Generation of a mouse model of Von Hippel-Lindau kidney disease leading to renal cancers by expression of a constitutively active mutant of HIF1α

Cancer Research

Volumn 71, Issue 21, 2011, Pages 6848-6856

  Fu, Leiping ^a   Wang, Gang ^a   Shevchuk, Maria M ^a   Nanus, David M ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE IX; GLUTAMIC ACID; GLYCOGEN; HISTONE H2AX; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIPID; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CARCINOGENESIS; CD70 GENE; CELL COUNT; CELL PROLIFERATION; CLEAR CELL CARCINOMA; CONTROLLED STUDY; CYTOPLASM; DISEASE ASSOCIATION; DISEASE COURSE; ENDOTHELIUM CELL; GENE; GENE EXPRESSION; GENOMIC INSTABILITY; HIF1ALPHA GENE; HISTOPATHOLOGY; KIDNEY CARCINOMA; KIDNEY CELL; KIDNEY CYST; KIDNEY DISEASE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DISORDER; LIPID STORAGE; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TRANSGENIC MOUSE; TUMOR VASCULARIZATION; VON HIPPEL LINDAU DISEASE;

AMINO ACID SUBSTITUTION; ANIMALS; CARCINOMA, RENAL CELL; CELL DIVISION; CELL HYPOXIA; DISEASE MODELS, ANIMAL; GAMMA-GLUTAMYLTRANSFERASE; GENOMIC INSTABILITY; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY DISEASES, CYSTIC; KIDNEY NEOPLASMS; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTAGENESIS, SITE-DIRECTED; NEOVASCULARIZATION, PATHOLOGIC; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION; VON HIPPEL-LINDAU DISEASE;

EID: 80155184068     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1745     Document Type: Article

References (49)

1. Kaelin WG. Von hippel-lindau disease. Annu Rev Pathol 2007;2:145-73.
2. Maher ER, Yates JR, Harries R, Benjamin C, Harris R, Moore AT, et al. Clinical features and natural history of von Hippel-Lindau disease. Q J Med 1990;77:1151-63. (Pubitemid 20379533)
3. Kaelin WG Jr. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res 2007;13:680-4s.
4. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010;29:625-34.
5. Gordan JD, Simon MC. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr Opin Genet Dev 2007;17:71-7. (Pubitemid 46109295)
6. Mandriota SJ, Turner KJ, Davies DR, Murray PG, Morgan NV, Sowter HM, et al. HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 2002;1:459-68. (Pubitemid 41039126)
7. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
8. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271-5. (Pubitemid 29246458)
9. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001;292:464-8. (Pubitemid 32335941)
10. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001; 292:468-72. (Pubitemid 32335942)
11. Semenza GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007;2007:cm8.
12. Mahon PC, Hirota K, Semenza GL. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Gen Dev 2001;15:2675-86. (Pubitemid 32988878)
13. Dames SA, Martinez-Yamout M, DeGuzman RN, Dyson HJ, Wright PE. Structural basis for Hif-1 alpha/CBP recognition in the cellular hypoxic response. Proc Natl Acad Sci U S A 2002;99:5271-6. (Pubitemid 34411538)
14. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci U S A 2001;98:1583-8. (Pubitemid 32165542)
15. Kleymenova E, Everitt JI, Pluta L, Portis M, Gnarra JR, Walker CL. Susceptibility to vascular neoplasms but no increased susceptibility to renal carcinogenesis in Vhl knockout mice. Carcinogenesis 2004; 25:309-15. (Pubitemid 38344396)
16. Rankin EB, Tomaszewski JE, Haase VH. Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res 2006;66:2576-83.
17. Jacquemin E, Bulle F, Bernaudin JF, Wellman M, Hugon RN, Guellaen G, et al. Pattern of expression of gamma-glutamyl transpeptidase in rat liver and kidney during development: study by immunochemistry and in situ hybridization. J Pediatric Gastroenterol Nutr 1990;11:89-95. (Pubitemid 20203899)
18. Terzi F, Burtin M, Hekmati M, Federici P, Grimber G, Briand P, et al. Targeted expression of a dominant-negative EGF-R in the kidney reduces tubulo-interstitial lesions after renal injury. J Clin Invest 2000;106:225-34. (Pubitemid 30483126)
19. Liu L, Gudas LJ. Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin A deficiency. J Biol Chem 2005;280:40226-34. (Pubitemid 41779160)
20. Sheren-Manoff M, Shin SJ, Su D, Bok D, Rando RR, Gudas LJ. Reduced lecithin:retinol acyltransferase expression in human breast cancer. Int J Oncol 2006;29:1193-9.
21. Gillespie RF, Gudas LJ. Retinoic acid receptor isotype specificity in F9 teratocarcinoma stem cells results from the differential recruitment of coregulators to retinoic response elements. J Biol Chem 2007;282:33421-34. (Pubitemid 350159505)
22. Tang XH, Vivero M, Gudas LJ. Overexpression of CRABPI in suprabasal keratinocytes enhances the proliferation of epidermal basal keratinocytes in mouse skin topically treated with all-trans retinoic acid. Exp Cell Res 2008;314:38-51. (Pubitemid 350180773)
23. Sjolund J, Johansson M, Manna S, Norin C, Pietras A, Beckman S, et al. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo. J Clin Invest 2008;118:217-28.
24. Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994;79:1147-56.
25. Gebhard RL, Clayman RV, Prigge WF, Figenshau R, Staley NA, Reesey C, et al. Abnormal cholesterol metabolismin renal clear cell carcinoma. J Lipid Res 1987;28:1177-84. (Pubitemid 17151580)
26. Motzer RJ, Bander NH, Nanus DM. Renal-cell carcinoma. N Engl J Med 1996;335:865-75.
27. Montani M, Heinimann K, von Teichman A, Rudolph T, Perren A, Moch H. VHL-gene deletion in single renal tubular epithelial cells and renal tubular cysts: further evidence for a cyst-dependent progression pathway of clear cell renal carcinoma in von Hippel-Lindau disease. Am J Surg Pathol 2010;34:806-15.
28. Haase VH. The VHL tumor suppressor in development and disease: functional studies in mice by conditional gene targeting. Semin Cell Dev Biol 2005;16:564-74. (Pubitemid 41247880)
29. Newman PJ, Berndt MC, Gorski J, White GC 2nd, Lyman S, Paddock C, et al. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 1990;247:1219-22.
30. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev 2003;3: 721-32. (Pubitemid 37328811)
31. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000;60:7075-83. (Pubitemid 32059187)
32. Bui MH, Seligson D, Han KR, Pantuck AJ, Dorey FJ, Huang Y, et al. Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implications for prognosis and therapy. Clin Cancer Res 2003;9:802-11. (Pubitemid 36182618)
33. Sandlund J, Oosterwijk E, Grankvist K, Oosterwijk-Wakka J, Ljungberg B, Rasmuson T. Prognostic impact of carbonic anhydrase IX expression in human renal cell carcinoma. BJU Int 2007;100:556-60. (Pubitemid 47205465)
34. Adam PJ, Terrett JA, Steers G, Stockwin L, Loader JA, Fletcher GC, et al. CD70 (TNFSF7) is expressed at high prevalence in renal cell carcinomas and is rapidly internalised on antibody binding. Br J Cancer 2006;95:298-306. (Pubitemid 44187590)
35. Prelich G, Tan CK, Kostura M, Mathews MB, So AG, Downey KM, et al. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 1987;326:517-20. (Pubitemid 17055499)
36. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000;182:311-22. (Pubitemid 30054364)
37. Charames GS, Bapat B. Genomic instability and cancer. Curr Mol Med 2003;3:589-96. (Pubitemid 37236402)
38. Loeb KR, Loeb LA. Genetic instability and the mutator phenotype. Studies in ulcerative colitis. Am J Pathol 1999;154:1621-6. (Pubitemid 29262841)
39. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, et al. GammaH2AX and cancer. Nat Rev 2008;8: 957-67.
40. Wallace AC, Nairn RC. Renal tubular antigens in kidney tumors. Cancer 1972;29:977-81.
41. Dworniczak B, Skryabin B, Tchinda J, Heuck S, Seesing FJ, Metzger D, et al. Inducible Cre/loxP recombination in the mouse proximal tubule. Nephron Exp Nephrol 2007;106:e11-20. (Pubitemid 46701516)
42. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000;35:71-103. (Pubitemid 30253678)
43. Grabmaier K, MC AdW, Verhaegh GW, Schalken JA, Oosterwijk E. Strict regulation of CAIX(G250/MN) by HIF-1alpha in clear cell renal cell carcinoma. Oncogene 2004;23:5624-31. (Pubitemid 39093040)
44. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306-9. (Pubitemid 20066716)
45. Parkkila S. Significance of pH regulation and carbonic anhydrases in tumour progression and implications for diagnostic and therapeutic approaches. BJU Int 2008;101(Suppl 4):16-21.
46. McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet 2007;8:37-55.
47. Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME, et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 2004;24:8504-18. (Pubitemid 39245072)
48. Pascual D, Borque A. Epidemiology of kidney cancer. Adv Urol 2008:782381.
49. 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 2002;1:247-55. (Pubitemid 41039149)