Paracrine effects of embryo-derived FGF4 and BMP4 during pig trophoblast elongation

Developmental Biology

Volumn 387, Issue 1, 2014, Pages 15-27

  Valdez Magaña, Griselda ^a,b   Rodríguez, Aida ^a   Zhang, Haixin ^a   Webb, Robert ^a   Alberio, Ramiro ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b CENID Fisiología y Mejoramiento Animal INIFAP   (Mexico)

Author keywords

BMP4; Embryo; FGF4; Gene regulatory network; Pig; Trophoblast elongation

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 4; MITOGEN ACTIVATED PROTEIN KINASE; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; TRANSCRIPTION FACTOR CDX2;

ANIMAL CELL; ARTICLE; CDX2 GENE; CELL ELONGATION; CONTROLLED STUDY; ECTODERM; ELF5 GENE; EMBRYO; ENZYME PHOSPHORYLATION; GASTRULATION; GENE; GENE EXPRESSION; IN SITU HYBRIDIZATION; MESODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TROPHOBLAST; BINDING AFFINITY; EMBRYO DEVELOPMENT; FEMALE; MOUSE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SWINE; TRANSCRIPTION FACTOR CDX2 GENE; TRANSCRIPTION REGULATION;

RODENTIA; SUIDAE;

BMP4; EMBRYO; FGF4; GENE REGULATORY NETWORK; PIG; TROPHOBLAST ELONGATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL MEMBRANE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 4; GASTRULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM LAYERS; HOMEODOMAIN PROTEINS; MESODERM; MICE; PARACRINE COMMUNICATION; PHOSPHORYLATION; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SWINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TROPHOBLASTS;

EID: 84893725267     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.01.008     Document Type: Article

References (75)

1. Alberio R., Croxall N., Allegrucci C. Pig epiblast stem cells depend on activin/nodal signaling for pluripotency and self-renewal. Stem Cells Dev. 2010, 19:1627-1636.
2. Amita M., Adachi K., Alexenko A.P., Sinha S., Schust D.J., Schulz L.C., Roberts R.M., Ezashi T. Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E1212-E1221.
3. Anderson L.L. Growth, protein content and distribution of early pig embryos. Anat. Rec. 1978, 190:143-153.
4. Arnold S.J., Robertson E.J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 2009, 10:91-103.
5. Barends P.M., Stroband H.W., Taverne N., te Kronnie G., Leen M.P., Blommers P.C. 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. J. Reprod. Fertil. 1989, 87:715-726.
6. Bazer F.W. Contributions of an animal scientist to reproductive biology. Biol. Reprod. 2011, 85:228-242.
7. Bazer F.W., Spencer T.E., Johnson G.A., Burghardt R.C., Wu G. Comparative aspects of implantation. Reproduction 2009, 138:195-209.
8. Beck F., Erler T., Russell A., James R. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev. Dyn. 1995, 204:219-227.
9. Berg D.K., Smith C.S., Pearton D.J., Wells D.N., Broadhurst R., Donnison M., Pfeffer P.L. Trophectoderm lineage determination in cattle. Dev. Cell 2011, 20:244-255.
10. Bernardo A.S., Faial T., Gardner L., Niakan K.K., Ortmann D., Senner C.E., Callery E.M., Trotter M.W., Hemberger M., Smith J.C., Bardwell L., Moffett A., Pedersen R.A. BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 2011, 9:144-155.
11. Blomberg L.A., Schreier L.L., Guthrie H.D., Sample G.L., Vallet J., Caperna T., Ramsay T. The effect of intrauterine growth retardation on the expression of developmental factors in porcine placenta subsequent to the initiation of placentation. Placenta 2010, 31:549-552.
12. Blomberg L.A., Schreier L.L., Talbot N.C. Expression analysis of pluripotency factors in the undifferentiated porcine inner cell mass and epiblast during in vitro culture. Mol. Reprod. Dev. 2008, 75:450-463.
13. Blomberg le A., Garrett W.M., Guillomot M., Miles J.R., Sonstegard T.S., Van Tassell C.P., Zuelke K.A. Transcriptome profiling of the tubular porcine conceptus identifies the differential regulation of growth and developmentally associated genes. Mol. Reprod. Dev. 2006, 73:1491-1502.
14. Chai N., Patel Y., Jacobson K., McMahon J., McMahon A., Rappolee D.A. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev. Biol. 1998, 198:105-115.
15. Chawengsaksophak K., de Graaff W., Rossant J., Deschamps J., Beck F. Cdx2 is essential for axial elongation in mouse development. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7641-7645.
16. Chen A.E., Egli D., Niakan K., Deng J., Akutsu H., Yamaki M., Cowan C., Fitz-Gerald C., Zhang K., Melton D.A., Eggan K. Optimal timing of inner cell mass isolation increases the efficiency of human embryonic stem cell derivation and allows generation of sibling cell lines. Cell Stem Cell 2009, 4:103-106.
17. Christen B., Slack J.M. Spatial response to fibroblast growth factor signalling in Xenopus embryos. Development 1999, 126:119-125.
18. Conley A.J., Christenson L.K., Ford S.P., Christenson R.K. Immunocytochemical localization of cytochromes P450 17 alpha-hydroxylase and aromatase in embryonic cell layers of elongating porcine blastocysts. Endocrinology 1994, 135:2248-2254.
19. Corson L.B., Yamanaka Y., Lai K.M., Rossant J. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 2003, 130:4527-4537.
20. Coucouvanis E., Martin G.R. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 1995, 83:279-287.
21. Coucouvanis E., Martin G.R. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 1999, 126:535-546.
22. Dailey L., Ambrosetti D., Mansukhani A., Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 2005, 16:233-247.
23. Dantzer V. Electron microscopy of the initial stages of placentation in the pig. Anat. Embryol. (Berl) 1985, 172:281-293.
24. Degrelle S.A., Campion E., Cabau C., Piumi F., Reinaud P., Richard C., Renard J.P., Hue I. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev. Biol. 2005, 288:448-460.
25. Donnison M., Beaton A., Davey H.W., Broadhurst R., L'Huillier P., Pfeffer P.L. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 2005, 132:2299-2308.
26. Feldman B., Poueymirou W., Papaioannou V.E., DeChiara T.M., Goldfarb M. Requirement of FGF-4 for postimplantation mouse development. Science 1995, 267:246-249.
27. Fujii T., Sakurai N., Osaki T., Iwagami G., Hirayama H., Minamihashi A., Hashizume T., Sawai K. Changes in the expression patterns of the genes involved in the segregation and function of inner cell mass and trophectoderm lineages during porcine preimplantation development. J. Reprod. Dev. 2013, 59:151-158.
28. Geisert R.D., Brookbank J.W., Roberts R.M., Bazer F.W. Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biol. Reprod. 1982, 27:941-955.
29. Guillomot M. Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 1995, 49:39-51.
30. Guillomot M., Turbe A., Hue I., Renard J.P. Staging of ovine embryos and expression of the T-box genes Brachyury and Eomesodermin around gastrulation. Reproduction 2004, 127:491-501.
31. Guzman-Ayala M., Ben-Haim N., Beck S., Constam D.B. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15656-15660.
32. Hall V.J., Christensen J., Gao Y., Schmidt M.H., Hyttel P. Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev. Dyn. 2009, 238:2014-2024.
33. Hall V.J., Jacobsen J.V., Rasmussen M.A., Hyttel P. Ultrastructural and molecular distinctions between the porcine inner cell mass and epiblast reveal unique pluripotent cell states. Dev. Dyn. 2010, 239:2911-2920.
34. Heap R.B., Flint A.P., Gadsby J.E. Role of embryonic signals in the establishment of pregnancy. Br. Med. Bull. 1979, 35:129-135.
35. Hirai H., Karian P., Kikyo N. Regulation of embryonic stem cell self-renewal and pluripotency by leukaemia inhibitory factor. Biochem. J. 2011, 438:11-23.
36. Hopf C., Viebahn C., Puschel B. BMP signals and the transcriptional repressor BLIMP1 during germline segregation in the mammalian embryo. Dev. Genes Evol. 2011, 221:209-223.
37. Hue I., Degrelle S.A., Campion E., Renard J.P. Gene expression in elongating and gastrulating embryos from ruminants. Soc. Reprod. Fertil. Suppl. 2007, 64:365-377.
38. Hue I., Renard J.P., Viebahn C. Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Dev. Genes Evol. 2001, 211:157-159.
39. Ka H., Al-Ramadan S., Erikson D.W., Johnson G.A., Burghardt R.C., Spencer T.E., Jaeger L.A., Bazer F.W. Regulation of expression of fibroblast growth factor 7 in the pig uterus by progesterone and estradiol. Biol. Reprod. 2007, 77:172-180.
40. Ka H., Jaeger L.A., Johnson G.A., Spencer T.E., Bazer F.W. Keratinocyte growth factor is up-regulated by estrogen in the porcine uterine endometrium and functions in trophectoderm cell proliferation and differentiation. Endocrinology 2001, 142:2303-2310.
41. Kuijk E.W., Du Puy L., Van Tol H.T., Oei C.H., Haagsman H.P., Colenbrander B., Roelen B.A. Differences in early lineage segregation between mammals. Dev. Dyn. 2008, 237:918-927.
42. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999, 13:424-436.
43. Li Y., Moretto-Zita M., Soncin F., Wakeland A., Wolfe L., Leon-Garcia S., Pandian R., Pizzo D., Cui L., Nazor K., Loring J.F., Crum C.P., Laurent L.C., Parast M.M. BMP4-directed trophoblast differentiation of human embryonic stem cells is mediated through a DeltaNp63+ cytotrophoblast stem cell state. Development 2013, 140:3965-3976.
44. Lu C.W., Yabuuchi A., Chen L., Viswanathan S., Kim K., Daley G.Q. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat. Genet. 2008, 40:921-926.
45. Mattson B.A., Overstrom E.W., Albertini D.F. Transitions in trophectoderm cellular shape and cytoskeletal organization in the elongating pig blastocyst. Biol. Reprod. 1990, 42:195-205.
46. Murohashi M., Nakamura T., Tanaka S., Ichise T., Yoshida N., Yamamoto T., Shibuya M., Schlessinger J., Gotoh N. An FGF4-FRS2alpha-Cdx2 axis in trophoblast stem cells induces Bmp4 to regulate proper growth of early mouse embryos. Stem Cells 2010, 28:113-121.
47. Ng R.K., Dean W., Dawson C., Lucifero D., Madeja Z., Reik W., Hemberger M. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat. Cell Biol. 2008, 10:1280-1290.
48. Nowak M., Machate A., Yu S.R., Gupta M., Brand M. Interpretation of the FGF8 morphogen gradient is regulated by endocytic trafficking. Nat. Cell Biol. 2011, 13:153-158.
49. Ornitz D.M. FGFs, heparan sulfate and FGFRs: complex interactions essential for development. Bioessays 2000, 22:108-112.
50. Ostrup E., Bauersachs S., Blum H., Wolf E., Hyttel P. Differential endometrial gene expression in pregnant and nonpregnant sows. Biol. Reprod. 2010, 83:277-285.
51. Ostrup E., Hyttel P., Ostrup O. Embryo-maternal communication: signalling before and during placentation in cattle and pig. Reprod. Fertil. Dev. 2011, 23:964-975.
52. Pearton D.J., Broadhurst R., Donnison M., Pfeffer P.L. Elf5 regulation in the trophectoderm. Dev. Biol. 2011, 360:343-350.
53. Perry J.S., Heap R.B., Burton R.D., Gadsby J.E. Endocrinology of the blastocyst and its role in the establishment of pregnancy. J. Reprod. Fertil. Suppl. 1976, 85-104.
54. Pfeffer P.L., Pearton D.J. Trophoblast development. Reproduction 2012, 143:231-246.
55. Ralston A., Cox B.J., Nishioka N., Sasaki H., Chea E., Rugg-Gunn P., Guo G., Robson P., Draper J.S., Rossant J. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 2010, 137:395-403.
56. Roberts R.M., Chen Y., Ezashi T., Walker A.M. Interferons and the maternal-conceptus dialog in mammals. Semin. Cell Dev. Biol. 2008, 19:170-177.
57. Roberts R.M., Fisher S.J. Trophoblast stem cells. Biol. Reprod. 2011, 84:412-421.
58. Rodriguez A., Allegrucci C., Alberio R. Modulation of pluripotency in the porcine embryo and iPS cells. PLoS One 2012, 7:e49079.
59. Ross J.W., Ashworth M.D., Stein D.R., Couture O.P., Tuggle C.K., Geisert R.D. Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium. Physiol. Genomics 2009, 36:140-148.
60. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
61. Shimokawa K., Kimura-Yoshida C., Nagai N., Mukai K., Matsubara K., Watanabe H., Matsuda Y., Mochida K., Matsuo I. Cell surface heparan sulfate chains regulate local reception of FGF signaling in the mouse embryo. Dev. Cell 2011, 21:257-272.
62. Smith C.S., Berg D.K., Berg M., Pfeffer P.L. Nuclear transfer-specific defects are not apparent during the second week of embryogenesis in cattle. Cell. Reprogram. 2010, 12:699-707.
63. Spencer T.E., Bazer F.W. Uterine and placental factors regulating conceptus growth in domestic animals. J. Anim. Sci. 2004, 82:E4-13. (E-Suppl).
64. Sritanaudomchai H., Sparman M., Tachibana M., Clepper L., Woodward J., Gokhale S., Wolf D., Hennebold J., Hurlbut W., Grompe M., Mitalipov S. CDX2 in the formation of the trophectoderm lineage in primate embryos. Dev. Biol. 2009, 335:179-187.
65. Stroband H.W., Van der Lende T. Embryonic and uterine development during early pregnancy in pigs. J. Reprod. Fertil. Suppl. 1990, 40:261-277.
66. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
67. Sudheer S., Bhushan R., Fauler B., Lehrach H., Adjaye J. FGF inhibition directs BMP4-mediated differentiation of human embryonic stem cells to syncytiotrophoblast. Stem Cells Dev. 2012, 21:2987-3000.
68. Tam P.P., Loebel D.A. Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 2007, 8:368-381.
69. Tanaka S., Kunath T., Hadjantonakis A.K., Nagy A., Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282:2072-2075.
70. Vejlsted M., Du Y., Vajta G., Maddox-Hyttel P. Post-hatching development of the porcine and bovine embryo-defining criteria for expected development in vivo and in vitro. Theriogenology 2006, 65:153-165.
71. Vejlsted M., Offenberg H., Thorup F., Maddox-Hyttel P. Confinement and clearance of OCT4 in the porcine embryo at stereomicroscopically defined stages around gastrulation. Mol. Reprod. Dev. 2006, 73:709-718.
72. White F.J., Kimball E.M., Wyman G., Stein D.R., Ross J.W., Ashworth M.D., Geisert R.D. Estrogen and interleukin-1beta regulation of trophinin, osteopontin, cyclooxygenase-1, cyclooxygenase-2, and interleukin-1beta system in the porcine uterus. Soc. Reprod. Fertil. Suppl. 2009, 66:203-204.
73. Winnier G., Blessing M., Labosky P.A., Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995, 9:2105-2116.
74. Wolf E., Arnold G.J., Bauersachs S., Beier H.M., Blum H., Einspanier R., Frohlich T., Herrler A., Hiendleder S., Kolle S., Prelle K., Reichenbach H.D., Stojkovic M., Wenigerkind H., Sinowatz F. Embryo-maternal communication in bovine - strategies for deciphering a complex cross-talk. Reprod. Domest. Anim. 2003, 38:276-289.
75. Young T., Rowland J.E., van de Ven C., Bialecka M., Novoa A., Carapuco M., van Nes J., de Graaff W., Duluc I., Freund J.-N., Beck F., Mallo M., Deschamps J. Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev. Cell 2009, 17:516-526.