Hedgehog signaling in the posterior region of the mouse gastrula suggests manifold roles in the fetal-umbilical connection and posterior morphogenesis

Developmental Dynamics

Volumn 240, Issue 9, 2011, Pages 2175-2193

  Daane, Jacob M ^a   Downs, Karen M ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Allantois; Amnion; Body wall; Dorsal aortae; Dorsal Cuboidal Mesothelium (DCM); Flk 1; Hedgehog; Hindgut; Intraplacental yolk sac (IPY); Mouse; Oct 3 4; Omphalocoele; Omphalomesenteric artery; PECAM 1; Placenta; Primitive streak; Sinuses of Duval; Somatopleure; Splanchnopleure; Umbilical cord; Umbilical ring; Ventral Cuboidal Mesothelium (VCM); Ventral Ectodermal Ridge (VER); Vessel of confluence (VOC); Visceral endoderm; Yolk sac

Indexed keywords

BETA GALACTOSIDASE; CD31 ANTIGEN; PROTEIN PATCHED 1; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX1; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY ENDOTHELIUM; ARTICLE; CHORIONIC ECTODERM; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO (ANATOMY); FEMALE; FETUS; FETUS MEMBRANE; GASTRULA; HEMATOPOIESIS; HEMATOPOIETIC CELL; HINDGUT; IMMUNOHISTOCHEMISTRY; MALE; MORPHOGENESIS; MOUSE; NEUROECTODERM; NONHUMAN; PLACENTA; POSTERIOR MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REPORTER GENE; SIGNAL TRANSDUCTION; SOMITE; UMBILICUS; VENTRAL ECTODERMAL RIDGE; YOLK SAC;

ANIMALS; EMBRYO, MAMMALIAN; FEMALE; FETUS; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, MUTANT STRAINS; MORPHOGENESIS; SIGNAL TRANSDUCTION; UMBILICAL CORD;

ERINACEIDAE; MUS;

EID: 80051678714     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22711     Document Type: Article

References (64)

1. Astorga J, Carlsson P. 2007. Hedgehog induction of murine vasculogenesis is mediated by Foxf1 and Bmp4. Development 134: 3753-3761.
2. Bitgood MJ, McMahon AP. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 172: 126-138.
3. Brewer S, Williams T. 2004. Finally, a sense of closure? Animal models of human ventral wall defects. Bioessays 26: 1307-1321.
4. Bruns ME, Kleeman E, Mils SE, Bruns DE, Herr JC. 1985. Immunochemical localization of vitamin D-dependent calcium-binding protein in mouse placenta and yolk sac. Anat Rec 213: 514-517, 532-535.
5. Carter AM. 2007. Sources for comparative studies of placentation. I. Embryological collections. Placenta 29: 95-98.
6. Champlin AK, Dorr DL, Gates AH. 1973. Determining the stage of the estrous cycle in the mouse by the appearance of the vagina. Biol Reprod 8: 491-494.
7. Chang H, Li Q, Moraes RC, Lewis MT, Hamel PA. 2010. Activation of Erk by sonic hedgehog independent of canonical hedgehog signaling. Int J Biochem Cell Biol 42: 1462-1471.
8. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
9. Corbel C, Salaun J, Belo-Diabangouaya P, Dieterlen-Lievre F. 2007. Hematopoietic potential of the pre-fusion allantois. Dev Biol 301: 478-488.
10. Cross JC. 2005. How to make a placenta: mechanisms of trophoblast cell differentiation in mice: a review. Placenta 26(SupplA): S3-9.
11. Cross JC, Simmons GJ, Watson ED. 2003. Chorio-allantoic morphogenesis and formation of the placental villous tree. Ann NY Acad Sci 995: 84-93.
12. Daane J, Enders AC, Downs KM. 2011. Mesothelium of the murine allantois exhibits distinct regional properties. J Morphol 272: 536-556.
13. Dannenberg AM, Suga M. 1981. Histochemical stains for macrophages in cell smears and tissue sections: beta-galactosidase, acid phosphatase, nonspecific esterase, succinic dehydrogenase, and cytochrome oxidase. In: Adams DO, Edelson PJ, Koren HS, editors. Methods for studying mononuclear phagocytes. New York: Academic Press. p 375-396.
14. Dawson AB. 1922. The origin and occurrence of the single umbilical artery in normal and abnormal human fetuses. Anat Rec 24: 321-349.
15. Downs KM. 2002. Early placentation in the mouse. Placenta 23: 116-131.
16. Downs KM. 2003. Historical perspective: Florence Sabin and the mechanism of blood vessel lumenization during vasculogenesis. Microcirculation 10: 5-25.
17. Downs KM. 2006. In vitro methods for studying vascularization of the murine allantois and allantoic union with the chorion. Methods Mol Med 121: 241-272.
18. Downs KM. 2008. Systematic localization of Oct-3/4 to the gastrulating mouse conceptus suggests manifold roles in mammalian development. Dev Dyn 237: 464-475.
19. Downs KM, Davies T. 1993. Staging of gastrulation in mouse embryos by morphological landmarks in the dissection microscope. Development 118: 1255-1266.
20. Downs KM, Gardner RL. 1995. An investigation into early placental ontogeny: allantoic attachment to the chorion is selective and developmentally regulated. Development 121: 407-416.
21. Downs KM, Harmann C. 1997. Developmental potency of the murine allantois. Development 124: 2769-2780.
22. Downs KM, Gifford S, Blahnik M, Gardner RL. 1998. The murine allantois undergoes vasculogenesis that is not accompanied by erythropoiesis. Development 125: 4507-4521.
23. Downs KM, Hellman ER, McHugh J, Barrickman K, Inman K. 2004. Investigation into a role for the primitive streak in development of the murine allantois. Development 131: 37-55.
24. Downs KM, Inman KE, Jin DX, Enders AC. 2009. The Allantoic Core Domain (ACD): New insights into development of the murine allantois and its relation to the primitive streak. Dev Dyn 238: 532-553.
25. Duval M. 1892. Le placenta des rongeurs. [The rodent placenta.] In: Alcan F, editor. Journal of Anatomy and Physiology 1889-1892. Paris: Ancienne Librarie Gemner Bailliere.
26. Epstein DJ, McMahon AP, Joyner AL. 1999. Regionalizaiton of Sonic hedgehog transcription along the anteroposterior axis of the mouse central nervous system is regulated by Hnf3-dependent and -independent mechanisms. Development 126: 281-292.
27. Garcia-Porrero JA, Godin IE, Dieterlen-Lievre F. 1995. Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat Embryol 192: 425-435.
28. Gekas C, Dieterlen-Lievre F, Orkin SH, Mikkola HKA. 2005. The placenta is a niche for hematopoietic stem cells. Dev Cell 8: 365-375.
29. Gest TR, Carron MA. 2003. Embryonic origin of the caudal mesenteric artery in the mouse. Anat Rec 271: 192-201.
30. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP. 1995. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 10: 301-312.
31. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277: 1109-1113.
32. Green EL. 1966. Breeding systems. In: The Laboratory Mouse.
33. Holt SJ, Sadler PW. 1958. Studies in enzyme cytochemistry III. Relationships between solutbility, molecular association and structure in indigoid dyes. Proc R Soc (Lond) 148B: 495.
34. Inman KE, Downs KM. 2006. Brachyury is required for elongation and vasculogenesis in the murine allantois Development 133: 2947-2959.
35. Inman KE, Downs KM. 2007. The murine allantois: emerging paradigms in formation and development of the mammalian umbilical cord and its relation to the fetus. Genesis 45: 237-258.
36. Jenkins D. 2009. Hedgehog signalling: emerging evidence for non-canonical pathways. Cell Signal 21: 1023-1034.
37. Jiang G, Herman GE. 2006. Analysis of Nsdhl-deficient embryos reveals a role for Hedgehog signaling in early placental development. Hum Mol Genet 15: 3293-3305.
38. Lojda Z. 1970. Indigogenic methods for glycosidases. Histochimie 22: 3.
39. Matsumaru D, Haraguchi R, Miyagawa S, Motoyama J, Nakagata N, Meijlink F, Yamada G. 2011. Genetic analysis of hedgehog signaling in ventral body wall development and the onset of omphalocele formation. PLos One 6: e16260.
40. Motoyama J, Takabatake T, Takeshima T, Hui C-C. 1998. Ptch2, a second mouse Patched gene is co-expressed with Sonic Hedgehog. Nature Genet. 18: 104-106.
41. Naiche LA, Papaioannou VE. 2003. Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130: 2681-2693.
42. Newman PJ. 1997. The biology of PECAM-1. J Clin Invest 99: 3-8.
43. Newman PJ, Newman DK. 2003. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol 23: 953-964.
44. North TE, Gu T-L, Stacy T, Wang Q, Howard L, Binder M, Marin-Padilla M, Speck NA. 1999. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126: 2563-2575.
45. North TE, deBruijn MF, Stacy T, Talebian L, Lind E, Robin C, Binder M, Dzierzak E, Speck NA. 2002. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 16: 661-672.
46. Otterbach K, Dzierzak E. 2005. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 8: 377-387.
47. Peeters M, Ottersbach K, Bollerot K, Orelio C, deBruijn M, Wijgerde M, Dzierzak E. 2009. Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development. Development 136: 13-21.
48. Poulsen LK, Dalton HM, Angles ML, Marshall KC, Molin S, Goodman AE. 1997. Simultaneous determination of gene expression and bacterial identity in single cells in defined mixtures of pure cultures. Appl Environ Microbiol 63: 3698-3702.
49. Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, Tsui LC, Muenke M. 1996. Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 14: 357-360.
50. Rossant J, Cross JC. 2001. Placental development: lessons from mouse mutants. Nat Rev Genet 2: 538-548.
51. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu X-F, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1 deficient mice. Nature 376: 62-66.
52. Snell GB, Stevens LC. 1966. Early embryology. In: Green EL, editor. Biology of the Laboratory Mouse. New York: McGraw Hill. p 205-245.
53. Stevenson RE, Hall JG, editors. 2006. Human malformations and related anomalies. Oxford: Oxford University Press.
54. Swiers G, deBruijn M, Speck NA. 2010. Hematopoietic stem cell emergence in the conceptus and the role of Runx1. Int J Dev Biol 54: 1151-1163.
55. Takabatake T, Ogawa M, Takahashi TC, Mizuno M, Okamoto M, Takeshima K. 1997. Hedgehog and patched gene expression in adult ocular tissues. FEBS Lett 410: 485-489.
56. Trempus CS, Morris RJ, Bortner CD, Cotsarelis G, Faircloth RS, reece JM, Tennant RW. 2003. Enrichment for living murine karatinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 120: 501-511.
57. Walls JR, Coultras L, Rossant J, Henkelman RM. 2008. Three-dimensional analysis of vascular development in the mouse embryo. PLoS One 3: e2843.
58. Williams C, Kim S-H, Ni TT, Mitchell L, Ro H, Penn JS, Baldwin SH, Solnica-Krezel L, Zhong TP. 2010. Hedgehog signaling induces arterial endothelial cell formation by repressing venous cell fate. Dev Biol 341: 196-204.
59. Wilson CW, Chuang PT. 2010. Mechanism and evolution of cytosolic Hedgehog signal transduction. Development 137: 2079-2094.
60. Yamaguchi TP, Dumont DJ, Conlon RA, Breitman ML, Rossant J. 1993. flk-1, an flt-related receptor tyrosine kinase, is an early marker for endothelial cell precursors. Development 118: 488-498.
61. Yokomizo T, Dzierzak E. 2010. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 137: 3651-3661.
62. Zeigler BM, Sugiyama D, Chen M, Guo Y, Downs KM, Speck NA. 2006. The allantois and chorion, which are isolated before circulation or chorio-allantoic fusion, have hematopoietic potential. Development 133: 4183-4192.
63. Zovein AC, Turlo KA, Ponec RM, Lynch MR, Chen KC, Hofmann JJ, Cox TC, Gasson JC, Iruela-Arispe ML. 2010. Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters. Blood 116: 3435-3544.