Hypoxia-inducible factor (HIF)-independent expression mechanism and novel function of HIF prolyl hydroxylase-3 in renal cell carcinoma

Journal of Cancer Research and Clinical Oncology

Volumn 140, Issue 3, 2014, Pages 503-513

  Tanaka, Toshiaki ^a   Torigoe, Toshihiko ^a   Hirohashi, Yoshihiko ^a   Sato, Eiji ^a   Honma, Ichiya ^a   Kitamura, Hiroshi ^a   Masumori, Naoya ^a   Tsukamoto, Taiji ^a   Sato, Noriyuki ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

EGLN3; HIF prolyl hydroxylase; HIFPH3; Hypoxia inducible factor; Renal cell carcinoma; Signal transduction; VHL

Indexed keywords

COMPLEMENTARY DNA; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE 3; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CELL PROLIFERATION; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MALE; MEDICAL RECORD REVIEW; NEPHRECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; RETROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, RENAL CELL; DISEASE-FREE SURVIVAL; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM PROTEINS; NEOPLASM STAGING; PHOSPHATIDYLINOSITOL 3-KINASE; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 84896728402     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1593-7     Document Type: Article

References (43)

1. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, Ratcliffe PJ, Gleadle JM (2004) Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 279:38458-38465
2. Aprelikova O, Chandramouli GV, Wood M, Vasselli JR, Riss J, Maranchie JK, Linehan WM, Barrett JC (2004) Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J Cell Biochem 92:491-501
3. Atkins DJ, Gingert C, Justenhoven C, Schmahl GE, Bonato MS, Brauch H, Störkel S (2005) Concomitant deregulation of HIF1a and cell cycle proteins in VHL-mutated renal cell carcinomas. Virchows Arch 447:634-642
4. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssegur J (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1a in normoxia. EMBO J 22:4082-4090
5. Blancher C, Moore JW, Robertson N, Harris AL (2001) Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1α, HIF-2α, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3′-kinase/Akt signaling pathway. Cancer Res 61:7349-7355
6. Brugarolas JB, Vazquez F, Reddy A, Sellers WR, Kaelin WG Jr (2003) TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4:147-158
7. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337-1340
8. Cioffi CL, Liu XQ, Kosinski PA, Garay M, Bowen BR (2003) Differential regulation of HIF-1α prolyl-4-hydroxylase genes by hypoxia in human cardiovascular cells. Biochem Biophys Res Commun 303:947-953
9. Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH (2000) Hypoxia inducible factor-a binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 275:25733-25741
10. del Peso L, Castellanos MC, Temes E, Martin-Puig S, Cuevas Y, Olmos G, Landazuri MO (2003) The von Hippel Lindau/hypoxia-inducible factor (HIF) pathway regulates the transcription of the HIF-proline hydroxylase genes in response to low oxygen. J Biol Chem 278:48690-48695
11. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (2010) American Joint Committee on Cancer (AJCC) staging manual, 7th edn. Springer, Philadelphia
12. Fuhrman S, Lasky LC, Limas L (1982) Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6:655
13. Gordan JD, Lal P, Dondeti VR, Letrero R, Parekh KN, Oquendo CE, Greenberg RA, Flaherty KT, Rathmell WK, Keith B, Simon MC, Nathanson KL (2008) HIF-α effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma. Cancer Cell 14:435-446
14. Hirsila M, Koivunen P, Gunzler V, Kivirikko KI, Myllyharju J (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem 278:30772-30780
15. Huang J, Zhao Q, Mooney SM, Lee FS (2002) Sequence determinants in hypoxia-inducible factor-1a for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J Biol Chem 277:39792-39800
16. Hudson CC, Liu M, Chiang GG, Otterness DM, Loomis DC, Kaper F, Giaccia AJ, Abraham RT (2002) Regulation of hypoxia-inducible factor 1a expression and function by the mammalian target of rapamycin. Mol Cell Biol 22:7004-7014
17. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr (2001) HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468
18. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, von Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ (2001) Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468-472
19. Klatte T, Seligson DB, Riggs SB, Leppert JT, Berkman MK, Kleid MD, Yu H, Kabbinavar FF, Pantuck AJ, Belldegrun AS (2007) Hypoxia-inducible factor 1α in clear cell renal cell carcinoma. Clin Cancer Res 13:7388-7393
20. Kroeze SG, Vermaat JS, van Brussel A, van Melick HH, Voest EE, Jonges TG, van Diest PJ, Hinrichs J, Bosch JL, Jans JJ (2010) Expression of nuclear FIH independently predicts overall survival of clear cell renal cell carcinoma patients. Eur J Cancer 46:3375-3382
21. Ku JH, Park YH, Myung JK, Moon KC, Kwak C, Kim HH (2011) Expression of hypoxia inducible factor-1α and 2α in conventional renal cell carcinoma with or without sarcomatoid differentiation. Urol Oncol 29:731-737
22. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 21:3995-4004
23. Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG Jr, Schlisio S (2005) Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 8:155-167
24. Lieb ME, Menzies K, Moschella MC, Ni R, Taubman MB (2002) Mammalian EGLN genes have distinct patterns of mRNA expression and regulation. Biochem Cell Biol 80:421-426
25. Lipscomb E, Sarmiere P, Crowder R, Freeman RS (1999) Expression of the SM-20 gene promotes death in nerve growth factor-dependent sympathetic neurons. J Neurochem 73:429-432
26. Lipscomb E, Sarmiere P, Freeman RS (2001) SM-20 is a novel mitochondrial protein that causes caspase-dependent cell death in nerve growth factor-dependent neurons. J Biol Chem 276:11775-11782
27. Marxsen JH, Stengel P, Doege K, Heikkinen P, Jokilehto T, Wagner T, Jelkmann W, Jaakkola P, Metzen E (2004) Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-α-prolyl-4-hydroxylases. Biochem J 381:761-767
28. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275
29. Maynard MA, Ohh M (2007) The role of hypoxia-inducible factors in cancer. Cell Mol Life Sci 64:2170-2180
30. Pescador N, Cuevas Y, Naranjo S, Alcaide M, Villar D (2005) Landázuri MO, del Peso L: identification of a functional hypoxia-responsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem J 390:189-197
31. Pore N, Jiang Z, Shu HK, Bernhard E, Kao GD, Maity A (2006) Akt1 activation can augment hypoxia-inducible factor-1a expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol Cancer Res 4:471-479
32. Sato E, Torigoe T, Hirohashi Y, Kitamura H, Tanaka T, Honma I, Asanuma H, Harada K, Takasu H, Masumori N, Ito N, Hasegawa T, Tsukamoto T, Sato N (2008) Identification of an immunogenic CTL epitope of HIFPH3 for immunotherapy of renal cell carcinoma. Clin Cancer Res 14:6916-6923
33. Semenza GL, Wang GL (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12:5447-5454
34. Shinojima T, Oya M, Takayanagi A, Mizuno R, Shimizu N, Murai M (2007) Renal cancer cells lacking hypoxia-inducible factor (HIF)-1α expression maintain vascular endothelial growth factor expression through HIF-2α. Carcinogenesis 28:529-536
35. Straub JA, Lipscomb EA, Yoshida ES, Freeman RS (2003) Induction of SM-20 in PC12 cells leads to increased cytochrome c levels, accumulation of cytochrome c in the cytosol, and caspase-dependent cell death. J Neurochem 85:318-328
36. Su Y, Loos M, Giese N, Hines OJ, Diebold I, Görlach A, Metzen E, Pastorekova S, Friess H, Büchler P (2010) PHD3 regulates differentiation, tumour growth and angiogenesis in pancreatic cancer. Br J Cancer 103:1571-1579
37. Tanaka T, Kitamura H, Torigoe T, Hirohashi Y, Sato E, Masumori N, Sato N, Tsukamoto T (2011) Autoantibody against hypoxia-inducible factor prolyl hydroxylase-3 is a potential serological marker for renal cell carcinoma. J Cancer Res Clin Oncol 137:789-794
38. Volpe A, Jewett MAS (2005) The natural history of small renal masses. Nat Clin Pract Urol 2:384-390
39. Wang GL, Semenza GL (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270:1230-1237
40. Wang GL, Jiang BH, Rue EA, Semenza GL (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92:5510-5514
41. Yamamoto M, Torigoe T, Kamiguchi K, Hirohashi Y, Nakanishi K, Nabeta C, Asanuma H, Tsuruma T, Sato T, Hata F, Ohmura T, Yamaguchi K, Kurotaki T, Hirata K, Sato N (2005) A novel isoform of TUCAN is overexpressed in human cancer tissues and suppresses both caspase-8- and caspase-9-mediated apoptosis. Cancer Res 65:8709-8714
42. Yu F, White SB, Zhao Q, Lee FS (2001) HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 98:9630-9635
43. Zhong H, Agani F, Baccala AA, Laughner E, Rioseco-Camacho N, Isaacs WB, Simons JW, Semenza GL (1998) Increased expression of hypoxia inducible factor-1a in rat and human prostate cancer. Cancer Res 58:5280-5284