Tumor microvasculature with endothelial fenestrations in VHL null clear cell renal cell carcinomas as a potent target of anti-angiogenic therapy

Cancer Science

Volumn 103, Issue 11, 2012, Pages 2027-2037

  Yamasaki, Toshinari ^a   Kamba, Tomomi ^a   Kanno, Toru ^a   Inoue, Takahiro ^a   Shibasaki, Noboru ^a   Arakaki, Ryuichiro ^a   Yamada, Tomomi ^b   Kondo, Keiichi ^c   Kamoto, Toshiyuki ^d   Nishiyama, Hiroyuki ^e   Ogawa, Osamu ^a   Nakamura, Eijiro ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; BEVACIZUMAB; MAB 679; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC THERAPY; ARTICLE; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG SCREENING; ENDOTHELIUM CELL; FEMALE; HUMAN; KIDNEY CARCINOMA; MALE; MICROVASCULATURE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TUMOR VASCULARIZATION; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAPILLARIES; CARCINOMA, RENAL CELL; CELL HYPOXIA; CHEMOKINE CCL2; FEMALE; HUMANS; KIDNEY NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROVESSELS; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84868213294     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2012.02412.x     Document Type: Article

References (42)

1. Cohen HT, McGovern FJ. Renal-cell carcinoma. N Engl J Med 2005; 353: 2477-90.
2. Kim WY, Kaelin WG. Role of VHL gene mutation in human cancer. J Clin Oncol 2004; 22: 4991-5004.
3. Gnarra JR, Zhou S, Merrill MJ et al. Post-transcriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene. Proc Nat Acad Sci USA 1996; 93: 10589-94.
4. Gunaratnam L, Morley M, Franovic A et al. 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 2003; 278: 44966-74.
5. Kaelin WG Jr. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 2008; 8: 865-73.
6. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-76.
7. Motzer RJ, Hutson TE, Tomczak P et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007; 356: 115-24.
8. Escudier B, Pluzanska A, Koralewski P et al. Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial. Lancet 2007; 370: 2103-11.
9. Escudier B, Eisen T, Stadler WM et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356: 125-34.
10. Brugarolas J. Renal-cell carcinoma-molecular pathways and therapies. N Engl J Med 2007; 356: 185-7.
11. Yang JC, Haworth L, Sherry RM et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 2003; 349: 427-34.
12. Rini BI, Atkins MB. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol 2009; 10: 992-1000.
13. Kamba T, Tam BY, Hashizume H et al. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am J Physiol Heart Circ Physiol 2006; 290: H560-76.
14. Inai T, Mancuso M, Hashizume H et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004; 165: 35-52.
15. Hamano K, Esumi M, Igarashi H et al. Biallelic inactivation of the von Hippel-Lindau tumor suppressor gene in sporadic renal cell carcinoma. Journal Urol 2002; 167: 713-7.
16. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Nat Acad Sci USA 1996; 93: 9821-6.
17. Iliopoulos O, Levy AP, Jiang C, Kaelin WG Jr, Goldberg MA. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc Nat Acad Sci USA 1996; 93: 10595-9.
18. Nakamura E, Abreu-e-Lima P, Awakura Y et al. Clusterin is a secreted marker for a hypoxia-inducible factor-independent function of the von Hippel-Lindau tumor suppressor protein. Am J Pathol 2006; 168: 574-84.
19. Kondo K, Kim WY, Lechpammer M, Kaelin WG Jr. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biol 2003; 1: E83.
20. 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 2002; 1: 237-46.
21. Shen C, Beroukhim R, Schumacher SE et al. Genetic and functional studies implicate HIF1alpha as a 14q kidney cancer suppressor gene. Cancer Discov 2011; 1: 222-35.
22. Gerber HP, Ferrara N. Pharmacology and pharmacodynamics of bevacizumab as monotherapy or in combination with cytotoxic therapy in preclinical studies. Cancer Res 2005; 65: 671-80.
23. Lu X, Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J Biol Chem 2009; 284: 29087-96.
24. Turner KJ, Moore JW, Jones A et al. Expression of hypoxia-inducible factors in human renal cancer: relationship to angiogenesis and to the von Hippel-Lindau gene mutation. Cancer Res 2002; 62: 2957-61.
25. Weidner N. Intratumor microvessel density as a prognostic factor in cancer. Am J Pathol 1995; 147: 9-19.
26. Kanno T, Kamba T, Yamasaki T et al. JunB promotes cell invasion and angiogenesis in VHL-defective renal cell carcinoma. Oncogene 2012; 31: 3098-110.
27. Gumz ML, Zou H, Kreinest PA et al. Secreted frizzled-related protein 1 loss contributes to tumor phenotype of clear cell renal cell carcinoma. Clin Cancer Res 2007; 13: 4740-9.
28. Gordan JD, Lal P, Dondeti VR et al. HIF-alpha effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma. Cancer Cell 2008; 14: 435-46.
29. Yang H, Minamishima YA, Yan Q et al. pVHL acts as an adaptor to promote the inhibitory phosphorylation of the NF-kappaB agonist Card9 by CK2. Mol Cell 2007; 28: 15-27.
30. Flaherty KT, Rosen MA, Heitjan DF et al. Pilot study of DCE-MRI to predict progression-free survival with sorafenib therapy in renal cell carcinoma. Cancer Biol Ther 2008; 7: 496-501.
31. Eriksson A, Cao R, Roy J et al. Small GTP-binding protein Rac is an essential mediator of vascular endothelial growth factor-induced endothelial fenestrations and vascular permeability. Circulation 2003; 107: 1532-8.
32. Choueiri TK, Vaziri SA, Jaeger E et al. von Hippel-Lindau gene status and response to vascular endothelial growth factor targeted therapy for metastatic clear cell renal cell carcinoma. Journal Urol 2008; 180: 860-5; discussion 5-6.
33. Rini BI, Jaeger E, Weinberg V et al. Clinical response to therapy targeted at vascular endothelial growth factor in metastatic renal cell carcinoma: impact of patient characteristics and Von Hippel-Lindau gene status. BJU Int 2006; 98: 756-62.
34. Cao R, Eriksson A, Kubo H, Alitalo K, Cao Y, Thyberg J. Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability. Circ Res 2004; 94: 664-70.
35. DeLeve LD, Wang X, Hu L, McCuskey MK, McCuskey RS. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol 2004; 287: G757-63.
36. Yokomori H, Oda M, Yoshimura K et al. Vascular endothelial growth factor increases fenestral permeability in hepatic sinusoidal endothelial cells. Liver Int 2003; 23: 467-75.
37. Maharaj AS, D'Amore PA. Roles for VEGF in the adult. Microvasc Res 2007; 74: 100-13.
38. Kurban G, Hudon V, Duplan E, Ohh M, Pause A. Characterization of a von Hippel Lindau pathway involved in extracellular matrix remodeling, cell invasion, and angiogenesis. Cancer Res 2006; 66: 1313-9.
39. Verheul HM, van Erp K, Homs MY et al. The relationship of vascular endothelial growth factor and coagulation factor (fibrin and fibrinogen) expression in clear cell renal cell carcinoma. Urology 2010; 75: 608-14.
40. Cao R, Brakenhielm E, Wahlestedt C, Thyberg J, Cao Y. Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF. Proc Nat Acad Sci USA 2001; 98: 6390-5.
41. Willett CG, Boucher Y, di Tomaso E et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004; 10: 145-7.
42. Jubb AM, Harris AL. Biomarkers to predict the clinical efficacy of bevacizumab in cancer. Lancet Oncol 2010; 11: 1172-83.