Genomic heterogeneity meets cellular energetics: crosstalk between the mitochondria and the cell cycle

Erica L. Herrera , Seham Z. Azzam , Madison C. Berger , Laura A. Diaz-Martinez

Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4 : 42

PDF
Journal of Cancer Metastasis and Treatment ›› 2018, Vol. 4:42 DOI: 10.20517/2394-4722.2018.35
Review
review-article

Genomic heterogeneity meets cellular energetics: crosstalk between the mitochondria and the cell cycle

Author information +
History +
PDF

Abstract

Changes in cellular energetics and genomic instability are two characteristics of cancers that have been studied independently. Evidence of cross-talk between mitochondria function and nuclear function has started to emerge, suggesting that these pathways can influence one another. Here we review recent evidence that links the mitochondria and the cell cycle. This evidence indicates bidirectional cross-talk where mitochondria function can regulate the cell cycle and induce genomic instability, and conversely, the cell cycle machinery regulates mitochondria function. Implications for this cross-talk in the development of cancer are discussed.

Keywords

Mitochondria dynamics / cell cycle / mitochondria heterogeneity / genomic heterogeneity

Cite this article

Download citation ▾
Erica L. Herrera, Seham Z. Azzam, Madison C. Berger, Laura A. Diaz-Martinez. Genomic heterogeneity meets cellular energetics: crosstalk between the mitochondria and the cell cycle. Journal of Cancer Metastasis and Treatment, 2018, 4: 42 DOI:10.20517/2394-4722.2018.35

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Boveri T.Concerning the origin of malignant tumours by Theodor Boveri Translated and annotated by Henry Harris..J Cell Sci2008;8;121 Suppl:1-84

[2]

Warburg O,Negelein E.The metabolism of tumors in the body.J Gen Physiol1927;8:519-30 PMCID:PMC2140820

[3]

Warburg O.On the origin of cancer cells.Science1956;123:309-14

[4]

Nowell PC.The clonal evolution of tumor cell populations.Science1976;194:23-8

[5]

Reddy EP,Santos E.A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene.Nature1982;300:149-52

[6]

Srivastava S,Pirollo K,Chang EH.Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li-Fraumeni syndrome.Nature1990;348:747-9

[7]

Stephens PJ,Fu B,Bignell GR,Pleasance ED,Beare D,McLaren S,McBride DJ,Nik-Zainal S,Jia M,Butler AP,Quail MA,Swerdlow H,Morsberger LA,Follows GA,Flanagan AM,Futreal PA.Massive genomic rearrangement acquired in a single catastrophic event during cancer development.Cell2011;144:27-40 PMCID:PMC3065307

[8]

Crasta K,Dagher R,Ivanova EV,Nezi L,Chowdhury D.DNA breaks and chromosome pulverization from errors in mitosis.Nature2012;482:53-8 PMCID:PMC3271137

[9]

Salk JJ,Loeb LA.Mutational heterogeneity in human cancers: origin and consequences.Annu Rev Pathol Mech Dis2010;5:51-75 PMCID:PMC3375045

[10]

Campbell PJ,Pleasance ED,Li H,Stebbings LA,Edkins S,Teague JW,Goodhead I,Clee CM,Cox A,Durbin R,Edwards PA,Stratton MR.Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing.Nat Genet2008;40:722-9 PMCID:PMC2705838

[11]

Stephens PJ,Lin ML,Pleasance ED,Stebbings LA,Edkins S,Greenman CD,Latimer C,Lau KW,Quail MA,Churcher C,Sieuwerts AM,Silver DP,Russnes HE,Reis-Filho JS,Richardson AL,Campbell PJ,Stratton MR.Complex landscapes of somatic rearrangement in human breast cancer genomes.Nature2009;462:1005-10 PMCID:PMC3398135

[12]

Smida J,Zhang Y,Ribi S,von Luettichau I,O'Leary VB,Frishman D.Genome-wide analysis of somatic copy number alterations and chromosomal breakages in osteosarcoma.Int J Cancer2017;141:816-28

[13]

Zhang LL,Zhang MM,Xie HJ,Wang HN,Zhou GB,Zheng CX.Multiregion sequencing reveals the intratumor heterogeneity of driver mutations in TP53-driven non-small cell lung cancer.Int J Cancer2017;140:103-8

[14]

Gerlinger M,Horswell S,Larkin J,Gronroos E,Matthews N,Tarpey P,Phillimore B,McDonald NQ,Jones D,Latimer C,Nohadani M,Spencer-Dene B,Pickering L,Gore M,Downward J,Swanton C.Intratumor heterogeneity and branched evolution revealed by multiregion sequencing.N Engl J Med2012;366:883-92 PMCID:PMC4878653

[15]

Martinez P,Gerlinger M,Burrell RA,Joshi T,Larkin J,Swanton C.Parallel evolution of tumour subclones mimics diversity between tumours.J Pathol2013;230:356-64

[16]

Rasche L,Stephens OW,Tytarenko R,Bauer M,Deshpande S,Buzder T,Zangari M,Thanendrarajan S,Epstein J,Walker BA,Barlogie B,Weinhold N.Spatial genomic heterogeneity in multiple myeloma revealed by multi-region sequencing.Nat Commun2017;8:268 PMCID:PMC5559527

[17]

Jamal-Hanjani M,McGranahan N,Watkins TBK,Shafi S,Mitter R,Salm M,Escudero M,Rowan A,Moore DA,Xu H,Forster MD,Hiley CT,Falzon M,Marafioti T,Hayward M,Panagiotopoulos N,Thakrar R,Blackhall F,Shah R,Quinn AM,Naidu B,Langman G,Nicolson M,Kerr K,Gomersall L,Nakas A,Anand G,Russell P,Ismail B,Prakash V,Kornaszewska M,Adams H,Dentro S,O'Sullivan B,Hartley JA,Bell H,Shaw JA,Szallasi Z,Stewart A,Le Quesne J,Dive C,Swanton C.Tracking the evolution of non-small-cell lung cancer.N Engl J Med2017;376:2109-21

[18]

Zhao Z,Liu S,Zhou W,Yu Q,Jiang M,McMaster M,Lin X,Xu L,Li G,Yeager M,Xu X,Li B,Caporaso N.Evolution of multiple cell clones over a 29-year period of a CLL patient.Nat Commun2016;7:13765 PMCID:PMC5171825

[19]

Bolli N,Wedge DC,Alexandrov LB,Dawson KJ,Nik-Zainal S,Hinton JW,Tubio JM,O' Meara S,Teague JW,Anderson E,Tai YT,Sperling AS,Richardson PG,Magrangeas F,Moreau P,Facon T,Anderson KC,Munshi NC.Heterogeneity of genomic evolution and mutational profiles in multiple myeloma.Nat Commun2014;5:2997 PMCID:PMC3905727

[20]

Keats JJ,Egan JB,Palmer SE,Van Wier S,Baker AS,Kumar S,Carpten JD,Fonseca R,Bergsagel PL.Clonal competition with alternating dominance in multiple myeloma.Blood2012;120:1067-76 PMCID:PMC3412330

[21]

Shah SP,Khattra J,Pugh T,Delaney A,Guliany R,Steidl C,Jones S,Leung G,Severson T,Teschendorff AE,Turashvili G,Warren RL,Zhao Y,Huntsman D,Marra MA.Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution.Nature2009;461:809-13

[22]

Thomsen MBH,Lamy P,Vang S,Borre M,Ørntoft TF.Spatial and temporal clonal evolution during development of metastatic urothelial carcinoma.Mol Oncol2016;10:1450-60 PMCID:PMC5423216

[23]

Mroz EA,Hammon RJ,Rocco JW.Intra-tumor genetic heterogeneity and mortality in head and neck cancer: analysis of data from the Cancer Genome Atlas.PLoS Med2015;12:e1001786 PMCID:PMC4323109

[24]

Sveen A,Alagaratnam S,Høland M,Sorbye H,Horn A,Knappskog S,Lothe RA.Intra-patient inter-metastatic genetic heterogeneity in colorectal cancer as a key determinant of survival after curative liver resection.PLoS Genet2016;12:e1006225 PMCID:PMC4966938

[25]

Sedgwick B.Repairing DNA-methylation damage.Nat Rev Mol Cell Biol2004;5:148-57

[26]

Pfeifer GP.How the environment shapes cancer genomes.Curr Opin Oncol2015;27:71-7 PMCID:PMC4299863

[27]

Poirier MC.Linking DNA adduct formation and human cancer risk in chemical carcinogenesis.Environ Mol Mutagen2016;57:499-507

[28]

Poon S,Tan P,Rozen SG.Mutation signatures of carcinogen exposure: genome-wide detection and new opportunities for cancer prevention.Genome Med2014;6:24 PMCID:PMC4062065

[29]

Aguilera A.Causes of genome instability.Annu Rev Genet2013;47:1-32

[30]

Tubbs A.Endogenous DNA damage as a source of genomic instability in cancer.Cell2017;168:644-56

[31]

Olinski R,Cooke MS.Endogenously generated DNA nucleobase modifications source, and significance as possible biomarkers of malignant transformation risk, and role in anticancer therapy.Biochim Biophys Acta2018;1869:29-41

[32]

Moyano M.piRNA involvement in genome stability and human cancer.J Hematol Oncol2015;8:38 PMCID:PMC4412036

[33]

Rodgers K.Error-prone repair of DNA double-strand breaks.J Cell Physiol2016;231:15-24 PMCID:PMC4586358

[34]

Shadel GS.Mitochondrial ROS signaling in organismal homeostasis.Cell2015;163:560-9 PMCID:PMC4634671

[35]

Sabharwal SS.Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles' heel?.Nat Rev Cancer2014;14:709-21 PMCID:PMC4657553

[36]

Tokarz P.Role of mitochondria in carcinogenesis.Acta Biochim Pol2014;61:671-8

[37]

Stehling O,Lill R.Mitochondrial iron-sulfur protein biogenesis and human disease.Biochimie2014;100:61-77

[38]

Danese A,Bonora M,Previati M,Pinton P.Calcium regulates cell death in cancer: roles of the mitochondria and mitochondria-associated membranes (MAMs).Biochim Biophys Acta2017;1858:615-27

[39]

Kasahara A.Mitochondria: from cell death executioners to regulators of cell differentiation.Trends Cell Biol2014;24:761

[40]

Vyas S,Haigis MC.Mitochondria and cancer.Cell2016;166:555-66 PMCID:PMC5036969

[41]

Weinberg SE.Targeting mitochondria metabolism for cancer therapy.Nat Chem Biol2015;11:9-15 PMCID:PMC4340667

[42]

Zong WX,White E.Mitochondria and cancer.Mol Cell2016;61:667-76 PMCID:PMC4779192

[43]

Guerra F,Moro L.Mitochondria and cancer chemoresistance.Biochim Biophys Acta2017;1858:686-99

[44]

Hensley CT,Yuan Q,Jin E,Jiang L,Skelton R,Wodzak M,McMillan E,Ni M,Torrealba J,Kernstine K,DeBerardinis RJ.Metabolic heterogeneity in human lung tumors.Cell2016;164:681-94 PMCID:PMC4752889

[45]

Maher EA,Bachoo RM,Raisanen J,Jindal A,Choi C,Mathews D,Mickey BE,DeBerardinis RJ.Metabolism of [U-13 C]glucose in human brain tumors in vivo.NMR Biomed2012;25:1234-44 PMCID:PMC3406255

[46]

Stewart JB,Sabarinathan R,Gorodkin J,Larsson E.Simultaneous DNA and RNA mapping of somatic mitochondrial mutations across diverse human cancers.PLoS Genet2015;11:e1005333 PMCID:PMC4488357

[47]

Ju YS,Gerstung M,Nik-Zainal S,Davies HR,Gundem G,Bolli N,Tarpey PS,Massie CE,Teague JW,Green AR,Unnikrishnan A,Teh BT,Greaves M,El-Naggar AK,Collins VP,Taylor JA,Malkin D,Foster CS,Whitaker HC,Eeles R,Neal D,Isaacs WB,Flanagan AM,Lynch AG,McDermott U,Campbell PJ.Origins and functional consequences of somatic mitochondrial DNA mutations in human cancer.Elife2014;3:02935

[48]

Hertweck KL.The landscape of mtDNA modifications in cancer: a tale of two cities.Front Oncol2017;7:262 PMCID:PMC5673620

[49]

Bussard KM.Understanding mitochondrial polymorphisms in cancer.Cancer Res2017;77:6051-9

[50]

Choudhury AR.Mitochondrial determinants of cancer health disparities.Semin Cancer Biol2017;47:125-46

[51]

van Gisbergen MW,Starmans MHW,Yadak R,Boutros PC,Dubois L.How do changes in the mtDNA and mitochondrial dysfunction influence cancer and cancer therapy? Challenges, opportunities and models.Mutat Res Mutat Res2015;764:16-30

[52]

Kleine T.Retrograde signaling: organelles go networking.Biochim Biophys Acta2016;1857:1313-25

[53]

Liu Z.Mitochondrial retrograde signaling.Annu Rev Genet2006;40:159-85

[54]

Parikh VS,Scott R,Butow RA.The mitochondrial genotype can influence nuclear gene expression in yeast.Science1987;235:576-80

[55]

Guha M.Mitochondrial retrograde signaling at the crossroads of tumor bioenergetics, genetics and epigenetics.Mitochondrion2013;13:577-91 PMCID:PMC3832239

[56]

Nurse P.A long twentieth century of the cell cycle and beyond.Cell2000;100:71-8

[57]

Knoblach B.Motors, anchors, and connectors: orchestrators of organelle inheritance.Annu Rev Cell Dev Biol2015;31:55-81

[58]

Ouellet J.Organelle segregation during mitosis: lessons from asymmetrically dividing cells.J Cell Biol2012;196:305-13 PMCID:PMC3275374

[59]

Conduit PT,Raff JW.Centrosome function and assembly in animal cells.Nat Rev Mol Cell Biol2015;16:611-24

[60]

Hartwell LH,Pringle JR.Genetic control of the cell division cycle in yeast.Science1974;183:46-51

[61]

Aon MA,Cortassa S.Carbon and energetic uncoupling are associated with block of division at different stages of the cell cycle in several cdc mutants of saccharomyces cerevisiae.Exp Cell Res1995;217:42-51

[62]

Genta HD,Aon MA.Decreased mitochondrial biogenesis in temperature-sensitive cell division cycle mutants of Saccharomyces cerevisiae.Curr Microbiol1995;31:327-31

[63]

Tu BP,Liu JC,Young ET,McKnight SL.Cyclic changes in metabolic state during the life of a yeast cell.Proc Natl Acad Sci U S A2007;104:16886-91 PMCID:PMC2040445

[64]

Cai L.Driving the cell cycle through metabolism.Annu Rev Cell Dev Biol2012;28:59-87

[65]

Slavov N,Caudy A.Metabolic cycling without cell division cycling in respiring yeast.Proc Natl Acad Sci U S A2011;108:19090-5 PMCID:PMC3223432

[66]

Papagiannakis A,Wit EC.Autonomous metabolic oscillations robustly gate the early and late cell cycle.Mol Cell2017;65:285-95

[67]

Posakony JW,Attardi G.Mitochondrial growth and division during the cell cycle in HeLa cells.J Cell Biol1977;74:468-91 PMCID:PMC2110063

[68]

Newton CS.Mitochondrial DNA synthesis in cell cycle mutants of saccharomyces cerevisiae.Cell1975;5:423-8

[69]

Smirnova E,Ryazantsev SN.A human dynamin-related protein controls the distribution of mitochondria.J Cell Biol1998;143:351-8 PMCID:PMC2132828

[70]

Smirnova E,Shurland DL.Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells.Mol Biol Cell2001;12:2245-56 PMCID:PMC58592

[71]

Osellame LD,Stroud DA,Stojanovski D,Ryan MT.Cooperative and independent roles of the Drp1 adaptors Mff, MiD49 and MiD51 in mitochondrial fission.J Cell Sci2016;129:2170-81

[72]

Loson OC,Chen H.Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission.Mol Biol Cell2013;24:659-67 PMCID:PMC3583668

[73]

Arakaki N,Owaki H,Suenaga M,Emoto Y,Shono M.Dynamics of mitochondria during the cell cycle.Biol Pharm Bull2006;29:1962-5

[74]

Mitra K,Roysam B,Lippincott-Schwartz J.A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase.Proc Natl Acad Sci U S A2009;106:11960-5 PMCID:PMC2710990

[75]

Lee S,Sun X,Cho H.Cell cycle-dependent mitochondrial biogenesis and dynamics in mammalian cells.Biochem Biophys Res Commun2007;357:111-7

[76]

Taguchi N,Jofuku A,Mihara K.Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission.J Biol Chem2007;282:11521-9

[77]

Kashatus DF,Brady DC,Cox AD.RALA and RALBP1 regulate mitochondrial fission at mitosis.Nat Cell Biol2011;13:1108-15 PMCID:PMC3167028

[78]

Díaz-Martínez LA,Warrington R,Wei S,Roth MG.Genome-wide siRNA screen reveals coupling between mitotic apoptosis and adaptation.EMBO J2014;33:1960-76 PMCID:PMC4195789

[79]

Park YY,Cho MG.ATP depletion during mitotic arrest induces mitotic slippage and APC/CCdh1-dependent cyclin B1 degradation.Exp Mol Med2018;50:46 PMCID:PMC5938023

[80]

Diaz-Martinez LA.The complexity of life and death decisions in mitosis.Mol Cell Oncol2015;2:e969658 PMCID:PMC4904892

[81]

Horn SR,Johnson ES,Wu JQ,Yang CS,An J,Rathmell JC,Kornbluth S.Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability.Mol Biol Cell2011;22:1207-16 PMCID:PMC3078078

[82]

Wang C,Lu Y,Katiyar S,Fu M,Quong A,Pestell RG.Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function.Proc Natl Acad Sci U S A2006;103:11567-72 PMCID:PMC1518800

[83]

Lee Y,Choi YJ,Tolliday N,Chim H,Ruan HB,Vazquez F,Shulman GI.Cyclin D1-Cdk4 controls glucose metabolism independently of cell cycle progression.Nature2014;510:547-51 PMCID:PMC4076706

[84]

Wang Z,Candas D,Qin L,Wachsmann-Hogiu S,Chromy BA,Duru N,Chen M,Weinstein LS.Cyclin B1/Cdk1 coordinates mitochondrial respiration for cell-Cycle G2/M progression.Dev Cell2014;29:217-32 PMCID:PMC4156313

[85]

Choi E,Xing C.Mitotic checkpoint regulators control insulin signaling and metabolic homeostasis.Cell2016;166:567-81 PMCID:PMC5560052

[86]

Zhang X,Guo Y,Shi X,Tan P,Wei C,Ramirez A,Cao C,Xu Q.Mps1 kinase regulates tumor cell viability via its novel role in mitochondria.Cell Death Dis2016;7:e2292 PMCID:PMC4973343

[87]

Dohi T,Wall NR,Altieri DC.Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis.J Clin Invest2004;114:1117-27 PMCID:PMC522254

[88]

Gemin A,Preston TJ.Regulation of the cell cycle in response to inhibition of mitochondrial generated energy.Biochem Biophys Res Commun2005;332:1122-32

[89]

Schieke SM,Finkel T.Coordination of mitochondrial bioenergetics with G 1 phase cell cycle progression.Cell Cycle2008;7:1782-7 PMCID:PMC3399174

[90]

Qian W,Gibson GA,Bakkenist CJ.Mitochondrial hyperfusion induced by loss of the fission protein Drp1 causes ATM-dependent G2/M arrest and aneuploidy through DNA replication stress.J Cell Sci2012;125:5745 PMCID:PMC4074216

[91]

Marsboom G,Ryan JJ,Wu X,Thenappan T,Zhang HJ,Chen Y,Weir EK,Archer SL.Dynamin-related protein 1-mediated mitochondrial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension.Circ Res2012;110:1484-97 PMCID:PMC3539779

[92]

Westrate LM,Burgenske DM.Persistent mitochondrial hyperfusion promotes G2/M accumulation and caspase-dependent cell death.PLoS One2014;9:e91911 PMCID:PMC3954829

[93]

Lee S,Kim SH,Yoo YS,Sun X.Human mitochondrial Fis1 links to cell cycle regulators at G2/M transition.Cell Mol Life Sci2014;71:711-25

[94]

Xie X.Knockout of Drosophila RNase Z-L impairs mitochondrial transcript processing, respiration and cell cycle progression.Nucleic Acids Res2015;43:gkv1149 PMCID:PMC4666369

[95]

Donthamsetty S,Pannu V,Ramarathinam S,Cheng A,Aneja R.Mitochondrial genome regulates mitotic fidelity by maintaining centrosomal homeostasis.Cell Cycle2014;13:2056-63 PMCID:PMC4111697

[96]

Tanwar DK,Gupta P,Alvarez RD,Mitra K.Crosstalk between the mitochondrial fission protein, Drp1, and the cell cycle is identified across various cancer types and can impact survival of epithelial ovarian cancer patients.Oncotarget2016;7:60021-37 PMCID:PMC5312366

[97]

Salazar-Roa M.Fueling the cell division cycle.Trends Cell Biol2017;27:69-81

[98]

Kidd T,Katzen A,Jiménez G,Sullivan W.The epsilon-subunit of mitochondrial ATP synthase is required for normal spindle orientation during the Drosophila embryonic divisions.Genetics2005;170:697-708 PMCID:PMC1450411

[99]

Yamamori T,Bo T,Sakai Y,Yamamoto K,Yasui H.Inhibition of the mitochondrial fission protein dynamin-related protein 1 (Drp1) impairs mitochondrial fission and mitotic catastrophe after x-irradiation.Mol Biol Cell2015;26:4607-17 PMCID:PMC4678018

[100]

Liu L,Smith PJS.Mitochondrial dysfunction leads to telomere attrition and genomic instability.Aging Cell2002;1:40-6

[101]

Veatch JR,Nelson ZW.Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect.Cell2009;137:1247-58 PMCID:PMC2759275

[102]

Choudhury AR.Numtogenesis as a mechanism for development of cancer.Semin Cancer Biol2017;47:101-9

[103]

Chen D,Xiang J.The intra-nucleus integration of mitochondrial DNA (mtDNA) in cervical mucosa cells and its relation with c-myc expression.J Exp Clin Cancer Res2008;27:36 PMCID:PMC2543008

[104]

Srinivasainagendra V,Singh B,Mooga VP,Tiwari HK.Migration of mitochondrial DNA in the nuclear genome of colorectal adenocarcinoma.Genome Med2017;9:31 PMCID:PMC5370490

[105]

Shay JW.New evidence for the insertion of mitochondrial DNA into the human genome: significance for cancer and aging.Mutat Res1992;275:227-35

[106]

Ichim G,Ahmed SU,Giampazolias E,Haller M,Mason SM,Parsons MJ,Bouchier-Hayes L,Rooswinkel RW,Blyth K,Murphy DJ.Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death.Mol Cell2015;57:860-72 PMCID:PMC4352766

[107]

Kitazumi I.Regulation of DNA fragmentation: the role of caspases and phosphorylation.FEBS J2011;278:427-41

[108]

Hangen E,Bénit P,Modjtahedi N.Life with or without AIF.Trends Biochem Sci2010;35:278-87

[109]

Joza N,Daugas E,Cho SK,Sasaki T,Cheng HY,Ferri KF,Wakeham A,Yoshida H,Mak TW,Kroemer G.Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death.Nature2001;410:549-54

[110]

Shelar SB,Reddy SA,Tan CT,Lu J,Hagen T.Thioredoxin-dependent regulation of AIF-mediated DNA damage.Free Radic Biol Med2015;87:125-36

[111]

Minocherhomji S,Singh KK.Mitochondrial regulation of epigenetics and its role in human diseases.Epigenetics2012;7:326-34 PMCID:PMC3368816

[112]

Castegna A,Infantino V.The mitochondrial side of epigenetics.Physiol Genomics2015;47:299-307

[113]

Smiraglia D,Bistulfi GL,Singh KK.A novel role for mitochondria in regulating epigenetic modifications in the nucleus.Cancer Biol Ther2008;7:1182-90 PMCID:PMC2639623

[114]

Bellizzi D,Giordano M,Passarino G.Global DNA methylation levels are modulated by mitochondrial DNA variants.Epigenomics2012;4:17-27

[115]

Amuthan G,Ananadatheerthavarada HK,Shephard HM.Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells.Oncogene2002;21:7839-49

[116]

Guha M,Ruthel G,Carstens RP,Khanna C,Avadhani NG.Mitochondrial retrograde signaling induces epithelial-mesenchymal transition and generates breast cancer stem cells.Oncogene2014;33:5238-50 PMCID:PMC4921233

[117]

Hanahan D.Hallmarks of cancer: the next generation.Cell2011;144:646-74

AI Summary AI Mindmap
PDF

14

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/