The identification of mitochondrial DNA variants in glioblastoma multiforme

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Yeung, Ka Yu ^a,b   Dickinson, Adam ^a,b   Donoghue, Jacqueline F ^a   Polekhina, Galina ^a   White, Stefan J ^a   Grammatopoulos, Dimitris K ^b,c   McKenzie, Matthew ^a   Johns, Terrance G ^a   St John, Justin C ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY HOSPITALS COVENTRY AND WARWICKSHIRE NHS TRUST   (United Kingdom)

Author keywords

Aerobic glycolysis; Depletion; Genetic variants; Mitochondrial DNA; Oxidative phosphorylation; Tumorigenesis

Indexed keywords

ANTIMETABOLITE; MITOCHONDRIAL DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ZALCITABINE;

ANIMAL; BRAIN; BRAIN TUMOR; CELL TRANSFORMATION; CHEMICAL STRUCTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GLIOBLASTOMA; GLYCOLYSIS; HIGH THROUGHPUT SEQUENCING; HUMAN; METABOLISM; MOUSE; NEURAL STEM CELL; OXIDATIVE PHOSPHORYLATION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIMETABOLITES; BRAIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DNA, MITOCHONDRIAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; GLIOBLASTOMA; GLYCOLYSIS; HETEROGRAFTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICE; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, MOLECULAR; NEURAL STEM CELLS; OXIDATIVE PHOSPHORYLATION; ZALCITABINE;

EID: 84911374273     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-2-1     Document Type: Article

References (59)

1. Taanman JW: The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1999, 1410(2):103-123. 10.1016/S0005-2728(98)00161-3
2. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG: Sequence and organization of the human mitochondrial genome. Nature 1981, 290(5806):457-465. 10.1038/290457a0
3. Gill PIP, Kimpton C, et al.: Identification of the remains of the Romanov family by DNA analysis. Nat Genet 1994, 6: 130-135. 10.1038/ng0294-130
4. Penta JS, Johnson FM, Wachsman JT, Copeland WC: Mitochondrial DNA in human malignancy. Mutat Res 2001, 488(2):119-133. 10.1016/S1383-5742(01)00053-9
5. Jakupciak JP, Maragh S, Markowitz ME, Greenberg AK, Hoque MO, Maitra A, Barker PE, Wagner PD, Rom WN, Srivastava S, Sidransky D, O'Connell CD: Performance of mitochondrial DNA mutations detecting early stage cancer. BMC Cancer 2008, 8: 285. doi:10.1186/1471-2407-8-285 10.1186/1471-2407-8-285
6. Fabrizi GM, Cardaioli E, Grieco GS, Cavallaro T, Malandrini A, Manneschi L, Dotti MT, Federico A, Guazzi G: The A to G transition at nt 3243 of the mitochondrial tRNALeu(UUR) may cause an MERRF syndrome. J Neurol Neurosurg Psychiatry 1996, 61(1):47-51. 10.1136/jnnp.61.1.47
7. Choi BO, Hwang JH, Kim J, Cho EM, Cho SY, Hwang SJ, Lee HW, Kim SJ, Chung KW: A MELAS syndrome family harboring two mutations in mitochondrial genome. Exp Mol Med 2008, 40(3):354-360. 10.3858/emm.2008.40.3.354
8. Oudard S, Arvelo F, Miccoli L, Apiou F, Dutrillaux AM, Poisson M, Dutrillaux B, Poupon MF: High glycolysis in gliomas despite low hexokinase transcription and activity correlated to chromosome 10 loss. Br J Cancer 1996, 74(6):839-845. 10.1038/bjc.1996.446
9. Warburg O: On respiratory impairment in cancer cells. Science 1956, 124(3215):269-270.
10. Pfeiffer T, Schuster S, Bonhoeffer S: Cooperation and competition in the evolution of ATP-producing pathways. Science 2001, 292(5516):504-507. doi:10.1126/science.1058079 10.1126/science.1058079
11. Elliott HR, Samuels DC, Eden JA, Relton CL, Chinnery PF: Pathogenic mitochondrial DNA mutations are common in the general population. Am J Hum Genet 2008, 83(2):254-260. doi:10.1016/j.ajhg.2008.07.004 10.1016/j.ajhg.2008.07.004
12. Vermulst M, Bielas JH, Loeb LA: Quantification of random mutations in the mitochondrial genome. Methods 2008, 46(4):263-268. doi:10.1016/j.ymeth.2008.10.008 10.1016/j.ymeth.2008.10.008
13. Goto H, Dickins B, Afgan E, Paul IM, Taylor J, Makova KD, Nekrutenko A: Dynamics of mitochondrial heteroplasmy in three families investigated via a repeatable re-sequencing study. Genome Biol 2011, 12(6):R59. doi:10.1186/gb-2011-12-6-r59 10.1186/gb-2011-12-6-r59
14. Zaragoza MV, Fass J, Diegoli M, Lin D, Arbustini E: Mitochondrial DNA variant discovery and evaluation in human Cardiomyopathies through next-generation sequencing. PloS one 2010, 5(8):e12295. doi:10.1371/journal.pone.0012295 10.1371/journal.pone.0012295
15. Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, Pallen MJ: Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 2012, 30(5):434-439. doi:10.1038/nbt.2198 10.1038/nbt.2198
16. Elliott AM, Radecki J, Moghis B, Li X, Kammesheidt A: Rapid detection of the ACMG/ACOG-recommended 23 CFTR disease-causing mutations using ion torrent semiconductor sequencing. J Biomol Tech 2012, 23(1):24-30. doi:10.7171/jbt.12-2301-003 10.7171/jbt.12-2301-003
17. Lloyd RE, Foster PG, Guille M, Littlewood DT: Next generation sequencing and comparative analyses of Xenopus mitogenomes. BMC Genomics 2012, 13(1):496. doi:10.1186/1471-2164-13-496 10.1186/1471-2164-13-496
18. Thusberg J, Olatubosun A, Vihinen M: Performance of mutation pathogenicity prediction methods on missense variants. Hum Mutat 2011, 32(4)):358-368.
19. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M: Epidemiology and molecular pathology of glioma. Nat Clin Pract Neurol 2006, 2(9):494-503. quiz 491 p following 516. doi:10.1038/ncpneuro0289
20. Kunkle B, Yoo C, Roy D: Discovering gene-environment interactions in Glioblastoma through a comprehensive data integration bioinformatics method. Neurotoxicology 2012. doi:10.1016/j.neuro.2012.11.001
21. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, Sabel M, Steinbach JP, Heese O, Reifenberger G, Weller M, Schackert G: Long-term survival with glioblastoma multiforme. Brain 2007, 130(Pt 10):2596-2606. doi:10.1093/brain/awm204
22. Maletinska L, Blakely EA, Bjornstad KA, Deen DF, Knoff LJ, Forte TM: Human glioblastoma cell lines: levels of low-density lipoprotein receptor and low-density lipoprotein receptor-related protein. Cancer Res 2000, 60(8):2300-2303.
23. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A: Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004, 64(19):7011-7021. doi:10.1158/0008-5472.CAN-04-1364 10.1158/0008-5472.CAN-04-1364
24. Pandita A, Aldape KD, Zadeh G, Guha A, James CD: Contrasting in vivo and in vitro fates of glioblastoma cell subpopulations with amplified EGFR. Genes Chromosomes Cancer 2004, 39(1):29-36. doi:10.1002/gcc.10300 10.1002/gcc.10300
25. Day B, Stringer B, Wilson J, Jeffree R, Jamieson P, Ensbey K, Bruce Z, Inglis P, Allan S, Winter C, Tollesson G, Campbell S, Lucas P, Findlay W, Kadrian D, Johnson D, Robertson T, Johns T, Bartlett P, Osborne G, Boyd A: Glioma surgical aspirate: a viable source of tumor tissue for experimental research. Cancers 2013, 5(2):357-371. 10.3390/cancers5020357
26. de Boer CM, Eini R, Gillis AM, Stoop H, Looijenga LH, White SJ: DICER1 RNase IIIb domain mutations are infrequent in testicular germ cell tumours. BMC research notes 2012, 5: 569. doi:10.1186/1756-0500-5-569 10.1186/1756-0500-5-569
27. Calabrese R, Capriotti E, Fariselli P, Martelli PL, Casadio R: Functional annotations improve the predictive score of human disease-related mutations in proteins. Hum Mutat 2009, 30(8):1237-1244. doi:10.1002/humu.21047 10.1002/humu.21047
28. Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P: Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 2009, 25(21):2744-2750. doi:10.1093/bioinformatics/btp528 10.1093/bioinformatics/btp528
29. Li M, Schonberg A, Schaefer M, Schroeder R, Nasidze I, Stoneking M: Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am J Hum Genet 2010, 87(2):237-249. doi:10.1016/j.ajhg.2010.07.014 10.1016/j.ajhg.2010.07.014
30. Parr RL, Maki J, Reguly B, Dakubo GD, Aguirre A, Wittock R, Robinson K, Jakupciak JP, Thayer RE: The pseudo-mitochondrial genome influences mistakes in heteroplasmy interpretation. BMC Genomics 2006, 7: 185. doi:10.1186/1471-2164-7-185 10.1186/1471-2164-7-185
31. Camilleri M, Carlson P, Zinsmeister AR, McKinzie S, Busciglio I, Burton D, Zaki EA, Boles RG: Mitochondrial DNA and gastrointestinal motor and sensory functions in health and functional gastrointestinal disorders. Am J Physiol Gastrointest Liver Physiol 2009, 296(3):G510-516. doi:10.1152/ajpgi.90650.2008 10.1152/ajpgi.90650.2008
32. Wong LJ: Pathogenic mitochondrial DNA mutations in protein-coding genes. Muscle Nerve 2007, 36(3):279-293. doi:10.1002/mus.20807 10.1002/mus.20807
33. Jakupciak JP, Dakubo GD, Maragh S, Parr RL: Analysis of potential cancer biomarkers in mitochondrial DNA. Curr Opin Mol Ther 2006, 8(6):500-506.
34. Ishikawa K, Hayashi J: A novel function of mtDNA: its involvement in metastasis. Ann N Y Acad Sci 2010, 1201: 40-43. doi:10.1111/j.1749-6632.2010.05616.x 10.1111/j.1749-6632.2010.05616.x
35. Hayashi JI, Yonekawa H, Tagashira Y: Nuclear but not mitochondrial genome involvement in 3-methylcholanthrene-induced expression of tumorigenicity in mouse somatic cells. Cancer Res 1989, 49(17):4715-4720.
36. Akimoto M, Niikura M, Ichikawa M, Yonekawa H, Nakada K, Honma Y, Hayashi J: Nuclear DNA but not mtDNA controls tumor phenotypes in mouse cells. Biochem Biophys Res Commun 2005, 327(4):1028-1035. doi:10.1016/j.bbrc.2004.12.105 10.1016/j.bbrc.2004.12.105
37. He Y, Wu J, Dressman DC, Iacobuzio-Donahue C, Markowitz SD, Velculescu VE, Diaz LA Jr, Kinzler KW, Vogelstein B, Papadopoulos N: Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 2010, 464(7288):610-614. doi:10.1038/nature08802 10.1038/nature08802
38. Polyak K, Li Y, Zhu H, Lengauer C, Willson JK, Markowitz SD, Trush MA, Kinzler KW, Vogelstein B: Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genet 1998, 20(3):291-293. doi:10.1038/3108 10.1038/3108
39. Shen L, Fang H, Chen T, He J, Zhang M, Wei X, Xin Y, Jiang Y, Ding Z, Ji J, Lu J, Bai Y: Evaluating mitochondrial DNA in cancer occurrence and development. Ann N Y Acad Sci 2010, 1201: 26-33. doi:10.1111/j.1749-6632.2010.05635.x 10.1111/j.1749-6632.2010.05635.x
40. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, Nakada K, Honma Y, Hayashi J: ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 2008, 320(5876):661-664. doi:10.1126/science.1156906 10.1126/science.1156906
41. Ohta S: Contribution of somatic mutations in the mitochondrial genome to the development of cancer and tolerance against anticancer drugs. Oncogene 2006, 25(34):4768-4776. doi:10.1038/sj.onc.1209602 10.1038/sj.onc.1209602
42. Mito T, Kikkawa Y, Shimizu A, Hashizume O, Katada S, Imanishi H, Ota A, Kato Y, Nakada K, Hayashi J: Mitochondrial DNA mutations in mutator mice confer respiration defects and B-cell lymphoma development. PloS one 2013, 8(2):e55789. doi:10.1371/journal.pone.0055789 10.1371/journal.pone.0055789
43. Takibuchi G, Imanishi H, Morimoto M, Ishikawa K, Nakada K, Toyama-Sorimachi N, Kikkawa Y, Takenaga K, Hayashi JI: Polymorphic mutations in mouse mitochondrial DNA regulate a tumor phenotype. Mitochondrion 2013. doi:10.1016/j.mito.2013.07.117
44. Imanishi H, Hattori K, Wada R, Ishikawa K, Fukuda S, Takenaga K, Nakada K, Hayashi J: Mitochondrial DNA mutations regulate metastasis of human breast cancer cells. PloS one 2011, 6(8):e23401. doi:10.1371/journal.pone.0023401 10.1371/journal.pone.0023401
45. Hashizume O, Shimizu A, Yokota M, Sugiyama A, Nakada K, Miyoshi H, Itami M, Ohira M, Nagase H, Takenaga K, Hayashi J: Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development. Proc Natl Acad Sci U S A 2012, 109(26):10528-10533. doi:10.1073/pnas.1202367109 10.1073/pnas.1202367109
46. Khaidakov M, Shmookler Reis RJ: Possibility of selection against mtDNA mutations in tumors. Mol Cancer 2005, 4: 36. doi:10.1186/1476-4598-4-36 10.1186/1476-4598-4-36
47. Kirches E, Krause G, Warich-Kirches M, Weis S, Schneider T, Meyer-Puttlitz B, Mawrin C, Dietzmann K: High frequency of mitochondrial DNA mutations in glioblastoma multiforme identified by direct sequence comparison to blood samples. Int J Cancer 2001, 93(4):534-538. doi:10.1002/ijc. 10.1002/ijc.1375
48. Kirches E, Krause G, Weis S, Mawrin C, Dietzmann K: Comparison between mitochondrial DNA sequences in low grade astrocytomas and corresponding blood samples. Mol Pathol 2002, 55(3):204-206. 10.1136/mp.55.3.204
49. Kiebish MA, Seyfried TN: Absence of pathogenic mitochondrial DNA mutations in mouse brain tumors. BMC Cancer 2005, 5: 102. doi:10.1186/1471-2407-5-102 10.1186/1471-2407-5-102
50. Seoane M, Mosquera-Miguel A, Gonzalez T, Fraga M, Salas A, Costoya JA: The mitochondrial genome is a "genetic sanctuary" during the oncogenic process. PloS one 2011, 6(8):e23327. doi:10.1371/journal.pone.0023327 10.1371/journal.pone.0023327
51. Iglesias P, Salas A, Costoya JA: The maintenance of mitochondrial genetic stability is crucial during the oncogenic process. Communicative & integrative biology 2012, 5(1):34-38. 10.4161/cib.18160
52. Dickinson A, Yeung KY, Donoghue J, Baker MJ, Kelly RD, McKenzie M, Johns TG, St John JC: The regulation of mitochondrial DNA copy number in glioblastoma cells. Cell Death Differ 2013, 20(12):1644-1653. doi:10.1038/cdd.2013.115 10.1038/cdd.2013.115
53. Zhou Y, Shingu T, Feng L, Chen Z, Ogasawara M, Keating MJ, Kondo S, Huang P: Metabolic alterations in highly tumorigenic glioblastoma cells: preference for hypoxia and high dependency on glycolysis. J Biol Chem 2011, 286(37):32843-32853. doi:10.1074/jbc.M111.260935 10.1074/jbc.M111.260935
54. Casson RJ, Chidlow G, Han G, Wood JP: An explanation for the Warburg effect in the adult mammalian retina. Clin Experiment Ophthalmol 2012. doi:10.1111/ceo.12050
55. Abu Dawud R, Schreiber K, Schomburg D, Adjaye J: Human embryonic stem cells and embryonal carcinoma cells have overlapping and distinct metabolic signatures. PloS one 2012, 7(6):e39896. doi:10.1371/journal.pone.0039896 10.1371/journal.pone.0039896
56. Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC: Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 2007, 120(Pt 22):4025-4034. doi:10.1242/jcs.016972
57. Kelly RD, Mahmud A, McKenzie M, Trounce IA, St John JC: Mitochondrial DNA copy number is regulated in a tissue specific manner by DNA methylation of the nuclear-encoded DNA polymerase gamma A. Nucleic Acids Res 2012, 40(20):10124-10138. doi:10.1093/nar/gks770 10.1093/nar/gks770
58. Facucho-Oliveira JM, St John JC: The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 2009, 5(2):140-158. doi:10.1007/s12015-009-9058-0 10.1007/s12015-009-9058-0
59. Kelly RD, Sumer H, McKenzie M, Facucho-Oliveira J, Trounce IA, Verma PJ, St John JC: The effects of nuclear reprogramming on mitochondrial DNA replication. Stem Cell Rev 2013, 9(1):1-15. doi:10.1007/s12015-011-9318-7 10.1007/s12015-011-9318-7