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Review
, 31 (8), 892-902

The Enigmatic Primitive Streak: Prevailing Notions and Challenges Concerning the Body Axis of Mammals

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Review

The Enigmatic Primitive Streak: Prevailing Notions and Challenges Concerning the Body Axis of Mammals

Karen M Downs. Bioessays.

Abstract

The primitive streak establishes the antero-posterior body axis in all amniote species. It is thought to be the conduit through which mesoderm and endoderm progenitors ingress and migrate to their ultimate destinations. Despite its importance, the streak remains poorly defined and one of the most enigmatic structures of the animal kingdom. In particular, the posterior end of the primitive streak has not been satisfactorily identified in any species. Unexpectedly, and contrary to prevailing notions, recent evidence suggests that the murine posterior primitive streak extends beyond the embryo proper. In its extraembryonic site, the streak creates a node-like cell reservoir from which the allantois, a universal caudal appendage of all amniotes and the future umbilical cord of placental mammals, emerges. This new insight into the fetal/umbilical relationship may explain the etiology of a large number of umbilical-associated birth defects, many of which are correlated with abnormalities of the embryonic midline.

Figures

Figure 1
Figure 1
The posterior primitive streak is confined to the embryo proper and gives rise to the allantois. Modified from Sobotta (1911)(10), Figs. 9, 10, and 12, with kind permission of Springer Science + Business Media. Staging of Sobotta's sections was according to Ref. 14 with recent further refinements at the headfold stages in Ref. 8. A: Presumptive late streak (LS) stage (~7.0 dpc) showing the formation of the exocoelom (x) and the extent of the primitive streak (ps) within the embryonic compartment of the conceptus. The nascent amnion (am) is forming. B: Presumptive very early headfold (vEHF) stage (~7.75 dpc) depicts the allantoic bud (al) in association with the intraembryonic primitive streak, whose posterior limit is within the embryo proper, just beneath the amnion. C: Presumptive early headfold (EHF) stage (~7.75–8.0 dpc) shows an enlarging allantois. The primitive streak, black line within the nascent amniotic cavity, traced from Sobotta's original figures, is limited to the embryo proper.
Figure 2
Figure 2
The allantois as depicted by other investigators. A: Modified from Dalcq (p. 125, Fig. 51)(11), after Mulnard(12), Fig. 43a, with permission from the Oxford University Press and Informa Clinical Medicine-Journals. The allantois contains a “posterior node” (p.n.) contiguous with the intraembryonic primitive streak. Estimated stage: early headfold (EHF, ~7.75 dpc). B–D: Figs. 18–20 reproduced and adapted with permission from the Company of Biologists,(13) showing an increasingly elongated bifurcation of the outer visceral endoderm into the base of the allantois. Estimated stages: B: late headfold (LHF, ~8.0 dpc); C: 1–2-somite pairs (1–2-s, ~8.0–8.25 dpc); D: 6-s (~8.5 dpc). al, allantois; ex, exocoelom; H.n., Henson's node; ve, visceral endoderm.
Figure 3
Figure 3
The posterior primitive streak extends into the extraembryonic region where it establishes the ACD. Reprinted from Ref. 15 with permission from John Wiley and Sons, Inc. Key features of this model: A: The posterior primitive streak establishes the extraembryonic primitive streak (xps). B: The allantoic bud emerges from the distal part of the xps, over which lies allantois-associated extraembryonic visceral endoderm (AX).(8,15) C: In collaboration with the AX, the xps begins to expand. D: By the early headfold (EHF) stage, the ACD (orange) is visible, and enlarging. Together with the distal region of the allantois, the ACD may regulate allantoic length. The AX is becoming transformed and contains T- and Oct-3/4-positive cells (represented by the orange circle). E: The ACD is fully mature, while the AX continues to be transformed into a squamous cell type containing T- and Oct-3/4 cells. F: Arrows indicate the contributions of the ACD and intraembryonic primitive streak (IPS) to the allantois.
Figure 4
Figure 4
The posterior primitive streak of the guinea pig may extend its reach into the exocoelom. Modified from Huber, 1918(17) with permission from John Wiley and Sons, Inc. The arrowhead was not in the original figure; it indicates what appears morphologically to be a similar extension of the posterior primitive streak into the exocoelom in this embryonic specimen of the guinea pig. Stage estimated to be neural plate/no bud (OB; ~7.0 dpc) stage. am, amnion; ps, intraembryonic primitive streak.
Figure 5
Figure 5
Experimental strategies to discover ACD function. A: TC/TC mutants, In the TC/TC mutant, left, the ACD dies, resulting in a highly blebbed remnant allantois that has a tendency to spread over the amnion and does not elongate to fuse with the chorion. Data from Ref. 42. B: −ACD allantoic regenerates. Left, the entire allantois and its ACD are removed by aspiration. Right, a short −ACD allantoic regenerate forms that does not elongate far enough to fuse with the chorion but displays a properly patterned vasculature that is fused with the paired embryonic dorsal aortae. Data from Refs. 15, . C: +ACD regenerates. Left, all but the proximal ACD-containing region was removed by aspiration. Right, the ACD-containing allantoic regenerate elongates, fuses with the chorion, and displays an appropriately patterned vasculature that is fused with the embryonic dorsal aortae. Data from Ref. 15. D: Center, the allantois (“−ACD”) is removed from wildtype (+/+) or TC/TC mutant hosts, and replaced by a graft (left, blue) containing the ACD. Right, the regenerated allantois contains a patterned donor midline that fans out and contributes largely to the distal region, while the flanks are composed of host cells emanating from the intraembryonic primitive streak. From Ref. 15. E: In situ fate mapping of the ACD. Left, DiI (blue) is applied to the center of the ACD. Right, ACD-labeled cells remain in place and form a midline file through the length of the allantois, fanning throughout the distal region. Data from Ref. 15. F: In situ fate mapping of the intraembryonic primitive streak. Left, DiI (blue) is applied to the posterior midline of the intraembryonic primitive streak. Right, labeled descendants, when they contributed to the allantois (only 66% of the time), were found in the allantoic flanks. The original labeled cells did not appear to remain in place. Data from Ref. 15. G: Legend: 1, allantois prior to genetic analysis or manipulation; 2, ACD; 3, node; 4, intraembryonic primitive streak; 5, blebbed TC/TC allantois; 6, −ACD regenerate allantois exhibiting correctly patterned vasculature; 7, elongated fused allantois with correctly patterned vasculature; horizontal bar separates distal (top) and proximal (bottom) regions; 8, ACD-containing donor graft; 9, DiI-labeled cell cluster; 10, paired embryonic dorsal aortae; 11, chorion.

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