Klf5 regulates lineage formation in the pre-implantation mouse embryo

Development

Volumn 137, Issue 23, 2010, Pages 3953-3963

  Lin, Suh Chin J ^a   Wani, Maqsood A ^a   Whitsett, Jeffrey A ^a   Wells, James M ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Embryonic stem cells; Epiblast; Klf5; Lineage specification; Mouse; Pluripotency; Primitive endoderm; Trophectoderm

Indexed keywords

EOMESODERMIN; KRUPPEL LIKE FACTOR 5; MUTANT PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX17;

ARTICLE; BLASTOCYST; CELL ASSAY; CELL CULTURE; CELL CYCLE ARREST; CELL LINEAGE; CELL POLARITY; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; GROWTH CURVE; IMPLANTATION; INNER CELL MASS; MOUSE; MOUSE EMBRYO; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSGENICS;

ANIMALS; BIOLOGICAL MARKERS; BLASTOCYST; CELL COUNT; CELL DEATH; CELL LINEAGE; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; CROSSES, GENETIC; ECTODERM; ENDODERM; FEMALE; FIBROBLAST GROWTH FACTOR 4; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; GERM LAYERS; HMGB PROTEINS; HOMEODOMAIN PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; SOXF TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 78649850946     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.054775     Document Type: Article

References (71)

1. Benahmed, F., Gross, I., Gaunt, S. J., Beck, F., Jehan, F., Domon-Dell, C., Martin, E., Kedinger, M., Freund, J. N. and Duluc, I. (2008). Multiple regulatory regions control the complex expression pattern of the mouse Cdx2 homeobox gene. Gastroenterology 135, 1238-1247.
2. Chai, N., Patel, Y., Jacobson, K., McMahon, J., McMahon, A. and Rappolee, D. A. (1998). FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev. Biol. 198, 105-115.
3. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. and Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655. (Pubitemid 36694189)
4. Chazaud, C., Yamanaka, Y., Pawson, T. and Rossant, J. (2006). Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624.
5. Cheng, A. M., Saxton, T. M., Sakai, R., Kulkarni, S., Mbamalu, G., Vogel, W., Tortorice, C. G., Cardiff, R. D., Cross, J. C., Muller, W. J. et al. (1998). Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 95, 793-803.
6. Cockburn, K. and Rossant, J. (2010). Making the blastocyst: lessons from the mouse. J. Clin. Invest. 120, 995-1003.
7. Conkright, M. D., Wani, M. A., Anderson, K. P. and Lingrel, J. B. (1999). A gene encoding an intestinal-enriched member of the Kruppel-like factor family expressed in intestinal epithelial cells. Nucleic Acids Res. 27, 1263-1270.
8. Dang, D. T., Pevsner, J. and Yang, V. W. (2000). The biology of the mammalian Kruppel-like family of transcription factors. Int. J. Biochem. Cell Biol. 32, 1103-1121.
9. Ema, M., Mori, D., Niwa, H., Hasegawa, Y., Yamanaka, Y., Hitoshi, S., Mimura, J., Kawabe, Y., Hosoya, T., Morita, M. et al. (2008). Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 3, 555-567.
10. Evans, M. J. and Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
11. Fujikura, J., Yamato, E., Yonemura, S., Hosoda, K., Masui, S., Nakao, K., Miyazaki Ji, J. and Niwa, H. (2002). Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 16, 784-789.
12. Gardner, R. L., Papaioannou, V. E. and Barton, S. C. (1973). Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass. J. Embryol. Exp. Morphol. 30, 561-572.
13. Gerbe, F., Cox, B., Rossant, J. and Chazaud, C. (2008). Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst. Dev. Biol. 313, 594-602.
14. Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W. and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069.
15. Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M. and Nagy, A. (1998). Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 76, 79-90.
16. Hall, J., Guo, G., Wray, J., Eyres, I., Nichols, J., Grotewold, L., Morfopoulou, S., Humphreys, P., Mansfield, W., Walker, R. et al. (2009). Oct4 and LIF/Stat3 additively induce Kruppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell 5, 597-609.
17. Hochedlinger, K., Yamada, Y., Beard, C. and Jaenisch, R. (2005). Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121, 465-477.
18. Home, P., Ray, S., Dutta, D., Bronshteyn, I., Larson, M. and Paul, S. (2009). GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J. Biol. Chem. 284, 28729-28737.
19. Jiang, J., Chan, Y. S., Loh, Y. H., Cai, J., Tong, G. Q., Lim, C. A., Robson, P., Zhong, S. and Ng, H. H. (2008). A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 10, 353-360.
20. Johnson, M. H. and McConnell, J. M. (2004). Lineage allocation and cell polarity during mouse embryogenesis. Semin. Cell Dev. Biol. 15, 583-597.
21. Kanai-Azuma, M., Kanai, Y., Gad, J. M., Tajima, Y., Taya, C., Kurohmaru, M., Sanai, Y., Yonekawa, H., Yazaki, K., Tam, P. P. et al. (2002). Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129, 2367-2379.
22. Kuo, C. T., Veselits, M. L., Barton, K. P., Lu, M. M., Clendenin, C. and Leiden, J. M. (1997). The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis. Genes Dev. 11, 2996-3006.
23. Kurimoto, K., Yabuta, Y., Ohinata, Y., Ono, Y., Uno, K. D., Yamada, R. G., Ueda, H. R. and Saitou, M. (2006). An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 34, e42.
24. Kyba, M., Perlingeiro, R. C. and Daley, G. Q. (2002). HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109, 29-37.
25. Li, Y., McClintick, J., Zhong, L., Edenberg, H. J., Yoder, M. C. and Chan, R. J. (2005). Murine embryonic stem cell differentiation is promoted by SOCS-3 and inhibited by the zinc finger transcription factor Klf4. Blood 105, 635-637. (Pubitemid 40070746)
26. Lim, C. Y., Tam, W. L., Zhang, J., Ang, H. S., Jia, H., Lipovich, L., Ng, H. H., Wei, C. L., Sung, W. K., Robson, P. et al. (2008). Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. Cell Stem Cell 3, 543-554.
27. Lu, C. W., Yabuuchi, A., Chen, L., Viswanathan, S., Kim, K. and Daley, G. Q. (2008). Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat. Genet. 40, 921-926.
28. Martin, G. R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 78, 7634-7638.
29. McConnell, B. B., Ghaleb, A. M., Nandan, M. O. and Yang, V. W. (2007). The diverse functions of Kruppel-like factors 4 and 5 in epithelial biology and pathobiology. BioEssays 29, 549-557.
30. Meilhac, S. M., Adams, R. J., Morris, S. A., Danckaert, A., Le Garrec, J. F. and Zernicka-Goetz, M. (2009). Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst. Dev. Biol. 331, 210-221.
31. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. and Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642.
32. Molkentin, J. D., Lin, Q., Duncan, S. A. and Olson, E. N. (1997). Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11, 1061-1072.
33. Morris, S. A., Teo, R. T., Li, H., Robson, P., Glover, D. M. and Zernicka-Goetz, M. (2010). Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl. Acad. Sci. USA 107, 6364-6369.
34. Morrisey, E. E., Tang, Z., Sigrist, K., Lu, M. M., Jiang, F., Ip, H. S. and Parmacek, M. S. (1998). GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12, 3579-3590.
35. Nagy, A., Gertsenstein, M., Vintersten, K. and Behringer, R. (2003). Manipulating the Mouse Embryo: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
36. Nakagawa, M., Koyanagi, M., Tanabe, K., Takahashi, K., Ichisaka, T., Aoi, T., Okita, K., Mochiduki, Y., Takizawa, N. and Yamanaka, S. (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol. 26, 101-106.
37. Niakan, K. K., Ji, H., Maehr, R., Vokes, S. A., Rodolfa, K. T., Sherwood, R. I., Yamaki, M., Dimos, J. T., Chen, A. E., Melton, D. A. et al. (2010). Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes Dev. 24, 312-326.
38. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H. and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391.
39. Nishioka, N., Yamamoto, S., Kiyonari, H., Sato, H., Sawada, A., Ota, M., Nakao, K. and Sasaki, H. (2008). Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125, 270-283.
40. Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N. et al. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398-410.
41. Niwa, H. (2007). How is pluripotency determined and maintained? Development 134, 635-646.
42. Niwa, H., Miyazaki, J. and Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372-376.
43. Niwa, H., Toyooka, Y., Shimosato, D., Strumpf, D., Takahashi, K., Yagi, R. and Rossant, J. (2005). Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917-929.
44. Nuez, B., Michalovich, D., Bygrave, A., Ploemacher, R. and Grosveld, F. (1995). Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375, 316-318.
45. Parisi, S., Passaro, F., Aloia, L., Manabe, I., Nagai, R., Pastore, L. and Russo, T. (2008). Klf5 is involved in self-renewal of mouse embryonic stem cells. J. Cell Sci. 121, 2629-2634.
46. Pease, S., Braghetta, P., Gearing, D., Grail, D. and Williams, R. L. (1990). Isolation of embryonic stem (ES) cells in media supplemented with recombinant leukemia inhibitory factor (LIF). Dev. Biol. 141, 344-352.
47. Perkins, A. C., Sharpe, A. H. and Orkin, S. H. (1995). Lethal beta-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375, 318-322.
48. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29, e45.
49. Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. and Hadjantonakis, A. K. (2008). Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091.
50. Qu, X. B., Pan, J., Zhang, C. and Huang, S. Y. (2008). Sox17 facilitates the differentiation of mouse embryonic stem cells into primitive and definitive endoderm in vitro. Dev. Growth Differ. 50, 585-593.
51. Ralston, A. and Rossant, J. (2008). Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 313, 614-629.
52. Ralston, A., Cox, B. J., Nishioka, N., Sasaki, H., Chea, E., Rugg-Gunn, P., Guo, G., Robson, P., Draper, J. S. and Rossant, J. (2010). Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137, 395-403.
53. Rossant, J. (2004). Lineage development and polar asymmetries in the periimplantation mouse blastocyst. Semin. Cell Dev. Biol. 15, 573-581.
54. Rossant, J. and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538-548.
55. Rossant, J. and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
56. Segre, J. A., Bauer, C. and Fuchs, E. (1999). Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat. Genet. 22, 356-360.
57. Seguin, C. A., Draper, J. S., Nagy, A. and Rossant, J. (2008). Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells. Cell Stem Cell 3, 182-195.
58. Shimoda, M., Kanai-Azuma, M., Hara, K., Miyazaki, S., Kanai, Y., Monden, M. and Miyazaki, J. (2007). Sox17 plays a substantial role in late-stage differentiation of the extraembryonic endoderm in vitro. J. Cell Sci. 120, 3859-3869.
59. Shindo, T., Manabe, I., Fukushima, Y., Tobe, K., Aizawa, K., Miyamoto, S., Kawai-Kowase, K., Moriyama, N., Imai, Y., Kawakami, H. et al. (2002). Kruppel-like zinc-finger transcription factor KLF5/BTEB2 is a target for angiotensin II signaling and an essential regulator of cardiovascular remodeling. Nat. Med. 8, 856-863.
60. Silva, J., Nichols, J., Theunissen, T. W., Guo, G., van Oosten, A. L., Barrandon, O., Wray, J., Yamanaka, S., Chambers, I. and Smith, A. (2009). Nanog is the gateway to the pluripotent ground state. Cell 138, 722-737.
61. Sinner, D., Kirilenko, P., Rankin, S., Wei, E., Howard, L., Kofron, M., Heasman, J., Woodland, H. R. and Zorn, A. M. (2006). Global analysis of the transcriptional network controlling Xenopus endoderm formation. Development 133, 1955-1966.
62. Soudais, C., Bielinska, M., Heikinheimo, M., MacArthur, C. A., Narita, N., Saffitz, J. E., Simon, M. C., Leiden, J. M. and Wilson, D. B. (1995). Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121, 3877-3888.
63. Strumpf, D., Mao, C. A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. and Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102.
64. Sur, I., Rozell, B., Jaks, V., Bergstrom, A. and Toftgard, R. (2006). Epidermal and craniofacial defects in mice overexpressing Klf5 in the basal layer of the epidermis. J. Cell Sci. 119, 3593-3601. (Pubitemid 44501863)
65. Takahashi, K. and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
66. Wang, H. and Dey, S. K. (2006). Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7, 185-199.
67. Wan, H., Luo, F., Wert, S. E., Zhang, L., Xu, Y., Ikegami, M., Maeda, Y., Bell, S. M. and Whitsett, J. A. (2008). Kruppel-like factor 5 is required for perinatal lung morphogenesis and function. Development 135, 2563-2572.
68. Wani, M. A., Means, R. T., Jr and Lingrel, J. B. (1998). Loss of LKLF function results in embryonic lethality in mice. Transgenic Res. 7, 229-238.
69. Yagi, R., Kohn, M. J., Karavanova, I., Kaneko, K. J., Vullhorst, D., DePamphilis, M. L. and Buonanno, A. (2007). Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827-3836.
70. Yamanaka, Y., Ralston, A., Stephenson, R. O. and Rossant, J. (2006). Cell and molecular regulation of the mouse blastocyst. Dev. Dyn. 235, 2301-2314.
71. Zernicka-Goetz, M., Morris, S. A. and Bruce, A. W. (2009). Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat. Rev. Genet. 10, 467-477.