Mitochondrial changes in endometrial carcinoma: Possible role in tumor diagnosis and prognosis (Review)
- Authors:
- Antonella Cormio
- Gennaro Cormio
- Clara Musicco
- Anna Maria Sardanelli
- Giuseppe Gasparre
- Maria Nicola Gadaleta
-
Affiliations: Department of Biosciences, Biotechnologies and Biopharmaceutics, University of Bari, Bari, Italy, Gynecologic Oncology Unit, IRCCS Istituto Oncologico ‘Giovanni Paolo II’, Bari, Italy, CNR-Institute of Biomembranes and Bioenergetics, Bari, Italy, Department of Basical Medical Sciences, Neurosciences and Sensory Organs, University of Bari, Bari, Italy, Department of Medical and Surgical Sciences, Unit of Medical Genetics, University of Bologna, Bologna, Italy - Published online on: December 22, 2014 https://doi.org/10.3892/or.2014.3690
- Pages: 1011-1018
This article is mentioned in:
Abstract
Hecht JL and Mutter GL: Molecular and pathologic aspects of endometrial carcinogenesis. J Clin Oncol. 24:4783–4791. 2006. View Article : Google Scholar : PubMed/NCBI | |
Matias-Guiu X, Catasus L, Bussaglia E, et al: Molecular pathology of endometrial hyperplasia and carcinoma. Hum Pathol. 32:569–577. 2001. View Article : Google Scholar : PubMed/NCBI | |
Murphy MP: How mitochondria produce reactive oxygen species. Biochem J. 417:1–13. 2009. View Article : Google Scholar | |
Brookes PS, Yoon Y, Robotham JL, Anders MW and Sheu SS: Calcium, ATP and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 287:C817–C833. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cadenas E and Davies K: Mitochondrial free radical generation, oxidative stress and aging. Free Radic Biol Med. 29:222–230. 2000. View Article : Google Scholar : PubMed/NCBI | |
Hüttemann M, Lee I, Samavati L, Yu H and Doan JW: Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta. 1773:1701–1720. 2007. View Article : Google Scholar | |
Warburg O: On respiratory impairment in cancer cells. Science. 124:269–270. 1956.PubMed/NCBI | |
Bonuccelli G, Tsirigos A, Whitaker-Menezes D, et al: Ketones and lactate ‘fuel’ tumor growth and metastasis: Evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle. 9:3506–3514. 2010. View Article : Google Scholar : PubMed/NCBI | |
Smolkova K, Plecita-Hlavata L, Bellance N, Benard G, Rossignol R and Jezek P: Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells. Int J Biochem Cell Biol. 43:950–968. 2011. View Article : Google Scholar | |
Pedersen PL: Tumor mitochondria and the bioenergetics of cancer cells. Prog Exp Tumor Res. 22:190–274. 1978.PubMed/NCBI | |
Yu M: Generation, function and diagnostic value of mitochondrial DNA copy number alterations in human cancer. Life Sci. 89:65–71. 2011. View Article : Google Scholar : PubMed/NCBI | |
Baracca A, Chiaradonna F, Sgarbi G, Solaini G, Alberghina L and Lenaz G: Mitochondrial complex I decrease is responsible for bioenergetic dydfunction in K-ras transformed cells. Biochim Biophys Acta. 1797:314–323. 2010. View Article : Google Scholar | |
Larman TC, DePalma SR, Hadjipanayis AG, et al: Spectrum of somatic mitochondrial mutations in five cancers. Proc Nat Acad Sci USA. 109:14087–14091. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kulawiec M, Salk JJ, Ericson NG, Wanagat J and Bielas JH: Generation, function and prognostic utility of somatic mitochondrial DNA mutations in cancer. Environ Mol Mutagen. 51:427–439. 2010.PubMed/NCBI | |
Ward PS, Patel J, Wise DR, et al: The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell. 17:225–234. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chandra D and Singh KK: Genetic insights into OXPHOS defect and its role in cancer. Biochim Biophys Acta. 1807:620–625. 2011. View Article : Google Scholar | |
Picaud S, Kavanagh KL, Yue WW, et al: Structural basis of fumarate hydratase deficiency. J Inherit Metab Dis. 34:671–676. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bardella C, Pollard P and Tomlinson I: SDH mutations in cancer. Biochim Biophys Acta. 1807:1432–1443. 2011. View Article : Google Scholar : PubMed/NCBI | |
Anderson S, Bankier AT, Barrell BG, et al: Sequence and organization of the human mitochondrial genome. Nature. 290:457–465. 1981. View Article : Google Scholar : PubMed/NCBI | |
Attardi G: Animal mitochondrial DNA: an extreme example of genetic economy. Int Rev Cytol. 93:93–145. 1985. View Article : Google Scholar : PubMed/NCBI | |
Chen X and Butow RA: The organization and inheritance of the mitochondrial genome. Nat Rev Genet. 6:815–825. 2005. View Article : Google Scholar : PubMed/NCBI | |
Lightowlers RN, Chinnery PF, Turnbull DM and Howell N: Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet. 13:450–455. 1997. View Article : Google Scholar | |
Johns DR: Paternal transmission of mitochondrial DNA is (fortunately) rare. Ann Neurol. 54:422–424. 2003. View Article : Google Scholar : PubMed/NCBI | |
DiMauro S, Tanji K, Bonilla E, Pallotti F and Schon EA: Mitochondrial abnormalities in muscle and other aging cells: classification, causes and effects. Muscle Nerve. 26:597–607. 2002. View Article : Google Scholar : PubMed/NCBI | |
Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP and Letellier T: Mitochondrial threshold effects. Biochem J. 370:751–762. 2003. View Article : Google Scholar | |
Musicco C, Cormio A, Calvaruso MA, et al: Analysis of the mitochondrial proteome of cybrid cells harbouring a truncative mitochondrial DNA mutation in respiratory complex I. Mol Biosyst. 10:1313–1319. 2014. View Article : Google Scholar : PubMed/NCBI | |
Torroni A, Achilli A, Macaulay V, Richards M and Bandelt HJ: Harvesting the fruit of the human mtDNA tree. Trends Genet. 22:339–345. 2006. View Article : Google Scholar : PubMed/NCBI | |
Wallace DC: Bioenergetics in human evolution and disease: implications for the origins of biological complexity and the missing genetic variation of common diseases. Philos Trans R Soc Lond B Biol Sci. 368:2012–2067. 2013. View Article : Google Scholar | |
Brandon M, Baldi P and Wallace DC: Mitochondrial mutations in cancer. Oncogene. 25:4647–4662. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: the next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI | |
McKenzie M, Lazarou M, Thorburn DR and Ryan MT: Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J Mol Biol. 361:462–469. 2006. View Article : Google Scholar : PubMed/NCBI | |
Burke WM, Orr J, Mario L, et al: Endometrial Cancer: A review and current management strategies: part I. SGO Clinical Practice Endometrial Cancer Working Group. Gynecol Oncol. 134:385–392. 2014. View Article : Google Scholar : PubMed/NCBI | |
Bonadona V, Bonaïti B, Olschwang S, et al: Cancer risks associated with germline mutations in MLH1, MSH2 and MSH6 genes in Lynch syndrome. JAMA. 305:2304–2310. 2011. View Article : Google Scholar : PubMed/NCBI | |
Levine DA, Lin O, Barakat RR, et al: Risk of endometrial carcinoma associated with BRCA mutation. Gynecol Oncol. 80:395–398. 2001. View Article : Google Scholar : PubMed/NCBI | |
Liu VW, Wang Y, Yang HJ, et al: Mitochondrial DNA variant 16189T>C is associated with susceptibility to endometrial cancer. Hum Mutat. 22:173–174. 2003. View Article : Google Scholar : PubMed/NCBI | |
Xu L, Hu Y, Chen B, Tang W, Han X, Yu H and Xiao C: Mitochondrial polymorphisms as risk factors for endometrial cancer in southwest China. Int J Gynecol Cancer. 16:1661–1667. 2006. View Article : Google Scholar : PubMed/NCBI | |
Czarnecka AM, Klemba A, Semczuk A, et al: Common mitochondrial polymorphisms as risk factor for endometrial cancer. Int Arch Med. 2:332009. View Article : Google Scholar : PubMed/NCBI | |
Matias-Guiu X and Davidson B: Prognostic biomarkers in endometrial and ovarian carcinoma. Virchows Arch. 464:315–331. 2014. View Article : Google Scholar : PubMed/NCBI | |
Liu VW, Yang HJ, Wang Y, et al: High frequency of mitochondrial genome instability in human endometrial carcinomas. Br J Cancer. 89:697–701. 2003. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Liu VW, Tsang PC, et al: Microsatellite instability in mitochondrial genome of common female cancers. Int J Gynecol Cancer. 16:259–266. 2006. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Xue WC, Liu VW and Ngan HY: Detection of mosaic pattern of mitochondrial DNA alterations in different populations of cells from the same endometrial tumor. Mitochondrion. 7:171–175. 2007. View Article : Google Scholar : PubMed/NCBI | |
Pejovic T, Ladner D and Intengan M: Somatic D-loop mitochondrial DNA mutations are frequent in uterine serous carcinoma. Eur J Cancer. 40:2519–2524. 2004. View Article : Google Scholar : PubMed/NCBI | |
Futyma K, Putowski L, Cybulski M, Miotla P, Rechberger T and Semczuk A: The prevalence of mtDNA4977 deletion in primary human endometrial carcinomas and matched control samples. Oncol Rep. 20:683–688. 2008.PubMed/NCBI | |
Semczuk A, Lorenc A, Putowski L, Futyma K, Bryk J, Miotla P and Bartnik E: Clinicoprognostical features of endometrial cancer patients with somatic mtDNA mutations. Oncol Rep. 16:1041–1045. 2006.PubMed/NCBI | |
Wang Y, Liu VW, Xue WC, Tsang PC, Cheung AN and Ngan HY: The increase of mitochondrial DNA content in endometrial adenocarcinoma cells: a quantitative study using laser-captured microdissected tissues. Gynecol Oncol. 98:104–110. 2005. View Article : Google Scholar : PubMed/NCBI | |
Guerra F, Kurelac I, Cormio A, et al: Placing mitochondrial DNA mutations within the progression model of type I endometrial carcinoma. Hum Mol Genet. 20:2394–2405. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wenz T: Regulation of mitochondrial biogenesis and PGC-1α under cellular stress. Mitochondrion. 13:134–142. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhu J, Wang KZ and Chu CT: After the banquet: mitochondrial biogenesis, mitophagy and cell survival. Autophagy. 9:1663–1676. 2013. View Article : Google Scholar : PubMed/NCBI | |
Piantadosi CA and Suliman HB: Redox regulation of mitochondrial biogenesis. Free Radic Biol Med. 53:2043–2053. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wredenberg A, Wibom R, Wilhelmsson H, et al: Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci USA. 99:15066–15071. 2002. View Article : Google Scholar : PubMed/NCBI | |
Puigserver P and Spiegelman BM: Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev. 24:78–90. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lin J, Handschin C and Spiegelman BM: Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1:361–370. 2005. View Article : Google Scholar : PubMed/NCBI | |
Scarpulla RC: Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 88:611–638. 2008. View Article : Google Scholar : PubMed/NCBI | |
Malik AN and Czajka A: Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion. 13:481–492. 2013. View Article : Google Scholar | |
Cormio A, Guerra F, Cormio G, Pesce V, et al: The PGC-1alpha-dependent pathway of mitochondrial biogenesis is upregulated in type I endometrial cancer. Biochem Biophys Res Commun. 390:1182–1185. 2009. View Article : Google Scholar : PubMed/NCBI | |
Montgomery BE, Daum GS and Dunton CJ: Endometrial hyperplasia: a review. Obstet Gynecol Surv. 59:368–378. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cormio A, Guerra F, Cormio G, et al: Mitochondrial DNA content and mass increase in progression from normal to hyperplastic to cancer endometrium. BMC Res Notes. 5:2792012. View Article : Google Scholar : PubMed/NCBI | |
Mayr JA, Meierhofer D, Zimmermann F, et al: Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res. 14:2270–2275. 2008. View Article : Google Scholar : PubMed/NCBI | |
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. 71:6220–6229. 2011. View Article : Google Scholar : PubMed/NCBI | |
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. 22:226–238. 2013. View Article : Google Scholar | |
Gasparre G, Bonora E, Tallini G and Romeo G: Molecular features of thyroid oncocytic tumors. Mol Cell Endocrinol. 321:67–76. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gasparre G, Romeo G, Rugolo M and Porcelli AM: Learning from oncocytic tumors: Why choose inefficient mitochondria? Biochim Biophys Acta. 1807:633–642. 2011. View Article : Google Scholar | |
Gasparre G, Porcelli AM, Lenaz G and Romeo G: Relevance of mitochondrial genetics and metabolism in cancer development. Cold Spring Harb Perspect Biol. 5:pii: a011411. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hirst J, King MS and Pryde KR: The production of reactive oxygen species by complex I. Biochem Soc Trans. 36:976–980. 2008. View Article : Google Scholar : PubMed/NCBI | |
Murphy MP: How mitochondria produce reactive oxygen species. Biochem J. 417:1–13. 2009. View Article : Google Scholar | |
Papa S, De Rasmo D, Technikova-Dobrova Z, et al: Respiratory chain complex I, a main regulatory target of The cAMP/PKA pathway is defective in different human diseases. FEBS Lett. 586:568–577. 2012. View Article : Google Scholar | |
Porcelli AM, Ghelli A, Ceccarelli C, et al: The genetic and metabolic signature of oncocytic transformation implicates HIF1alpha destabilization. Hum Mol Genet. 19:1019–1032. 2010. View Article : Google Scholar | |
Calabrese C, Iommarini L, Kurelac I, et al: Respiratory complex I is essential to induce a Warburg profile in mitochondria-defective tumor cells. Cancer Metab. 1:112013. View Article : Google Scholar : PubMed/NCBI | |
Chen JQ, Cammarata PR, Baines CP and Yager JD: Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta. 1793:1540–1570. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chen JQ and Russo J: Mitochondrial oestrogen receptors and their potential implications in oestrogen carcinogenesis in human breast cancer. J Nutr Environ Med. 17:76–89. 2008. View Article : Google Scholar | |
Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ and Klinge CM: Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol. 22:609–622. 2008. View Article : Google Scholar | |
Felty Q, Xiong WC, Sun D, Sarkar S, Singh KP, Parkash J and Roy D: Estrogen induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry. 44:6900–6909. 2005. View Article : Google Scholar : PubMed/NCBI | |
Stankov K, Biondi A, D’Aurelio M, Gasparre G, Falasca A, Romeo G and Lenaz G: Mitochondrial activities of a cell line derived from thyroid Hürthle cell tumors. Thyroid. 16:325–331. 2006. View Article : Google Scholar : PubMed/NCBI | |
Guerra F, Kurelac I, Magini P, Cormio A, Santini D, Ceccarelli C and Gasparre G: Mitochondrial DNA genotyping reveals synchronous nature of simultaneously detected endometrial and ovarian cancers. Gynecol Oncol. 122:457–458. 2011. View Article : Google Scholar : PubMed/NCBI | |
Guerra F, Girolimetti G, Perrone AM, et al: Mitochondrial DNA genotyping efficiently reveals clonality of synchronous endometrial and ovarian cancers. Mod Pathol. 39:1412–1420. 2014. View Article : Google Scholar |