Mitochondrial DNA in tumor initiation, progression, and metastasis: Role of horizontal mtDNA transfer

Cancer Research

Volumn 75, Issue 16, 2015, Pages 3203-3208

  Berridge, Michael V ^a   Dong, Lanfeng ^b   Neuzil, Jiri ^b,c  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^b GRIFFITH UNIVERSITY   (Australia)

^c INSTITUTE OF BIOTECHNOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BREAST CARCINOMA; CARCINOGENESIS; CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; CYTOPLASM; CYTOPLASMIC BRIDGE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA POLYMORPHISM; DNA SEQUENCE; DNA TRANSFER; ELECTRON TRANSPORT; ENDOCYTOSIS; ENERGY METABOLISM; GLYCOLYSIS; HORIZONTAL GENE TRANSFER; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; LUNG ADENOCARCINOMA; METABOLIC REGULATION; METASTASIS; MITOCHONDRIAL RESPIRATION; MUTATION; NONHUMAN; OSTEOSARCOMA; OXIDATIVE STRESS; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; TRIPLE NEGATIVE BREAST CANCER; TUMOR CELL; TUMOR CELL CULTURE; TUMOR GROWTH; ANIMAL; DISEASE COURSE; GENE TRANSFER; GENETIC PROCEDURES; GENETICS; METABOLISM; MITOCHONDRION; NEOPLASM; PATHOLOGY; TRANSPLANTATION; TRENDS;

ANIMALS; DISEASE PROGRESSION; DNA, MITOCHONDRIAL; GENE TRANSFER TECHNIQUES; GENETIC TECHNIQUES; HUMANS; MITOCHONDRIA; MUTATION; NEOPLASM METASTASIS; NEOPLASMS;

EID: 84942895449     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0859     Document Type: Article

References (41)

1. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004;303: 1007-10.
2. Spees JL, Olson SD, Whitney MJ, Prockop DJ. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci U S A 2006;103:1283-8.
3. Cho YM, Kim JH, Kim M, Park SJ, Koh SH, Ahn HS, et al. Mesenchymal stem cells transfer mitochondria to the cells with virtually no mitochondrial function but not with pathogenic mtDNA mutations. PLoS One 2012;7: e32778.
4. Lou E, Fujisawa S, Morozov A, Barlas A, Romin Y, Dogan Y, et al. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One 2012;7: e33093.
5. Pasquier J, Guerrouahen BS, Al Thawadi H, Ghiabi P, Maleki M, Abu-Kaoud N, et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 2013;11:94.
6. Antanaviciuté I, Rysevaite K, Liutkevicius V, Marandykina A, Rimkuté L, Sveikatiené R, et al. Long-distance communication between laryngeal carcinoma cells. PLoS One 2014;9:e99196.
7. Wang X, Gerdes HH. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ 2015;22:1181-91.
8. Caicedo A, Fritz V, Brondello JM, Ayala M, Dennemont I, Abdellaoui N, et al. MitoCeption as a new tool to assess the effects of mesenchymal stem/stromal cell mitochondria on cancer cellmetabolism and function. Sci Rep 2015;5:9073.
9. Onfelt B, Nedvetzki S, Benninger RK, Purbhoo MA, Sowinski S, Hume AN, et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol 2006;177:8476-83.
10. Gerdes HH, Carvalho RN. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol 2008;20:470-5.
11. Plotnikov EY, Khryapenkova TG, Galkina SI, Sukhikh GT, Zorov DB. Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture. Exp Cell Res 2010; 316:2447-55.
12. Acquistapace A, Bru T, Lesault PF, Figeac F, Coudert AE, le Coz O, et al. Humanmesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells 2011;29:812-24.
13. Vallabhaneni KC, Haller H, Dumler I. Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes. Stem Cells Dev 2012; 21:3104-13.
14. Liu K, Chi L, Guo L, Liu X, Luo C, Zhang S, et al. The interactions between brain microvascular endothelial cells and mesenchymal stem cells under hypoxic conditions. Microvasc Res 2008;75:59-67.
15. Liu K, Ji K, Guo L, WuW, Lu H, Shan P, et al. Mesenchymal stem cells rescue injured endothelial cells in an in vitro ischemia-reperfusion model via tunneling nanotube like structure-mediatedmitochondrial transfer. Microvasc Res 2014;92:10-8.
16. Rebbeck CA, Leroi AM, Burt A. Mitochondrial capture by a transmissible cancer. Science 2011;331:303.
17. Strakova A, Murchison EP. The cancer which survived: insights from the genome of an 11000 year-old cancer. Curr Opin Genet Dev 2015;30: 49-55.
18. Islam MN, Das SR, Emin MT, Wei M, Sun L, Westphalen K, et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 2012; 18:759-65.
19. Ahmad T, Mukherjee S, Pattnaik B, Kumar M, Singh S, Kumar M, et al. Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J 2014;33:994-1010.
20. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
21. Ito K, Suda T. Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol 2014;15:243-56.
22. Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J, et al. Mitochondrial genome acquisition restores respiratory function and tumorigenic potential in cancer cells without mitochondrial DNA. Cell Metab 2015;21:81-94.
23. Zu XL, Guppy M. Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun 2004;313:459-65.
24. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
25. Herst PM, Berridge MV. Cell surface oxygen consumption: a major contributor to cellular oxygen consumption in glycolytic cancer cell lines. Biochim Biophys Acta 2007;1767:170-7.
26. Kulawiec M, Safina A, Desouki MM, Still I, Matsui S, Bakin A, et al. Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion. Cancer Biol Ther 2008;7:1732-43.
27. Brandon M, Baldi P, Wallace DC. Mitochondrial mutations in cancer. Oncogene 2006;25:4647-62.
28. Wallace DC. Mitochondria and cancer. Nat Rev Cancer 2012;12: 685-98.
29. Hayashi J, Takemitsu M, Nonaka I. Recovery of themissing tumorigenicity in mitochondrial DNA-less HeLa cells by introduction of mitochondrial DNA from normal human cells. Somat Cell Mol Genet 1992;18:123-9.
30. Imanishi H, Hattori K, Wada R, Ishikawa K, Fukuda S, Takenaga K, et al. Mitochondrial DNA mutations regulate metastasis of human breast cancer cells. PLoS One 2011;6:e23401.
31. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, et al. ROS-generatingmitochondrialDNAmutations can regulate tumor cell metastasis. Science 2008;320:661-4.
32. Berridge MV, Tan AS. Effects of mitochondrial gene deletion on tumorigenicity of metastatic melanoma: reassessing the Warburg effect. Rejuvenation Res 2010;13:139-41.
33. Davis DM, Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 2008;9:431-6.
34. Sowinski S, Alakoskela JM, Jolly C, Davis DM. Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1. Methods 2011;53:27-33.
35. Davis CH, Kim KY, Bushong EA, Mills EA, Boassa D, Shih T, et al. Transcellular degradation of axonal mitochondria. Proc Natl Acad Sci U S A 2014;111:9633-8.
36. Rogers RS, Bhattacharya J. When cells become organelle donors. Physiology 2013;28:414-22.
37. Villanueva MT. Metabolism: the mitochondria thief. Nat Rev Cancer 2015;15:70.
38. LeBleu VS, O'Connell JT, Gonzalez Herrera KN, Wikman H, Pantel K, HaigisMC, et al. PGC-1a mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol 2014;16:992-1003.
39. Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sánchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014;514:628-32.
40. Bukoreshtliev NV, Wang X, Hodneland E, Gurke S, Barroso JF, Gerdes HH. Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett 2009; 583:1481-8.
41. Lin HY, Liou CW, Chen S, Hsu TY, Chuang JH, Wang PW, et al. Mitochondrial transfer from Wharton's jelly-derived mesenchymal stem cells to mitochondria-defective cells recaptures impaired mitochondrial function. Mitochondrion 2015;22:31-4.