Mitochondrial DNA mutations distinguish bilateral multifocal renal oncocytomas from familial Birt-Hogg-Dubé tumors

Modern Pathology

Volumn 28, Issue 11, 2015, Pages 1458-1469

  Lang, Martin ^a   Vocke, Cathy D ^a   Merino, Maria J ^a   Schmidt, Laura S ^a,b   Linehan, W Marston ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; BILATERAL MULTIFOCAL RENAL ONCOCYTOMA; BIRT HOGG DUBE SYNDROME; DIFFERENTIAL DIAGNOSIS; DNA SEQUENCE; GENE MUTATION; GENOTYPE; HUMAN; KIDNEY BIOPSY; MAJOR CLINICAL STUDY; MITOCHONDRIAL GENOME; MULTIPLE CANCER; ONCOCYTOMA; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; SOMATIC MUTATION; ADENOMA, OXYPHILIC; AGED; COMPLICATION; DNA MUTATIONAL ANALYSIS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; MUTATION; POLYMERASE CHAIN REACTION;

ADENOMA, OXYPHILIC; AGED; BIRT-HOGG-DUBE SYNDROME; DIAGNOSIS, DIFFERENTIAL; DNA MUTATIONAL ANALYSIS; DNA, MITOCHONDRIAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; MUTATION; POLYMERASE CHAIN REACTION;

EID: 84946500158     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2015.101     Document Type: Article

References (43)

1. Schon EA, DiMauro S, Hirano M. Human mitochondrial DNA: roles of inherited and somatic mutations. Nat Rev Genet 2012;13:878-890.
2. Garcia-Rodriguez LJ. Appendix 1. Basic properties of mitochondria. Methods Cell Biol 2007;80:809-812.
3. Handschin C, Spiegelman BM. Peroxisome proliferatoractivated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocrine Rev 2006;27:728-735.
4. Linehan WM, Bratslavsky G, Pinto PA et al. Molecular diagnosis and therapy of kidney cancer. Annu Rev Med 2010;61:329-343.
5. Sahni VA, Silverman SG. Biopsy of renal masses: when and why. Cancer Imaging 2009;9:44-55.
6. Trpkov K, Yilmaz A, Uzer D et al. Renal oncocytoma revisited: a clinicopathological study of 109 cases with emphasis on problematic diagnostic features. Histopathology 2010;57:893-906.
7. Yusenko MV. Molecular pathology of renal oncocytoma: a review. Int J Urol 2010;17:602-612.
8. Kurelac I, MacKay A, Lambros MB et al. Somatic complex I disruptive mitochondrial DNA mutations are modifiers of tumorigenesis that correlate with low genomic instability in pituitary adenomas. Hum Mol Genet 2013;22:226-238.
9. Bonora E, Porcelli AM, Gasparre G et al. Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. Cancer Res 2006;66:6087-6096.
10. Gasparre G, Porcelli AM, Bonora E et al. Disruptive mitochondrial DNA mutations in complex I subunits are markers of oncocytic phenotype in thyroid tumors. Proc Natl Acad Sci USA 2007;104: 9001-9006.
11. Mayr JA, Meierhofer D, Zimmermann F et al. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res 2008;14: 2270-2275.
12. Simonnet H, Demont J, Pfeiffer K et al. Mitochondrial complex I is deficient in renal oncocytomas. Carcinogenesis 2003;24:1461-1466.
13. Gasparre G, Hervouet E, de Laplanche E et al. Clonal expansion of mutated mitochondrial DNA is associated with tumor formation and complex I deficiency in the benign renal oncocytoma. Hum Mol Genet 2008;17: 986-995.
14. Yusenko MV, Ruppert T, Kovacs G. Analysis of differentially expressed mitochondrial proteins in chromophobe renal cell carcinomas and renal oncocytomas by 2-D gel electrophoresis. Int J Biol Sci 2010;6: 213-224.
15. Gasparre G, Kurelac I, Capristo M et al. A mutation threshold distinguishes the antitumorigenic effects of the mitochondrial gene MTND1, an oncojanus function. Cancer Res 2011;71:6220-6229.
16. Meierhofer D, Mayr JA, Fink K et al. Mitochondrial DNA mutations in renal cell carcinomas revealed no general impact on energy metabolism. Br J Cancer 2006;94:268-274.
17. Nagy A, Wilhelm M, Sukosd F et al. Somatic mitochondrial DNA mutations in human chromophobe renal cell carcinomas. Genes Chromosomes Cancer 2002;35:256-260.
18. Davis CF, Ricketts CJ, Wang M et al. The somatic genomic landscape of chromophobe renal cell carcinoma. Cancer Cell 2014;26:319-330.
19. He Y, Wu J, Dressman DC et al. Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 2010;464:610-614.
20. McMahon S, Laframboise T. Mutational patterns in the breast cancer mitochondrial genome, with clinical correlates. Carcinogenesis 2014;35:1046-1054.
21. Larman TC, DePalma SR, Hadjipanayis AG et al. Spectrum of somatic mitochondrial mutations in five cancers. Proc Natl Acad Sci USA 2012;109: 14087-14091.
22. Yadav N, Chandra D. Mitochondrial DNA mutations and breast tumorigenesis. Biochim Biophys Acta 2013;1836:336-344.
23. Warfel KA, Eble JN. Renal oncocytomatosis. J Urol 1982;127:1179-1180.
24. Tickoo SK, Reuter VE, Amin MB et al. Renal oncocytosis: a morphologic study of fourteen cases. Am J Surg Pathol 1999;23:1094-1101.
25. Adamy A, Lowrance WT, Yee DS et al. Renal oncocytosis: management and clinical outcomes. J Urol 2011;185:795-801.
26. Kuroda N, Tanaka A, Ohe C et al. Review of renal oncocytosis (multiple oncocytic lesions) with focus on clinical and pathobiological aspects. Histol Histopathol 2012;27:1407-1412.
27. Gobbo S, Eble JN, Delahunt B et al. Renal cell neoplasms of oncocytosis have distinct morphologic, immunohistochemical, and cytogenetic profiles. Am J Surg Pathol 2010;34:620-626.
28. Hasumi H, Baba M, Hasumi Y et al. Regulation of mitochondrial oxidative metabolism by tumor suppressor FLCN. J Natl Cancer Inst 2012;104:1750-1764.
29. Rubino F, Piredda R, Calabrese FM et al. HmtDB, a genomic resource for mitochondrion-based human variability studies. Nucleic Acids Res 2012;40: D1150-D1159.
30. Ruiz-Pesini E, Lott MT, Procaccio V et al. An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Res 2007;35:D823-D828.
31. Adzhubei IA, Schmidt S, Peshkin L et al. A method and server for predicting damaging missense mutations. Nat Methods 2010;7:248-249.
32. Kurelac I, Lang M, Zuntini R et al. Searching for a needle in the haystack: comparing six methods to evaluate heteroplasmy in difficult sequence context. Biotechnol Adv 2012;30:363-371.
33. Baba M, Furihata M, Hong SB et al. Kidney-targeted Birt-Hogg-Dube gene inactivation in a mouse model: Erk1/2 and Akt-mTOR activation, cell hyperproliferation, and polycystic kidneys. J Natl Cancer Inst 2008;100:140-154.
34. Gasparre G, Porcelli AM, Lenaz G et al. Relevance of mitochondrial genetics and metabolism in cancer development. Cold Spring Harb Perspect Biol 2013;5.
35. Thoenes W, Storkel S, Rumpelt HJ et al. Chromophobe cell renal carcinoma and its variants-a report on cases. J Pathology 1988;155:277-287.
36. Vocke CD, Yang Y, Pavlovich CP et al. High frequency of somatic frameshift BHD gene mutations in Birt-Hogg-Dube-associated renal tumors. J Natl Cancer Inst 2005;97:931-935.
37. Nickerson ML, Warren MB, Toro JR et al. Mutations in a novel gene lead to kidney tumors, lung wall defects, and benign tumors of the hair follicle in patients with the Birt-Hogg-Dube syndrome. Cancer Cell 2002;2: 157-164.
38. Pavlovich CP, Walther MM, Eyler RA et al. Renal tumors in the Birt-Hogg-Dube syndrome. Am J Surg Pathol 2002;26:1542-1552.
39. Klomp JA, Petillo D, Niemi NM et al. Birt-Hogg-Dube renal tumors are genetically distinct from other renal neoplasias and are associated with up-regulation of mitochondrial gene expression. BMC Med Genomics 2010;3:59.
40. Pradella LM, Lang M, Kurelac I et al. Where Birt-Hogg-Dube meets Cowden syndrome: mirrored genetic defects in two cases of syndromic oncocytic tumours. Eur J Hum Genet 2013;21:1169-1172.
41. Gasparre G, Romeo G, Rugolo M et al. Learning from oncocytic tumors: why choose inefficient mitochondria? Biochim Biophys Acta 2011;1807:633-642.
42. Gomez-Roca CA, Lacroix L, Massard C et al. Sequential research-related biopsies in phase I trials: acceptance, feasibility and safety. Ann Oncol 2012;23: 1301-1306.
43. Maki J, Robinson K, Reguly B et al. Mitochondrial genome deletion aids in the identification of false-and true-negative prostate needle core biopsy specimens. Am J Clin Pathol 2008;129:57-66.