The nuclear envelope protein MAN1 regulates TGFβ signaling and vasculogenesis in the embryonic yolk sac

Development

Volumn 134, Issue 7, 2007, Pages 1385-1395

  Cohen, Tatiana V ^a   Kosti, Ourania ^a   Stewart, Colin L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Man1 (Lemd3); Nuclear envelope; TGF ; Vasculogenesis

Indexed keywords

NUCLEAR PROTEIN; PROTEIN MAN1; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLELE; ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS MEMBRANE; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; NUCLEAR PROTEINS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; YOLK SAC;

MUS;

EID: 34248154716     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02816     Document Type: Article

References (74)

1. Abbondanzo, S. J., Gadi, I. and Stewart, C. L. (1993), Derivation of embryonic stem cell lines. Meth. Enzymol. 225, 803-823.
2. Agah, R., Prasad, K. S., Linnemann, R., Firpo, M. T., Quertermous, T. and Dichek, D. A. (2000). Cardiovascular overexpression of transforming growth factor-beta(l) causes abnormal yolk sac vasculogenesis and early embryonic death. Circ. Res. 86, 1024-1030.
3. Arthur, H. M., Ure, J., Smith, A. J., Renforth, G., Wilson, D. I., Torsney, E., Charlton, R., Parums, D. V., Jowett, T., Marchuk, D. A. et al. (2000). Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev. Biol. 217, 42-53.
4. Baldwin, H. S. (1996). Early embryonic vascular development. Cardiovasc. Res. 31, E34-E45.
5. Baron, M. H. (2003). Embryonic origins of mammalian hematopoiesis. Exp. Hematol. 31, 1160-1169.
6. Bertolino, R, Deckers, M., Lebrin, F. and ten Dijke, P. (2005). Transforming growth factor-beta signal transduction in angiogenesis and vascular disorders. Chest 128, 585S-590S.
7. Burke, B. and Stewart, C. L. (2002). Life at the edge: the nuclear envelope and human disease. Nat. Rev. Mol. Cell Biol. 3, 575-585.
8. Byrd, N., Becker, S., Maye, R, Narasimhaiah, R., St-Jacques, B., Zhang, X., McMahon, J., McMahon, A. and Grabel, L. (2002). Hedgehog is required for murine yolk sac angiogenesis. Development 129, 361-372.
9. Cai, M., Huang, Y., Ghirlando, R., Wilson, K. L., Craigie, R. and Clore, G. M. (2001). Solution structure of the constant region of nuclear envelope protein LAP2 reveals two LEM-domain structures: one binds BAF and the other binds DNA. EMBO J. 20, 4399-4407.
10. Capelson, M. and Corces, V. G. (2005). The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator. Mol. Cell 20, 105-116.
11. Chen, H. B., Shen, J., Ip, Y. T. and Xu, L. (2006). Identification of phosphatases for Smad in the BMP/DPP pathway. Genes Dev. 20, 648-653.
12. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S. and Akhurst, R. J. (1995). Defective haernatopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121, 1845-1854.
13. Edwards, D. R., Murphy, G., Reynolds, J. J., Whitham, S. E., Docherty, A. J., Angel, P. and Heath, J. K. (1987). Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J. 6, 1899-1904.
14. Escalante-Alcalde, D., Hernandez, L., Le Stunff, H., Maeda, R., Lee, H. S., Jr, Gang, C., Sciorra, V. A., Daar, I., Spiegel, S., Morris, A. J. et al. (2003). The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 130, 4623-4637.
15. Feinberg, M. W., Watanabe, M., Lebedeva, M. A., Depina, A. S., Hanai, J., Mammoto, T., Frederick, J. P., Wang, X. F., Sukhatme, V. P. and Jain, M. K. (2004). Transforming growth factor-beta1 inhibition of vascular smooth muscle cell activation is mediated via Smad3. J. Biol. Chem. 279, 16388-16393.
16. Feng, X. H. and Derynck, R. (2005). Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693.
17. Goumans, M. J. and Mummery, C. (2000). Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44, 253-265.
18. Goumans, M. J., Zwijsen, A., van Rooijen, M. A., Huylebroeck, D., Roelen, B. A. and Mummery, C. L. (1999). Transforming growth factor-beta signalling in extraembryonic mesoderm is required for yolk sac vasculogenesis in mice. Development 126, 3473-3483.
19. Goumans, M. J., Valdimarsdottir, G., Itoh, S., Rosendahl, A., Sideras, P. and ten Dijke, P. (2002). Balancing the activation state of the endothelium via two distinct TGF-Ibeta type I receptors. EMBO J. 21, 1743-1753.
20. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. and Wilson, K. L. (2005). The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31.
21. Hannon, G. J. and Beach, D. (1994). p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 371, 257-261.
22. Hellemans, J., Preobrazhenska, O., Willaert, A., Debeer, P., Verdonk, P. C., Costa, T., Janssens, K., Menten, B., Van Roy, N., Vermeulen, S. J. et al. (2004). Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis. Nat. Genet. 36, 1213-1218.
23. Hellemans, J., Debeer, P., Wright, M., Janecke, A., Kjaer, K. W., Verdonk, P. C., Savarirayan, R., Basel, L., Moss, C., Roth, J. et al. (2006). Germline LEMD3 mutations are rare in sporadic patients with isolated melorheostosis. Hum. Mutat. 27, 290.
24. Ignotz, R. A. and Massague, J. (1986). Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261, 4337-4345.
25. Ishimura, A., Ng, J. K., Taira, M., Young, S. G. and Osada, S. (2006). Man1, an inner nuclear membrane protein, regulates vascular remodeling by modulating transforming growth factor beta signaling. Development 133, 3919-3928.
26. Ivorra, C., Kubicek, M., Gonzalez, J. M., Sanz-Gonzalez, S. M., Alvarez-Barrientos, A., O'Connor, J. E., Burke, B. and Andres, V. (2006). A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes Dev. 20, 307-320.
27. Karlsson, G., Liu, Y., Larsson, J., Goumans, M. J., Lee, J. S., Thorgeirsson, S. S., Ringner, M. and Karlsson, S. (2005). Gene expression profiling demonstrates that TGF-betal signals exclusively through receptor complexes involving Alk5 and identifies targets of TGF-beta signaling. Physiol. Genomics 21, 396-403.
28. Knockaert, M., Sapkota, G., Alarcon, C., Massague, J. and Brivanlou, A. H. (2006). Unique players in the BMP pathway: small C-terminal domain phosphatases dephosphorylate Smad1 to attenuate BMP signaling. Proc. Natl. Acad. Sci. USA 103, 11940-11945.
29. Laguri, C., Gilquin, B., Wolff, N., Romi-Lebrun, R., Courchay, K., Callebaut, I., Worman, H. J. and Zinn-Justin, S. (2001). Structural characterization of the LEM motif common to three human inner nuclear membrane proteins. Structure 9, 503-511.
30. Larsson, J., Goumans, M. J., Sjostrand, L. J., van Rooijen, M. A., Ward, D., Leveen, P., Xu, X., ten Dijke, P., Mummery, C. L. and Karlsson, S. (2001). Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20, 1663-1671.
31. Lee, H., Quinn, J. C., Prasanth, K. V., Swiss, V. A., Economides, K. D., Camacho, M. M., Spector, D. L. and Abate-Shen, C. (2006). PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev. 20, 784-794.
32. Lee, K. K. and Wilson, K. L, (2004). All in the family: evidence for four new LEM-domain proteins Lem2 (NET-25), Lem3, Lem4 and Lem5 in the human genome. Symp. Sec. Exp, Biol. 2004, 329-339.
33. Levenberg, S., Golub, J. S., Amit, M., Itskovitz-Eldor, J. and Langer, R. (2002). Endothelial cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 99, 4391-4396.
34. Li, D. Y., Sorensen, L. K., Brooke, B. S., Urness, L. D., Davis, E. C., Taylor, D. G., Boak, B. B. and Wendel, D. P. (1999). Defective angiogenesis in mice lacking endoglin. Science 284, 1534-1537.
35. Lin, F., Blake, D. L., Callebaut, I., Skerjanc, I. S., Holmer, L., McBurney, M. W., Paulin-Levasseur, M. and Worman, H. J. (2000). MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin. J. Biol. Chem. 275, 4840-4847.
36. Lin, F., Morrison, J. M., Wu, W. and Worman, H. J. (2005). MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling. Hum. Mol. Genet. 14, 437-445.
37. Lin, X., Duan, X., Liang, Y. Y., Su, Y., Wrighton, K. H., Long, J., Hu, M., Davis, C. M., Wang, J., Brunicardi, F. C. et al. (2006). PPM1A functions as a Smad phosphatase to terminate TGFbeta signaling. Cell 125, 915-928.
38. Luo, K. (2004). Ski and SnoN: negative regulators of TGF-beta signaling. Curr. Opin. Genet. Dev. 14, 65-70.
39. Markiewicz, E., Dechat, T., Foisner, R., Quinlan, R. A. and Hutchison, C. J. (2002). Lamin A/C binding protein LAP2alpha is required for nuclear anchorage of retinoblastoma protein. Mol. Biol. Cell 13, 4401-4413.
40. Massague, J. and Chen, Y. G. (2000). Controlling TGF-beta signaling. Genes Dev. 14, 627-644.
41. Massague, J. and Wotton, D. (2000). Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19, 1745-1754.
42. Massague, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
43. McIlroy, M., O'Rourke, M., McKeown, S. R., Hirst, D. G. and Robson, T. (2006). Pericytes influence endothelial cell growth characteristics: role of plasminogen activator inhibitor type 1 (PAI-1). Cardiovasc. Res. 69, 207-217.
44. Melcon, G., Kozlov, S., Cutler, D. A., Sullivan, T, Hernandez, L., Zhao, P., Mitchell, S., Nader, G., Bakay, M., Rottman, J. N. et al. (2006). Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum. Mol. Genet. 15, 637-651.
45. Morris, G. E. (2004). Protein interactions, right or wrong, in Emery-Dreifuss muscular dystrophy. Symp. Soc. Exp. Biol. 2004, 57-68.
46. Mummery, C. L. (2001). Transforming growth factor beta and mouse development. Microsc. Res. Tech. 52, 374-386.
47. O'Connell, K. A. and Edidin, M. (1990). A mouse lymphoid endothelial cell line immortalized by simian virus 40 binds lymphocytes and retains functional characteristics of normal endothelial cells. J Immunol. 144, 521-525.
48. Oh, S. P., Seki, T., Goss, K. A., Imamura, T., Yi, Y., Donahoe, P. K., Li, L., Miyazono, K., ten Dijke, P., Kim, S. et al. (2000). Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. USA 97, 2626-2631.
49. Orkin, S. H., Harosi, F. I. and Leder, P. (1975). Differentiation in erythroleukemic cells and their somatic hybrids, Proc. Natl. Acad. Sci. USA 72, 98-102.
50. Osada, S., Ohmori, S. Y. and Taira, M. (2003). XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos. Development 130, 1783-1794.
51. Oshima, M., Oshima, H. and Taketo, M. M. (1996). TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179, 297-302.
52. Pan, D., Estevez-Salmeron, L. D., Stroschein, S. L., Zhu, X., He, J., Zhou, S. and Luo, K. (2005). The integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-{beta} superfamily of cytokines. J. Biol. Chem. 280, 15992-16001.
53. Pepper, M. S. (1997). Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8, 21-43.
54. Raju, G. P., Dimova, N., Klein, P. S. and Huang, H. C. (2003). SANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with Smad1. J. Biol. Chem. 278, 428-437.
55. Risau, W. and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91,
56. Rossant, J. and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538-548.
57. Rossant, J. and Howard, L. (2002). Signaling pathways in vascular development. Annu. Rev. Cell Dev. Biol. 18, 541-573.
58. Schirmer, E. C., Florens, L., Guan, T., Yates, J. R., 3rd and Gerace, L. (2003). Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301, 1380-1382.
59. Schlaeger, T. M., Qin, Y., Fujiwara, Y., Magram, J. and Sato, T. N. (1995). Vascular endothelial cell lineage-specific promoter in transgenic mice. Development 121, 1089-1098,
60. Skarnes, W. C. (1990). Entrapment vectors: a new tool for mammalian genetics. Biotechnology N. Y. 8, 827-831.
61. Stewart, C. L. (1993). Production of chimeras between embryonic stem cells and embryos. Meth. Enzymol. 225, 823-855.
62. Stewart, C. L., Abbondanzo, S. J. and Cullinan, E. B. (1995). [Regulation by maternally derived cytokines of pre-implantation development and uterine receptiveness]. Contracept. Fertil. Sex. 23, 555-561.
63. Taddei, A., Hediger, F., Neumann, F. R. and Gasser, S. M. (2004). The function of nuclear architecture: a genetic approach. Annu. Rev. Genet. 38, 305-345.
64. Taylor, M. R., Slavov, D., Gajewski, A., Vlcek, S., Ku, L., Fain, P. R., Carniel, E., Di Lenarda, A., Sinagra, G., Boucek, M. M. et al. (2005). Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Hum. Mutat. 26, 566-574.
65. Van Berlo, J. H., Voncken, J. W., Kubben, N., Broers, J. L., Duisters, R., van Leeuwen, R. E., Crijns, H. J., Ramaekers, F. C., Hutchison, C. J. and Pinto, Y. M. (2005). A-type lamins are essential for TGF-beta1 induced PP2A to dephosphorylate transcription factors. Hum. Mol. Genet. 14, 2839-2849.
66. van den Driesche, S., Mummery, C. L. and Westermann, C. J. (2003). Hereditary hemorrhagic telangiectasia: an update on transforming growth factor beta signaling in vasculogenesis and angiogenesis. Cardiovasc. Res. 58, 20-31.
67. Wolff, N., Gilquin, B., Courchay, K., Callebaut, I., Worman, H. J. and Zinn-Justin, S. (2001). Structural analysis of emerin, an inner nuclear membrane protein mutated in X-linked Emery-Dreifuss muscular dystrophy. FEBS Lett. 501, 171-176.
68. Worman, H. J. (2005). Components of the nuclear envelope and their role in human disease. Novartis Found. Symp. 264, 35-42; discussion 42-50, 227-230.
69. Wrana, J. L. (2000). Regulation of Smad activity. Cell 100, 189-192.
70. Xiao, Z., Watson, N., Rodriguez, C. and Lodish, H. F. (2001). Nucleocytoplasmic shuttling of Smad1 conferred by its nuclear localization and nuclear export signals. J. Biol. Chem. 276, 39404-39410.
71. Xu, L., Kang, Y., Col, S. and Massague, J. (2002). Smad2 nucleocytoplasmic shuttling by nucleoporins CAN/Nup214 and Nup153 feeds TGFbeta signaling complexes in the cytoplasm and nucleus. Mol. Cell 10, 271-282.
72. Ying, Q. L., Nichols, J., Chambers, I. and Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292.
73. Zhu, J. Y., Abate, M., Rice, P. W. and Cole, C. N. (1991). The ability of simian virus 40 large T antigen to immortalize primary mouse embryo fibroblasts cosegregates with its ability to bind to p53. J. Virol. 65, 6872-6880.
74. Zwijsen, A., Goumans, M. J., Lawson, K. A., Van Rooijen, M. A. and Mummery, C. L. (1999). Ectopic expression of the transforming growth factor beta type II receptor disrupts mesoderm organisation during mouse gastrulation. Dev. Dyn. 214, 141-151.