An allelic series uncovers novel roles of the BRCT domain-cbntaining protein PTIP in mouse embryonic vascular development

Molecular and Cellular Biology

Volumn 28, Issue 20, 2008, Pages 6439-6451

  Mu, Weipeng ^a   Wang, Wei ^a   Schimenti, John C ^a  

^a Animal Health Diagnostic Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLNITROSOUREA; PAX TRANSACTIVATION DOMAIN INTERACTING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLELE; ANGIOGENESIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DNA MODIFICATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION PROFILING; MISSENSE MUTATION; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; VASCULARIZATION;

ALLELES; ANIMALS; APOPTOSIS; BASE SEQUENCE; BLOOD VESSELS; CARRIER PROTEINS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOME MAPPING; CLONING, MOLECULAR; DNA BREAKS, DOUBLE-STRANDED; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY;

EID: 53549093600     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00727-08     Document Type: Article

References (68)

1. Adams, R. H., G. A. Wilkinson, C. Weiss, F. Diella, N. W. Gale, U. Deutsch, W. Risau, and R. Klein. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 13:295-306.
2. Boner, W., E. R. Taylor, E. Tsirimonaki, K. Yamane, M. S. Campo, and I. M. Morgan. 2002. A functional interaction between the human papillomavirus 16 transcription/replication factor E2 and the DNA damage response protein TopBPl. J. Biol. Chem. 277:22297-22303.
3. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, C. Declercq, J. Pawling, L. Moons, D. Collen, W. Risau, and A. Nagy. 1996. Abnormal blood vessel development and lethality in embiyos lacking a single VEGF allele. Nature 380:435-439.
4. Chang, H., D. Huylebroeck, K. Verschueren, Q. Guo, M. M. Matzuk, and A. Zwijsen. 1999. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126:1631-1642.
5. Cho, E. A., M. J. Prindle, and G. R. Dressier. 2003. BRCT domain-containing protein PTIP is essential for progression through mitosis. Mol. Cell. Biol. 23:1666-1673.
6. Conway, S. J., D. J. Henderson, and A. J. Copp. 1997. Pax3 is required for cardiac neural crest migration in the mouse: evidence from the splotch (Sp2H) mutant. Development 124:505-514.
7. Cross, J. C., D. G. Simmons, and E. D. Watson. 2003. Chorioallantoic morphogenesis and formation of the placental villous tree. Ann. N. Y. Acad. Sci. 995:84-93.
8. Dickson, M. C., J. S. Martin, F. M. Cousins, A. B. Kulkarni, S. Karlsson, and R. J. Akhurst. 1995. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121:1845-1854.
9. Diehl, F., L. Rossig, A. M. Zeiher, S. Dimmeler, and C. Urbich. 2007. The histone methyltransferase MLL is an upstream regulator of endothelial-cell sprout formation. Blood 109:1472-1478.
10. Eklund, L., and B. R. Olsen. 2006. Tie receptors and their angiopoietin ligands are context-dependent regulators of vascular remodeling. Exp. Cell Res. 312:630-641.
11. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K. S. O'Shea, L. Powell-Braxton, K. J. Hillan, and M. W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
12. Gale, N. W., M. G. Dominguez, I. Noguera, L. Pan, V. Hughes, D. M. Valenzuela, A. J. Murphy, N. C. Adams, H. C. Lin, J. Holash, G. Thurston, and G. D. Yancopoulos. 2004. Haploinsufficiency of delta-like 4 ligand results in embiyonic lethality due to major defects in arterial and vascular development. Proc. Natl. Acad. Sci. USA 101:15949-15954.
13. Garcia, V., K. Furuya, and A. M. Carr. 2005. Identification and functional analysis of TopBP1 and its homologs. DNA Repair (Amsterdam) 4:1227-1239.
14. Glover, J. N., R. S. Williams, and M. S. Lee. 2004. Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem. Sci. 29:579-585.
15. Gohler, T., I. M. Munoz, J. Rouse, and J. J. Blow. 2008. PTIP/Swift is required for efficient PCNA ubiquitination in response to DNA damage. DNA Repair (Amsterdam) 7:775-787.
16. Goumans, M. J., F. Lebrin, and G. Valdimarsdottir. 2003. Controlling the angiogenic switch: a balance between two distinct TGF-b receptor signaling pathways. Trends Cardiovasc. Med. 13:301-307.
17. Grailhe, R., C. Waeber, S. C. Dulawa, J. P. Hornung, X. Zhuang, D. Brunner, M. A. Geyer, and R. Hen. 1999. Increased exploratory activity and altered response to LSD in mice lacking the 5-HT(5A) receptor. Neuron 22:581-591.
18. He, C., and X. Chen. 2005. Transcription regulation of the vegf gene by the BMP/Smad pathway in the angioblast of zebrafish embryos. Biochem. Biophys. Res. Commun. 329:324-330.
19. Herold, S., M. Wanzel, V. Beuger, C. Frohme, D. Beul, T. Hillukkala, J. Syvaoja, H. P. Saluz, F. Haenel, and M. Eilers. 2002. Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol. Cell 10:509-521.
20. Heyer, J., D. Escalante-Alcalde, M. Lia, E. Boettinger, W. Edelmann, C. L. Stewart, and R. Kucherlapati. 1999. Postgastrulation Smad2-deficient embryos show defects in embryo turning and anterior morphogenesis. Proc. Natl. Acad. Sci. USA 96:12595-12600.
21. Hoffmeister, A., A. Ropolo, S. Vasseur, G. V. Mallo, H. Bodeker, B. Ritz-Laser, G. R. Dressier, M. I. Vaccaro, J. C. Dagorn, S. Moreno, and J. L. Iovanna. 2002. The HMG-I/Y-related protein p8 binds to p300 and Pax2 trans-activation domain-interacting protein to regulate the trans-activation activity of the Pax2A and Pax2B transcription factors on the glucagon gene promoter. J. Biol. Chem. 277:22314-22319.
22. Issaeva, I., Y. Zonis, T. Rozovskaia, K. Orlovsky, C. M. Croce, T. Nakamura, A. Mazo, L. Eisenbach, and E. Canaani. 2007. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol. Cell. Biol. 27:1889-1903.
23. Jeon, S. H., B. C. Chae, H. A. Kim, G. Y. Seo, D. W. Seo, G. T. Chun, N. S. Kim, S. W. Yie, W. H. Byeon, S. H. Eom, K. S. Ha, Y. M. Kim, and P. H. Kim. 2007. Mechanisms underlying TGF-beta1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J. Leukoc. Biol. 81:557-566.
24. Jowsey P. A., A. J. Doherty, and J. Rouse. 2004. Human PTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionizing radiation. J. Biol. Chem. 279:55562-55569.
25. Krebs, L. T., J. R. Shutter, K. Tanigaki, T. Honjo, K. L. Stark, and T. Gridley. 2004. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18:2469-2473.
26. Krebs, L. T., Y. Xue, C. R. Norton, J. R. Shutter, M. Maguire, J. P. Sundberg, D. Gallahan, V. Closson, J. Kitajewski, R. Callahan, G. H. Smith, K. L. Stark, and T. Gridley. 2000. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14:1343-1352.
27. Lamalice, L., F. Le Boeuf, and J. Huot. 2007. Endothelial cell migration during angiogenesis. Circ. Res. 100:782-794.
28. Larsson, J., M. J. Goumans, L. J. Sjostrand, M. A. van Rooijen, D. Ward, P. Leveen, X. Xu, P. ten Dijke, C. L. Mummery, and S. Karlsson. 2001. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20:1663-1673.
29. Lechleider, R. J., J. L. Ryan, L. Garrett, C. Eng, C. Deng, A. Wynshaw-Boris, and A. B. Roberts. 2001. Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion. Dev. Biol. 240:157-167.
30. Lechner, M. S., I. Levitan, and G. R. Dressier. 2000. PTIP, a novel BRCT domain-containing protein interacts with Pax2 and is associated with active chromatin. Nucleic Acids Res. 28:2741-2751.
31. Liu, K., F. T. Lin, J. M. Ruppert, and W. C. Lin. 2003. Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol. Cell. Biol. 23:3287-3304.
32. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
33. Lowndes, N. F., and G. W. Toh. 2005. DNA repair: the importance of phosphorylating histone H2AX. Curr. Biol. 15:R99-R102.
34. Manke, I. A., D. M. Lowery, A. Nguyen, and M. B. Yaffe. 2003. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636-639.
35. Mansouri, A. 1998. The role of Pax3 and Pax7 in development and cancer. Crit. Rev. Oncog. 9:141-149.
36. Massague, J., J. Seoane, and D. Wotton. 2005. Smad transcription factors. Genes Dev. 19:2783-2810.
37. McCarthy, E. E., J. T. Celebi, R. Baer, and T. Ludwig. 2003. Loss of Bard1, the heterodimeric partner of the Brca1 tumor suppressor, results in early embiyonic lethality and chromosomal instability. Mol. Cell. Biol. 23:5056-5063.
38. Miller, M. 2006. Phospho-dependent protein recognition motifs contained in C/EBP family of transcription factors: in silico studies. Cell Cycle 5:2501-2508.
39. Miquerol, L., B. L. Langille, and A. Nagy. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127:3941-3946.
40. Mitchell, C. A., C. S. Rutland, M. Walker, M. Nasir, A. J. Foss, C. Stewart, H. Gerhardt, M. A. Konerding, W. Risau, and H. C. Drexler. 2006. Unique vascular phenotypes following over-expression of individual VEGFA isoforms from the developing lens. Angiogenesis 9:209-224.
41. Murr, R., J. I. Loizou, Y. G. Yang, C. Cuenin, H. Li, Z. Q. Wang, and Z. Herceg. 2006. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8:91-99.
42. Oh, S. P., T. Seki, K. A. Goss, T. Imamura, Y. Yi, P. K. Donahoe, L. Li, K. Miyazono, P. ten Dijke, S. Kim, and E. Li. 2000. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc. Nad. Acad. Sci. USA 97:2626-2631.
43. Papaioannou, V. E., and R. R. Behringer. 2004. Mouse phenotypes: a hand book of mutation analysis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Patel, S. R., D. Kim, I. Levitan, and G. R. Dressier. 2007. The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev. Cell 13:580-592.
45. Peters, H., B. Wilm, N. Sakai, K. Imai, R. Maas, and R. Balling. 1999. Paxl and Pax9 synergistically regulate vertebral column development. Development 126:5399-5408.
46. Ponce, M. 2000. In vitro matrigel angiogenesis assays, p. 205-209. In J. Murray (ed.), Angiogenesis protocols. Humana Press, Totowa, NJ.
47. Puebla-Osorio, N., D. B. Lacey, F. W. Alt, and C. Zhu. 2006. Early embryonic lethality due to targeted inactivation of DNA ligase III. Mol. Cell. Biol. 26:3935-3941.
48. Rossant, J., and P. P. L. Tam (ed.). 2002. Mouse development: patterning, morphology, and organogenesis. Academic Press, San Diego, CA.
49. Sato, T. N. 1999. Gene trap, gene knockout, gene knock-in, and transgenics in vascular development. Thromb. Haemost. 82:865-869.
50. Semenza, G. L. 1999. Regulation of mammalian O2 homeostasis by hypoxiainducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-578.
51. Shen, S. X., Z. Weaver, X. Xu, C. Li, M. Weinstein, L. Chen, X. Y. Guan, T. Ried, and C. X. Deng. 1998. A targeted disruption of the murine Brca1 gene causes gamma-irradiation hypersensitivity and genetic instability. Oncogene 17:3115-3124.
52. Shen, T. L., A. Y. Park, A. Alcaraz, X. Peng, I. Jang, P. Koni, R. A. Flavell, H. Gu, and J. L. Guan. 2005. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169:941-952.
53. Shi, Y., and J. Massague. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700.
54. Shimizu, K., P.-Y. Bourillot, S. J. Nielsen, A. M. Zorn, and J. B. Gurdon. 2001. Swift is a novel BRCT domain coactivator of Smad2 in transforming growth factor β signaling. Mol. Cell. Biol. 21:3901-3912.
55. Sjottem, E., C. Rekdal, G. Svineng, S. S. Johnsen, H. Klenow, R. D. Uglehus, and T. Johansen. 2007. The ePHD protein SPBP interacts with TopBPl and together they cooperate to stimulate Ets1-mediated transcription. Nucleic Acids Res. 35:6648-6662.
56. Spiess, A. N., N. Walther, N. Muller, M. Balvers, C. Hansis, and R Ivell. 2003. SPEER - a new family of testis-specific genes from the mouse. Biol. Reprod. 68:2044-2054.
57. Stainier, D. Y., B. Fouquet, J. N. Chen, K. S. Warren, B. M. Weinstein, S. E. Meiler, M. A. Mohideen, S. C. Neuhauss, L. Solnica-Krezel, A. F. Schier, F. Zwartkruis, D. L. Stemple, J. Malicki, W. Driever, and M. C. Fishman. 1996. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 123:285-292.
58. Tebbs, R. S., M. L. Flannery, J. J. Meneses, A. Hartmann, J. D. Tucker, L. H. Thompson, J. E. Cleaver, and R. A. Pedersen. 1999. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol. 208:513-529.
59. Tremblay, K. D., N. R. Dunn, and E. J. Robertson. 2001. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128:3609-3621.
60. Urness, L. D., L. K. Sorensen, and D. Y. Li. 2000. Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26:328-331.
61. Wang, H. U., Z. F. Chen, and D. J. Anderson. 1998. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93:741-753.
62. Weiss, R. S., T. Enoch, and P. Leder. 2000. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev. 14:1886-1898.
63. Welsh, I. C., and T. P. O'Brien. 2000. Loss of late primitive streak mesoderm and interruption of left-right morphogenesis in the Ednrb(s-lAcrg) mutant mouse. Dev. Biol. 225:151-168.
64. Wilson, L., Y. H. Ching, M. Farias, S. A. Hartford, G. Howell, H. Shao, M. Bucan, and J. C. Schimenti. 2005. Random mutagenesis of proximal mouse chromosome 5 uncovers predominantly embryonic lethal mutations. Genome Res. 15:1095-1105.
65. Wu, Z., H. Guo, N. Chow, J. Sallstrom, R. D. Bell, R Deane, A. I. Brooks, S. Kanagala, A. Rubio, A. Sagare, D. Liu, F. Li, D. Armstrong, T. Gasiewicz, R. Zidovetzki, X. Song, F. Hofman, and B. V. Zlokovic. 2005. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat. Med. 11:959-965.
66. Yang, X., L. H. Castilla, X. Xu, C. Li, J. Gotay, M. Weinstein, P. P. Liu, and C. X. Deng. 1999. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 126:1571-1580.
67. Yu, Q., Y. Shen, B. Chatterjee, B. H. Siegfried, L. Leatherbury, J. Rosenthal, J. F. Lucas, A. Wessels, C. F. Spurney, Y. J. Wu, M. L. Kirby, K. Svenson, and C. W. Lo. 2004. ENU induced mutations causing congenital cardiovascular anomalies. Development 131:6211-6223.
68. Zlot, C., G. Ingle, J. Hongo, S. Yang, Z. Sheng, R. Schwall, N. Paoni, F. Wang, F. V. Peale, Jr., and M. E. Gerritsen. 2003. Stanniocalcin 1 is an autocrine modulator of endothelial angiogenic responses to hepatocyte growth factor. J. Biol. Chem. 278:47654-47659.