JAK kinases promote invasiveness in VHL-mediated renal cell carcinoma by a suppressor of cytokine signaling-regulated, HIF-independent mechanism

American Journal of Physiology - Renal Physiology

Volumn 293, Issue 6, 2007, Pages

  Wu, Karen L ^a   Miao, Hui ^a   Khan, Shenaz ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Janus kinase; Suppressor of cytokine signaling; Von Hippel Lindau syndrome

Indexed keywords

4 (3 BROMOANILINO) 6,7 DIMETHOXYQUINAZOLINE; 6,7 DIMETHOXY 2 PHENYLQUINOXALINE; HYPOXIA INDUCIBLE FACTOR 1; JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE 3; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 2; TRANILAST; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL INVASION; CELL LYSATE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; KIDNEY CARCINOMA; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; UPREGULATION; VON HIPPEL LINDAU DISEASE;

EID: 36549016039     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00096.2007     Document Type: Article

References (77)

1. Aaronson DS, Horvath CM. A road map for those who know JAKSTAT. Science 296: 1653-1655, 2002.
2. Amin HM, Medeiros LJ, Ma Y, Feretzaki M, Das P, Leventaki V, Rassidakis GZ, O'Connor SL, McDonnell TJ, Lai R. Inhibition of JAK3 induces apoptosis and decreases anaplastic lymphoma kinase activity in anaplastic large cell lymphoma. Oncogene 22: 5399-5407, 2003.
3. Ananth S, Knebelmann B, Gruning W, Dhanabal M, Walz G, Stillman IE, Sukhatme VP. Transforming growth factor beta1 is a target for the von Hippel-Lindau tumor suppressor and a critical growth factor for clear cell renal carcinoma. Cancer Res 59: 2210-2216, 1999.
4. Andl CD, Mizushima T, Oyama K, Bowser M, Nakagawa H, Rustgi AK. EGFR-induced cell migration is mediated predominantly by the JAK-STAT pathway in primary esophageal keratinocytes. Am J Physiol Gastrointest Liver Physiol 287: G1227-G1237, 2004.
5. Barton BE, Karras JG, Murphy TF, Barton A, Huang HF. Signal transducer and activator of transcription 3 (STAT3) activation in prostate cancer: direct STAT3 inhibition induces apoptosis in prostate cancer lines. Mol Cancer Ther 3: 11-20, 2004.
6. Bindra RS, Vasselli JR, Stearman R, Linehan WM, Klausner RD. VHL-mediated hypoxia regulation of cyclin D1 in renal carcinoma cells. Cancer Res 62: 3014-3019, 2002.
7. + exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J Biol Chem 279: 26991-27007, 2004.
8. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 109: 1139-1142, 2002.
9. Calzada MJ, Esteban MA, Feijoo-Cuaresma M, Castellanos MC, Naranjo-Suarez S, Temes E, Mendez F, Yanez-Mo M, Ohh M, Landazuri MO. von Hippel-Lindau tumor suppressor protein regulates the assembly of intercellular junctions in renal cancer cells through hypoxia-inducible factor-independent mechanisms. Cancer Res 66: 1553-1560, 2006.
10. Chen XP, Losman J, Cowan S, Donahue E, Fay S, Vuong BQ, Nawijn M, Capece D, Cohan VL, Rothman P. Pim serine/threonine kinases regulate the stability of Socs-1 protein. Proc Natl Acad Sci USA 99: 2175-2180, 2002.
11. Chen XP, Losman JA, Rothman P. SOCS proteins, regulators of intracellular signaling. Immunity 13: 287-290, 2000.
12. Clifford SC, Cockman ME, Smallwood AC, Mole DR, Woodward ER, Maxwell PH, Ratcliffe PJ, Maher ER. Contrasting effects on HIF-1alpha regulation by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease. Hum Mol Genet 10: 1029-1038, 2001.
13. Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 275: 25733-25741, 2000.
14. Datta K, Sundberg C, Karumanchi SA, Mukhopadhyay D. The 104-123 amino acid sequence of the beta-domain of von Hippel-Lindau gene product is sufficient to inhibit renal tumor growth and invasion. Cancer Res 61: 1768-1775, 2001.
15. Denker SP, Barber DL. Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159: 1087-1096, 2002.
16. Dowlati A, Nethery D, Kern JA. Combined inhibition of epidermal growth factor receptor and JAK/STAT pathways results in greater growth inhibition in vitro than single agent therapy. Mol Cancer Ther 3: 459-463, 2004.
17. Dumler I, Kopmann A, Weis A, Mayboroda OA, Wagner K, Gulba DC, Haller H. Urokinase activates the Jak/Stat signal transduction pathway in human vascular endothelial cells. Arterioscler Thromb Vasc Biol 19: 290-297, 1999.
18. Ebong S, Yu CR, Carper DA, Chepelinsky AB, Egwuagu CE. Activation of STAT signaling pathways and induction of suppressors of cytokine signaling (SOCS) proteins in mammalian lens by growth factors. Invest Ophthalmol Vis Sci 45: 872-878, 2004.
19. Eriksen KW, Kaltoft K, Mikkelsen G, Nielsen M, Zhang Q, Geisler C, Nissen MH, Ropke C, Wasik MA, Odum N. Constitutive STAT3-activation in Sezary syndrome: tyrphostin AG490 inhibits STAT3-activation, interleukin-2 receptor expression and growth of leukemic Sezary cells. Leukemia 15: 787-793, 2001.
20. Esteban-Barragan MA, Avila P, Alvarez-Tejado M, Gutierrez MD, Garcia-Pardo A, Sanchez-Madrid F, Landazuri MO. Role of the von Hippel-Lindau tumor suppressor gene in the formation of beta1-integrin fibrillar adhesions. Cancer Res 62: 2929-2936, 2002.
21. Fujimoto M, Naka T. Regulation of cytokine signaling by SOCS family molecules. Trends Immunol 24: 659-666, 2003.
22. George DJ, Kaelin WG Jr. The von Hippel-Lindau protein, vascular endothelial growth factor, and kidney cancer. N Engl J Med 349: 419-421, 2003.
23. Gunaratnam L, Morley M, Franovic A, De Paulsen N, Mekhail K, Parolin DA, Nakamura E, Lorimer IA, Lee S. Hypoxia inducible factor activates the transforming growth factor-alpha/epidermal growth factor receptor growth stimulatory pathway in VHL(-/-) renal cell carcinoma cells. J Biol Chem 278: 44966-44974, 2003.
24. Haan S, Ferguson P, Sommer U, Hiremath M, McVicar DW, Heinrich PC, Johnston JA, Cacalano NA. Tyrosine phosphorylation disrupts elongin interaction and accelerates SOCS3 degradation. J Biol Chem 278: 31972-31979, 2003.
25. He B, You L, Uematsu K, Zang K, Xu Z, Lee AY, Costello JF, McCormick F, Jablons DM. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci USA 100: 14133-14138, 2003.
26. Hilton DJ. Negative regulators of cytokine signal transduction. Cell Mol Life Sci 55: 1568-1577, 1999.
27. Hoffman MA, Ohh M, Yang H, Klco JM, Ivan M, Kaelin WG Jr. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum Mol Genet 10: 1019-1027, 2001.
28. Hsu T, Adereth Y, Kose N, Dammai V. Endocytic function of von Hippel-Lindau tumor suppressor protein regulates surface localization of fibroblast growth factor receptor 1 and cell motility. J Biol Chem 281: 12069-12080, 2006.
29. Humphreys RC, Hennighausen L. Transforming growth factor alpha and mouse models of human breast cancer. Oncogene 19: 1085-1091, 2000.
30. Kaelin WG Jr. Molecular basis of the VHL hereditary cancer syndrome. Nat Rev Cancer 2: 673-682, 2002.
31. Kaelin WG Jr. The von hippel-lindau gene, kidney cancer, and oxygen sensing. J Am Soc Nephrol 14: 2703-2711, 2003.
32. Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway RC, Conaway JW, Nakayama KI. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev 18: 3055-3065, 2004.
33. Kamura T, Sato S, Haque D, Liu L, Kaelin WG Jr, Conaway RC, Conaway JW. 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 12: 3872-3881, 1998.
34. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci USA 97: 10430-10435, 2000.
35. Komazaki T, Nagai H, Emi M, Terada Y, Yabe A, Jin E, Kawanami O, Konishi N, Moriyama Y, Naka T, Kishimoto T. Hypermethylation-associated inactivation of the SOCS-1 gene, a JAK/STAT inhibitor, in human pancreatic cancers. Jpn J Clin Oncol 34: 191-194, 2004.
36. Kondo K, Klco J, Nakamura E, Lechpammer M, Kaelin WG Jr. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1: 237-246, 2002.
37. Kralovics R, Passamonti F, Buser AS, Teo SS, Tiedt R, Passweg JR, Tichelli A, Cazzola M, Skoda RC. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med 352: 1779-1790, 2005.
38. Lai SY, Childs EE, Xi S, Coppelli FM, Gooding WE, Wells A, Ferris RL, Grandis JR. Erythropoietin-mediated activation of JAK-STAT signaling contributes to cellular invasion in head and neck squamous cell carcinoma. Oncogene 24: 4442-4449, 2005.
39. Levine RL, Wadleigh M, Cools J, Ebert BL, Wernig G, Huntly BJ, Boggon TJ, Wlodarska I, Clark JJ, Moore S, Adelsperger J, Koo S, Lee JC, Gabriel S, Mercher T, D'Andrea A, Frohling S, Dohner K, Marynen P, Vandenberghe P, Mesa RA, Tefferi A, Griffin JD, Eck MJ, Sellers WR, Meyerson M, Golub TR, Lee SJ, Gilliland DG. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7: 387-397, 2005.
40. Limnander A, Danial NN, Rothman PB. v-Abl signaling disrupts SOCS-1 function in transformed pre-B cells. Mol Cell 15: 329-341, 2004.
41. Limnander A, Rothman PB. Abl oncogene bypasses normal regulation of JAK/STAT activation. Cell Cycle 3: 1486-1488, 2004.
42. Liu J, Kern JA. Neuregulin-1 activates the JAK-STAT pathway and regulates lung epithelial cell proliferation. Am J Respir Cell Mol Biol 27: 306-313, 2002.
43. Lonergan KM, Iliopoulos O, Ohh M, Kamura T, Conaway RC, Conaway JW, Kaelin WG Jr. Regulation of hypoxia-inducible mRNAs by the von Hippel-Lindau tumor suppressor protein requires binding to complexes containing elongins B/C and Cul2. Mol Cell Biol 18: 732-741, 1998.
44. Lonser RR, Glenn GM, Walther M, Chew EY, Libutti SK, Linehan WM, Oldfield EH. von Hippel-Lindau disease. Lancet 361: 2059-2067, 2003.
45. Maher ER, Yates JR, Harries R, Benjamin C, Harris R, Moore AT, Ferguson-Smith MA. Clinical features and natural history of von Hippel-Lindau disease. QJM 77: 1151-1163, 1990.
46. Mandriota SJ, Turner KJ, Davies DR, Murray PG, Morgan NV, Sowter HM, Wykoff CC, Maher ER, Harris AL, Ratcliffe PJ, Maxwell PH. HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 1: 459-468, 2002.
47. Maranchie JK, Vasselli JR, Riss J, Bonifacino JS, Linehan WM, Klausner RD. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1: 247-255, 2002.
48. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
49. Maynard MA, Ohh M. Von Hippel-Lindau tumor suppressor protein and hypoxia-inducible factor in kidney cancer. Am J Nephrol 24: 1-13, 2004.
50. Narazaki M, Fujimoto M, Matsumoto T, Morita Y, Saito H, Kajita T, Yoshizaki K, Naka T, Kishimoto T. Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc Natl Acad Sci USA 95: 13130-13134, 1998.
51. Niwa Y, Kanda H, Shikauchi Y, Saiura A, Matsubara K, Kitagawa T, Yamamoto J, Kubo T, Yoshikawa H. Methylation silencing of SOCS-3 promotes cell growth and migration by enhancing JAK/STAT and FAK signalings in human hepatocellular carcinoma. Oncogene 24: 6406-6417, 2005.
52. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, Pavletich N, Chau V, Kaelin WG. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2: 423-427, 2000.
53. Ohh M, Yauch RL, Lonergan KM, Whaley JM, Stemmer-Rachamimov AO, Louis DN, Gavin BJ, Kley N, Kaelin WG Jr, Iliopoulos O. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol Cell 1: 959-968, 1998.
54. Okuda H, Hirai S, Takaki Y, Kamada M, Baba M, Sakai N, Kishida T, Kaneko S, Yao M, Ohno S, Shuin T. Direct interaction of the beta-domain of VHL tumor suppressor protein with the regulatory domain of atypical PKC isotypes. Biochem Biophys Res Commun 263: 491-497, 1999.
55. Okuda H, Saitoh K, Hirai S, Iwai K, Takaki Y, Baba M, Minato N, Ohno S, Shuin T. The von Hippel-Lindau tumor suppressor protein mediates ubiquitination of activated atypical protein kinase C. J Biol Chem 276: 43611-43617, 2001.
56. Opdam FJ, Kamp M, De Bruijn R, Roos E. Jak kinase activity is required for lymphoma invasion and metastasis. Oncogene 23: 6647-6653, 2004.
57. Pal S, Claffey KP, Cohen HT, Mukhopadhyay D. Activation of Sp1-mediated vascular permeability factor/vascular endothelial growth factor transcription requires specific interaction with Protein Kinase Czeta. J Biol Chem 273: 26277-26280, 1998.
58. Pal S, Claffey KP, Dvorak HF, Mukhopadhyay D. The von Hippel-Lindau gene product inhibits vascular permeability factor/vascular endothelial growth factor expression in renal cell carcinoma by blocking protein kinase C pathways. J Biol Chem 272: 27509-27512, 1997.
59. Richard S, Campello C, Taillandier L, Parker F, Resche F. Haemangioblastoma of the central nervous system in von Hippel-Lindau disease. French VHL Study Group. J Intern Med 243: 547-553, 1998.
60. Safran M, Kaelin WG Jr. HIF hydroxylation and the mammalian oxygen-sensing pathway. J Clin Invest 111: 779-783, 2003.
61. Sitko JC, Guevara CI, Cacalano NA. Tyrosine phosphorylated SOCS3 interacts with the Nck and Crk-L adapter proteins and regulates Nck activation. J Biol Chem 279: 37662-37669, 2004.
62. Sosman JA. Targeting of the VHL-hypoxia-inducible factor-hypoxiainduced gene pathway for renal cell carcinoma therapy. J Am Soc Nephrol 14: 2695-2702, 2003.
63. Stearns ME, Wang M, Hu Y, Garcia FU. Interleukin-10 activation of the interleukin-10E1 pathway and tissue inhibitor of metalloproteinase-1 expression is enhanced by proteasome inhibitors in primary prostate tumor lines. Mol Cancer Res 1: 631-642, 2003.
64. Stebbins CE, Kaelin WG Jr, Pavletich NP. Structure of the VHLElongin C-Elongin B complex: implications for VHL tumor suppressor function. Science 284: 455-461, 1999.
65. Steensma DP, Dewald GW, Lasho TL, Powell HL, McClure RF, Levine RL, Gilliland DG, Tefferi A. The JAK2 V617F activating tyrosine kinase mutation is an infrequent event in both "atypical" myeloproliferative disorders and myelodysplastic syndromes. Blood 106: 1207-1209, 2005.
66. Sutherland KD, Lindeman GJ, Choong DY, Wittlin S, Brentzell L, Phillips W, Campbell IG, Visvader JE. Differential hypermethylation of SOCS genes in ovarian and breast carcinomas. Oncogene 23: 7726-7733, 2004.
67. Tannahill GM, Elliott J, Barry AC, Hibbert L, Cacalano NA, Johnston JA. SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol Cell Biol 25: 9115-9126, 2005.
68. Ungureanu D, Saharinen P, Junttila I, Hilton DJ, Silvennoinen O. Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol Cell Biol 22: 3316-3326, 2002.
69. Velazquez L, Mogensen KE, Barbieri G, Fellous M, Uze G, Pellegrini S. Distinct domains of the protein tyrosine kinase tyk2 required for binding of interferon-alpha/beta and for signal transduction. J Biol Chem 270: 3327-3334, 1995.
70. Verma A, Kambhampati S, Parmar S, Platanias LC. Jak family of kinases in cancer. Cancer Metastasis Rev 22: 423-434, 2003.
71. Watanabe S, Mu W, Kahn A, Jing N, Li JH, Lan HY, Nakagawa T, Ohashi R, Johnson RJ. Role of JAK/STAT pathway in IL-6-induced activation of vascular smooth muscle cells. Am J Nephrol 24: 387-392, 2004.
72. Witthuhn BA, Williams MD, Kerawalla H, Uckun FM. Differential substrate recognition capabilities of Janus family protein tyrosine kinases within the interleukin 2 receptor (IL2R) system: Jak3 as a potential molecular target for treatment of leukemias with a hyperactive Jak-Stat signaling machinery. Leuk Lymphoma 32: 289-297, 1999.
73. + exchanger recruits ezrin/radixin/moesin proteins to regulate Akt-dependent cell survival. J Biol Chem 279: 26280-26286, 2004.
74. + exchanger. Am J Physiol Renal Physiol 284: F829-F839, 2003.
75. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet 28: 29-35, 2001.
76. Zhang JG, Farley A, Nicholson SE, Willson TA, Zugaro LM, Simpson RJ, Moritz RL, Cary D, Richardson R, Hausmann G, Kile BJ, Kent SB, Alexander WS, Metcalf D, Hilton DJ, Nicola NA, Baca M. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci USA 96: 2071-2076, 1999.
77. Zimmer M, Doucette D, Siddiqui N, Iliopoulos O. Inhibition of hypoxia-inducible factor is sufficient for growth suppression of VHL-/-tumors. Mol Cancer Res 2: 89-95, 2004.