Activin/Nodal signalling before implantation: Setting the stage for embryo patterning

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1657, 2014, Pages

  Papanayotou, Costis ^a   Collignon, Jérôme ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Activin; Blastocyst; Epiblast maturation; Nodal; Pluripotency; Smads

Indexed keywords

EMBRYO; GENE EXPRESSION; GERM CELL; GROWTH RATE; PHENOTYPE; SIGNALING;

ACTIVIN; NODAL PROTEIN, MOUSE; PROTEIN NODAL; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN; SMAD3 PROTEIN, MOUSE;

ANIMAL; BIOLOGICAL MODEL; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACTIVINS; ANIMALS; BODY PATTERNING; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MODELS, BIOLOGICAL; NODAL PROTEIN; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN;

EID: 84908248237     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0539     Document Type: Review

References (94)

1. Robertson EJ. 2014 Dose-dependent Nodal/Smad signals pattern the early mouse embryo. Semin. Cell Dev. Biol. 32, 1717-1728. (doi:10.1016/j.semcdb. 2014.03.028)
2. Rossant J, Tam PP. 2009 Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713. (doi:10.1242/dev. 017178)
3. Schier AF. 2009 Nodal morphogens. Cold Spring Harb. Perspect. Biol. 1, a003459. (doi:10.1101/ cshperspect.a003459)
4. Shen MM. 2007 Nodal signaling: developmental roles and regulation. Development 134, 1023-1034. (doi:10.1242/dev.000166)
5. Takaoka K, Yamamoto M, Hamada H. 2011 Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat. Cell Biol. 13, 743-752. (doi:10.1038/ncb2251)
6. Constam DB. 2014 Regulation of TGF-β and related signals by precursor processing. Semin. Cell Dev. Biol. 32, 85-97. (doi:10.1016/j.semcdb. 2014.01.008)
7. Massague J, Seoane J, Wotton D. 2005 Smad transcription factors. Genes Dev. 19, 2783-2810. (doi:10.1101/gad.1350705)
8. Mullen AC et al. 2011 Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell 147, 565-576. (doi:10.1016/j.cell. 2011.08.050)
9. Oshimori N, Fuchs E. 2012 The harmonies played by TGF-β in stem cell biology. Cell Stem Cell 11, 751-764. (doi:10.1016/j.stem.2012.11.001)
10. Gaarenstroom T, Hill CS. 2014 TGF-β signaling to chromatin: how Smads regulate transcription during self-renewal and differentiation. Semin. Cell Dev. Biol. 32, 107-118. (doi:10.1016/j.semcdb.2014.01.009)
11. Massague J. 2012 TGF-β signaling in development and disease. FEBS Lett. 586, 1833. (doi:10.1016/j. febslet.2012.05.030)
12. Wu MY, Hill CS. 2009 Tgf-β superfamily signaling in embryonic development and homeostasis. Dev. Cell 16, 329-343. (doi:10.1016/j.devcel.2009. 02.012)
13. Schier AF. 2003 Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 19, 589-621. (doi:10.1146/annurev.cellbio.19.041603.094522)
14. Cheng SK, Olale F, Brivanlou AH, Schier AF. 2004 Lefty blocks a subset of TGF-β signals by antagonizing EGF-CFC coreceptors. PLoS Biol. 2, E30. (doi:10.1371/journal.pbio.0020030)
15. Adkins HB et al. 2003 Antibody blockade of the Cripto CFC domain suppresses tumor cell growth in vivo. J. Clin. Invest. 112, 575-587. (doi:10.1172/ JCI17788)
16. Gray PC, Harrison CA, Vale W. 2003 Cripto forms a complex with activin and type II activin receptors and can block activin signaling. Proc. Natl Acad. Sci. USA 100, 5193-5198. (doi:10.1073/pnas.0531290100)
17. Gray PC, Shani G, Aung K, Kelber J, Vale W. 2006 Cripto binds transforming growth factor beta (TGFβ) and inhibits TGF-β signaling. Mol. Cell. Biol. 26, 9268-9278. (doi:10.1128/MCB.01168-06)
18. Guardiola O et al. 2012 Cripto regulates skeletal muscle regeneration and modulates satellite cell determination by antagonizing myostatin. Proc. Natl Acad. Sci. USA 109, E3231-E3240. (doi:10.1073/ pnas.1204017109)
19. Furtado MB et al. 2008 BMP/SMAD1 signaling sets a threshold for the left/right pathway in lateral plate mesoderm and limits availability of SMAD4. Genes Dev. 22, 3037-3049. (doi:10.1101/gad. 1682108)
20. Yamamoto M, Beppu H, Takaoka K, Meno C, Li E, Miyazono K, Hamada H. 2009 Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J. Cell Biol. 184, 323-334. (doi:10.1083/ jcb.200808044)
21. Massague J. 2003 Integration of Smad and MAPK pathways: a link and a linker revisited. Genes Dev. 17, 2993-2997. (doi:10.1101/gad.1167003)
22. Andersson O, Bertolino P, Ibanez CF. 2007 Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev. Biol. 311, 500-511. (doi:10. 1016/j.ydbio.2007.08.060)
23. Granier C et al. 2011 Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. Dev. Biol. 349, 350-362. (doi:10.1016/j. ydbio.2010.10.036)
24. Levine AJ, Brivanlou AH. 2006 GDF3, a BMP inhibitor, regulates cell fate in stem cells and early embryos. Development 133, 209-216. (doi:10. 1242/dev.02192)
25. Tanaka C, Sakuma R, Nakamura T, Hamada H, Saijoh Y. 2007 Long-range action of Nodal requires interaction with GDF1. Genes Dev. 21, 3272-3282. (doi:10.1101/gad.1623907)
26. Fuerer C, Nostro MC, Constam DB. 2014 Nodal-Gdf1 hetrodimers with bound prodomains enable serum-independent Nodal signaling and endoderm differentiation. J. Biol. Chem. 289, 17854-17871. (doi:10.1074/jbc.M114.550301)
27. ten Dijke P, Hill CS. 2004 New insights into TGF-β-Smad signalling. Trends Biochem. Sci. 29, 265-273. (doi:10.1016/j.tibs.2004.03.008)
28. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massague J. 2007 Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol. Cell 25, 441-454. (doi:10.1016/j.molcel.2007.01.006)
29. Feng XH, Derynck R. 2005 Specificity and versatility in TGF-β signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693. (doi:10.1146/annurev. cellbio.21.022404.142018)
30. Conlon FL et al. 1994 A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928.
31. Iannaccone PM, Zhou X, Khokha M, Boucher D, Kuehn MR. 1992 Insertional mutation of a gene involved in growth regulation of the early mouse embryo. Dev. Dyn. 194, 198-208. (doi:10.1002/aja.1001940305)
32. Camus A, Perea-Gomez A, Moreau A, Collignon J. 2006 Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev. Biol. 295, 743-755. (doi:10.1016/j. ydbio.2006.03.047)
33. Mesnard D, Guzman-Ayala M, Constam DB. 2006 Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133, 2497-2505.
34. Brennan J, Lu CC, Norris DP, Rodriguez TA, Beddington RS, Robertson EJ. 2001 Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411, 965-969. (doi:10.1038/ 35082103)
35. Lowe LA, Yamada S, Kuehn MR. 2001 Genetic dissection of nodal function in patterning the mouse embryo. Development 128, 1831-1843.
36. Matzuk MM, Kumar TR, Bradley A. 1995 Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374, 356-360. (doi:10.1038/374356a0)
37. Vassalli A, Matzuk MM, Gardner HA, Lee KF, Jaenisch R. 1994 Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 8, 414-427. (doi:10.1101/gad.8.4.414)
38. Gu Z et al. 1998 The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12, 844-857. (doi:10.1101/gad.12.6.844)
39. Jörnvall H, Reissmann E, Andersson O, Mehrkash M, Ibáñez CF. 2004 ALK7, a receptor for nodal, is dispensable for embryogenesis and left-right patterning in the mouse. Mol. Cell. Biol. 24, 9383-9389. (doi:10.1128/MCB.24.21.9383-9389.2004)
40. Song J, Oh SP, Schrewe H, Nomura M, Lei H, Okano M, Gridley T, Li E. 1999 The type II activin receptors are essential for egg cylinder growth, gastrulation, and rostral head development in mice. Dev. Biol. 213, 157-169. (doi:10.1006/dbio.1999.9370)
41. Oh SP, Li E. 1997 The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 11, 1812-1826. (doi:10.1101/gad.11. 14.1812)
42. Ding J, Yang L, Yan YT, Chen A, Desai N, Wynshaw-Boris A. 1998 Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395, 702-707. (doi:10. 1038/27215)
43. Xu C, Liguori G, Persico MG, Adamson ED. 1999 Abrogation of the Cripto gene in mouse leads to failure of postgastrulation morphogenesis and lack of differentiation of cardiomyocytes. Development 126, 483-494.
44. Gaio U et al. 1999 A role of the cryptic gene in the correct establishment of the left-right axis. Curr. Biol. 9, 1339-1342. (doi:10.1016/S0960-9822(00)80059-7)
45. Yan YT et al. 1999 Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation. Genes Dev. 13, 2527-2537. (doi:10.1101/gad.13. 19.2527)
46. Chu J, Shen MM. 2010 Functional redundancy of EGF-CFC genes in epiblast and extraembryonic patterning during early mouse embryogenesis. Dev. Biol. 342, 63-73. (doi:10.1016/j.ydbio.2010. 03.009)
47. Rankin CT, Bunton T, Lawler AM, Lee SJ. 2000 Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat. Genet. 24, 262-265. (doi:10.1038/73472)
48. Andersson O, Reissmann E, Jörnvall H, Ibáñez CF. 2006 Synergistic interaction between Gdf1 and Nodal during anterior axis development. Dev. Biol. 293, 370-381. (doi:10.1016/j.ydbio.2006.02.002)
49. Chen C et al. 2006 The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pregastrulation mouse embryo. Development 133, 319-329. (doi:10.1242/dev.02210)
50. Hoodless PA, Pye M, Chazaud C, Labbé E, Attisano L, Rossant J, Wrana JL. 2001 FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev. 15, 1257-1271. (doi:10.1101/ gad.881501)
51. Waldrip WR, Bikoff EK, Hoodless PA, Wrana JL, Robertson EJ. 1998 Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92, 797-808. (doi:10.1016/S0092-8674(00)81407-5)
52. Heyer J, Escalante-Alcalde D, Lia M, Boettinger E, Edelmann W, Stewart CL, Kucherlapati R. 1999 Postgastrulation Smad2-deficient embryos show defects in embryo turning and anterior morphogenesis. Proc. Natl Acad. Sci. USA 96, 12595-12600. (doi:10.1073/pnas.96.22.12595)
53. Zhu Y, Richardson JA, Parada LF, Graff JM. 1998 Smad3 mutant mice develop metastatic colorectal cancer. Cell 94, 703-714. (doi:10.1016/S0092-8674(00)81730-4)
54. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, Wang XF. 1999 Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol. Cell. Biol. 19, 2495-2504.
55. Yang X et al. 1999 Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J. 18, 1280-1291. (doi:10.1093/emboj/18.5.1280)
56. Dunn NR, Vincent SD, Oxburgh L, Robertson EJ, Bikoff EK. 2004 Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo. Development 131, 1717-1728. (doi:10.1242/dev.01072)
57. Sirard C et al. 1998 The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 12, 107-119. (doi:10.1101/gad.12.1.107)
58. Birsoy B, Kofron M, Schaible K, Wylie C, Heasman J. 2006 Vg 1 is an essential signaling molecule in Xenopus development. Development 133, 15-20. (doi:10.1242/dev.02144)
59. Dohrmann CE, Kessler DS, Melton DA. 1996 Induction of axial mesoderm by zDVR-1, the zebrafish orthologue of Xenopus Vg1. Dev. Biol. 175, 108-117. (doi:10.1006/dbio.1996.0099)
60. Hagos EG, Fan X, Dougan ST. 2007 The role of maternal Activin-like signals in zebrafish embryos. Dev. Biol. 309, 245-258. (doi:10.1016/j.ydbio. 2007.07.010)
61. Range R, Lapraz F, Quirin M, Marro S, Besnardeau L, Lepage T. 2007 Cis-regulatory analysis of nodal and maternal control of dorsal-ventral axis formation by Univin, a TGF-β related to Vg1. Development 134, 3649-3664. (doi:10.1242/dev.007799)
62. Skromne I, Stern CD. 2001 Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128, 2915-2927.
63. Albano RM, Groome N, Smith JC. 1993 Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development 117, 711-723.
64. Albano RM, Smith JC. 1994 Follistatin expression in ES and F9 cells and in preimplantation mouse embryos. Int. J. Dev. Biol. 38, 543-547.
65. Jones RL, Findlay JK, Farnworth PG, Robertson DM, Wallace E, Salamonsen LA. 2006 Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinology 147, 724-732. (doi:10.1210/en. 2005-1183)
66. Johnson MH, Ziomek CA. 1983 Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16 to the 32 cell stage. Dev. Biol. 95, 211-218.
67. James D, Levine AJ, Besser D, Hemmati-Brivanlou A. 2005 TGF-β/Activin/Nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132, 1273-1282. (doi:10.1242/dev.01706)
68. Lu RZ, Matsuyama S, Nishihara M, Takahashi M. 1993 Developmental expression of activin/inhibin beta A, beta B, and alpha subunits, and activin receptor-IIB genes in preimplantation mouse embryos. Biol. Reprod. 49, 1163-1169. (doi:10. 1095/biolreprod49.6.1163)
69. Orimo T, Taga M, Matsui H, Minaguchi H. 1996 The effect of activin-A on the development of mouse preimplantation embryos in vitro. J. Assist. Reprod. Genet. 13, 669-674. (doi:10.1007/BF02069647)
70. Yoshioka K, Suzuki C, Iwamura S. 1998 Activin A and follistatin regulate developmental competence of in vitro-produced bovine embryos. Biol. Reprod. 59, 1017-1022. (doi:10.1095/biolreprod59.5.1017)
71. Takaoka K, Yamamoto M, Shiratori H, Meno C, Rossant J, Saijoh Y, Hamada H. 2006 The mouse embryo autonomously acquires anterior-posterior polarity at implantation. Dev. Cell 10, 451-459. (doi:10.1016/j.devcel.2006.02.017)
72. Park CB, Dufort D. 2011 Nodal expression in the uterus of the mouse is regulated by the embryo and correlates with implantation. Biol. Reprod. 84, 1103-1110. (doi:10.1095/biolreprod.110.087239)
73. Chazaud C, Rossant J. 2006 Disruption of early proximodistal patterning and AVE formation in Apc mutants. Development 133, 3379-3387. (doi:10. 1242/dev.02523)
74. Coucouvanis E, Martin GR. 1999 BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126, 535-546.
75. Lu CC, Robertson EJ. 2004 Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev. Biol. 273, 149-159. (doi:10.1016/j.ydbio. 2004.06.004)
76. Torres-Padilla ME, Richardson L, Kolasinska P, Meilhac SM, Luetke-Eversloh MV, Zernicka-Goetz M. 2007 The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation. Dev. Biol. 309, 97-112. (doi:10. 1016/j.ydbio.2007.06.020)
77. Morris SA, Grewal S, Barrios F, Patankar SN, Strauss B, Buttery L, Alexander M, Shakesheff KM, Zernicka-Goetz M. 2012 Dynamics of anterior-posterior axis formation in the developing mouse embryo. Nat. Commun. 3, 673. (doi:10.1038/ncomms1671)
78. Gardner RL. 1968 Mouse chimeras obtained by the injection of cells into the blastocyst. Nature 220, 596-597. (doi:10.1038/220596a0)
79. Gardner RL. 1998 Contributions of blastocyst micromanipulation to the study of mammalian development. Bioessays 20, 168-180. (doi:10. 1002/(SICI)1521-1878(199802)20:2<168::AIDBIES9>3.0. CO;2-P)
80. Rossant J. 2008 Stem cells and early lineage development. Cell 132, 527-531. (doi:10.1016/j. cell.2008.01.039)
81. Nichols J, Smith A. 2009 Naive and primed pluripotent states. Cell Stem Cell 4, 487-492. (doi:10.1016/j.stem.2009.05.015)
82. Tesar PJ et al. 2007 New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199. (doi:10.1038/nature05972)
83. Conlon FL, Barth KS, Robertson EJ. 1991 A novel retrovirally induced embryonic lethal mutation in the mouse: assessment of the developmental fate of embryonic stem cells homozygous for the 413.d proviral integration. Development 111, 969-981.
84. Brons IG et al. 2007 Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195. (doi:10.1038/nature05950)
85. Vallier L et al. 2009 Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136, 1339-1349. (doi:10. 1242/dev.033951)
86. Guo G, Yang J, Nichols J, Hall JS, Eyres I, Mansfield W, Smith A. 2009 Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069. (doi:10.1242/dev.030957)
87. Buecker C et al. 2014 Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell 14, 838-853. (doi:10. 1016/j.stem.2014.04.003)
88. Factor DC et al. 2014 Epigenomic comparison reveals activation of 'seed' enhancers during transition from naive to primed pluripotency. Cell Stem Cell 14, 854-863. (doi:10.1016/j.stem.2014.05.005)
89. Karwacki-Neisius V et al. 2013 Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog. Cell Stem Cell 12, 531-545. (doi:10.1016/j.stem.2013.04.023)
90. Radzisheuskaya A et al. 2013 A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages. Nat. Cell Biol. 15, 579-590. (doi:10.1038/ ncb2742)
91. Xi Q et al. 2011 A poised chromatin platform for TGF-β access to master regulators. Cell 147, 1511-1524. (doi:10.1016/j.cell.2011.11.032)
92. Papanayotou C et al. 2014 A novel Nodal enhancer dependent on pluripotency factors and Smad2/3 signaling conditions a regulatory switch during epiblast maturation. PLoS Biol. 12, e1001890. (doi:10.1371/journal.pbio.1001890)
93. Dahle O, Kumar A, Kuehn MR. 2010 Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci Signal. 3, ra48. (doi:10.1126/scisignal.2000841)
94. Norris DP, Brennan J, Bikoff EK, Robertson EJ. 2002 The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129, 3455-3468.