Evidence of increased microvessel density and activation of the hypoxia pathway in tumours from the hereditary leiomyomatosis and renal cell cancer syndrome

Journal of Pathology

Volumn 205, Issue 1, 2005, Pages 41-49

  Pollard, Patrick ^a   Wortham, Noel ^a   Barclay, Ella ^a   Alam, Afrina ^a   Elia, George ^a   Manek, Sanjiv ^b   Poulsom, Richard ^a   Tomlinson, Ian ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Hereditary leiomyomatosis and renal cell cancer syndrome; Hypoxia; Microvessel density

Indexed keywords

PROTEIN BNIP3; THROMBOSPONDIN 1; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CARCINOGENESIS; CITRIC ACID CYCLE; CONTROLLED STUDY; FAMILIAL CANCER; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; KIDNEY CANCER; LEIOMYOMATOSIS; MICROVASCULATURE; MYOMETRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR GROWTH; UTERUS MYOMA; VASCULARIZATION;

ADULT; CARCINOMA, RENAL CELL; CELL HYPOXIA; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; KIDNEY NEOPLASMS; LEIOMYOMATOSIS; NEOPLASTIC SYNDROMES, HEREDITARY; NEOVASCULARIZATION, PATHOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; UTERINE NEOPLASMS;

EID: 11144284227     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1686     Document Type: Article

References (35)

1. Astuti D, Latif F, Dallol A, et al. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 2001; 69: 49-54.
2. Baysal BE, Ferrell RE, Willett-Brozick JE, et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000; 287: 848-851.
3. Niemann S, Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nature Genet 2000; 26: 268-270.
4. Yankovskaya V, Horsefield R, Tornroth S, et al. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 2003; 299: 700-704.
5. Tomlinson IP, Alam NA, Rowan AJ, et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nature Genet 2002; 30: 406-410.
6. Weaver T, Banaszak L. Crystallographic studies of the catalytic and a second site in fumarase C from Escherichia coli. Biochemistry 1996; 35: 13 955-13 965.
7. Weaver TM, Levitt DG, Donnelly MI, Stevens PP, Banaszak LJ. The multisubunit active site of fumarase C from Escherichia coli. Nature Struct Biol 1995; 2: 654-662.
8. Eng C, Kiuru M, Fernandez MJ, Aaltonen LA. A role for mitochondrial enzymes in inherited neoplasia and beyond. Nature Rev Cancer 2003; 3: 193-202.
9. Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399: 271-275.
10. Jones A, Fujiyama C, Blanche C, et al. Relation of vascular endothelial growth factor production to expression and regulation of hypoxia-inducible factor-1 alpha and hypoxia-inducible factor-2 alpha in human bladder tumors and cell lines. Clin Cancer Res 2001; 7: 1263-1272.
11. Brugarolas JB, Vazquez F, Reddy A, Sellers WR, Kaelin WG Jr. TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 2003; 4: 147-158.
12. Gimenez-Roqueplo AP, Favier J, Rustin P, et al. Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Res 2003; 63: 5615-5621.
13. Clifford SC, Maher ER. Von Hippel - Lindau disease: clinical and molecular perspectives. Adv Cancer Res 2001; 82: 85-105.
14. 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: 2957-2961.
15. Baysal BE. Hereditary paraganglioma targets diverse paraganglia. J Med Genet 2002; 39: 617-622.
16. Gimenez-Roqueplo AP, Favier J, Rustin P, et al. The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am J Hum Genet 2001; 69: 1186-1197.
17. Pollard PJ, Wortham NC, Tomlinson IP. The TCA cycle and tumorigenesis: the examples of fumarate hydratase and succinate dehydrogenase. Ann Med 2003; 35: 632-639.
18. Onita T, Ji PG, Xuan JW, et al. Hypoxia-induced, perinecrotic expression of endothelial Per-ARNT-Sim domain protein-1/hypoxia-inducible factor-2 alpha correlates with tumor progression, vascularization, and focal macrophage infiltration in bladder cancer. Clin Cancer Res 2002; 8: 471-480.
19. Berse B, Brown LF, Van de Water L, Dvorak HF, Senger DR. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol Biol Cell 1992; 3: 211-220.
20. Poulsom R, Longcroft JM, Jeffery RE, Rogers LA, Steel JH. A robust method for isotopic riboprobe in situ hybridisation to localise mRNAs in routine pathology specimens. Eur J Histochem 1998; 42: 121-132.
21. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 1999; 13: 9-22.
22. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246: 1306-1309.
23. Nor JE, Mitra RS, Sutorik MM, Mooney DJ, Castle VP, Polverini PJ. Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J Vasc Res 2000; 37: 209-218.
24. Miao WM, Seng WL, Duquette M, Lawler P, Laus C, Lawler J. Thrombospondin-1 type 1 repeat recombinant proteins inhibit tumor growth through transforming growth factor-beta-dependent and -independent mechanisms. Cancer Res 2001; 61: 7830-7839.
25. Chen H, Herndon ME, Lawler J. The cell biology a thrombospondin-1. Matrix Biol 2000; 19: 597-614.
26. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci U S A 2000; 97: 9082-9087.
27. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci U S A 2002; 99: 12825-12830.
28. Webster KA, Discher DJ, Kaiser S, Hernandez O, Sato B, Bishopric NH. Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J Clin Invest 1999; 104: 239-252.
29. Enomoto N, Koshikawa N, Gassmann M, Hayashi J, Takenaga K. Hypoxic induction of hypoxia-inducible factor-1 alpha and oxygen-regulated gene expression in mitochondrial DNA-depleted HeLa cells. Biochem Biophys Res Commun 2002; 297: 346-352.
30. Lin B, Kolluri SK, Lin F, et al. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 2004; 116: 527-540.
31. Poncelet C, Fauvet R, Feldmann G, Walker F, Madelenat P, Darai E. Prognostic value of von Willebrand factor, CD34, CD31, and vascular endothelial growth factor expression in women with uterine leiomyosarcomas. J Surg Oncol 2004; 86: 84-90.
32. Poncelet C, Madelenat P, Feldmann G, Walker F, Darai E. Expression of von Willebrand's factor, CD34, CD31, and vascular endothelial growth factor in uterine leiomyomas. Fertil Steril 2002; 78: 581-586.
33. Lehtonen R, Kiuru M, Vanharanta S, et al. Biallelic inactivation of fumarate hydratase (FH) occurs in nonsyndromic uterine leiomyomas but is rare in other tumors. Am J Pathol 2004; 164 17-22.
34. Kiuru M, Lehtonen R, Arola J, et al. Few FH mutations in sporadic counterparts of tumor types observed in hereditary leiomyomatosis and renal cell cancer families. Cancer Res 2002; 62: 4554-4557.
35. Barker KT, Bevan S, Wang R, et al. Low frequency of somatic mutations in the FH/multiple cutaneous leiomyomatosis gene in sporadic leiomyosarcomas and uterine leiomyomas. Br J Cancer 2002; 87: 446-448.