Negative regulation of the JAK/STAT: Pathway implication in tumorigenesis;Les régulations négatives de la voie JAK/STAT: Implication dans la tumorigenèse

Bulletin du Cancer

Volumn 92, Issue 10, 2005, Pages 845-857

  Espert, Lucile ^a   Dusanter Fourt, Isabelle ^b   Chelbi Alix, Mounira K ^a  

^a INSTITUT ANDRÉ LWOFF   (France)

^b INSTITUT COCHIN   (France)

Author keywords

Cytokines; JAK STAT; Phosphotyrosine phosphatases; PIAS; SOCS

Indexed keywords

CD45 ANTIGEN; CELL SURFACE RECEPTOR; CYTOKINE; CYTOKINE RECEPTOR; DIMER; GROWTH FACTOR; HORMONE; JANUS KINASE; JANUS KINASE 4; PROTEASOME; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; STAT PROTEIN; STAT7 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; TRANSCRIPTION FACTOR; TYROSINE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHOSPHORYLATION; CARCINOGENESIS; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; COMPLEX FORMATION; CYTOPLASM; DEPHOSPHORYLATION; DIMERIZATION; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; NEGATIVE FEEDBACK; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; ENZYME ACTIVATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASMS; PHOSPHORYLATION; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN-TYROSINE-PHOSPHATASE; STAT TRANSCRIPTION FACTORS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 27744507520     PISSN: 00074551     EISSN: 17696917     Source Type: Journal    
DOI: None     Document Type: Review

References (126)

1. Darnell Jr. JE, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994; 264: 1415-21.
2. Pellegrini S, Dusanter-Fourt I. The structure, regulation and function of the Janus kinases (JAKs) and the signal transducers and activators of transcription (STATs). Eur J Biochem 1997; 248: 615-33.
3. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 2002; 109: 1139-42.
4. Ward AC, Touw I, Yoshimura A. The Jak-Stat pathway in normal and perturbed hematopoiesis. Blood 2000; 95: 19-29.
5. Gongora C, Mechti N. Interferon signaling pathways. Bull Cancer 1999; 86: 911-9.
6. Wormald S, Hilton DJ. Inhibitors of cytokine signal transduction. J Biol Chem 2004; 279: 821-4.
7. Velazquez L, Fellous M, Stark GR, Pellegrini S. A protein tyrosine kinase in the interferon alpha/beta signaling pathway. Cell 1992; 70: 313-22.
8. Leonard WJ, O'Shea JJ. Jaks and STATs : biological implications. Annu Rev Immunol 1998; 16: 293-322.
9. Chen M, Cheng A, Candotti F, Zhou YJ, Hymel A, Fasth A, et al. Complex effects of naturally occurring mutations in the JAK3 pseudokinase domain: evidence for interactions between the kinase and pseudokinase domains. Mol Cell Biol 2000; 20: 947-56.
10. Saharinen P, Takaluoma K, Silvennoinen O. Regulation of the Jak2 tyrosine kinase by its pseudokinase domain. Mol Cell Biol 2000; 20: 3387-95.
11. Yeh TC, Dondi E, Uze G, Pellegrini S. A dual role for the kinase-like domain of the tyrosine kinase Tyk2 in interferon-alpha signaling. Proc Natl Acad Sci USA 2000; 97: 8991-6.
12. Ihle JN. The Stat family in cytokine signaling. Curr Opin Cell Biol 2001; 13: 211-7.
13. Hilkens CM, Is'harc H, Lillemeier BF, Strobl B, Bates PA, Behrmann I, et al. A region encompassing the FERM domain of Jak1 is necessary for binding to the cytokine receptor gp130. FEBS Lett 2001; 505: 87-91.
14. Yamaoka K, Saharinen P, Pesu M, Holt 3rd VE, Silvennoinen O, O'Shea JJ. The Janus kinases (Jaks). Genome Biol 2004; 5: 253.
15. Schuringa JJ, Wierenga AT, Kruijer W, Vellenga E. Constitutive Stat3, Tyr705, and Ser727 phosphorylation in acute myeloid leukemia cells caused by the autocrine secretion of interleukin-6. Blood 2000; 95: 3765-70.
16. Dobbeling U, Dummer R, Laine E, Potoczna N, Qin JZ, Burg G. Interleukin-15 is an autocrine/paracrine viability factor for cutaneous T-cell lymphoma cells. Blood 1998; 92: 252-8.
17. Lacronique V, Boureux A, Valle VD, Poirel H, Quang CT, Mauchauffe M, et al. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science 1997; 278: 1309-12.
18. Migone TS, Lin JX, Cereseto A, Mulloy JC, O'Shea JJ, Franchini G, et al. Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 1995; 269: 79-81.
19. Maritano D, Sugrue ML, Tininini S, Dewilde S, Strobl B, Fu X, et al. The STAT3 isoforms alpha and beta have unique and specific functions. Nature Immunol 2004; 5: 401-9.
20. Kisseleva T, Bhattacharya S, Braunstein J, Schindlet CW. Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 2002; 285: 1-24.
21. John S, Vinkemeier U, Soldaini E, Darnell JE, Leonard WJ. The significance of tetramerization in promoter recruitment by Stat5. Mol Cell Biol 1999; 19: 1910-8.
22. Horvath CM. STAT proteins and transcriptional responses to extracellular signals. Trends Biochem Sci 2000; 25: 496-502.
23. Shuai K. Modulation of STAT signaling by STAT-interacting proteins. Oncogene 2000; 19: 2638-44.
24. Zhang T, Kee WH, Seow KT, Fung W, Cao X. The coiled-coil domain of Stat3 is essential for its SH2 domain-mediated receptor binding and subsequent activation induced by epidermal growth factor and interleukin-6. Mol Cell Biol 2000; 20: 7132-9.
25. Ma J, Zhang T, Novotny-Diermayr V, Tan AL, Cao X. A novel sequence in the coiled-coil domain of Stat3 essential for its nuclear translocation. J Biol Chem 2003; 278: 29252-60.
26. Melen K, Kinnunen L, Julkunen I. Arginine/lysine-rich structural element is involved in interferon-induced nuclear import of STATs. J Biol Chem 2001; 276: 16447-55.
27. Yang E, Wen Z, Haspel RL, Zhang JJ, Darnell JE. The linker domain of Stat1 is required for gamma interferon-driven transcription. Mol Cell Biol 1999; 19: 5106-12.
28. Wang T, Niu G, Kortylewski M, Burdelya L, Shain K, Zhang S, et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nature Med 2004; 10: 48-54.
29. Teng CB, Diao HL, Ma XH, Xu LB, Yang ZM. Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol Reprod Dev 2004; 69: 1-10.
30. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 1997; 11: 179-86.
31. Kofoed EM, Hwa V, Little B, Woods KA, Buckway CK, Tsubaki J, et al. Growth hormone insensitivity associated with a STAT5b mutation. N Engl J Med 2003; 349: 1139-47.
32. Baskiewicz-Masiuk M, Masiuk M, Czajka R, Machalinski B. The role of STAT5 proteins in the regulation of normal hematopoiesis in a cord blood model. Cell Mol Biol Lett 2003; 8: 317-31.
33. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood 2003; 101: 2940-54.
34. Weber-Nordt RM, Egen C, Wehinger J, Ludwig W, Gouilleux-Gruart V, Mertelsmann R, et al. Constitutive activation of STAT proteins in primary lymphoid and myeloid leukemia cells and in Epstein-Barr virus (EBV)-related lymphoma cell lines. Blood 1996; 88: 809-16.
35. Niu G, Heller R, Catlett-Fakone R, Coppola D, Jaroszeski M, Dalton W, et al. Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. Cancer Res 1999; 59: 5059-63.
36. Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, et al. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 2001; 20: 2499-513.
37. Chan KS, Sano S, Kiguchi K, Anders J, Komazawa N, Takeda J, et al. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis.J Clin Invest 2004; 114: 720-8.
38. Schwaller J, Parganas E, Wang D, Cain D, Aster JC, Williams IR, et al. Stat5 is essential for the myelo- and lymphoproliferative disease induced by TEL/JAK2. Mol Cell 2000; 6: 693-704.
39. Stephanou A, Latchman DS. STAT-1: a novel regulator of apoptosis. Int J Exp Pathol 2003; 84: 239-44.
40. Durbin JE, Hackenmiller R, Simon MC, Levy DE. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996; 84: 443-50.
41. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 1998; 95: 7556-61.
42. Tonks NK, Neel BG. Combinatorial control of the specificity of protein tyrosine phosphatases. Curr Opin Cell Biol 2001; 13: 182-95.
43. Yetter A, Uddin S, Krolewski JJ, Jiao H, Yi T, Platanias LC. Association of the interferon-dependent tyrosine kinase Tyk-2 with the hematopoietic cell phosphatase. J Biol Chem 1995; 270: 18179-82.
44. Banville D, Stocco R, Shen SH. Human protein tyrosine phosphatase 1C (PTPN6) gene structure: alternate promoter usage and exon skipping generate multiple transcripts. Genomics 1995; 27: 165-73.
45. Shultz LD, Coman DR, Bailey CL, Beamer WG, Sidman CL. Viable motheaten, a new allele at the motheaten locus. I. Pathology. Am J Pathol 1984; 116: 179-92.
46. Shultz LD, Rajan TV, Greiner DL. Severe defects in immunity and hematopoiesis caused by SHP-1 protein-tyrosine-phosphatase deficiency. Trends Biotechnol 1997; 15: 302-7.
47. David M, Chen HE, Goelz S, Larner AC, Neel BG. Differential regulation of the alpha/beta interferon-stimulated Jak/Stat pathway by the SH2 domain-containing tyrosine phosphatase SHPTP1. Mol Cell Biol 1995; 15: 7050-8.
48. Klingmuller U, Lorenz U, Cantley LC, Neel BG, Lodish HF. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 1995; 80: 729-38.
49. Wu C, Sun M, Liu L, Zhou GW. The function of the protein tyrosine phosphatase SHP-1 in cancer. Gene 2003; 306: 1-12.
50. Reddy J, Shivapurkar N, Takahashi T, Parikh G, Stastny V, Echebiri C, et al. Differential methylation of genes that regulate cytokine signaling in lymphoid and hematopoietic tumors. Oncogene 2005; 24: 732-6.
51. Fischer P, Lehmann U, Sobota RM, Schmitz J, Niemand C, Linnemann S, et al. The role of the inhibitors of interleukin-6 signal transduction SHP2 and SOCS3 for desensitization of interleukin-6 signalling. Biochem J 2004; 378: 449-60.
52. Ali S, Nouhi Z, Chughtai N. SHP-2 regulates SOCS-1-mediated Janus kinase-2 ubiquitination/degradation downstream of the prolactin receptor. J Biol Chem 2003; 278: 52021-31.
53. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T, et al. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 2004; 13: 341-55.
54. Van Vactor D, O'Reilly AM, Neel BG. Genetic analysis of protein tyrosine phosphatases. Curr Opin Genet Dev 1998; 8: 112-26.
55. Trowbridge IS, Thomas ML. CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu Rev Immunol 1994; 12: 85-116.
56. Hermiston ML, Xu Z, Weiss A. CD45: a critical regulator of signaling thresholds in immune cells. Annu Rev Immunol 2003; 21: 107-37.
57. Byth KF, Conroy LA, Hewlett S, Smith AJ, May J, Alexander DR, et al. CD45-null transgenic mice reveal a positive regulatory role for CD45 in early thymocyte development, in the selection of CD4+CD8+ thymocytes, and B cell maturation. J Exp Med 1996; 183: 1707-18.
58. Yamada T, Zhu D, Saxon A, Zhang K. CD45 controls interleukin-4-mediated IgE class switch recombination in human B cells through its function as a Janus kinase phosphatase. J Biol Chem 2002; 277: 28830-5.
59. Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG. The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 1992; 68: 545-60.
60. Myers MP, Andersen JN, Cheng A, Tremblay ML, Horvath CM, Parisien JP, et al. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem 2001; 276: 47771-4.
61. Simoncic PD, Lee-Loy A, Barber DL, Tremblay ML, McGlade CJ. The T cell protein tyrosine phosphatase is a negative regulator of janus family kinases 1 and 3. Curr Biol 2002; 12: 446-53.
62. ten Hoeve J, de Jesus Ibarra-Sanchez M, Fu Y, Zhu W, Tremblay M, David M, et al. Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol Cell Biol 2002; 22: 5662-8.
63. Aoki N, Matsuda T. A nuclear protein tyrosine phosphatase TC-PTP is a potential negative regulator of the PRL-mediated signaling pathway: dephosphorylation and deactivation of signal transducer and activator of transcription 5a and 5b by TC-PTP in nucleus. Mol Endocrinol 2002; 16: 58-69.
64. Greenhalgh CJ, Hilton DJ. Negative regulation of cytokine signaling. J Leukoc Biol 2001; 70: 348-56.
65. De Sepulveda P, Okkenhaug K, Rose JL, Hawley RG, Dubreuil P, Rottapel R. Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation. EMBO J 1999; 18: 904-15.
66. Stoiber D, Kovarik P, Cohney S, Johnston JA, Steinlein P, Decker T. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 1999; 163: 2640-7.
67. Kario E, Marmor MD, Adamsky K, Citri A, Amit I, Amariglio N, et al. Suppressors of cytokine signaling 4 and 5 regulate epidermal growth factor receptor signaling. J Biol Chem 2004; 8: 7038-48.
68. Kile BT, Alexander WS. The suppressors of cytokine signalling (SOCS). Cell Mol Life Sci 2001; 58: 1627-35.
69. Kamura T, Sato S, Haque D, Liu L, Kaelin Jr. WG, Conaway RC, et al. The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev 1998; 12: 3872-81.
70. Vuong BQ, Arenzana TL, Showalter BM, Losman J, Chen XP, Mostecki J, et al. SOCS-1 Localizes to the Microtubule Organizing Complex-Associated 20S Proteasome. Mol Cell Biol 2004; 24: 9092-101.
71. Yoshimura A, Ohkubo T, Kiguchi T, Jenkins NA, Gilbert DJ, Copeland NG, et al. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J 1995; 14: 2816-26.
72. Ketteler R, Moghraby CS, Hsiao JG, Sandra O, Lodish HF, Klingmuller U. The cytokine-inducible Scr homology domain-containing protein negatively regulates signaling by promoting apoptosis in erythroid progenitor cells. J Biol Chem 2003; 278: 2654-60.
73. Endo TA, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 1997; 387: 921-4.
74. Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, Aono A, et al. Structure and function of a new STAT-induced STAT inhibitor. Nature 1997; 387: 924-9.
75. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, et al. A family of cytokine-inducible inhibitors of signalling. Nature 1997; 387: 917-21.
76. Fujimoto M, Naka T. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol 2003; 24: 659-66.
77. Narazaki M, Fujimoto M, Matsumoto T, Morita Y, Saito H, Kajita T, et al. Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc Natl Acad Sci USA 1998; 95: 13130-4.
78. Galm O, Yoshikawa H, Esteller M, Osieka R, Herman JG. SOCS-1, a negative regulator of cytokine signaling, is frequently silenced by methylation in multiple myeloma. Blood 2003; 101: 2784-8.
79. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, et al. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nature Genet 2001; 28: 29-35.
80. Watanabe D, Naka T, Kishimoto T. Implication of SOCS-1 gene methylation in acute myeloid leukaemia. Br J Haematol 2004; 127: 608-9.
81. Melzner I, Bucur AJ, Bruderlein S, Dorsch K, Hasel C, Barth TF, et al. Biallelic mutation of SOCS-1 impairs JAK2 degradation and sustains phospho-JAK2 action in the MedB-1 mediastinal lymphoma line. Blood 2005; 105: 2535-42.
82. Kishimoto T, Kikutani H. Knocking the SOCS off a tumor suppressor. Nature Genet 2001; 28: 4-5.
83. Sakamoto H, Yasukawa H, Masuhara M, Tanimura S, Sasaki A, Yuge K, et al. A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 1998; 92: 1668-76.
84. Kamio M, Yoshida T, Ogata H, Douchi T, Nagata Y, Inoue M, et al. SOCS1 [corrected] inhibits HPV-E7-mediated transformation by inducing degradation of E7 protein. Oncogene 2004; 23: 3107-15.
85. Kamizono S, Hanada T, Yasukawa H, Minoguchi S, Kato R, Minoguchi M, et al. The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2. J Biol Chem 2001; 276: 12530-8.
86. Metcalf D, Greenhalgh CJ, Viney E, Willson TA, Starr R, Nicola NA, et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 2000; 405: 1069-73.
87. Goldshmit Y, Walters CE, Scott HJ, Greenhalgh CJ, Turnley AM. SOCS2 induces neurite outgrowth by regulation of epidermal growth factor receptor activation. J Biol Chem 2004; 279: 16349-55.
88. Tollet-Egnell P, Flores-Morales A, Stavreus-Evers A, Sahlin L, Norstedt G. Growth hormone regulation of SOCS-2, SOCS-3, and CIS messenger ribonucleic acid expression in the rat. Endocrinology 1999; 140: 3693-704.
89. Marine JC, McKay C, Wang D, Topham DJ, Parganas E, Nakajima H, et al. SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell 1999; 98: 617-27.
90. Sakai I, Takeuchi K, Yamauchi H, Narumi H, Fujita S. Constitutive expression of SOCS3 confers resistance to IFN-alpha in chronic myelogenous leukemia cells. Blood 2002; 100: 2926-31.
91. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, Baca M, et al. Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J 1999; 18: 375-85.
92. Mooney RA, Senn J, Cameron S, Inamdar N, Boivin LM, Shang Y, et al. Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance. J Biol Chem 2001; 276: 25889-93.
93. Song MM, Shuai K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J Biol Chem 1998; 273: 35056-62.
94. Cacalano NA, Sanden D. Johnston JA. Tyrosine-phosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nature Cell Biol 2001; 3: 460-5.
95. Liu B, Liao J, Rao X, Kushner SA, Chung CD, Chang DD, et al. Inhibition of Stat1-mediated gene activation by PIAS1. Proc Natl Acad Sci USA 1998; 95: 10626-31.
96. Johnson ES, Gupta AA. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 2001; 106: 735-44.
97. Arora T, Liu B, He H, Kim J, Murphy TL, Murphy KM, et al. PIASx is a transcripcional co-repressor of signal transducer and activator of transcription 4. J Biol Chem 2003; 278: 21327-30.
98. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 2001; 15: 3088-103.
99. Mowen KA, Tang J, Zhu W, Schurter BT, Shuai K, Herschman HR, et al. Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription. Cell 2001; 104: 731-41.
100. Jackson PK. A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases. Genes Dev 2001; 15: 3053-8.
101. Hilgarth RS, Murphy LA, Skaggs HS, Wilkerson DC, Xing H, Sarge KD. Regulation and function of SUMO modification. J Biol Chem 2004; 52: 53899-902.
102. Ungureanu D, Vanhatupa S, Kotaja N, Yang J, Aittomaki S, Janne OA, et al. PIAS proteins promote SUMO-1 conjugation to STAT1. Blood 2003; 102: 3311-3.
103. Rogers RS, Horvath CM, Matunis MJ. SUMO modification of STAT1 and its role in PIAS-mediated inhibition of gene activation. J Biol Chem 2003; 278: 30091-7.
104. Lui B, Mink S, Wong KA, Stein N, Getman C, Dempsey PW, et al. PIAS1l selectively inhibits interferon-inducible genes and is important in innate immunity. Nature Immunol 2004; 5: 891-8.
105. Zhang Q, Raghunath PN, Xue L, Majewski M, Carpentieri DF, Odum N, et al. Multilevel dysregulation of STAT3 activation in anaplastic lymphoma kinase-positive T/null-cell lymphoma. J Immunol 2002; 168: 466-74.
106. Ohshima T, Koga H, Shimotohno K. Transcriptional activity of peroxisome proliferator-activated receptor gamma is modulated by SUMO-1 modification. J Biol Chem 2004; 279: 29551-7.
107. Gross M, Liu B, Tan J, French FS, Carey M, Shuai K. Distinct effects of PIAS proteins on androgen-mediated gene activation in prostate cancer cells. Oncogene 2001; 20: 3880-7.
108. Pelicano L, Chelbi-Alix MK. Interferon and retinoic acid in the treatment of human cancer: mechanisms of action. Bull Cancer 1998; 85: 313-8.
109. Espert L, Gongora C, Mechti N. Interferon: antiviral mechanisms and viral escape. Bull Cancer 2003; 90: 131-41.
110. Marine JC, Topham DJ, McKay C, Wang D, Parganas E, Stravopodis D, et al. SOCS1l deficiency causes a lymphocyte-dependent perinatal lethality. Cell 1999; 98: 609-16.
111. Krebs DL, Uren RT, Metcalf D, Rakar S, Zhang JG, Starr R, et al. SOCS-6 binds to insulin receptor substrate 4, and mice lacking the SOCS-6 gene exhibit mild growth retardation. Mol Cell Biol 2002; 22: 4567-78.
112. Matsumoto A, Seki Y, Kubo M, Ohtsuka S, Suzuki A, Hayashi I, et al. Suppression of STAT5 functions in liver, mammary glands, and T cells in cytokine-inducible SH2-containing protein 1 transgenic mice. Mol Cell Biol 1999; 19: 6396-407.
113. Seki Y, Hayashi K, Matsumoto A, Seki N, Tsukada J, Ransom J, et al. Expression of the suppressor of cytokine signaling-5 (SOCS5) negatively regulates IL-4-dependent STAT6 activation and Th2 differentiation. Proc Natl Acad Sci USA 2002; 99: 13003-8.
114. Wang J, Feng XH, Schwartz RJ. SUMO-1 modification activated GATA4 dependent cardiogenic gene activity. J Biol Chem 2004; 47: 49091-8.
115. Zheng G, Yang YC. ZNF76, a novel transcriptional repressor targeting TATA-binding protein, is modulated by sumoylation. J Biol Chem 2004; 279: 42410-21.
116. Liang M, Melchior F, Feng XH, Lin X. Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1. J Biol Chem 2004; 279: 22857-65.
117. Okubo S, Hara F, Tsuchida Y, Shimotakahara S, Suzuki S, Hatanaka H, et al. NMR structure of the N-terminal domain of SUMO ligase PIAS1 and its interaction with tumor suppressor p53 and A/T-rich DNA oligomers. J Biol Chem 2004; 279: 31455-61.
118. Schmidt D, Muller S. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci USA 2002; 99: 2872-7.
119. Tallec LP, Kirsh O, Lecomte MC, Viengchareun S, Zennaro MC, Dejean A, et al. 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 ubiquitin-related modifier 1 modification. Mol Endocrinol 2003; 17: 2529-42.
120. Kadare G, Toutant M, Formstecher E, Corvol JC, Carnaud M, Boutterin MC, et al. PIAS1-mediated sumoylation of focal adhesion kinase activates its autophosphorylation. J Biol Chem 2003; 278: 47434-40.
121. Sapetschnig A, Rischitor G, Braun H, Doll A, Schergaut M, Melchior F, et al. Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J 2002; 21: 5206-15.
122. Nishida T, Yasuda H. PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J Biol Chem 2002; 277: 41311-7.
123. Collavin L, Gostissa M, Avolio F, Secco P, Ronchi A, Santoro C, et al. Modification of the erythroid transcription factor GATA-1 by SUMO-1. Proc Natl Acad Sci USA 2004; 101: 8870-5.
124. Dahle O, Andersen TO, Nordgard O, Matre V, Del Sal G, Gabrielsen OS. Transactivation properties of c-Myb are critically dependent on two SUMO-1 acceptor sites that are conjugated in a PIASy enhanced manner. Eur J Biochem 2003; 270: 1338-48.
125. Chun TH, Itoh H, Subramanian L, Iniguez-Lluhi JA, Nakao K. Modification of GATA-2 transcriptional activity in endothelial cells by the SUMO E3 ligase PIASy. Circ Res 2003; 92: 1201-8.
126. Nakagawa K, Yokosawa H. PIAS3 induces SUMO-1 modification and transcriptional repression of IRF-1. FEBS Lett 2002; 530: 204-8.