The absence of Prep1 causes p53-dependent apoptosis of mouse pluripotent epiblast cells

Development

Volumn 137, Issue 20, 2010, Pages 3393-3403

  Fernandez Diaz, Luis C ^a   Laurent, Audrey ^a   Girasoli, Sara ^a   Turco, Margherita ^b   Longobardi, Elena ^a   Iotti, Giorgio ^a   Jenkins, Nancy A ^c   Fiorenza, Maria Teresa ^d   Copeland, Neal G ^c   Blasi, Francesco ^a,e  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Embryo development; Epiblast; Gastrulation; Mouse; p53 (trp53); Prep1 (Pknox1)

Indexed keywords

ATM PROTEIN; BONE MORPHOGENETIC PROTEIN 4; MEIS PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; PROTEIN P16; PROTEIN P53; PROTEIN PREP1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; PKNOX1 PROTEIN, MOUSE; PRIMER DNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL LINEAGE; CELL MATURATION; CELL SIZE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ECTODERM; EMBRYO; EMBRYONIC STEM CELL; GASTRULATION; GENE DISRUPTION; GENE EXPRESSION; KNOCKOUT GENE; LETHALITY; MOUSE; MOUSE EMBRYO; NIDATION; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; CYTOLOGY; EMBRYO DEVELOPMENT; FLUORESCENT ANTIBODY TECHNIQUE; GEL MOBILITY SHIFT ASSAY; GENETICS; GENOTYPE; GERM LAYER; KNOCKOUT MOUSE; METABOLISM; NICK END LABELING; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, SOUTHERN; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EMBRYONIC DEVELOPMENT; FLUORESCENT ANTIBODY TECHNIQUE; GENOTYPE; GERM LAYERS; HOMEODOMAIN PROTEINS; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; PLURIPOTENT STEM CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77957685888     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.050567     Document Type: Article

References (78)

1. Albazerchi, A. and Stern, C. D. (2007). A role for the hypoblast (AVE) in the initiation of neural induction, independent of its ability to position the primitive streak. Dev. Biol. 301, 489-503.
2. Ang, S. L. and Constam, D. B. (2004). A gene network establishing polarity in the early mouse embryo. Semin. Cell Dev. Biol. 15, 555-561.
3. Ang, S. L., Conlon, R. A., Jin, O. and Rossant, J. (1994). Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120, 2979-2989.
4. Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N. and Lovell- Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126-140. (Pubitemid 36062514)
5. Azcoitia, V., Aracil, M., Martinez, A. C. and Torres, M. (2005). The homeodomain protein Meis1 is essential for definitive hematopoiesis and vascular patterning in the mouse embryo. Dev. Biol. 280, 307-320.
6. Bachiller, D., Klingensmith, J., Kemp, C., Belo, J. A., Anderson, R. M., May, S. R., McMahon, J. A., McMahon, A. P., Harland, R. M., Rossant, J. et al. (2000). The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658-661. (Pubitemid 30104006)
7. Beck, F., Erler, T., Russell, A. and James, R. (1995). Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev. Dyn. 204, 219-227.
8. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
9. Belo, J. A., Bachiller, D., Agius, E., Kemp, C., Borges, A. C., Marques, S., Piccolo, S. and De Robertis, E. M. (2000). Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development. Genesis 26, 265-270.
10. Berthelsen, J., Vandekerkhove, J. and Blasi, F. (1996). Purification and characterization of UEF3, a novel factor involved in the regulation of the urokinase and other AP-1 controlled promoters. J. Biol. Chem. 271, 3822-3830. (Pubitemid 26065703)
11. Bertocchini, F. and Stern, C. D. (2002). The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. Dev. Cell 3, 735-744.
12. Biben, C., Stanley, E., Fabri, L., Kotecha, S., Rhinn, M., Drinkwater, C., Lah, M., Wang, C. C., Nash, A., Hilton, D. et al. (1998). Murine cerberus homologue mCer-1: a candidate anterior patterning molecule. Dev. Biol. 194, 135-151.
13. Borghesani, P. R., Alt, F. W., Bottaro, A., Davidson, L., Aksoy, S., Rathbun, G. A., Roberts, T. M., Swat, W., Segal, R. A. and Gu, Y. (2000). Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc. Natl. Acad. Sci. USA 97, 3336-3341.
14. Brennan, J., Lu, C. C., Norris, D. P., Rodriguez, T. A., Beddington, R. S. and Robertson, E. J. (2001). Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411, 965-969. (Pubitemid 32601495)
15. Brons, I. G., Smithers, L. E., Trotter, M. W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S. M., Howlett, S. K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R. A. et al. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195. (Pubitemid 47067373)
16. Capellini, T. D., Di Giacomo, G., Salsi, V., Brendolan, A., Ferretti, E., Srivastava, D., Zappavigna, V. and Selleri, L. (2006). Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 133, 2263-2273. (Pubitemid 43986136)
17. 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.
18. 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.
19. Coucouvanis, E. and Martin, G. R. (1995). Signals for death and survival: a twostep mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287.
20. Coucouvanis, E. and Martin, G. R. (1999). BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126, 535-346.
21. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
22. Di Rosa, P., Villaescusa, J. C., Longobardi, E., Iotti, G., Ferretti, E., Diaz, V. M., Miccio, A., Ferrari, G. and Blasi, F. (2007). The homeodomain transcription factor Prep1 (pKnox1) is required for hematopoietic stem and progenitor cell activity. Dev. Biol. 311, 324-334.
23. Ding, J., Yang, L., Yan, Y. T., Chen, A., Desai, N., Wynshaw-Boris, A. and Shen, M. M. (1998). Cripto is required for correct orientation of the anteriorposterior axis in the mouse embryo. Nature 395, 702-707.
24. Evans, M. J. and Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
25. Ferretti, E., Schulz, H., Talarico, D., Blasi, F. and Berthelsen, J. (1999). The PBX-regulating protein PREP1 is present in different PBX-complexed forms in mouse. Mech. Dev. 83, 53-64.
26. Ferretti, E., Marshall, H., Popperl, H., Maconochie, M., Krumlauf, R. and Blasi, F. (2000). Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 127, 155-166. (Pubitemid 30064397)
27. Ferretti, E., Villaescusa, J. C., Di Rosa, P., Fernandez-Diaz, L. C., Longobardi, E., Mazzieri, R., Miccio, A., Micali, N., Selleri, L., Ferrari, G. et al. (2006). Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol. Cell. Biol. 26, 5650-5662. (Pubitemid 44134323)
28. Fiorenza, M. T., Bevilacqua, A., Canterini, S., Torcia, S., Pontecorvi, M. and Mangia, F. (2004). Early transcriptional activation of the hsp70.1 gene by osmotic stress in one-cell embryos of the mouse. Biol. Reprod. 70, 1606-1613.
29. Friedrich, G. and Soriano, P. (1991). Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5, 1513-1523. (Pubitemid 21906058)
30. Gurley, L. R., D'Anna, J. A., Barham, S. S., Deaven, L. L. and Tobey, R. A. (1978). Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur. J. Biochem. 84, 1-15.
31. Heyer, B. S., MacAuley, A., Behrendtsen, O. and Werb, Z. (2000). Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev. 14, 2072-2084.
32. Hisa, T., Spence, S. E., Rachel, R. A., Fujita, M., Nakamura, T., Ward, J. M., Devor-Henneman, D. E., Saiki, Y., Kutsuna, H., Tessarollo, L. et al. (2004). Hematopoietic, angiogenic and eye defects in Meis1 mutant animals. EMBO J. 23, 450-459.
33. Ibanez-Tallon, I., Ferrai, C., Longobardi, E., Facetti, I., Blasi, F. and Crippa, M. P. (2002). Binding of Sp1 to the proximal promoter links constitutive expression of the human uPA gene and invasive potential of PC3 cells. Blood 100, 3325-3332.
34. Kimura, C., Yoshinaga, K., Tian, E., Suzuki, M., Aizawa, S. and Matsuo, I. (2000). Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev. Biol. 225, 304-321.
35. Kimura-Yoshida, C., Nakano, H., Okamura, D., Nakao, K., Yonemura, S., Belo, J. A., Aizawa, S., Matsui, Y. and Matsuo, I. (2005). Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev. Cell 9, 639-650. (Pubitemid 41555146)
36. Krimpenfort, P., Quon, K. C., Mooi, W. J., Loonstra, A. and Berns, A. (2001). Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413, 83-86.
37. Lawson, K. A., Meneses, J. J. and Pedersen, R. A. (1991). Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
38. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
39. Liguori, G. L., Echevarria, D., Improta, R., Signore, M., Adamson, E., Martinez, S. and Persico, M. G. (2003). Anterior neural plate regionalization in cripto null mutant mouse embryos in the absence of node and primitive streak. Dev. Biol. 264, 537-549.
40. Lin, T. P., Labosky, P. A., Grabel, L. B., Kozak, C. A., Pitman, J. L., Kleeman, J. and MacLeod, C. L. (1994). The Pem homeobox gene is X-linked and exclusively expressed in extraembryonic tissues during early murine development. Dev. Biol. 166, 170-179.
41. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R. and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361-365.
42. Longobardi, E., Iotti, G., Di Rosa, P., Mejetta, S., Bianchi, F., Fernandez-Diaz, L. C., Micali, N., Nuciforo, P., Lenti, E., Ponzoni, M. et al. (2010). Prep1 (pKnox1)-deficiency leads to spontaneous tumor development in mice and accelerates EmuMyc lymphomagenesis: a tumor suppressor role for Prep1. Mol. Oncol. 4, 126-134.
43. Maclean, J. A., 2nd, Chen, M. A., Wayne, C. M., Bruce, S. R., Rao, M., Meistrich, M. L., Macleod, C. and Wilkinson, M. F. (2005). Rhox: a new homeobox gene cluster. Cell 120, 369-382.
44. 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.
45. Meno, C., Gritsman, K., Ohishi, S., Ohfuji, Y., Heckscher, E., Mochida, K., Shimono, A., Kondoh, H., Talbot, W. S., Robertson, E. J. et al. (1999). Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol. Cell 4, 287-298. (Pubitemid 29499782)
46. Mesnard, D., Guzman-Ayala, M. and Constam, D. B. (2006). Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133, 2497-2505.
47. Micali, N., Ferrai, C., Fernandez-Diaz, L. C., Blasi, F. and Crippa, M. P. (2009). Prep1 directly regulates the intrinsic apoptotic pathway by controlling Bcl-XL levels. Mol. Cell. Biol. 29, 1143-1151.
48. 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. (Pubitemid 36694188)
49. 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.
50. Niwa, H. (2007). How is pluripotency determined and maintained? Development 134, 635-646.
51. O'Farrell, P. H., Stumpff, J. and Su, T. T. (2004). Embryonic cleavage cycles: how is a mouse like a fly? Curr. Biol. 14, R35-R45.
52. Perea-Gomez, A., Rhinn, M. and Ang, S. L. (2001). Role of the anterior visceral endoderm in restricting posterior signals in the mouse embryo. Int. J. Dev. Biol. 45, 311-320.
53. Perea-Gomez, A., Vella, F. D., Shawlot, W., Oulad-Abdelghani, M., Chazaud, C., Meno, C., Pfister, V., Chen, L., Robertson, E., Hamada, H. et al. (2002). Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 3, 745-756.
54. Perea-Gomez, A., Camus, A., Moreau, A., Grieve, K., Moneron, G., Dubois, A., Cibert, C. and Collignon, J. (2004). Initiation of gastrulation in the mouse embryo is preceded by an apparent shift in the orientation of the anteriorposterior axis. Curr. Biol. 14, 197-207.
55. Pfister, S., Steiner, K. A. and Tam, P. P. (2007). Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr. Patterns 7, 558-573. (Pubitemid 46464655)
56. Power, M. A. and Tam, P. P. (1993). Onset of gastrulation, morphogenesis and somitogenesis in mouse embryos displaying compensatory growth. Anat. Embryol. 187, 493-504.
57. Rands, G. F. (1986). Size regulation in the mouse embryo. II. The development of half embryos. J. Embryol. Exp. Morphol. 98, 209-217. (Pubitemid 17200316)
58. Rhee, J. W., Arata, A., Selleri, L., Jacobs, Y., Arata, S., Onimaru, H. and Cleary, M. L. (2004). Pbx3 deficiency results in central hypoventilation. Am. J. Pathol. 165, 1343-1350.
59. Richardson, L., Torres-Padilla, M. E. and Zernicka-Goetz, M. (2006). Regionalised signalling within the extraembryonic ectoderm regulates anterior visceral endoderm positioning in the mouse embryo. Mech. Dev. 123, 288-296. (Pubitemid 43782699)
60. Rivera-Perez, J. A. and Magnuson, T. (2005). Primitive streak formation in mice is preceded by localized activation of Brachyury and Wnt3. Dev. Biol. 288, 363-371.
61. Rodriguez, T. A., Srinivas, S., Clements, M. P., Smith, J. C. and Beddington, R. S. (2005). Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development 132, 2513-2520.
62. Selleri, L., Depew, M. J., Jacobs, Y., Chanda, S. K., Tsang, K. Y., Cheah, K. S., Rubenstein, J. L., O'Gorman, S. and Cleary, M. L. (2001). Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 128, 3543-3557.
63. Selleri, L., DiMartino, J., van Deursen, J., Brendolan, A., Sanyal, M., Boon, E., Capellini, T., Smith, K. S., Rhee, J., Popperl, H. et al. (2004). The TALE homeodomain protein Pbx2 is not essential for development and long-term survival. Mol. Cell. Biol. 24, 5324-5331. (Pubitemid 38738167)
64. Sharpless, N. E. (2005). INK4a/ARF: a multifunctional tumor suppressor locus. Mutat. Res. 576, 22-38.
65. Shawlot, W., Deng, J. M. and Behringer, R. R. (1998). Expression of the mouse cerberus-related gene, Cerr1, suggests a role in anterior neural induction and somitogenesis. Proc. Natl. Acad. Sci. USA 95, 6198-6203.
66. Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D'Apice, M. R., Nigro, V. and Boncinelli, E. (1993). A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12, 2735-2747. (Pubitemid 23218323)
67. Snow, M. H. L. (1977). Gastrulation in the mouse: growth and regionalization of the epiblast. J. Embryol. Exp. Morphol. 42, 293-303.
68. Stern, C. D. (2006). Neural induction: 10 years on since the 'default model'. Curr. Opin. Cell Biol. 18, 692-697.
69. Takaoka, K., Yamamoto, M., Shiratori, H., Meno, C., Rossant, J., Saijoh, Y. and Hamada, H. (2006). The mouse embryo autonomously acquires anteriorposterior polarity at implantation. Dev. Cell 10, 451-459.
70. Tam, P. P. and Behringer, R. R. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68, 3-25.
71. Tam, P. P. and Loebel, D. A. (2007). Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 8, 368-381.
72. Tam, P. P., Loebel, D. A. and Tanaka, S. S. (2006). Building the mouse gastrula: signals, asymmetry and lineages. Curr. Opin. Genet. Dev. 16, 419-425.
73. Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L. and McKay, R. D. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199.
74. Wassarman, K. M., Lewandoski, M., Campbell, K., Joyner, A. L., Rubenstein, J. L., Martinez, S. and Martin, G. R. (1997). Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124, 2923-2934.
75. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
76. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
77. Wood, H. B. and Episkopou, V. (1999). Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 86, 197-201.
78. Yamaguchi, T. P., Dumont, D. J., Conlon, R. A., Breitman, M. L. and Rossant, J. (1993). flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 118, 489-498.