Nodal signaling from the visceral endoderm is required to maintain Nodal gene expression in the epiblast and drive DVE/AVE migration

Developmental Biology

Volumn 400, Issue 1, 2015, Pages 1-9

  Kumar, Amit ^a,e   Lualdi, Margaret ^b   Lyozin, George T ^c   Sharma, Prashant ^a   Loncarek, Jadranka ^a   Fu, Xin Yuan ^d   Kuehn, Michael R ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

DVE AVE; Epiblast; Nodal signaling; Ttr Cre; Visceral endoderm

Indexed keywords

MESSENGER RNA; PROTEIN NODAL; 5-BROMO-4-CHLORO-3-INDOLYL BETA-GALACTOSIDE; GALACTOSIDE; INDOLE DERIVATIVE; NODAL PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; ENDODERM; FEMALE; GENE EXPRESSION; GENE LOSS; MALE; MOUSE; MUTAGENESIS; NODAL GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENE; VISCERAL ENDODERM; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; GERM LAYER; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; REPORTER GENE;

ANIMALS; BODY PATTERNING; CELL MOVEMENT; ENDODERM; GALACTOSIDES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GERM LAYERS; IN SITU HYBRIDIZATION; INDOLES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MUTAGENESIS; NODAL PROTEIN; SIGNAL TRANSDUCTION;

EID: 84924858912     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.12.016     Document Type: Article

References (44)

1. Adachi H., Saijoh Y., Mochida K., Ohishi S., Hashiguchi H., Hirao A., Hamada H. Determination of left/right asymmetric expression of nodal by a left side-specific enhancer with sequence similarity to a lefty-2 enhancer. Genes Dev. 1999, 13:1589-1600.
2. Beck S., Le Good J.A., Guzman M., Ben Haim N., Roy K., Beermann F., Constam D.B. Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat. Cell Biol. 2002, 4:981-985.
3. Bedzhov I., Zernicka-Goetz M. Self-organizing properties of mouse pluripotent cells initiate morphogenesis upon implantation. Cell 2014, 156:1032-1044.
4. Ben-Haim N., Lu C., Guzman-Ayala M., Pescatore L., Mesnard D., Bischofberger M., Naef F., Robertson E.J., Constam D.B. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell 2006, 11:313-323.
5. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 2001, 411:965-969.
6. Granier C., Gurchenkov V., Perea-Gomez A., Camus A., Ott S., Papanayotou C., Iranzo J., Moreau A., Reid J., Koentges G., Saberan-Djoneidi D., Collignon J. Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. Dev. Biol. 2011, 349:350-362.
7. 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. USA 2004, 101:15656-15660.
8. Hayashi S., Lewis P., Pevny L., McMahon A.P. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 2002, 119(Suppl. 1):S97-S101.
9. Hiramatsu R., Matsuoka T., Kimura-Yoshida C., Han S.W., Mochida K., Adachi T., Takayama S., Matsuo I. External mechanical cues trigger the establishment of the anterior-posterior axis in early mouse embryos. Dev. Cell 2013, 27:131-144.
10. Kimura-Yoshida C., Nakano H., Okamura D., Nakao K., Yonemura S., Belo J.A., Aizawa S., Matsui Y., Matsuo I. Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev. Cell 2005, 9:639-650.
11. Kumar A., Lualdi M., Lewandoski M., Kuehn M.R. Broad mesodermal and endodermal deletion of Nodal at postgastrulation stages results solely in left/right axial defects. Dev. Dyn. 2008, 237:3591-3601.
12. Kumar A., Lualdi M., Loncarek J., Cho Y.W., Lee J.E., Ge K., Kuehn M.R. Loss of function of mouse Pax-Interacting Protein 1-associated glutamate rich protein 1a (Pagr1a) leads to reduced Bmp2 expression and defects in chorion and amnion development. Dev. Dyn. 2014, 243:937-947.
13. Kumar A., Yamaguchi T., Sharma P., Kuehn M.R. Transgenic mouse lines expressing Cre recombinase specifically in posterior notochord and notochord. Genesis 2007, 45:729-736.
14. Kwon G.S., Hadjantonakis A.K. Transthyretin mouse transgenes direct RFP expression or Cre-mediated recombination throughout the visceral endoderm. Genesis 2009, 47:447-455.
15. Li C., Li Y.P., Fu X.Y., Deng C.X. Anterior visceral endoderm SMAD4 signaling specifies anterior embryonic patterning and head induction in mice. Int. J. Biol. Sci. 2010, 6:569-583.
16. Lowe L.A., Yamada S., Kuehn M.R. Genetic dissection of nodal function in patterning the mouse embryo. Development 2001, 128:1831-1843.
17. Lu C.C., Robertson E.J. Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev. Biol. 2004, 273:149-159.
18. Lyozin G.T., Bressloff P.C., Kumar A., Kosaka Y., Demarest B.L., Yost H.J., Kuehn M.R., Brunelli L. Isolation of rare recombinants without using selectable markers for one-step seamless BAC mutagenesis. Nat. Methods 2014, 9:966-970.
19. Mesnard D., Guzman-Ayala M., Constam D.B. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 2006, 133:2497-2505.
20. Moh A., Iwamoto Y., Chai G.X., Zhang S.S., Kano A., Yang D.D., Zhang W., Wang J., Jacoby J.J., Gao B., Flavell R.A., Fu X.Y. Role of STAT3 in liver regeneration: survival, DNA synthesis, inflammatory reaction and liver mass recovery. Lab. Investig. 2007, 87:1018-1028.
21. Morris S.A., Grewal S., Barrios F., Patankar S.N., Strauss B., Buttery L., Alexander M., Shakesheff K.M., Zernicka-Goetz M. Dynamics of anterior-posterior axis formation in the developing mouse embryo. Nat. Commun. 2012, 3:673.
22. Norris D.P., Brennan J., Bikoff E.K., Robertson E.J. The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 2002, 129:3455-3468.
23. Norris D.P., Robertson E.J. Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements. Genes Dev. 1999, 13:1575-1588.
24. Papanayotou C., Benhaddou A., Camus A., Perea-Gomez A., Jouneau A., Mezger V., Langa F., Ott S., Saberan-Djoneidi D., Collignon J. A novel nodal enhancer dependent on pluripotency factors and smad2/3 signaling conditions a regulatory switch during epiblast maturation. PLoS Biol. 2014, 12:e1001890.
25. Perea-Gomez A., Vella F.D., Shawlot W., Oulad-Abdelghani M., Chazaud C., Meno C., Pfister V., Chen L., Robertson E., Hamada H., Behringer R.R., Ang S.L. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 2002, 3:745-756.
26. Rivera-Perez J.A., Mager J., Magnuson T. Dynamic morphogenetic events characterize the mouse visceral endoderm. Dev. Biol. 2003, 261:470-487.
27. Rodriguez T.A., Casey E.S., Harland R.M., Smith J.C., Beddington R.S. Distinct enhancer elements control Hex expression during gastrulation and early organogenesis. Dev. Biol. 2001, 234:304-316.
28. Rodriguez T.A., Srinivas S., Clements M.P., Smith J.C., Beddington R.S. Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development 2005, 132:2513-2520.
29. Saijoh Y., Oki S., Tanaka C., Nakamura T., Adachi H., Yan Y.T., Shen M.M., Hamada H. Two nodal-responsive enhancers control left-right asymmetric expression of Nodal. Dev. Dyn. 2005, 232:1031-1036.
30. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
31. Srinivas S., Rodriguez T., Clements M., Smith J.C., Beddington R.S. Active cell migration drives the unilateral movements of the anterior visceral endoderm. Development 2004, 131:1157-1164.
32. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
33. Stern C.D., Downs K.M. The hypoblast (visceral endoderm): an evo-devo perspective. Development 2012, 139:1059-1069.
34. Stuckey D.W., Clements M., Di-Gregorio A., Senner C.E., Le Tissier P., Srinivas S., Rodriguez T.A. Coordination of cell proliferation and anterior-posterior axis establishment in the mouse embryo. Development 2011, 138:1521-1530.
35. Takaoka K., Hamada H. Cell fate decisions and axis determination in the early mouse embryo. Development 2012, 139:3-14.
36. Takaoka K., Yamamoto M., Hamada H. Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat. Cell Biol. 2011, 13:743-752.
37. Takaoka K., Yamamoto M., Shiratori H., Meno C., Rossant J., Saijoh Y., Hamada H. The mouse embryo autonomously acquires anterior-posterior polarity at implantation. Dev. Cell 2006, 10:451-459.
38. Thomas P., Beddington R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 1996, 6:1487-1496.
39. Varlet I., Collignon J., Robertson E.J. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 1997, 124:1033-1044.
40. Vincent S.D., Dunn N.R., Hayashi S., Norris D.P., Robertson E.J. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev. 2003, 17:1646-1662.
41. Vincent S.D., Norris D.P., Le Good J.A., Constam D.B., Robertson E.J. Asymmetric Nodal expression in the mouse is governed by the combinatorial activities of two distinct regulatory elements. Mech. Dev. 2004, 121:1403-1415.
42. Yamamoto M., Beppu H., Takaoka K., Meno C., Li E., Miyazono K., Hamada H. Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J. Cell Biol. 2009, 184:323-334.
43. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 2004, 428:387-392.
44. Zernicka-Goetz M., Morris S.A., Bruce A.W. Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat. Rev. Genet. 2009, 10:467-477.