Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells

Blood

Volumn 113, Issue 22, 2009, Pages 5568-5574

  Ghosh, Asish K ^a   Shanafelt, Tait D ^a   Cimmino, Amelia ^b   Taccioli, Cristian ^b   Volinia, Stefano ^b   Liu, Chang Gong ^b   Calin, George A ^b,c   Croce, Carlo M ^b   Chan, Denise A ^d   Giaccia, Amato J ^d   Secreto, Charla ^a   Wellik, Linda E ^a   Lee, Yean K ^a   Mukhopadhyay, Debabrata ^a   Kay, Neil E ^a  

^a MAYO CLINIC   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MICRORNA 92 1; PROTEIN P300; RNA POLYMERASE II; STAT3 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN; HISTONE ACETYLTRANSFERASE PCAF; HYPOXIA INDUCIBLE FACTOR 1; MIXED FUNCTION OXIDASE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN; VHL PROTEIN, HUMAN;

ARTICLE; AUTOCRINE EFFECT; CHRONIC LYMPHATIC LEUKEMIA; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; B LYMPHOCYTE; CELL CULTURE; CELL NUCLEUS; CULTURE TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; HYDROXYLATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN BINDING; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

B-LYMPHOCYTES; CELL CULTURE TECHNIQUES; CELL NUCLEUS; CELLS, CULTURED; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; HYDROXYLATION; HYPOXIA-INDUCIBLE FACTOR 1; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MICRORNAS; MIXED FUNCTION OXYGENASES; P300-CBP TRANSCRIPTION FACTORS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 67049096242     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-10-185686     Document Type: Article

References (49)

1. Montserrat E. Current and developing chemotherapy for CLL. Med Oncol. 2002;19:S11-19.
2. Keating MJ, Chiorazzi N, Messmer B, et al. Biology and treatment of chronic lymphocytic leukemia. Hematology Am Soc Hematol Educ Program. 2003:153-175.
3. Molica S, Vitelli G, Levato D, Gandolfo GM, Liso V. Increased serum levels of vascular endothelial growth factor predict risk of progression in early B-cell chronic lymphocytic leukaemia. Br J Haematol. 1999;107:605-610.
4. Kay NE, Bone ND, Tschumper RC, et al. B-CLL cells are capable of synthesis and secretion of both pro- and anti-angiogenic molecules. Leukemia. 2002;16:911-919.
5. Chen H, Treweeke AT, West DC, et al. In vitro and in vivo production of vascular endothelial growth factor by chronic lymphocytic leukemia cells. Blood. 2000;96:3181-3187.
6. Kini AR, Kay NE, Peterson LC. Increased bone marrow angiogenesis in B cell chronic lymphocytic leukemia. Leukemia. 2000;14:1414-1418.
7. Lee YK, Bone ND, Strege AK, Shanafelt TD, Jelinek DF, Kay NE. VEGF receptor phosphorylation status and apoptosis is modulated by a green tea component, epigallocatechin-3-gallate (EGCG), in B-cell chronic lymphocytic leukemia. Blood. 2004;104:788-794.
8. Lee YK, Shanafelt TD, Bone ND, Strege AK, Jelinek DF, Kay NE. VEGF receptors on chronic lymphocytic leukemia (CLL) B cells interact with STAT 1 and 3: implication for apoptosis resistance. Leukemia. 2005;19:513-523.
9. Kay NE, Bone ND, Lee YK, et al. A recombinant IL-4-pseudomonas exotoxin inhibits protein synthesis and overcomes apoptosis resistance in human CLL B cells. Leuk Res. 2005;29:1009-1018.
10. Gasparini G, Longo R, Toi M, Ferrara N. Angiogenic inhibitors: a new therapeutic strategy in oncology. Nat Clin Pract Oncol. 2005;2:562-577. (Pubitemid 41721816)
11. Skinner HD, Zheng JZ, Fang J, Agani F, Jiang BH. Vascular endothelial growth factor transcriptional activation is mediated by hypoxia-inducible factor 1alpha, HDM2, and p70S6K1 in response to phosphatidylinositol 3-kinase/AKT signaling. J Biol Chem. 2004;279:45643-45651. (Pubitemid 39491552)
12. Nilsson I, Shibuya M, Wennstrom S. Differential activation of vascular genes by hypoxia in primary endothelial cells. Exp Cell Res. 2004;299: 476-485. (Pubitemid 39179813)
13. Calin GA, Liu CG, Sevignani C, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci U S A. 2004;101:11755-11760. (Pubitemid 39095368)
14. Bemis L, Chan DA, Finkielstein CV, et al. Distinct aerobic and hypoxic mechanisms of HIF-alpha regulation by CSN5. Genes Dev. 2004;18:739-744. (Pubitemid 38480886)
15. Nelson JD, Denisenko O, Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc. 2006;1:179-185.
16. Gray MJ, Zhang J, Ellis LM, et al. HIF-1alpha, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene. 2005;24:3110-3120. (Pubitemid 40695080)
17. Pichiorri F, Suh SS, Ladetto M, et al. MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc Natl Acad Sci U S A. 2008;105:12885-12890.
18. Escuin D, Simons JW, Giannakakou P. Exploitation of the HIF axis for cancer therapy. Cancer Biol Ther. 2004;3:608-611. (Pubitemid 41351095)
19. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1: interaction between H-ras and hypoxia. J Biol Chem. 2001;276:9519-9525. (Pubitemid 37385542)
20. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001;294:1337-1340.
21. Pugh CW, Ratcliffe PJ. The von Hippel-Lindau tumor suppressor, hypoxia-inducible factor-1 (HIF-1) degradation, and cancer pathogenesis. Semin Cancer Biol. 2003;13:83-89.
22. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 2003;9:677-684.
23. Metzen E, Stiehl DP, Doege K, Marxsen JH, Hellwig-Burgel T, JelkmannW. Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: identification of a functional hypoxiaresponsive element. Biochem J. 2005;387:711-717.
24. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssegur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 2003;22: 4082-4090.
25. Kuwai T, Kitadai Y, Tanaka S, Hiyama T, Tanimoto K, Chayama K. Mutation of the von Hippel-Lindau (VHL) gene in human colorectal carcinoma: association with cytoplasmic accumulation of hypoxia-inducible factor (HIF)-1alpha. Cancer Sci. 2004;95:149-153.
26. Calin GA, Ferracin M, Cimmino A, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353:1793-1801.
27. Niu G, Wright KL, Huang M, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene. 2002;21:2000-2008.
28. Wei D, Le X, Zheng L, et al. Stat3 activation regulates the expression of vascular endothelial growth factor and human pancreatic cancer angiogenesis and metastasis. Oncogene. 2003;22: 319-329.
29. Arany Z, Huang LE, Eckner R, et al. An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci U S A. 1996;93:12969-12973.
30. Schuringa JJ, Schepers H, Vellenga E, Kruijer W. Ser727-dependent transcriptional activation by association of p300 with STAT3 upon IL-6 stimulation. FEBS Lett. 2001;495:71-76.
31. Choi KS, Bae MK, Jeong JW, Moon HE, Kim KW. Hypoxia-induced angiogenesis during carcinogenesis. J Biochem Mol Biol. 2003;36:120-127.
32. Kato H, Tamamizu-Kato S, Shibasaki F. Histone deacetylase 7 associates with hypoxia-inducible factor 1alpha and increases transcriptional activity. J Biol Chem. 2004;279:41966-41974.
33. Ringshausen I, Schneller F, Bogner C, et al. Constitutively activated phosphatidylinositol-3 kinase (PI-3K) is involved in the defect of apoptosis in B-CLL: association with protein kinase C-delta. Blood. 2002;100:3741-3748. (Pubitemid 35303946)
34. Frank DA, Mahajan S, Ritz J. B lymphocytes from patients with chronic lymphocytic leukemia contain signal transducer and activator of transcription (STAT) 1 and STAT3 constitutively phosphorylated on serine residues. J Clin Invest. 1997; 100:3140-3148. (Pubitemid 28022852)
35. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721-732.
36. Niu G, Briggs J, Deng J, et al. Signal transducer and activator of transcription 3 is required for hypoxia-inducible factor-1alpha RNA expression in both tumor cells and tumor-associated myeloid cells. Mol Cancer Res. 2008;6:1099-1105.
37. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature. 2008;455:58-63.
38. Pagès G, Pouyssegur J. Transcriptional regulation of the vascular endothelial growth factor gene-a concert of activating factors. Cardiovasc Res. 2005;65:564-573.
39. Kiriakidis S, Andreakos E, Monaco C, Foxwell B, Feldmann M, Paleolog E. VEGF expression in human macrophages is NF-kappaB-dependent: studies using adenoviruses expressing the endogenous NF-kappaB inhibitor IkappaBalpha and a kinase-defective form of the IkappaB kinase 2. J Cell Sci. 2003;116:665-674. (Pubitemid 36231305)
40. Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16:4604-4613. (Pubitemid 26272112)
41. Büchler P, Reber HA, Buchler M, et al. Hypoxia-inducible factor 1 regulates vascular endothelial growth factor expression in human pancreatic cancer. Pancreas. 2003;26:56-64. (Pubitemid 36020267)
42. Abraham SE, Lobo S, Yaciuk P, Wang HG, Moran E. p300, and p300-associated proteins, are components of TATA-binding protein (TBP) complexes. Oncogene. 1993;8:1639-1647. (Pubitemid 23189061)
43. Merika M, Williams AJ, Chen G, Collins T, Thanos D. Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription. Mol Cell. 1998;1:277-287. (Pubitemid 128378668)
44. Nakashima K, Yanagisawa M, Arakawa H, et al. Synergistic signaling in fetal brain by STAT3- Smad1 complex bridged by p300. Science. 1999; 284:479-482. (Pubitemid 29289619)
45. Höpfl G, Ogunshola O, Gassmann M. HIFs and tumors: causes and consequences. Am J Physiol Regul Integr Comp Physiol. 2004;286:R608-623.
46. Blagosklonny MV. Antiangiogenic therapy and tumor progression. Cancer Cell. 2004;5:13-17.
47. Akakura N, Kobayashi M, Horiuchi I, et al. Constitutive expression of hypoxia-inducible factor- 1alpha renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Research. 2001;61:6548-6554. (Pubitemid 32783263)
48. Salnikow K, Costa M, Figg WD, Blagosklonny MV. Hyperinducibility of hypoxia-responsive genes without p53/p21-dependent checkpoint in aggressive prostate cancer. Cancer Research. 2000;60:5630-5634. (Pubitemid 30808293)
49. Byrd JC, Stilgenbauer S, Flinn IW. Chronic lymphocytic leukemia. Hematology. 2004:163-183.