SUMO conjugation and cardiovascular development

Frontiers in Bioscience

Volumn 14, Issue 4, 2009, Pages 1219-1229

  Wang, Jun ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Cardiogenesis; Cardiogenic factors; Review; Signal transduction; Sumoylation pathway

Indexed keywords

SUMO PROTEIN;

AMINO ACID SEQUENCE; CARDIOVASCULAR SYSTEM; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CARDIOVASCULAR SYSTEM; HUMANS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 63849137548     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3304     Document Type: Article

References (114)

1. Goldstein, G.: Isolation of bovine thymin: a polypeptide hormone of the thymus. Nature, 247, 11-4 (1974).
2. Ciehanover, A., Y. Hod & A. Hershko: A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun, 81, 1100-5 (1978). (Pubitemid 8331462)
3. Matunis, M. J., E. Coutavas & G. Blobel: A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol, 135, 1457-70 (1996). (Pubitemid 26427644)
4. Mahajan, R., C. Delphin, T. Guan, L. Gerace & F. Melchior: A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell, 88, 97-107 (1997). (Pubitemid 27180334)
5. Okura, T., L. Gong, T. Kamitani, T. Wada, I. Okura, C. F. Wei, H. M. Chang & E. T. Yeh: Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J Immunol, 157, 4277- 81 (1996). (Pubitemid 126449343)
6. Lapenta, V., P. Chiurazzi, P. van der Spek, A. Pizzuti, F. Hanaoka & C. Brahe: SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family. Genomics, 40, 362-6 (1997). (Pubitemid 27124102)
7. Lammer, D., N. Mathias, J. M. Laplaza, W. Jiang, Y. Liu, J. Callis, M. Goebl & M. Estelle: Modification of yeast Cdc53p by the ubiquitin-related protein rub1p affects function of the SCFCdc4 complex. Genes Dev, 12, 914- 26 (1998). (Pubitemid 28204600)
8. Kamitani, T., K. Kito, H. P. Nguyen & E. T. Yeh: Characterization of NEDD8, a developmentally downregulated ubiquitin-like protein. J Biol Chem, 272, 28557-62 (1997). (Pubitemid 27517807)
9. Liakopoulos, D., G. Doenges, K. Matuschewski & S. Jentsch: A novel protein modification pathway related to the ubiquitin system. Embo J, 17, 2208-14 (1998). (Pubitemid 28171906)
10. Osaka, F., H. Kawasaki, N. Aida, M. Saeki, T. Chiba, S. Kawashima, K. Tanaka & S. Kato: A new NEDD8- ligating system for cullin-4A. Genes Dev, 12, 2263-8 (1998). (Pubitemid 28371347)
11. Hori, T., F. Osaka, T. Chiba, C. Miyamoto, K. Okabayashi, N. Shimbara, S. Kato & K. Tanaka: Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene, 18, 6829-34 (1999).
12. Kang, S. H., G. R. Kim, M. Seong, S. H. Baek, J. H. Seol, O. S. Bang, H. Ovaa, K. Tatsumi, M. Komatsu, K. Tanaka & C. H. Chung: Two novel ubiquitin-fold modifier 1 (Ufm1)-specific proteases, UfSP1 and UfSP2. J Biol Chem, 282, 5256-62 (2007). (Pubitemid 47093723)
13. Komatsu, M., T. Chiba, K. Tatsumi, S. Iemura, I. Tanida, N. Okazaki, T. Ueno, E. Kominami, T. Natsume & K. Tanaka: A novel protein-conjugating system for Ufm1, a ubiquitin-fold modifier. Embo J, 23, 1977-86 (2004). (Pubitemid 38902076)
14. Saitoh, H. & J. Hinchey: Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem, 275, 6252-8 (2000). (Pubitemid 30129915)
15. Yeh, E. T., L. Gong & T. Kamitani: Ubiquitin-like proteins: new wines in new bottles. Gene, 248, 1-14 (2000). (Pubitemid 30259196)
16. Nowak, M. & M. Hammerschmidt: Ubc9 Regulates Mitosis and Cell Survival during Zebrafish Development. Mol Biol Cell, 17, 5324-36 (2006). (Pubitemid 44907372)
17. Gutierrez, G. J. & Z. Ronai: Ubiquitin and SUMO systems in the regulation of mitotic checkpoints. Trends Biochem Sci, 31, 324-32 (2006). (Pubitemid 43903235)
18. Lois, L. M., C. D. Lima & N. H. Chua: Small ubiquitinlike modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell, 15, 1347-59 (2003). (Pubitemid 36715177)
19. Kurepa, J., J. M. Walker, J. Smalle, M. M. Gosink, S. J. Davis, T. L. Durham, D. Y. Sung & R. D. Vierstra: The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem, 278, 6862- 72 (2003). (Pubitemid 36800677)
20. Kim, K. I. & S. H. Baek: SUMOylation code in cancer development and metastasis. Mol Cells, 22, 247-53 (2006). (Pubitemid 46062287)
21. Hardeland, U., R. Steinacher, J. Jiricny & P. Schar: Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. Embo J, 21, 1456-64 (2002). (Pubitemid 34246524)
22. Dorval, V. & P. E. Fraser: SUMO on the road to neurodegeneration. Biochim Biophys Acta, 1773, 694-706 (2007). (Pubitemid 46830946)
23. Guo, D., M. Li, Y. Zhang, P. Yang, S. Eckenrode, D. Hopkins, W. Zheng, S. Purohit, R. H. Podolsky, A. Muir, J. Wang, Z. Dong, T. Brusko, M. Atkinson, P. Pozzilli, A. Zeidler, L. J. Raffel, C. O. Jacob, Y. Park, M. Serrano- Rios, M. T. Larrad, Z. Zhang, H. J. Garchon, J. F. Bach, J. I. Rotter, J. X. She & C. Y. Wang: A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat Genet, 36, 837-41 (2004). (Pubitemid 39014100)
24. Bohren, K. M., V. Nadkarni, J. H. Song, K. H. Gabbay & D. Owerbach: A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem, 279, 27233-8 (2004). (Pubitemid 38812561)
25. Owerbach, D., E. M. McKay, E. T. Yeh, K. H. Gabbay & K. M. Bohren: A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem Biophys Res Commun, 337, 517-20 (2005). (Pubitemid 41429315)
26. Cheng, J., T. Bawa, P. Lee, L. Gong & E. T. Yeh: Role of desumoylation in the development of prostate cancer. Neoplasia, 8, 667-76 (2006). (Pubitemid 44379793)
27. Desterro, J. M., J. Thomson & R. T. Hay: Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett, 417, 297- 300 (1997). (Pubitemid 27511608)
28. Cheng, J., D. Wang, Z. Wang & E. T. Yeh: SENP1 enhances androgen receptor-dependent transcription through desumoylation of histone deacetylase 1. Mol Cell Biol, 24, 6021-8 (2004). (Pubitemid 38787984)
29. Okuma, T., R. Honda, G. Ichikawa, N. Tsumagari & H. Yasuda: In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem Biophys Res Commun, 254, 693-8 (1999). (Pubitemid 29290530)
30. Wang, J., X. H. Feng & R. J. Schwartz: SUMO-1 modification activated GATA4-dependent cardiogenic gene activity. J Biol Chem, 279, 49091-8 (2004). (Pubitemid 39625791)
31. Miyauchi, Y., S. Yogosawa, R. Honda, T. Nishida & H. Yasuda: Sumoylation of Mdm2 by protein inhibitor of activated STAT (PIAS) and RanBP2 enzymes. J Biol Chem, 277, 50131-6 (2002). (Pubitemid 36014466)
32. Sachdev, S., L. Bruhn, H. Sieber, A. Pichler, F. Melchior & R. Grosschedl: PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev, 15, 3088-103 (2001). (Pubitemid 33115674)
33. Chun, T. H., H. Itoh, L. Subramanian, J. A. Iniguez-Lluhi & K. Nakao: Modification of GATA-2 transcriptional activity in endothelial cells by the SUMO E3 ligase PIASy. Circ Res, 92, 1201-8 (2003). (Pubitemid 36723647)
34. Pichler, A., A. Gast, J. S. Seeler, A. Dejean & F. Melchior: The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell, 108, 109-20 (2002). (Pubitemid 34137016)
35. Sapetschnig, A., G. Rischitor, H. Braun, A. Doll, M. Schergaut, F. Melchior & G. Suske: Transcription factor Sp3 is silenced through SUMO modification by PIAS1. Embo J, 21, 5206-15 (2002).
36. Weger, S., E. Hammer & R. Heilbronn: Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett, 579, 5007-12 (2005). (Pubitemid 41242844)
37. Azuma, Y., A. Arnaoutov, T. Anan & M. Dasso: PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes. Embo J, 24, 2172-82 (2005). (Pubitemid 40961801)
38. Jackson, P. K.: A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases. Genes Dev, 15, 3053-8 (2001). (Pubitemid 33115672)
39. Morita, Y., C. Kanei-Ishii, T. Nomura & S. Ishii: TRAF7 sequesters c-Myb to the cytoplasm by stimulating its sumoylation. Mol Biol Cell, 16, 5433-44 (2005). (Pubitemid 41566851)
40. Kagey, M. H., T. A. Melhuish & D. Wotton: The polycomb protein Pc2 is a SUMO E3. Cell, 113, 127-37 (2003). (Pubitemid 36411965)
41. Kotaja, N., U. Karvonen, O. A. Janne & J. J. Palvimo: PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol Cell Biol, 22, 5222-34 (2002). (Pubitemid 34700711)
42. Rodriguez, M. S., C. Dargemont & R. T. Hay: SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem, 276, 12654-9 (2001).
43. Melchior, F.: SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol, 16, 591-626 (2000).
44. Wang, J., A. Li, Z. Wang, X. Feng, E. N. Olson & R. J. Schwartz: Myocardin Sumoylation Transactivates Cardiogenic Genes in Pluripotent 10T1/2 Fibroblasts. Mol Cell Biol, 27, 622-632 (2007). (Pubitemid 46080129)
45. Jenkins, K. J., A. Correa, J. A. Feinstein, L. Botto, A. E. Britt, S. R. Daniels, M. Elixson, C. A. Warnes & C. L. Webb: Noninherited risk factors and congenital cardiovascular defects: current knowledge: a scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation, 115, 2995- 3014 (2007). (Pubitemid 46912106)
46. Watanabe, T. K., T. Fujiwara, A. Kawai, F. Shimizu, S. Takami, H. Hirano, S. Okuno, K. Ozaki, S. Takeda, Y. Shimada, M. Nagata, A. Takaichi, E. Takahashi, Y. Nakamura & S. Shin: Cloning, expression, and mapping of UBE2I, a novel gene encoding a human homologue of yeast ubiquitin-conjugating enzymes which are critical for regulating the cell cycle. Cytogenet Cell Genet, 72, 86-9 (1996).
47. Golebiowski, F., A. Szulc, M. Sakowicz, A. Szutowicz & T. Pawelczyk: Expression level of Ubc9 protein in rat tissues. Acta Biochim Pol, 50, 1065-73 (2003). (Pubitemid 38608836)
48. Molkentin, J. D., D. V. Kalvakolanu & B. E. Markham: Transcription factor GATA-4 regulates cardiac musclespecific expression of the alpha-myosin heavy-chain gene. Mol Cell Biol, 14, 4947-57 (1994). (Pubitemid 24196844)
49. Nemer, G. & M. Nemer: Regulation of heart development and function through combinatorial interactions of transcription factors. Ann Med, 33, 604-10 (2001). (Pubitemid 34081498)
50. Liang, Q., L. J. De Windt, S. A. Witt, T. R. Kimball, B. E. Markham & J. D. Molkentin: The transcription factors GATA4 and GATA6 regulate cardiomyocyte hypertrophy in vitro and in vivo. J Biol Chem, 276, 30245-53 (2001).
51. Narita, N., M. Bielinska & D. B. Wilson: Wild-type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev Biol, 189, 270-4 (1997). (Pubitemid 27428368)
52. Liang, Q., R. J. Wiese, O. F. Bueno, Y. S. Dai, B. E. Markham & J. D. Molkentin: The transcription factor GATA4 is activated by extracellular signal-regulated kinase 1- and 2- mediated phosphorylation of serine 105 in cardiomyocytes. Mol Cell Biol, 21, 7460-9 (2001). (Pubitemid 32953496)
53. Charron, F., G. Tsimiklis, M. Arcand, L. Robitaille, Q. Liang, J. D. Molkentin, S. Meloche & M. Nemer: Tissuespecific GATA factors are transcriptional effectors of the small GTPase RhoA. Genes Dev, 15, 2702-19 (2001). (Pubitemid 32988880)
54. Komatsu, T., H. Mizusaki, T. Mukai, H. Ogawa, D. Baba, M. Shirakawa, S. Hatakeyama, K. I. Nakayama, H. Yamamoto, A. Kikuchi & K. Morohashi: Small ubiquitin-like modifier 1 (SUMO-1) modification of the synergy control motif of Ad4 binding protein/steroidogenic factor 1 (Ad4BP/SF-1) regulates synergistic transcription between Ad4BP/SF-1 and Sox9. Mol Endocrinol, 18, 2451-62 (2004). (Pubitemid 39335980)
55. Kaiser, F. J., H. J. Ludecke & S. Weger: SUMOylation modulates transcriptional repression by TRPS1. Biol Chem, 388, 381-90 (2007). (Pubitemid 46514695)
56. Niu, Z., W. Yu, S. X. Zhang, M. Barron, N. S. Belaguli, M. D. Schneider, M. Parmacek, A. Nordheim & R. J. Schwartz: Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J Biol Chem, 280, 32531-8 (2005). (Pubitemid 41361867)
57. Weinhold, B., G. Schratt, S. Arsenian, J. Berger, K. Kamino, H. Schwarz, U. Ruther & A. Nordheim: Srf (-/-) ES cells display non-cell-autonomous impairment in mesodermal differentiation. Embo J, 19, 5835-44 (2000).
58. Matsuzaki, K., T. Minami, M. Tojo, Y. Honda, Y. Uchimura, H. Saitoh, H. Yasuda, S. Nagahiro, H. Saya & M. Nakao: Serum response factor is modulated by the SUMO-1 conjugation system. Biochem Biophys Res Commun, 306, 32-8 (2003). (Pubitemid 36629400)
59. Chen, C. Y. & R. J. Schwartz: Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol Cell Biol, 16, 6372-84 (1996). (Pubitemid 26360996)
60. Wang, D. Z., S. Li, D. Hockemeyer, L. Sutherland, Z. Wang, G. Schratt, J. A. Richardson, A. Nordheim & E. N. Olson: Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A, 99, 14855-60 (2002). (Pubitemid 35334573)
61. Aravind, L. & E. V. Koonin: SAP - a putative DNAbinding motif involved in chromosomal organization. Trends Biochem Sci, 25, 112-4 (2000). (Pubitemid 30122420)
62. Du, K. L., H. S. Ip, J. Li, M. Chen, F. Dandre, W. Yu, M. M. Lu, G. K. Owens & M. S. Parmacek: Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol, 23, 2425-37 (2003). (Pubitemid 36351024)
63. Wang, D., P. S. Chang, Z. Wang, L. Sutherland, J. A. Richardson, E. Small, P. A. Krieg & E. N. Olson: Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell, 105, 851-62 (2001). (Pubitemid 32635087)
64. Li, S., D. Z. Wang, Z. Wang, J. A. Richardson & E. N. Olson: The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci U S A, 100, 9366-70 (2003). (Pubitemid 37033934)
65. Ueyama, T., H. Kasahara, T. Ishiwata, Q. Nie & S. Izumo: Myocardin expression is regulated by Nkx2.5, and its function is required for cardiomyogenesis. Mol Cell Biol, 23, 9222-32 (2003). (Pubitemid 37499809)
66. Wang, Z., D. Z. Wang, G. C. Pipes & E. N. Olson: Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci U S A, 100, 7129-34 (2003). (Pubitemid 36706404)
67. Karamboulas, C., G. D. Dakubo, J. Liu, Y. De Repentigny, K. Yutzey, V. A. Wallace, R. Kothary & I. S. Skerjanc: Disruption of MEF2 activity in cardiomyoblasts inhibits cardiomyogenesis. J Cell Sci, 119, 4315-21 (2006). (Pubitemid 44774038)
68. Edmondson, D. G., G. E. Lyons, J. F. Martin & E. N. Olson: Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development, 120, 1251-63 (1994). (Pubitemid 24150050)
69. Riquelme, C., K. K. Barthel & X. Liu: SUMO-1 modification of MEF2A regulates its transcriptional activity. J Cell Mol Med, 10, 132-44 (2006). (Pubitemid 44874296)
70. Gregoire, S. & X. J. Yang: Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol Cell Biol, 25, 2273-87 (2005). (Pubitemid 40354624)
71. Zhao, X., T. Sternsdorf, T. A. Bolger, R. M. Evans & T. P. Yao: Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol Cell Biol, 25, 8456-64 (2005). (Pubitemid 41369167)
72. Molkentin, J. D., A. B. Firulli, B. L. Black, J. F. Martin, C. M. Hustad, N. Copeland, N. Jenkins, G. Lyons & E. N. Olson: MEF2B is a potent transactivator expressed in early myogenic lineages. Mol Cell Biol, 16, 3814-24 (1996). (Pubitemid 26199902)
73. Komuro, I. & S. Izumo: Csx: a murine homeoboxcontaining gene specifically expressed in the developing heart. Proc Natl Acad Sci U S A, 90, 8145-9 (1993). (Pubitemid 23260872)
74. Lints, T. J., L. M. Parsons, L. Hartley, I. Lyons & R. P. Harvey: Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development, 119, 419-31 (1993). (Pubitemid 23293185)
75. Azpiazu, N. & M. Frasch: tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev, 7, 1325-40 (1993). (Pubitemid 23210882)
76. Bodmer, R.: The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development, 118, 719-29 (1993). (Pubitemid 23232780)
77. Kasahara, H., S. Bartunkova, M. Schinke, M. Tanaka & S. Izumo: Cardiac and extracardiac expression of Csx/Nkx2.5 homeodomain protein. Circ Res, 82, 936-46 (1998). (Pubitemid 28225934)
78. Tanaka, M., Z. Chen, S. Bartunkova, N. Yamasaki & S. Izumo: The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development, 126, 1269-80 (1999). (Pubitemid 29182122)
79. Lyons, I., L. M. Parsons, L. Hartley, R. Li, J. E. Andrews, L. Robb & R. P. Harvey: Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev, 9, 1654-66 (1995).
80. Cheng, C. H., Y. H. Lo, S. S. Liang, S. C. Ti, F. M. Lin, C. H. Yeh, H. Y. Huang & T. F. Wang: SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev, 20, 2067-81 (2006).
81. Lyst, M. J., X. Nan & I. Stancheva: Regulation of MBD1-mediated transcriptional repression by SUMO and PIAS proteins. Embo J, 25, 5317-28 (2006). (Pubitemid 44764141)
82. Sepulveda, J. L., N. Belaguli, V. Nigam, C. Y. Chen, M. Nemer & R. J. Schwartz: GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol Cell Biol, 18, 3405-15 (1998). (Pubitemid 28240513)
83. Belaguli, N. S., J. L. Sepulveda, V. Nigam, F. Charron, M. Nemer & R. J. Schwartz: Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol Cell Biol, 20, 7550-8 (2000).
84. Oh, J., Z. Wang, D. Z. Wang, C. L. Lien, W. Xing & E. N. Olson: Target gene-specific modulation of myocardin activity by GATA transcription factors. Mol Cell Biol, 24, 8519-28 (2004). (Pubitemid 39245073)
85. Arnal, J. F., P. Y. Scarabin, F. Tremollieres, H. Laurell & P. Gourdy: Estrogens in vascular biology and disease: where do we stand today? Curr Opin Lipidol, 18, 554-60 (2007). (Pubitemid 47462209)
86. Liu, P. Y., A. K. Death & D. J. Handelsman: Androgens and cardiovascular disease. Endocr Rev, 24, 313-40 (2003). (Pubitemid 36724373)
87. Sheppard, K. E.: Corticosteroid receptors, 11 betahydroxysteroid dehydrogenase, and the heart. Vitam Horm, 66, 77-112 (2003). (Pubitemid 137640815)
88. Faus, H. & B. Haendler: Post-translational modifications of steroid receptors. Biomed Pharmacother, 60, 520-8 (2006).
89. Sentis, S., M. Le Romancer, C. Bianchin, M. C. Rostan & L. Corbo: Sumoylation of the estrogen receptor alpha hinge region regulates its transcriptional activity. Mol Endocrinol, 19, 2671-84 (2005). (Pubitemid 41577242)
90. Tallec, L. P., O. Kirsh, M. C. Lecomte, S. Viengchareun, M. C. Zennaro, A. Dejean & M. Lombes: Protein inhibitor of activated signal transducer and activator of transcription 1 interacts with the N-terminal domain of mineralocorticoid receptor and represses its transcriptional activity: implication of small ubiquitinrelated modifier 1 modification. Mol Endocrinol, 17, 2529- 42 (2003). (Pubitemid 37542215)
91. Tian, S., H. Poukka, J. J. Palvimo & O. A. Janne: Small ubiquitin-related modifier-1 (SUMO-1) modification of the glucocorticoid receptor. Biochem J, 367, 907-11 (2002). (Pubitemid 35305733)
92. Callewaert, L., G. Verrijdt, A. Haelens & F. Claessens: Differential effect of small ubiquitin-like modifier (SUMO)-ylation of the androgen receptor in the control of cooperativity on selective versus canonical response elements. Mol Endocrinol, 18, 1438-49 (2004). (Pubitemid 38692181)
93. Ai, D., X. Fu, J. Wang, M. F. Lu, L. Chen, A. Baldini, W. H. Klein & J. F. Martin: Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc Natl Acad Sci U S A, 104, 9319-24 (2007). (Pubitemid 47185777)
94. Lickert, H., S. Kutsch, B. Kanzler, Y. Tamai, M. M. Taketo & R. Kemler: Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev Cell, 3, 171-81 (2002).
95. Yamamoto, H., M. Ihara, Y. Matsuura & A. Kikuchi: Sumoylation is involved in beta-catenin-dependent activation of Tcf-4. Embo J, 22, 2047-59 (2003). (Pubitemid 36565530)
96. Maltepe, E., J. V. Schmidt, D. Baunoch, C. A. Bradfield & M. C. Simon: Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature, 386, 403-7 (1997). (Pubitemid 27154481)
97. Iyer, N. V., L. E. Kotch, F. Agani, S. W. Leung, E. Laughner, R. H. Wenger, M. Gassmann, J. D. Gearhart, A. M. Lawler, A. Y. Yu & G. L. Semenza: Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev, 12, 149-62 (1998). (Pubitemid 28060446)
98. Bae, S. H., J. W. Jeong, J. A. Park, S. H. Kim, M. K. Bae, S. J. Choi & K. W. Kim: Sumoylation increases HIF- 1alpha stability and its transcriptional activity. Biochem Biophys Res Commun, 324, 394-400 (2004). (Pubitemid 39311508)
99. Carbia-Nagashima, A., J. Gerez, C. Perez-Castro, M. Paez-Pereda, S. Silberstein, G. K. Stalla, F. Holsboer & E. Arzt: RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell, 131, 309-23 (2007). (Pubitemid 47592916)
100. Cheng, J., X. Kang, S. Zhang & E. T. Yeh: SUMOspecific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell, 131, 584-95 (2007). (Pubitemid 350007694)
101. Tojo, M., K. Matsuzaki, T. Minami, Y. Honda, H. Yasuda, T. Chiba, H. Saya, Y. Fujii-Kuriyama & M. Nakao: The aryl hydrocarbon receptor nuclear transporter is modulated by the SUMO-1 conjugation system. J Biol Chem, 277, 46576-85 (2002). (Pubitemid 35417656)
102. Shao, R., F. P. Zhang, F. Tian, P. Anders Friberg, X. Wang, H. Sjoland & H. Billig: Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF-1alpha in adult mouse brain and heart in vivo. FEBS Lett, 569, 293-300 (2004). (Pubitemid 38844635)
103. Euler-Taimor, G. & J. Heger: The complex pattern of SMAD signaling in the cardiovascular system. Cardiovasc Res, 69, 15-25 (2006). (Pubitemid 41814808)
104. Sinha, S., M. H. Hoofnagle, P. A. Kingston, M. E. McCanna & G. K. Owens: Transforming growth factorbeta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol, 287, C1560-8 (2004). (Pubitemid 39507673)
105. Lin, X., M. Liang, Y. Y. Liang, F. C. Brunicardi, F. Melchior & X. H. Feng: Activation of transforming growth factor-beta signaling by SUMO-1 modification of tumor suppressor Smad4/DPC4. J Biol Chem, 278, 18714-9 (2003). (Pubitemid 36799251)
106. Lee, P. S., C. Chang, D. Liu & R. Derynck: Sumoylation of Smad4, the common Smad mediator of transforming growth factor-beta family signaling. J Biol Chem, 278, 27853-63 (2003). (Pubitemid 36899978)
107. Long, J., G. Wang, D. He & F. Liu: Repression of Smad4 transcriptional activity by SUMO modification. Biochem J, 379, 23-9 (2004). (Pubitemid 38491355)
108. Chauchereau, A., L. Amazit, M. Quesne, A. Guiochon-Mantel & E. Milgrom: Sumoylation of the progesterone receptor and of the steroid receptor coactivator SRC-1. J Biol Chem, 278, 12335-43 (2003). (Pubitemid 36800217)
109. Girdwood, D., D. Bumpass, O. A. Vaughan, A. Thain, L. A. Anderson, A. W. Snowden, E. Garcia-Wilson, N. D. Perkins & R. T. Hay: P300 transcriptional repression is mediated by SUMO modification. Mol Cell, 11, 1043-54 (2003). (Pubitemid 36566325)
110. Kuo, H. Y., C. C. Chang, J. C. Jeng, H. M. Hu, D. Y. Lin, G. G. Maul, R. P. Kwok & H. M. Shih: SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci U S A, 102, 16973-8 (2005). (Pubitemid 41692668)
111. Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior & A. Dejean: The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. Embo J, 21, 2682-91 (2002). (Pubitemid 34619384)
112. David, G., M. A. Neptune & R. A. DePinho: SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J Biol Chem, 277, 23658-63 (2002). (Pubitemid 34952204)
113. Kerscher, O.: SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep, 8, 550-5 (2007). (Pubitemid 47214708)
114. Kurtzman, A. L. & N. Schechter: Ubc9 interacts with a nuclear localization signal and mediates nuclear localization of the paired-like homeobox protein Vsx-1 independent of SUMO-1 modification. Proc Natl Acad Sci U S A, 98, 5602-7 (2001). (Pubitemid 32435688)