A role for mitochondrial enzymes in inherited neoplasia and beyond

Nature Reviews Cancer

Volumn 3, Issue 3, 2003, Pages 193-202

  Eng, Charis ^a,b   Kiuru, Maija ^c   Fernandez, Magali J ^a   Aaltonen, Lauri A ^c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c BIOMEDICUM HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FUMARATE HYDRATASE; MITOCHONDRIAL ENZYME; SUCCINATE DEHYDROGENASE; FREE RADICAL; MULTIENZYME COMPLEX; OXIDOREDUCTASE; PROTEIN SUBUNIT; SUCCINATE DEHYDROGENASE (UBIQUINONE);

CANCER SUSCEPTIBILITY; CARCINOGENESIS; CITRIC ACID CYCLE; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; NEOPLASM; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANGIOGENESIS; APOPTOSIS; ENERGY METABOLISM; ENZYMOLOGY; FAMILIAL CANCER; FORECASTING; GENETICS; HETEROZYGOTE; HOMOZYGOTE; HUMAN; KIDNEY CARCINOMA; KIDNEY TUMOR; LEIOMYOMATOSIS; MITOCHONDRIAL ENCEPHALOMYOPATHY; MITOCHONDRION; MUTATION; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PHYSIOLOGY;

APOPTOSIS; CARCINOMA, RENAL CELL; CITRIC ACID CYCLE; ELECTRON TRANSPORT COMPLEX II; ENERGY METABOLISM; FORECASTING; FREE RADICALS; FUMARATE HYDRATASE; HETEROZYGOTE; HOMOZYGOTE; HUMANS; KIDNEY NEOPLASMS; LEIOMYOMATOSIS; MITOCHONDRIA; MITOCHONDRIAL ENCEPHALOMYOPATHIES; MULTIENZYME COMPLEXES; MUTATION; NEOPLASTIC SYNDROMES, HEREDITARY; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDOREDUCTASES; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PROTEIN SUBUNITS; SUCCINATE DEHYDROGENASE;

EID: 0037364314     PISSN: 1474175X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrc1013     Document Type: Review

References (61)

1. Latif, F. et al. Identification of the von Hippel-Lindau disease tumor suppressor gene Science 260, 1317-1320 (1993).
2. Mulligan, L. M. et al. Specific mutations of the RET protooncogene are related to disease phenotype in MEN 2A and FMTC. Nature Genet. 6, 70-74 (1994).
3. Eng, C. et al. The relationship between specific RET protooncogene mutations and disease phenotype in multiple endocrine neoplasia type 2: International RET Mutation Consortium analysis. JAMA 276, 1575-1579 (1996).
4. Kroll, A. J., Alexander, B., Cochios, F. & Pechet, L Hereditary deficiencies of clotting factors VII and X associated with carotid-body tumors. N. Engl. J. Med. 270, 6-13 (1964).
5. van der Mey, A. G., Maaswinkel-Mooy, P. D., Cornelisse, C. J., Schmidt, P. H. & van de Kamp, J. J. Genomic imprinting in hereditary glomus tumours: evidence for new genetic theory. Lancet 2, 1291-1294 (1989).
6. Heutink, P. et al. A gene subject to genomic imprinting and responsible for hereditary paragangliomas maps to 11q23-qter. Hum. Mol. Genet. 1, 7-10 (1992).
7. Heutink, P., van Schothorst, E. M. & van der Mey, A. G. L. Further localization of the gene for hereditary paragangliomas and evidence for linkage in unrelated families. Eur. J. Hum. Genet. 2, 148-158 (1994).
8. Baysal, B. E. et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848-851 (2000). Identification of SDHD as the susceptiblity gene for 11q-linked hereditary paraganglioma families. SDHD is the first nuclear gene that encodes a mitochondrial component and that has been shown to be involved in a cancer-susceptiblity syndrome.
9. Gimm, O., Armanios, M., Dziema, H., Neumann, H. P. H. & Eng, C. Somatic and occult germline mutations in SDHD, a mitochondrial complex II gene, in non-familial pheochromocytomas. Cancer Res. 60, 6822-6825 (2000).
10. Neumann, H. P. H. et al. Germ-line mutations in nonsyndromic pheochromocytoma. N. Engl. J. Med. 346, 1459-1466 (2002). Population-based study showing that 25% of unrelated non-syndromic, non-familial phaeochromocytoma cases are due to germline mutations in one of four genes, including SDHD and SDHB.
11. Baysal, B. E. et al. Prevalence of SDHB, SDHC and SDHD in clinic patients with head and neck paragangliomas. J. Med. Genet. 39, 178-183 (2002).
12. Niemann, S. & Muller, U. Mutations in SDHC cause autosomal dominant paraganglioma. Nature Genet. 26, 141-150 (2000).
13. Astuti, D. et al. Mutations in the mitochondrial complex II subunit SDHB cause susceptibility to familial paraganglioma and pheochromocytoma. Am. J. Hum. Genet. 69, 49-54 (2001). Identification of SDHB as the susceptibility gene for familial paraganglioma and/or phaeochromocytoma.
14. Baysal, B. E. Hereditary paraganglioma targets diverse paranglia. J. Med. Genet. 39, 617-622 (2002).
15. Kiuru, M. et al. Familial cutaneous leiomyomatosis is a two-hit condition associated with renal cell cancer of characteristic histopathology. Am. J. Pathol. 159, 825-829 (2001).
16. Launonen, V. et al. Inherited susceptibility to uterine leiomyomas and renal cell cancer Proc. Natl Acad. Sci. USA 98, 3387-3392 (2001).
17. Delahunt, B. & Eble, J. N. Renal cell neoplasia. Pathology 34, 13-20 (2002).
18. Kiuru, M. et al. Few FH mutations in sporadic counterparts of tumor types observed in hereditary leiomyomatosis and renal cell cancer families. Cancer Res. 62, 4554-4557 (2002).
19. Tomlinson, I. P. M. T. et al. Germline mutations in the fumarate hydratase gene predispose to dominantly inherited uterine fibroids, skin leiomyomata and renal cell cancer. Nature Genet. 30, 406-410 (2002). Identification of germline heterozygous mutations in FH that cause susceptibility to HLRCC.
20. Alam, N. A. et al. Localization of a gene (MCUL1) for multiple cutaneous leiomyomata and uterine fibroids to chromosome 1q42.3-q42. Am. J. Hum. Genet. 68, 1264-1269 (2001).
21. Gimenez-Roqueplo, A.-P. et al. The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes enzymatic activity of the complex II mitochondrial respiratory chain and activates the hypoxia pathway. Am. J. Hum. Genet. 69, 1186-1197 (2001). First demonstration of loss of enzymatic activity as a consequence of SDHD mutation and consequent alterations in molecules in the HIF pathway.
22. Gimenez-Roqueplo, A. P. et al. Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J. Clin. Endocrinol. Metab. 87, 4771-4774 (2002).
23. Maher, E. R. & Eng, C. The pressure rises: update on the genetics of phaeochromocytoma. Hum. Mol. Genet. 11, 2347-2354 (2002).
24. Schapira, A. H. Mitochondrial dysfunction in neurodegenerative disorders. Biochim. Biophys. Acta 1366, 225-233 (1998).
25. Leigh, D. Subacute necrotizing encephalomyelopathy in an infant. J. Neurol. Neurosurg. Psychiatr. 14, 216-221 (1951).
26. Bourgeron, T. et al. Mutation of the fumarase gene in two siblings with progressive encephalopathy and fumarase deficiency. J. Clin. Invest. 93, 2514-2518 (1994).
27. Parfait, B. et al. Compound heterozygous mutations in the flavoprotein gene of the respiratory chain complex II in a patient with Leigh syndrome. Hum. Genet. 106, 236-243 (2000).
28. Ackrell, B. A. C. Progress in understanding structure-function relationships in respiratory chain complex II. FEBS Lett. 466, 1-5 (2000).
29. Oyedotun, K. S. & Lemire, B. D. The quinone-binding sites of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase. J. Biol. Chem. 276, 16936-16943 (2001).
30. Iverson, T. M., Luna-Chavez, C., Cecchini, G. & Rees, D. C. Structure of the Escherichia coli fumarate reductase complex. Science 284, 1961-1966 (1999).
31. Vinogradov, A. D., Ackrell, B. A. C. & Singer, T. P. On the possible interrelations of the reactivity of soluble succinate dehydrogenase with ferricyanide, reconstitution activity and the Hipip iron-sulfur center. Biochem. Biophys. Res. Comm. 67, 803-809 (1975).
32. Schmidt, D. M., Saghbini, M. & Scheffler, I. E. The C-terminus of the succinate dehydrogenase IP peptide of the Saccharomyces cerevisiae is significant for assembly of complex II. Biochemistry 31, 8442-8448 (1992).
33. Arias-Sella, J. & Valcarcel, J. Chief cell hyperplasia in the human carotid body at high altitudes: physiologic and pathologic significance. Hum. Pathol. 7, 361-373 (1976).
34. Chandel, N. S. et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl Acad. Sci. USA 95, 11715-11720 (1998).
35. Clifford, S. C. et al. Contrasting effects on HIF-1α by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease. Hum. Mol. Genet. 10, 1029-1038 (2001).
36. Hoffman, M. A. et al. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum. Mol. Genet. 10, 1019-1027 (2001).
37. Teipel, J. W. & Hunt, R. L. The subunit interactions of fumarase. J. Biol. Chem. 246, 4859-4865 (1971).
38. van den Heuvel, L. et al. Demonstration of a new pathogenic mutation in human complex I deficiency: a 5-bp duplication in the nuclear gene encoding the 18kD (AQDQ) subunit. Am. J. Hum. Genet. 62, 262-268 (1998).
39. Loeffen, J. et al. The first nuclear-encoded complex I mutation in a patient with Leigh syndrome. Am. J. Hum. Genet. 63, 1598-1608 (1998).
40. Triepels, R. H., van den Heuvel, L. & Loeffen, J. Leigh syndrome associated with a mutation in the NDUFS7 (PSST) nuclear encoded subunit of complex I. Ann. Neurol. 45, 787-790 (1999).
41. Tiranti, V. et al. Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am. J. Hum. Genet. 63, 1609-1621 (1998).
42. Valnot, I., von Kleist-Retzow, J. C. & Barrientos, A. A mutation in the human heme A:farnesyltransferrase gene (COX 10) causes cytochrome c oxidase deficiency. Hum. Mol. Genet. 9, 1245-1249 (2000).
43. van Loo, G. et al. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9, 1031-1042 (2002).
44. Ravagnan, L., Roumier, T. & Kroemer G. Mitochondria, the killer organelles and their weapons. J. Cell. Physiol. 192. 131-137 (2002).
45. López-Barneo, J., Pardal, R. & Ortega-Sáez, P. Cellular mechanisms of oxygen sensing. Annu. Rev. Physiol. 63, 259-287 (2001).
46. Miramar, M. D. et al. NADH-oxidase activity of mitochondrial apoptosis inducing factor (AIF). J. Biol. Chem. 276, 16391-16398 (2001).
47. Scheulke, M., Smeitink, J. & Mariman, E. Mutant NDUFV1 subunit of mitochondrial complex I causes leukodystrophy and myoclonic epilepsy. Nature Genet. 21, 260-261 (1999).
48. Benit, P. et al. Large-scale deletion and point mutations of the nuclear NDUFV1 and NDUFS1 genes in mitochondrial complex I deficiency. Am. J. Hum. Genet. 68, 1344-1352 (2001).
49. Loeffen, J. et al. Mutations in the complex I NDUFS2 gene of patients with cardiomyopathy and encphalomyopathy. Am. J. Hum. Genet. 49, 195-201 (2001).
50. de Lonlay, P. et al. A mutant mitochondrial respiratory chain assembly protein causes complex III deficiency in patients with tubulopathy, encephalopathy and liver failure. Nature Genet. 29, 57-60 (2001).
51. Papadopoulou, L. C., Sue, C. M. & Davidson, M. Fatal infantile cardioencephalomyopathy with cytochrome c oxidase (COX) deficiency due to mutations in SCO2, a human COX assembly gene. Nature Genet. 23, 333-337 (1999).
52. Valnot, I., Ormond, S. & Gigarel, N. Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase (COX) deficiency with neonatal-onset hepatic failure and encephalopathy. Am. J. Hum. Genet. 67, 1104-1109 (2000).
53. Servidei, S. Mitochondrial encephalomyopathies: gene mutation. Neuromuscul. Disord. 12, 224-229 (2001).
54. Green, D. R. & Reed, J. C. Mitochondria and apoptosis. Science 281, 1309-1312 (1998).
55. Yeh, J. J. et al. Two-dimensonal gene scanning of the mitochondrial genome reveals somatic mutations in papillary thyroid carcinomas and multiple sequence vanants in cases with sporadic thyroid tumors. Oncogene 19, 2060-2066 (2000).
56. Polyak, K. et al. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nature Genet. 20, 291-293 (1998).
57. Jeronimo, C. et al. Mitochondrial mutations in early state prostate cancer and bodily fluids. Oncogene 20, 5195-5198 (2001).
58. Kirches, E. et al. High frequency of mitochondrial DNA mutations in glioblastoma multiforme identified by direct sequence comparison to blood samples. Int. J. Cancer 93, 534-538 (2001).
59. Liu, V. W. et al. High incidence of somatic mitochondrial DNA mutations in human ovarian carcinomas. Cancer Res. 61, 5998-6001 (2001).
60. Maximo, V. et al. Microsatellite instability, mitochondrial DNA large deletions, and mitochondrial DNA mutations in gastric carcinoma. Gene Chromosom. Cancer 32, 136-143 (2001).
61. Parrella, P. et al. Detection of mitochondrial DNA mutations in primary breast cancer and fine-needle aspirates. Cancer Res. 61, 7623-7626 (2001).