generally two or three relatively small, spherical, oval or irregular, pale staining, granular nuclei (figs. 23, 24 and 25). The nuclei may contain one or several nucleoli ; and the reticulum is more regular, more delicate, sometimes double (fig. 23) and less deeply chromatic. The cytoplasm is slightly acidophilic. Both nuclear and cytoplasmic features resemble those of the erythroblasts ('megaloblasts'). 3) A cell of similar or even larger size with numerous nuclei (as many as eight are common) of various shapes and sizes and differing in structure between the two extremes above described (figs. 11, 12 and 35). The cytoplasm of such a cell is also more or less basophilic.

The origin of giant cells can be definitely traced by means of transition stages to the haemoblasts. Type 1, above described, is simply a giant haemoblast (compare figs. 3 a, 7 and 33). Type 2 is a giant haemoblast with several nuclei (compare figs. 3 a and 11) derived by nuclear amitotic division — occasionally possibly also by nuclear mitosis — unaccompanied by cytoplasmic division. The cytoplasm has entered upon the early stages of differentiation into erythroblast cytoplasm. Type 3 is derived from type 1 by extreme and irregular fission of the single nucleus, accompanied by slight differentiation in the cytoplasm (figs. 12, 25 and 35).

Frequently a typical giant cell with two or even three nuclei may be seen in continuity with the endothelial wall of the blood vessel, and in late stages of separation (figs. 8 and 9). This observation further supports the conclusion of haemoblast derivation of giant cells. There is no evidence in favor of an entodermal origin of giant cells as held by Graf. v. Spee (22) in the case of the human yolk-sac.

A small number of giant cells contain one or several normoblasts. The normoblast periphery may be separated from the enveloping giant cell cytoplasm by a narrow space (fig. 10) ; or such space may be lacking, in which event the continuity between the two cytoplasms seems complete (fig. 26). Two possibilities of the origin of these intracellular normoblasts at once suggest themselves: 1) ingestion; 2) differentiation from the nuclei and portions of the surrounding cytoplasm of the giant cell. The fact that endothelial cells (potential haemoblasts) may ingest erythroblasts (fig. 28), as above described, lends much weight to the first suggestion. The further facts, however — 1) that in certain cells with more than one normoblast no haemoblast nucleus remains (fig. 26) ; 2) that giant cells of the yolk-sac are simply modified haemoblasts whose cytoplasm undergoes a chemical alteration, as indicated bj^ staining reactions, similar to that of haemoblasts in becoming erythroblasts; 3) that no multinucleated giant cells could be found in process of fragmentation into mononucleated cells; 4) that the cytoplasmic relationship between the two cells is frequently very intimate; 5) that such intracellular normoblasts are occasionally in mitosis, an unexpected phenomenon in ingested degenerating cells; and the possibility 6) that the cells interpreted as phagocytic endotheha may indeed be cells differentiating normoblasts intracellularly while still attached to the blood vessel wall — all indicate that the structure in question is one representing actual intracellular differentiation of normoblasts within a giant cell. This matter will be further discussed below.

In the yolk-sac of the 25 mm. pig embryo the blood vessels are relatively much larger. No blood-islands occur. The blood cells are predominantly of the normoblast type; there are also some erythroblasts and a few haemoblasts. Giant cells are apparently lacking; and the endothelium of the blood channels is apparently no longer capable of haemoblast formation.

IV. Discussion

a. Function of yolk-sac

1) Digestive. The yolk-sac entoderm is of course continuous with the epithelial lining of the gut through the yolk-stalk. Originally similarly undifferentiated, the yolk-sac entoderm already at the 5 mm. stage has far outstripped the gut entoderm in differentiation. Even at the 10 mm. stage the cells lining the gut are relatively little differentiated. The chief mark of functional activit}'- on the part of the yolk-sac entodermal cells is the presence of a generous amount of basal filaments. Such are lacking in the gut entoderm of this stage. These filaments resemble very closely mitochondria; they may be long or short, straight or variously curved, delicate or coarse, apparently homogeneous or segmented. While structurally very like mitochondria — on the basis of which, characters I previously so interpreted them — I now feel compelled to give them a different interpretation, and for the following reasons: 1) Identical filaments appear in the cells of the hepatic cords (compare figs. 31 and 32) and those of the mesonephric tubules of these embryos. These cells are functionally active in a secretory way, strengthening the presumption that the filaments in the yolk-sac entoderm also have secretory significance. 2) If these filaments were really mitochondria, many other cells should show such elements, for it is well established that mitochondria are practically universally present in embryonal cells. But no other cells, besides those mentioned, contain similar filaments in these embryos. It is quite unreasonable to suppose that the technic should have preserved mitochondria only in selected types of cells. The filaments in question most probably have nothing directly to do with mitochondria. 3) The filaments are apparently identical with the ergastoplasmic filaments described by Bensley (1) for the parenchymal cells of the pancreas of the adult guinea pig, readily distinguishable from mitochondria demonstrable by appropriate technics. Similar filaments have been described for other secretory cells, as for example, salivary glands and kidney.

On the basis of the above considerations the conclusion seems unavoidable that these filaments in the yolk-sac entoderm are of secretory significance. The manner in which they function in the secretion process is uncertain, but there is some evidence that they segment distally into granules. These filaments, then, may be presecretion filaments. In the 25 mm. stages, filaments are relatively less, and granules relatively more, abundant than at the 10 mm. stage.

Similar structures have been described in the human yolksac of about this same stage [Jordan (10, 11, and 12) ; Branca (2)]. Branca indeed interpreted them as 'functional protoplasm.' I first designated them by the term 'mucinous masses,' since they reacted to the specific stains for mucus. In my first study (1907) I inclined to the belief that they were degeneration prod ucts. In the* light of the data from pig embryos my subsequent ('10) interpretation as secretory structures appears to have been correct. The filaments have a basophilic staining reaction, hence stain well in specific mucous dyes. In later developmental (functional) stages they are limited to the basal ends of the cells, where they may become clumped into a deep staining irregularly oval mass. The 'mucinous masses' described for the yolk-sac of 9 and 13 mm. human embryos are essentially the same structure as the presecretion filaments of the 10 mm. pig embryo ; and their functional role is most probably secretory.

What then may be the meaning of the yolk-sac entoderm in terms of function? The additional evidence from the yolk-sac of the pig, further supports my earlier conclusion ('07) that this cell structure is to be interpreted in terms of the ancestral history of higher mammals. In the ancestors with yolk laden eggs the entodermal cells undoubtedly had the function primarily of elaborating a digestive fluid for the liquefaction and assimilation of the yolk. In yolkless umbilical vesicles, the entoderm apparently still develops and differentiates in accord with an 'ancestral memory,' though it can perform no true digestive function. The umbilical vesicle of the pig, as of man, is in large part — that is, as concerns digestive significance — a vestigial structure. But it has taken on a secondary function, now apparently become of great importance, as an early, perhaps original, center of haemopoiesis.

The above discussion would seem to dispose of Paladino's (20) suggestion that the yolk-sac entoderm of higher mammals has a hepatic function. The form and structure of the two classes of cells are indeed very closely similar (figs. 31 and 32), but this need not necessarily imply identity of function. The similarity is due more probably to the fact of common origin from the primitive gut, and the further fact that both are functionally active, and in a secretory manner. Nor need the presence of glycogen in both types of cells be interpreted in terms of functional identity, since many types of cells of embryos contain glycogen [Gage (8)].

Neither brush borders nor terminal bars occur on these cells. Such structures have been described for the entodermal cells of the human yolk-sac by Branca (2). However in my own specimens of the human yolk-sac (10, 11, and 12), I could never convince myself of the presence of these structures. Lewis (15) likewise was unable to find them in human yolk-sacs of similar ages.

The entodermal cells in the yolk-sac of the 10 mm. pig embryo are undergoing extensive mitotic proliferation. This fact, viewed in conjunction with the good cytologic preservation of the cells as indicated primarily by the abundance and character of the presecretion filaments, should remove all doubt as to the normal and healthy condition of these specimens.

Not a single entodermal cell can be found in process of amitotic division. Nor are any of these cells binucleated. This is significant in view of the fact that all types of cells in the mesenchyma and its derivatives show abundant examples which admit of interpretation in terms of direct division.

2) Haemopoietic. The first question under this caption concerns the origin of the angioblast. The term 'angioblast' is employed here to designate the original anlage of the vascular tissue in the yolk-sac. It is obvious that no sharp line can be drawn between original and secondary angioblast. Suffice it to note that angioblast is still in process of formation in the yolk-sac of the 10 mm. embryo. No information accrues from this study touching the question of the origin of the first mass of vascular anlages. Once formed, angioblast can of course spread by process of growth. However, it is also still being added to by previously discrete moieties. If these additions can be shown to be made from the mesenchyma, it would seem to afford a strong presumption against the derivation of the original angioblast from entoderm [Minot (19)]. Such anlages do arise by differentiation within the mesenchyma in the shape of discrete blood-islands, as described above. I conclude for the mesenchymal origin of the angioblast on the basis, then, mainly of these two observations: 1) the common origin of endothelium and haemoblasts, as described above, from niesenchyma;

2) the sharp (leiiiurciitioii between the.sench^'iiia and eiitotlerin in the embryos here considered. Where blood vessel and entoderm abut, the basement membrane of the entoderm and the endothelial cells of the vessel are never in direct continuity (fig- 2).

The close detailed structural similarity between the mesothelial cells and the endothelial cells, and between the nuclei of both and those of the mesenchyma, was noted above (figs. 13 to 20) . The criteria which Clark (4) applied in the chick embryo for the differentiation between endothelial nuclei and mesench}-mal nuclei are inapphcable to the yolk-sac mesenchyma of pig embryos of the 5 to 15 mm. stages of development. Number of nucleoli, character of nucleolar contour, and depth of tingibility of nucleoli are not features by which mesenchyma nuclei can be differentiated from endothelial nuclei. These are marks which characterize different cells (probably representing difTerent functional phases) of mesenchyma, mesothelium and endothelium ahke.

The moriDhologic evidence seems to force the conclusion that endothelium and mesothelium are both very similar difTerentiation products of mesenchyma, the factor chiefly operative in the differentiation being the mechanical factor of pressure, as maintained by Huntington (9), Schulte (21) and others. The pressure exerted upon the mesothelium operates from the relatively more rapidly growing entoderm; that upon the endothelium from the confined blood cells and plasma. The further fact that haemoblasts arise from l^oth mesenchyma and endothelium supports the conclusion of their essential identity.

If the above is correct then one would expect that the mesothelium also could produce haemoblasts. My material yields no data in support of this view. Indeed very careful study of the mesotlielium both of the yolk-sac and the chorion, with this point in view, gave only negative evidence. The mesothelial cells proliferate both mitotically and apparently amitotically but nothing appears closely similar to the phenomena described by Bremer (3) for the chorion of the young human embryo, where the mesothelium is said to invaginate the underlying meseiichynia of tlie body stalk in the form of cords and tubules (angiocysts) the cells of which differentiate into haemoblasts and endothelium. Bremer's observations, however, are a further \'ery strong support to the claim that angioblast is of mesenchymal origin, and that mesenchyma, mesothelium and endothelium are originally identical structures.

The monophyletic theory of blood cell origin considers the haemoblast the common parent of both erythrocytes and leucocytes. Its correspondence with fact, at least in essential outlines, is now widely accepted. The point which has stimulated most discussion concerns the origin of isolated haemoblasts within the mesenchyma. Are such differentiation products of the mesenchyma, or are they migrants from the blood vessels? The latter view was held by Minot (19); Maximow (16 and 17) and others champion the opposing view. In the case of the yolksac of the pig, the evidence seems definite in favor of the in situ differentiation of haemoblasts from the mesenchyma. The observations both from blood-islands and single cells have been given above. Haemoblasts of course are capable of amoeboid activity, and undoubtedly do leave the blood vessels under certain conditions, and invade the surrounding mesenchyma. But that the cell (h) illustrated in figure 30 cannot be interpreted as such is clear from: 1) the connection of its nucleus, through a delicate chromatic bridge, with the nucleus of the mesenchyma; and 2) its perfectly healthy condition, both from the viewpoint of its nucleus and its cytoplasm. Nor can there remain any doubt that it is actually a haemoblast when its cytoplasm and luicleus, in contrast to the cytoplasm and nucleus of the mesenchyma, is compared with an intravascular haemoblast.

The evidence given above for the extensive origin of haemoblasts from the endothelium seems conclusive for the 10 mm. pig embryo. Neither at earlier nor later stages is this jirocess so evident.

The haemogenic activity of the endothelium in the yolk-sac of the pig is of cardinal significance especially in view of Stockard's (23) findings in the case of the Fundulus embryo, where the problem was approached by the experimental method. This consisted in tho stoj^pafio of the embryonic circulation by means of anaesthetics. Stockard's observations led him to conclude that in the Fundulus embryos investigated (uj) to 20 days) the entlothelium plays no haemogenic role. In the pig embryo, on the contrary, the data leaves no escape from the opposite conclusion, a conclusion arrived at also by many investigators of \'ari()us embryo forms, [e.g., certain chelonians, Jordan and Flijipin (13)]. This conclusion is supported by the further imj^ortant fact that the endothelium of the sinusoids of the liver and of the glomeridar capillaries of the mesonephroi also produce haemoblasts.

The sole alternative interpretation that has an^' appearance of plausibility respecting the haemoblasts of the yolk-sac vessels here described as separating from the endothelium, is that they have become pressed against the wall and thus modified in shape and caused to adhere intimately to the endothelium, so as to stimulate endothelial continuity and derivation. This suggestion is rendered inapplicable by 1) the possibility of tracing a complete series of transition stages between a true endothelial cell, through intermediate haemoblast stages, to a free haemoblast; 2) the possibility of tracing a similar series through to multinucleated giant cells; 3) the fact that such haemoblasts in apparent continuity with the endothelium are cjuite as abundant in essentially empty vessels as in vessels crowded with blood cells, where alone an adecjuate factor of pressure would seem to prevail, and 4) that haemoblasts, though apparently naked cells, do not in general exhibit adhesive properties except among themselves.

b) Giant celh. The derivation and the morphologic and ca'tologic variations of the giant cells are clear, as described above. These cells are simply modified haemoblasts, capable of undergoing a similar differentiation into giant erythroblasts, and ai)ixirently ultimately diffcn-entiating normoblasts intracellularly. This last point may be thought perhaps to remain somewhat doubtful, and e\'en if the interpretation is accepted, the significance and economy of this process — for it is clearly not essential, since it is not the exclusive method for yolk-sac haemopoiesis still remains obscui'e.

That the giant cells have no genetic relationship to the entoderm, as urged by Graf. v. Spee (22), is certain. That the method of nuclear multiplication is largely a matter of budding and fission is also demonstrable (fig. 35). It may be stated also that these cells are much more abundant at about the 10 mm. than at earlier and later stages; and that while all the other types of erythrocytes are found in the embryonic circulatory system, giant cells are practically limited to the yolk-sac vessels. A few smaller varieties appear in the liver and the mesonephroi, and occasionally one appears in a capillary in the mesenchyma next the brain. Haemoblasts also are only sparingly found outside of the yolk-sac, liver, and the glomerular sinusoids of the mesonephroi. The normoblasts are in the vast majority in the intraembryonic circulatory system.

On the basis of their occasional normoblast content the giant cells might be interpreted 1) as erythrophages or 2) as multiple erythroblasts. The latter interpretation was urged by Graf V. Spee (22). The former interpretation is supported by the fact that endothelial cells — which are potential haemoblasts — may apparently function as phagocytes for erythroblasts. The latter more plausible conclusion rests upon my observations that in a giant cell with two normoblasts (fig. 26) no additional nucleus is present; and the further fact that frequently the cell membrane of the normoblast is not separated from the cytoplasm of the giant cell by any space, but the two structures appear continuous (fig. 26). Moreover in certain multinuclear giant cells the several nuclei and their enveloping cytoplasmic areas are at different stages of development. In figure 25 two of the nuclei are typical haemoblast nuclei, two are typical erythroblast nuclei. The upper right hand nucleus {x) is differentiated more than the other, and the enveloping cytoplasm is beginning to take on normoblast characteristics. Ne\'ertheless this interpretation must perhaps still be regarded as more oi* less tentative. But the fact that mega- and polykaryocytes are present in all haemopoietic foci, embryonic, foetal and adult, strongly supports the conclusion that they are closely associated with the haemopoietic process. As such, however, their function does not seem to be an essential one; they may represent simply atypical or possibly ancestral phenomena. Erythrocytes commonly develop from mononuclear haemoblasts; binucleated haemoblasts apparently sometimes divide to form two haemoblasts (fig. 3, e) ; multinucleated haemoblasts (polykaryocytes) do not break up into mononuclear haemoblasts, but may produce erythrocytes (normoblasts) intracellularly.

V. Summary

  1. In pig embryos of about 10 mm. length, the yolk-sac attains its highest stage of progressive histologic differentiation. This statement pertains both to the entoderm and to the angioblast.
  2. The entodemal cells are characterized chiefly by abundant presecretion filaments, in which feature they agree with the cells of the liver and mesonephroi.
  3. Angioblast arises from the mesenchyma.
  4. The mesothelium of the yolk-sac of pig embryos between 5 and 12 mm. does not produce haemoblasts. Nor is there any satisfactory evidence that the mesothelium of the body stalk and chorion function to this end.
  5. The mesenchyma may differentiate directly into endothelium or into haemoblasts.
  6. Haemoblasts arise extensively at the 10 mm. stage from the endothelium of the yolk-sac blood vessels. The endothelia of the hepatic sinusoids and mesonephric glomeruli of this stage also show extensive haemopoietic capacity.
  7. Giant cells, both mono- and polynuclear, are abundantly present in the yolk-sac only at about the 10 mm. stage of development. They may arise from endothelium or directly from haemoblasts. They are giant haemoblasts, and apparently function as multiple erythroblasts in which normoblasts differentiate intracellularl}^
  8. The several stages in haemopoiesis, represented successively by haemoblasts, erythroblasts and normoblasts, with transition stages, are abundantly present in the yolk-sac of embiyos from 5 to 15 mm.

Literature Cited

(1) Bensley, R. R. 1911 Studies on the pancreas of tlie p;uinea pig. Am. Jour. Anat., vol. 12, no. 3.

(2) Branca, A. 1908 Recherches sur la vesiculc omhilicale dc I'lioniine. Ann. de Gynec. et Obst., Paris, T. 2, p. 577.

(3) Bremer, John Lewis 1914 The earliest blood-vessels in man. Am. Jour. Anat., vol. 16, no. 4.

(4) Clark, Eliot R. 1914 On certain morphological and staining characteri.s tics of the nuclei of lymphatic and Ijlood-vascular endothelium and of mesenchymal cells, in chick embryos. Anat. Rec, vol. 8, no. 2, pp. 81-82.

(5) Dantschakoff, W. 1908 Ilntersuchungen fiber die Entwickhuig des Blutes unci Bindegewebes bei den Vogeln. I. Die erste Entstehung der Blutzellen beim Htihnerembryo und dcr Dottersack als blutl)ildendes Organ. Anat. Hefte, Bd. 37.

(6) Dantschakoff, W. 1910 IJber den Entwickhmg dcr eml)ryonalen Blut bildung bei Reptilien. Anat. Anz., Bd. 37 (Erganzungsheft).

(7) Emmel, Victor E. 1914 Concerning certain cytological characteristics of the erythroblasts in the ))ig embryo and the origin of non-nucleated erythrocytes by a i)rocess of cytojilasmic constriction. Am. Jour. Anat. vol., 16, no. 2.

(8) Gage, S. H. 1906 Glycogen in a 56-day human embryo and in pig embryos of 7 to 70 mm. Am. Jour. Anat., vol. 5, no. 2; Proc. Am. Assoc. Anat., pt. 13.

(9) Huntington, George S. 1914 The development of the mammalian jugular lymph-sac, etc. Am. Jour. Anat., vol. 16, no. 2.

(10) Jordan, H. E. 1907 The histology of the yolk-sac of a 9.2 mm. human embryo. Anat. Anz., Bd. 31, nos. 11 u. 12, ]). 291.

(11) Jordan, H. E. 1910 A further study of tlie luunan uml)ilical vesicle. Anat. Rec, vol. 4, no. 9.

(12) Jordan, H. E. 1910 A mit-roscopic study of the umbilical vesicle of a 13 mm. human embryo, with special reference to the entodermal tubules and the blood islands. Anat. Anz., Bd. 37, no. 1.

(13) Jordan, H. E. 1915 Haemopoiesis in the yolk-sac of the pig embryo. Proc. Am. Assoc. Anat., Anat. Rec, vol. 9, no. 1.

(14) Jordan, H. E. and Flippin, J. C. 1913 Hacmatopoiesis in Chelonia. Folia Haematologica, Bd. 15.

(15) Lewis, Frederick T. 1912 Chap. XVII, Human cm))ryology, Keil)el and Mall, vol. 2, p. 31S. Lippincott Company.

(16) Maximow, a. 1909 Ilntersuchungen ilber Blut und Bindegewebe. 1.

Die frlihesten Entwicklungsstadien der Blut- und Bindegewebszellen beim Saiigetierembryo, etc. Arch, f . mikr. Anat., Bd. 73, p. 444.

(17) Maximow, A. 1910 IJber embryonale Entwicklunge der Blutzellen l)ei

Selachiern und Amphibien. Anat. Anz., Bd. 37 (Ergiinzungsheft.)

(18) VIkyer, Arthur W. 1904 On the structure of the liuman um])ilical vesicle. Am. Jour. .\nat. vol.3.

(19) MiNoi', ("iiAKi.Ks S. 1912 Chap. Will, lluiiiaii Mmhrvolosy, Koibel and Mall, vol. '2. Lipj)intH)tt Company.

(20) P.\i.Ai)i\(), (;. 1901 Contribuzionc alia conoscciiza .sulla .struttura e runzionc dclla vpsicola ()inl)eli('ale nciruonio e nei niammiferi. Arch. Ital. (Jinecol.. Xapoli, vol. 8, p. 127.

(21) ScHi'LTZE, H. vo-V W . 1914 Early .stagesot' vasculogeuesis in the cat (Folis domestica ) with especial reference to the incsencliynial origin of endothcliuui. Meuioir, \\'istar Inst. Anat. and Biol., Philadelphia.

(22) Spee, Ghaf \ . 189(3 Zur Demon.stration iiher die Entwicklung der Driisen des Menschliehen Dottersackes. Anat. Auz., Bd. 12, p. 76.

(23) Stockard, Charles R. 1915 An exi)erimcntal .study of the origin of Blood and vascular endothelium in the Teleost embrj'o. Proc Atn. Assoc. Anat., Anat. Rec, vol. 9, no. 1 . (Complete paper in Am. Journ. Anat. 18: 2 and 3; and as ^Memoir, .\o. 7, of The AYistar Institute of Anatomy and Biology.)

Plate 1


(Unless otlu'iwisr specified the illustrations are from a single specimen of the 10 mm. stage, the magnification 1000, the fixation witli Zenker's fluid, and the stain employed the haematoxylin-eosin combination).

1 A group of blood cells from one of the larger yolk-sac vessels of a 6 mm. pig embryo (Helly's fixation; Giemsa stain; magnification, 1500 diameters). a) various types (differentiation stages) of haemoblasts; the sparse naked cytoplasm has a vague irregular granular character and stains intensely blue; the large vesicular nucleus stains a very light blue and contains a delicate, finely granvdar reticulum and one or several spheroidal or irregular nucleoli staining like the chromatic granules, a bluish orange, b) Young erythroblasts ('megaloblasts'); the nucleus is relatively smaller and the cytoplasm more voluminous than in the smaller younger haemoblasts; the cytoplasm stains a light blue (brownish graj^ or liluish pink) and contains fine, uniform, spherical granules (probably haemoglobin) ; a cell wall is distinct; the still vesicular nucleus contains a coarsely granular reticulum which stains blue; some of these nuclei still contain a nucleolus, c) Older erythroblasts; the nucleus has become still smaller and more chromatic; the homogeneous cytoplasm is relatively more voluminous and now stains pink, d) Normoblast; the nucleus is .small, granular and chromatic ; the cytoplasm stains brilliant red (in Zenker fixed tissue the cytoplasm consists merely of a coarse irregular unstainal)le reticulum enclosed by a robust cell membrane. 1

2 Narrow jxirtion of wall of yolk-sac including all of its layers. E, entoderm ; the cells contain many presecretion filaments. Between the entoderm and peripheral mesenchyma is a large blood vessel containing a few blood cells at various stages in the metamoriihosis into a normoblast (e) ; a) endothelial cell; b) haemoblast; c) binucleated haemoblast with long pseudopod; d) binucleatcd erythroblast. M, mesothelium; but., basement membrane; cml., endothelium.

3 A group of developing blood cells from a yolk-sac j^lood vessel, a and b) young haemoblasts; c) haemoblast with nucleus in process of amitotic division; d) binucleated haemoblast; e) binucleated haemoblast in process of cytoplasmic amitotic constriction, a fairly conunon form of cell; f ) erythroblast (Maximow's 'megaloblast') ; g) normoblast.

4 Portion of wall of yolk-sac of 10 nun. pig embryo including mesothelium, endothelium and the intervening mesenchyma. a) endothelial cells from wall of a blood vessel; b) endothelial cell in early stage of separation from wall of blood vessel to become a haemoblast; c) later stage; d) extravascular haemoblast, separating from the endothelium.

5 Haemoblast at late stage in process of separation from the endothelium.

6 Haemoblast, of spindle shape, just about to sejjarate from theendothelimn.

7 Ilninucleated giant cell; large haemoblast.

8 Trinucleated haemoblast (giant cell) in final stage of separation from the endothelium (e) .

9 Trinucleated giant cell, immediately after separation from endothelium. Note the lateral Inisal projections, the points of. final separation. One of the uuchM is ap])arcntly undergoing amitosis.

10 liinucleatetl haemoblast in which on(> of the nuclei and the surrounding cytoplasm have differentiated into a iu)rmol)last.

11 and 12 Triniideated giant cells.

Plate 2


l-J lliu'm()i)last (It) in liiial stage of separation i'i'(jiii endotlieliun; ; r, ctnlotlielial cell.

14, 15 and 16 Three successive stages in tlie transformation of an endothelial cell into a haemoblast. E, towards entoderm ; l', towards blood vessel.

17 Nucleus of endothelial cell in phase of amitotic division. Many nuclei also can be seen in mitosis.

18 Nucleus from mesenchyma. Note the similarity l)etween nuclei of endothelium, mesothelium and mesenchyma.

19 and 20 Two mesothelial cells, .s-, towards surface. Occasional cells can be seen in mitosis.

21 Haemoblast in mitosis. The spindle is apiiarently tripolar. Such irregidar mitoses if sufficiently common would explain the multinuclear haemoblast with nuclei of various sizes. Haemoblasts apparently divide both mitotically and amitotically.

22 Haemoblast with nuch'us apparently dividing amitotically.

23 Large binucleated giant cell; the cytoplasm is at an early phase of differentiation into the erythroblast type; the nuclei also are in early, but different, stages of differentiation.

24 Smaller binucleated giant cell (haemoblast); the nuclei are of the typical haemoblast tyi)e.

25 Giant cell from yolk-sac of 10 mm. pig embryo with four nuclei, which, with their envelo]iing cytoplasm, are at different stages of differentiation. Two of the nuclei have haemoblast characters, one erythroblast and one (.r) early normol)last characters. The cytoplasm also around .r has normoblast characteristics.

26 Binucleated haemoblast (giant cell) in late stage of lu'ocess of direct intracellular differentiation into two normoblasts.

27 Haemoblast with one long and several shorter stubby i)seudopods.

2S Endothelial phagocytic cell (perhaps a differentiating haemoblast) having ingested an erythroblast whose nucleus is Tmdergoing karyorrhexis, the cytoplasm appearing normal.

29 Portion of wall of yolk-sac of 10 mm. pig embryo showing a small blood island. The cells are allot the early haemoblast stage, and closely related peripherally to the surrounding mesenchyma, from which they have apparently differentiated. One haemoblast is binucleated. E, entoderm, schematically represented; V, blood vessel.

30 Portion of wall of yolk-sac of 10 mm. pig embryo showing the differentiation of a haemoblast {h) from the mesenchyma. 'The nucleus of the definitive haemoblast is still connected through a chromatic nuclear strand with the nucleus of its sister mesenchymal cell. E, entoderm, schematically represented; 1', blood vessel; mes., mesothelium.

31 Four adjacent entodermal cells to show especially the 'basal' or presecretion filaments.

32 A group of four adjaccul liver cells from the same cmbi'yo, to show the (dose siriiiiai'ity in luiclcar and cvtoi)lasmic struclurc and form between the hepatic and yolk-sac cnnbryonic ei)ithelium. INIany of the hejiatic cells (not here represented) show mitotic figures; amitotic divisions apparently do not yet occur.

33, 34 and 35 Various ty])es of giant haemoblasts. Figure 35 is typical of a large srroui) of giant cells whose nuclei ])roliferatc amitotically.

Cite this page: Hill, M.A. (2020, September 19) Embryology Paper - The microscopic structure of the yolk-sac of the pig embryo (1916). Retrieved from

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