Confinement and clearance of OCT4 in the porcine embryo at stereomicroscopically defined stages around gastrulation

Molecular Reproduction and Development

Volumn 73, Issue 6, 2006, Pages 709-718

  Vejlsted, Morten ^a   Offenberg, Hanne ^a   Thorup, Flemming ^b   Maddox Hyttel, Poul ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Hlth Prod Axelborg Axeltorv 3 D   (Denmark)

Author keywords

Alkaline phosphatase; C kit; Differentiation; Primordial germ cells; Staging; Vimentin

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL BIOLOGY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; GASTRULATION; GERM LAYER; IMMUNOHISTOCHEMISTRY; INNER CELL MASS; MESODERM; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEREOMICROSCOPY;

ANIMALS; EMBRYO; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GERM CELLS; GESTATIONAL AGE; MICE; MICROSCOPY; OCTAMER TRANSCRIPTION FACTOR-3; PREGNANCY; SWINE;

ANIMALIA; SUIDAE;

EID: 33646459149     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20461     Document Type: Article

References (105)

1. Anderson LL. 1978. Growth, protein content and distribution of early pig embryos. Anat Rec 190:143-154.
2. Anderson R, Copeland TK, Schöler H, Heasman J, Wylie C. 2000. The onset of germ cell migration in the mouse embryo. Mech Dev 91:61-68.
3. Artinger M, Blitz I, Inoue K, Tran U, Cho KWY. 1997. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech Dev 65:187-196.
4. Avilion AA, Nicolis SK, Pevny LH, Prez L, Vivian N, Loell-Badge R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes & Dev 17:126-140.
5. Banerjee A, Roach MC, Trcka P, Ludueña RF. 1990. Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J Biol Chem 265:1794-1799.
6. Barends PMG, Stroband HWJ, Taverne N, te Kronnie G, Leën MPJM, Blommers PCJ. 1989. Integrity of the preimplantation pig blastocyst during expansion and loss of polar trophectoderm (Rauber cells) and the morphology of the embryoblast as an indicator for developmental stage. Reprod Fertil 87:715-726.
7. Beddington RS, Robertson EJ. 1999. Axis development and early asymmetry in mammals. Cell 96:195-209.
8. Bendel-Stenzel MR, Gomperts M, Anderson R, Heasman J, Wylie C. 2000. The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91:143-152.
9. Black JL, Erickson BH. 1968. Oogenesis and ovarian development in the prenatal pig. Anat Rec 161:45-56.
10. Blum M, Gaunt SJ, Cho KWY, Steinbeisser H, Blumberg B, Bittner D, De Robertis EM. 1992. Gastrulation in the mouse: The role of the homeobox gene goosecoid. Cell 69:1097-1106.
11. Boucher DM, Schäffer M, Deissler K, Moore CA, Gold JD, Burdsal CA, Meneses JJ, Pedersen RA, Blum M. 2000. goosecoidexpression represses Brachyury in embryonic stem cells and affects craniofacial development in chimeric mice. Int J Dev Biol 44:279-288.
12. Brittis PA, Meiri K, Dent E, Silver J. 1995. The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system. Exp Neurol 134:1-12.
13. e mouse embryos. Dev Dyn 198:182-189.
14. Burdon T, Chambers I, Stracey C, Niwa H, Smith A. 1999. Signaling mechanisms regulating self-renewal and differentiation of pluripotent embryonic stem cells. Cells Tissues Organs 165:131-143.
15. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655.
16. Chen SS, Revoltella RP, Papini S, Michelini M, Fitzgerald W, Zimmerberg J, Margolis L. 2003. Multilineage differentiation of Rhesus monkey embryonic stem cells in three-dimensional culture systems. Stem Cells 21:281-295.
17. Chiquoine AD. 1954. The identification, origin and migration of the primordial germ cells of the mouse embryo. Anat Rec 118:135-146.
18. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow PN, Lovell-Badge R. 1996. A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122:509-520.
19. Curran S, Urven L, Ginther OJ. 1997. Distribution of putative primordial germ cells in equine embryos. Equine Vet J, Suppl 25:72-76.
20. Dolci S, Williams DE, Ernst MK, Resnick JL, Brannan CI, Fock LF, Lyman SD, Boswell SH, Donovan PJ. 1991. Requirements for mast cell growth factor for primordial germ cell survival in culture. Nature 352:809-811.
21. Dolci S, Levati L, Pellegrini M, Faraoni I, Graziani G, Di Carlo A, Geremia R. 2002. Stem cell factor activates telomerase in mouse mitotic spermatogonia and in primordial germ cells. J Cell Sci 115:1643-1649.
22. Downs KM, Davies T. 1993. Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 118:1255-1266.
23. Easter SS, Jr., Ross LS, Frankfurter A. 1993. Initial tract formation in the mouse brain. J Neurosci 13:285-299.
24. Eddy EM, Clark JM, Gong D, Fenderson BA. 1981. Origin and migration of primordial germ cells in mammals. Gamete Res 4:333-362.
25. Enders AC, Schlafke S, Hendrickx AG. 1986. Differentiation of the embryonic disc, amnion, and yolk sac in the Rhesus monkey. Am J Anat 177:161-185.
26. Fléchon JE, Degrouard J, Fléchon B. 2004. Gastrulation events in the prestreak pig embryo: Ultrastructure and cell markers. Genesis 38:13-25.
27. Franke WW, Grund C, Kuhn C, Jackson BW, Illmensee K. 1982. Formation of cytoskeletal elements during mouse embryogenesis. Differentiation 23:43-59.
28. Freeman B. 2003. The active migration of germ cells in the embryos of mice and men is a myth. Reproduction 125:635-643.
29. Fujiwara T, Dunn NR, Hogan BLM. 2001. Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc Nat Acad Sci USA 98:13739-13744.
30. Fujomoto T, Ukeshima A, Kiyofuji R. 1976. The origin, migration and morphology of the primordial germ cells in the chick embryo. Anat Rec 185:139-154.
31. Ginis I, Luo Y, Miura T, Thies S, Brandenberger R, Gerecht-Nir S, Amit M, Hoke A, Carpenter MK, Itskovitz-Eldor J, Rao MS. 2004. Differences between human and mouse embryonic stem cells. Dev Biol 269:360-380.
32. Ginsburg M, Snow MHL, McLaren A. 1990. Primordial germ cells in the mouse embryo during gastrulation. Development 110:521-528.
33. Gjørret JO, Maddox-Hyttel P. 2005. Attempts towards derivation and establishment of bovine embryonic stem cell-like cultures. Reprod Fertil Dev 17:113-124.
34. Godin I, Deed R, Cooke J, Zsebo K, Dexter M, Wylie CC. 1991. Effects of the Steel gene product on mouse primordial germ cells in culture. Nature 352:807-809.
35. Gomperts M, Garcia-Castro M, Wylie C, Heasman J. 1994. Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135-141.
36. Green WW, Winters LM. 1946. Cleavage and attachment stages of the pig. J Morph 78:305-316.
37. Guillemot M, Turbe A, Hue I, Renard JP. 2004. Staging of ovine embryos and expression of the T-box genes Brachyury and Eomesodermin around gastrulation. Reproduction 127:491-501.
38. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA. 2002. Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes & Dev 16:2650-2661.
39. Hart AH, Hartley L, Ibrahim M, Robb L. 2004. Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev Dyn 230:187-198.
40. Herrmann BG, Labeit S, Poustka A, King TR, Lehrach H. 1990. Cloning of the T gene required in mesoderm formation in the mouse. Nature 343:617-622.
41. Hue I, Renard JP, Viebahn C. 2001. Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Dev Genes Evol 211:157-159.
42. Idkowiak J, Weisheit G, Viebahn C. 2004. Polarity in the rabbit embryo. Sem Cells & Dev Biol 15:607-617.
43. Jackson BW, Grund C, Winter S, Franke WW, Ilmensee K. 1981. Formation of cytoskeletal elements during mouse embryogenesis. Differentiation 20:203-216.
44. Jung JG, Kim DK, Park TS, Lee SD, Lim JM, Han JY. 2005. Development of novel markers for the characterization of chicken primordial germ cells. Stem Cells 23:689-698.
45. Kamachi Y, Uchikawa M, Kondoh H. 2000. Pairing SOX off with partners in the regulation of embryonic development. Trends Gen 16:182-187.
46. Kehler J, Tolkunova E, Koschorz B, Pesce M, Gentile L, Boiani M, Lomeli H, Nagy A, McLaughlin KJ, Schöler HR, Tomilin A. 2004. Oct4 is required for primordial germ cell survival. EMBO Rep 5:1078-1083.
47. Kimura C, Yoshinaga K, Tian E, Suzuki M, Aizawa S, Matsuo I. 2000. Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev Biol 225:304-321.
48. Kirchhof N, Carnwath JW, Anastassiadis K, Schöler H, Niemann H. 2000. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 63:1698-1705.
49. Kispert A, Koschorz B, Herrmann BG. 1995. The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J 14:4763-4772.
50. Knoetgen H, Viebahn C, Kessel M. 1999. Head induction in the chick by primitive endoderm of mammalian, but not avian origin. Development 126:815-825.
51. Knoetgen H, Teichmann U, Wittier L, Viebahn C, Kessel M. 2000. Anterior neural induction by nodes from rabbits and mice. Dev Biol 225:370-380.
52. Kuroda T, Tada M, Kubota H, Kimura H, Hatano S, Suemori H, Nakatsuji N, Tada T. 2005. Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25:2475-2485.
53. Kurosaka S, Eckardt S, McLaughlin KJ. 2004. Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol Reprod 71:1578-1582.
54. Lawson KA, Meneses JJ, Pedersen RA. 1991. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113:891-911.
55. Lawson KA, Dunn NR, Roelen BAJ, Zeinstra LM, Davis AM, Wright CVE, Korving JPWFM, Hogan BLM. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes & Dev 13:424-436.
56. Lee KY, DeMayo FJ. 2004. Animal models of implantation. Reproduc-tion 128:679-695.
57. Lee GS, Kim HS, Lee SH, Kang MS, Kim DY, Lee CK, Kang SK, Lee BC, Hwang WS. 2005. Characterization of pig Vasa homolog gene and specific expression in germ cell lineage. Mol Reprod Dev 72:320-328.
58. Leichthammer F, Baunack E, Brem G. 1990. Behavior of living primordial germ cells of lifestock in vitro. Theriogenology 33:1221-1230.
59. LoebelDAF, Watson CM, De Young RA, Tam PPL. 2003. Lineage choice and differentiation in mouse embryos and embryonic stem cells. Dev Biol 264:1-14.
60. Maddox-Hyttel P, Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen H, Tveden-Nyborg P, Trounson A. 2003. Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125:607-623.
61. Manova K, Bachvarova RF. 1991. Expression of c-kit encoded at the W locus of mice in developing embryonic germ cells and presumptive melanoblasts. Dev Biol 146:312-324.
62. Manova K, Nocka K, Besmer P, Bachvarova RF. 1990. Gonadal expression of c-kit encoded at the Wlocus of the mouse. Development 110:1057-1069.
63. Matsui Y, Okamura D. 2005. Mechanisms of germ-cell specification in mouse embryos. BioEssays 27:136-143.
64. Matsui Y, Zsebo K, Hogan B. 1990. Embryonic expression of a haemopoietic growth factor encoded by the Steel locus and the ligand for c-kit. Nature 347:667-669.
65. Matsui Y, Toksoz D, Nishikawa S, Nishikawa SI, Williams D, Zsebo K, Hogan B. 1991. Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature 353:750-752.
66. Meijer HA, van de Pavert SA, Stroband HWJ, Boerjan ML. 2000. Expression of the organizer specific homeobox gene Goosecoid (gsc) in porcine embryos. Mol Reprod Dev 55:1-7.
67. Meyer DB. 1964. The migration of primordial germ cells in the chick embryo. Dev Biol 10:154-190.
68. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631-642.
69. Molyneaux KA, Stallock J, Schaible K, Wylie C. 2001. Time-lapse analysis of living mouse germ cell migration. Dev Biol 240:488-498.
70. Orr-Urtreger A, Avivi A, Zimmer Y, Givol D, Yarden Y, Lonai P. 1990. Developmental expression of c-kit, a proto-oncogene encoded at the Wlocus of the mouse. Development 109:911-923.
71. Palmieri SL, Peter W, Hess H, Shöler HR. 1994. Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev Biol 166:259-267.
72. Pan Y, Chen X, Wang S, Yang S, Bai X, Chi X, Li K, Liu B, Li L. 2005. In vitro neuronal differentiation of cultured human embryonic germ cells. Biochem Biophys Res Com 327:548-556.
73. Park TS, Han JY. 2000. Derivation and characterization of pluripotent embryonic germ cells in chicken. Mol Reprod Dev 56:475-482.
74. Patten BM. 1948. Embryology of the pig. 3rd edn. New York: Blakiston. p 37-106.
75. Perea-Gomez A, Rhinn M, Ang SL. 2001. Role of the anterior visceral endoderm in restricting posterior signals in the mouse embryo. Int J Dev Biol 45:311-320.
76. Perea-Gomez A, Vella FD, Shawlot W, Oulad-Abdelghani M, Chazaud C, Meno C, Pfister V, Chen L, Robertson E, Hamada H, Behringer RR, Ang SL. 2002. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3:745-756.
77. Pesce M, Gross MK, Schöler HR. 1998. In line with our ancestors: Oct-4 and the mammlian germ. BioEssays 20:722-732.
78. Pope WF, Xie S, Broermann DM, Nephew KP. 1990. Causes and consequences of early embryonic diversity in pigs. Reprod Fertil Suppl 40:251-260.
79. Prelle K, Vassiliev IM, Vassilieva SG, Wolf E, Wobus AM. 1999. Establishment of pluripotent cell lines from vertebrate species-present status and future prospects. Cells Tissues Organs 165:220-236.
80. Prelle K, Holtz W, Osborn M. 2001. Immunocytochemical analysis of vimentin expression patterns in porcine embryos suggests mesodermal differentiation from day 9 after conception. Anat Histol Embryol 30:339-344.
81. Prelle K, Zink N, Wolf E. 2002. Pluripotent stem cells-model of embryonic development, tool for gene targeting, and basis of cell therapy. Anat Histol Embryol 31:169-186.
82. Rosner MH, Vigano MA, Ozato K, Timmons PM, Poirier F, Rigby PWJ, Staudt LM. 1990. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345:686-692.
83. Saitou M, Barton SC, Surani MA. 2002. A molecular programme for the specification of germ cell fate in mice. Nature 418:293-300.
84. Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P. 1990. New type of POU domain in germ line-specific protein Oct-4. Nature 344:435-439.
85. Shim H, Anderson GB. 1998. In vitro survival and proliferation of porcine primordial germ cells. Theriogenology 49:521-528.
86. Shim H, Gutiérrez-Adán A, Chen LR, BonDurant RH, Behboodi E, Anderson GB. 1997. Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol Reprod 57:1089-1095.
87. Takagi Y, Talbot NC, Rexroad CE, Pursel VG. 1997. Identification of pig primordial germ cells by immunohistochemistry and lectin binding. Mol Reprod Dev 46:567-580.
88. Talbot NC, Rexroad CE, Pursel VG, Powell AM. 1993. Alkaline phosphatase staining of pig and sheep epiblast cells in culture. Mol Reprod Dev 36:139-147.
89. Talbot NC, Powell AM, Rexroad CE. 1995. In vitro pluripotency of epiblasts derived from bovine blastocysts. Mol Reprod Dev 42:35-52.
90. Talbot NC, Powell AM, Garrett WM. 2002. Spontaneous differentiation of porcine and bovine embryonic stem cells (epiblast) into astrocytes or neurons. In Vitro Cell Dev Biol-Anim 38:191-197.
91. Tam PPL, Zhou SX. 1996. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178:124-132.
92. Thomas PQ, Beddington RSP. 1996. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr Biol 6:1487-1496.
93. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. 2000. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93:139-149.
94. van de Pavert SA, Schipper H, de Wit AAC, Soede NM, van den Hurk R, Taverne MAM, Boerjan ML, Stroband HWJ. 2001. Comparison of anterior-posterior development in the porcine versus chicken embryo, using goosecoid expression as a marker. Reprod Fertil Dev 13:177-185.
95. van Eijk MJT, Van Rooijen MA, Modina S, Scesi L, Folkers G, Van Tol HTA, Bevers MM, Fisher SR, Lewin HA, Rakacolli D, Galli C, De Vaureix C, Trounson AO, Mummery CL, Gandolfi F. 1999. Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol Reprod 60:1093-1103.
96. Vejlsted M, Avery B, Schmidt M, Greve T, Alexopoulos N, Maddox-Hyttel P. 2005. Ultrastructural and immunohistochemical characterization of the bovine epiblast. Biol Reprod 72:678-686.
97. Viebahn C. 2004. Gastrulation in the rabbit. In: Stern CD, editor. Gastrulation. From cells to embryo. New York: Cold Spring Harbor Laboratory Press, pp 263-274.
98. Viebahn C, Lane EB, Ramaekers FCS. 1988. Keratin and vimentin expression in early organogenesis of the rabbit embryo. Cell Tissue Res 253:553-562.
99. Viebahn C, Mayer B, de Angelis MH. 1995. Signs of the principle body axes prior to primitive streak formation in the rabbit embryo. Anat Embryol 192:159-169.
100. Viebahn C, Miething A, Wartenberg H. 1998. Primordial germ cells of the rabbit are specifically recognized by a monoclonal antibody labelling the perimitochondrial cytoplasm. Histochem Cell Biol 109:49-58.
101. Viebahn C, Stortz C, Mitchell SA, Blum M. 2002. Low proliferative and high migratory activity in the area of Brachyury expressing mesoderm progenitor cells in the gastrulating rabbit embryo. Development 129:2355-2365.
102. Wartenberg H. 1983. Germ cell migration induced and guided by somatic cell interaction. Bibl Anat 24:93-110.
103. Wrobel KH, Süß F. 1998. Identification and temperospatial distribution of bovine primordial germ cells prior to gonadal sexual differentiation. Anat Embryol 197:451-467.
104. Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hübner K, Schöler HR. 1996. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122:881-894.
105. Ying Y, Qi X, Zhao GQ. 2001. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signalling pathways. Proc Nat Acad Sci USA 98:7858-7862.