Disrupting mitochondrial-nuclear coevolution affects OXPHOS complex i integrity and impacts human health

Genome Biology and Evolution

Volumn 6, Issue 10, 2014, Pages 2665-2680

  Gershoni, Moran ^a   Levin, Liron ^a   Ovadia, Ofer ^a   Toiw, Yasmin ^a   Shani, Naama ^a   Dadon, Sara ^a   Barzilai, Nir ^b   Bergman, Aviv ^b   Atzmon, Gil ^b   Wainstein, Julio ^c   Tsur, Anat ^d   Nijtmans, Leo ^e   Glaser, Benjamin ^f   Mishmar, Dan ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c WOLFSON MEDICAL CENTER   (Israel)

^d CLALIT HEALTH SERVICES   (Israel)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

coevolution; complex I; mitochondria; mitonuclear interaction; mtDNA; NDUFC2.

Indexed keywords

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

GENOTYPE; HUMAN; METABOLISM; MOLECULAR EVOLUTION; SITE DIRECTED MUTAGENESIS;

DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX I; EVOLUTION, MOLECULAR; GENOTYPE; HUMANS; MUTAGENESIS, SITE-DIRECTED;

EID: 84917720368     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu208     Document Type: Article

References (68)

1. Achilli A, et al. 2011. Mitochondrial DNA backgrounds might modulate diabetes complications rather than T2DM as a whole. PLoS One 6: E21029
2. Amar S, et al. 2007. Mitochondrial DNA HV lineage increases the susceptibility to schizophrenia among Israeli Arabs. Schizophr Res. 94: 354-358.
3. Balsa E, et al. 2012. NDUFA4 is a subunit of complex IV of the mammalian electron transport chain. Cell Metab. 16:378-386.
4. Barreto FS, Burton RS. 2013. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Mol Biol Evol. 30:310-314.
5. Barrientos A, Kenyon L, Moraes CT. 1998. Human xenomitochondrial cybrids. Cellular models of mitochondrial complex I deficiency. J Biol Chem. 273:14210-14217.
6. Bar-Yaacov D, Blumberg A, Mishmar D. 2012. Mitochondrial-nuclear coevolution and its effects on OXPHOS activity and regulation. Biochim Biophys Acta. 1819:1107-1111.
7. Bayona-Bafaluy MP, Sanchez-Cabo F, Fernandez-Silva P, Perez-Martos A, Enriquez JA. 2011. A genome-wide shRNA screen for new OxPhos related genes. Mitochondrion 11:467-475.
8. Brunmair B, et al. 2004. Thiazolidinediones, like metformin, inhibit respiratory complex I: A common mechanism contributing to their antidiabetic actions? Diabetes 53:1052-1059.
9. Burton RS, Ellison CK, Harrison JS. 2006. The sorry state of F2 hybrids: Consequences of rapid mitochondrial DNA evolution in allopatric populations. Am Nat. 168(Suppl 6): S14-S24.
10. Calvaruso MA, Smeitink J, Nijtmans L. 2008. Electrophoresis techniques to investigate defects in oxidative phosphorylation. Methods 46: 281-287.
11. Calvo SE, Mootha VK. 2010. The mitochondrial proteome and human disease. Annu Rev Genomics Hum Genet. 11:25-44.
12. Davis AA, et al. 1995. A human retinal pigment epithelial cell line that retains epithelial characteristics after prolonged culture. Invest Ophthalmol Vis Sci. 36:955-964.
13. Dowling DK. 2014. Evolutionary perspectives on the links between mitochondrial genotype and disease phenotype. Biochim Biophys Acta. 1840(4): 1393-1403.
14. Efremov RG, Sazanov LA. 2011. Structure of the membrane domain of respiratory complex I. Nature 476:414-420.
15. Ehrenberg B, Montana V, Wei MD, Wuskell JP, Loew LM. 1988. Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophys J. 53:785-794.
16. Feder J, Ovadia O, Glaser B, Mishmar D. 2007. Ashkenazi Jewish mtDNA haplogroup distribution varies among distinct subpopulations: Lessons of population substructure in a closed group. Eur J Hum Genet. 15: 498-500.
17. Feder J, et al. 2008. Differences in mtDNA haplogroup distribution among 3 Jewish populations alter susceptibility to T2DM complications. BMC Genomics 9:198.
18. Feder J, et al. 2009. Parental diabetes status reveals association of mitochondrial DNA haplogroup J1 with type 2 diabetes. BMC Med Genet. 10:60.
19. Fridman Y, et al. 2010. Subtle alterations in PCNA-partner interactions severely impair DNA replication and repair. PLoS Biol. 8:e1000507.
20. Fuku N, et al. 2007. Mitochondrial haplogroup N9a confers resistance against type 2 diabetes in Asians. Am J Hum Genet. 80: 407-415.
21. Gabaldon T, Rainey D, Huynen MA. 2005. Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I). J Mol Biol. 348:857-870.
22. Gaweda-Walerych K, et al. 2010. Mitochondrial transcription factor A variants and the risk of Parkinson's disease. Neurosci Lett. 469: 24-29.
23. Gershoni M, Templeton AR, Mishmar D. 2009. Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31: 642-650.
24. Gershoni M, et al. 2010. Coevolution predicts direct interactions between mtDNA-encoded and nDNA-encoded subunits of oxidative phosphorylation complex I. J Mol Biol. 404:158-171.
25. Gray MW. 2012. Mitochondrial evolution. Cold Spring Harb Perspect Biol. 4:a011403.
26. Grossman LI, Wildman DE, Schmidt TR, Goodman M. 2004. Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet. 20:578-585.
27. Guo LJ, et al. 2005. Mitochondrial genome polymorphisms associated with type-2 diabetes or obesity. Mitochondrion 5:15-33.
28. Guzmán-Fulgencio M, et al. 2013. Mitochondrial haplogroups are associated with clinical pattern of AIDS progression in HIV-infected patients. J Acquir Immune Defic Syndr. 63:178-183.
29. Haack TB, et al. 2012. Mutation screening of 75 candidate genes in 152 complex I deficiency cases identifies pathogenic variants in 16 genes including NDUFB9. J Med Genet. 49:83-89.
30. Hoekstra LA, Siddiq MA, Montooth KL. 2013. Pleiotropic effects of a mitochondrial- nuclear incompatibility depend upon the accelerating effect of temperature in Drosophila. Genetics 195:1129-1139.
31. Hudson G, et al. 2005. Identification of an X-chromosomal locus and haplotype modulating the phenotype of a mitochondrial DNA disorder. Am J Hum Genet. 77:1086-1091.
32. Hudson G, et al. 2013. Two-stage association study and meta-analysis of mitochondrial DNA variants in Parkinson disease. Neurology 80: 2042-2048.
33. Hunte C, Zickermann V, Brandt U. 2010. Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329:448-451.
34. Johnson KR, Zheng QY, Bykhovskaya Y, Spirina O, Fischel-Ghodsian N. 2001. A nuclear-mitochondrial DNA interaction affecting hearing impairment in mice. Nat Genet. 27:191-194.
35. Krempler F, et al. 2002. A functional polymorphism in the promoter of UCP2 enhances obesity risk but reduces type 2 diabetes risk in obese middle-aged humans. Diabetes 51:3331-3335.
36. Lapuente-Brun E, et al. 2013. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340: 1567-1570.
37. Lee HY, et al. 2008. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065-1073.
38. Lefort N, et al. 2010. Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulinresistant human skeletal muscle. Diabetes 59:2444-2452.
39. Lemasters JJ, Ramshesh VK. 2007. Imaging of mitochondrial polarization and depolarization with cationic fluorophores. Methods Cell Biol. 80: 283-295.
40. Lindholm E, Klannemark M, Agardh E, Groop L, Agardh CD. 2004. Putative role of polymorphisms in UCP1-3 genes for diabetic nephropathy. J Diabetes Complications. 18:103-107.
41. Ling C, et al. 2007. Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle. J Clin Invest. 117:3427-3435.
42. Maldonado EN, Patnaik J, Mullins MR, Lemasters JJ. 2010. Free tubulin modulates mitochondrial membrane potential in cancer cells. Cancer Res. 70:10192-10201.
43. Meiklejohn CD, et al. 2013. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9:e1003238.
44. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT. 2011. Understanding mitochondrial complex I assembly in health and disease. Biochim Biophys Acta. 1817:851-862.
45. Mishmar D, et al. 2006. Adaptive selection of mitochondrial complex I subunits during primate radiation. Gene 378:11-18.
46. Mohlke KL, et al. 2005.Mitochondrial polymorphisms and susceptibility to type 2 diabetes-related traits in Finns. Hum Genet. 118:1-10.
47. Muller YL, Bogardus C, Pedersen O, Baier L. 2003. A Gly482Ser missense mutation in the peroxisome proliferator-activated receptor gamma coactivator-1 is associated with altered lipid oxidation and early insulin secretion in Pima Indians. Diabetes 52:895-898.
48. Nishigaki Y, et al. 2007. Mitochondrial haplogroup N9b is protective against myocardial infarction in Japanese males. Hum Genet. 120: 827-836.
49. Olsson AH, et al. 2011. Two common genetic variants near nuclearencoded OXPHOS genes are associated with insulin secretion in vivo. Eur J Endocrinol. 164:765-771.
50. Potluri P, et al. 2009. A novel NDUFA1 mutation leads to a progressive mitochondrial complex I-specific neurodegenerative disease. Mol Genet Metab. 96:189-195.
51. Poulton J, et al. 2002. Type 2 diabetes is associated with a common mitochondrial variant: Evidence from a population-based case-control study. Hum Mol Genet. 11:1581-1583.
52. Rai E, et al. 2007. Interaction between the UCP2-866G/A, mtDNA 10398G/A and PGC1alpha p.Thr394Thr and p.Gly482Ser polymorphisms in type 2 diabetes susceptibility in North Indian population. Hum Genet. 122:535-540.
53. Reitzer LJ, Wice BM, Kennell D. 1979. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem. 254: 2669-2676.
54. Ritov VB, et al. 2010. Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Am J Physiol Endocrinol Metab. 298:E49-E58.
55. Saxena R, et al. 2006. Comprehensive association testing of common mitochondrial DNA variation in metabolic disease. Am J Hum Genet. 79:54-61.
56. Schapira AH. 2006. Mitochondrial disease. Lancet 368:70-82.
57. Stern A, et al. 2007. Selecton 2007: Advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res. 35:W506-W511.
58. Storey JD. 2002. A direct approach to false discovery rates. J R Stat Soc B. 64:479-498.
59. Storey JD, Taylor JE, Siegmund D. 2004. Strong control, conservative point estimation, and simultaneous conservative consistency of false discovery rates: A unified approach. J R Stat Soc B. 66:187-205.
60. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 100:9440-9445.
61. Ueki M, Cordell HJ. 2012. Improved statistics for genome-wide interaction analysis. PLoS Genet. 8:e1002625.
62. Vinothkumar KR, Zhu J, Hirst J. 2014. Architecture of mammalian respiratory complex I. Nature. Advance Access published September 7, 2014, doi: 10.1038/nature13686.
63. Vogel RO, Smeitink JA, Nijtmans LG. 2007. Humanmitochondrial complex I assembly: A dynamic and versatile process. Biochim Biophys Acta. 1767:1215-1227.
64. Wang H, et al. 2004. Uncoupling protein 2 polymorphisms in type 2 diabetes, obesity, and insulin secretion. Am J Physiol Endocrinol Metab. 286:E1-E7.
65. Winklhofer KF, Haass C. 2010. Mitochondrial dysfunction in Parkinson's disease. Biochim Biophys Acta. 1802:29-44.
66. Zeviani M, Di Donato S. 2004. Mitochondrial disorders. Brain 127: 2153-2172.
67. Zhu CT, Ingelmo P, Rand DM. 2014. GxGxE for lifespan in Drosophila: Mitochondrial, nuclear, and dietary interactions that modify longevity. PLoS Genet. 10:e1004354.
68. Zimmermann FA, et al. 2011. Respiratory chain complex I is a mitochondrial tumor suppressor of oncocytic tumors. Front Biosci (Elite Ed) 3: 315-325.