Mitochondrial DNA haplogroup B5 confers genetic susceptibility to Alzheimer's disease in Han Chinese

Neurobiology of Aging

Volumn 36, Issue 3, 2015, Pages 1604.e7-1604.e16

  Bi, Rui ^a,b   Zhang, Wen ^a   Yu, Dandan ^a   Li, Xiao ^a,b   Wang, Hui Zhen ^a,c   Hu, Qiu Xiang ^a,b   Zhang, Chen ^d   Lu, Weihong ^d   Ni, Jianliang ^e   Fang, Yiru ^d   Li, Tao ^f   Yao, Yong Gang ^a  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e Tongde Hospital of Zhejiang Province   (China)

^f SICHUAN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Chinese; Genetic susceptibility; MtDNA haplogroup

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; MT-ATP6 PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ALZHEIMER DISEASE; ARTICLE; CASE CONTROL STUDY; CELL FUNCTION; COHORT ANALYSIS; CONTROLLED STUDY; DNA SEQUENCE; GENE EXPRESSION; GENE FREQUENCY; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPING TECHNIQUE; HAN CHINESE; HELA CELL LINE; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; MAJOR CLINICAL STUDY; MITOCHONDRIAL GENE; MITOCHONDRIAL HAPLOGROUP; MITOCHONDRIAL HAPLOGROUP B5; MT ATP6 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; ALLELE; ASIAN CONTINENTAL ANCESTRY GROUP; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; HAPLOTYPE; METABOLISM; OXYGEN CONSUMPTION; RISK;

ALLELES; ALZHEIMER DISEASE; ASIAN CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; COHORT STUDIES; DNA, MITOCHONDRIAL; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HELA CELLS; HUMANS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES; RISK; SEQUENCE ANALYSIS, DNA;

EID: 84923549761     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.10.009     Document Type: Article

References (52)

1. Andrews R.M., Kubacka I., Chinnery P.F., Lightowlers R.N., Turnbull D.M., Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 1999, 23:147.
2. Bandelt H.J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999, 16:37-48.
3. Bi R., Zhao L., Zhang C., Lu W., Feng J.Q., Wang Y., Ni J., Zhang J., Li G.D., Hu Q.X., Wang D., Yao Y.G., Li T. No association of the LRRK2 genetic variants with Alzheimer's disease in Han Chinese individuals. Neurobiol. Aging 2014, 35:444.e5-444.e9.
4. Bonnet C., Augustin S., Ellouze S., Bénit P., Bouaita A., Rustin P., Sahel J.-A., Corral-Debrinski M. The optimized allotopic expression of ND1 or ND4 genes restores respiratory chain complex I activity in fibroblasts harboring mutations in these genes. Biochim. Biophys. Acta 2008, 1783:1707-1717.
5. Cho D.H., Nakamura T., Fang J., Cieplak P., Godzik A., Gu Z., Lipton S.A. S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 2009, 324:102-105.
6. Corbo R.M., Scacchi R. Apolipoprotein E (APOE) allele distribution in the world. Is APOE*4 a 'thrifty' allele?. Ann. Hum. Genet. 1999, 63:301-310.
7. Coto E., Gomez J., Alonso B., Corao A.I., Diaz M., Menendez M., Martinez C., Calatayud M.T., Moris G., Alvarez V. Late-onset Alzheimer's disease is associated with mitochondrial DNA 7028C/haplogroup H and D310 poly-C tract heteroplasmy. Neurogenetics 2011, 12:345-346.
8. Cruchaga C., Karch C.M., Jin S.C., Benitez B.A., Cai Y., Guerreiro R., Harari O., Norton J., Budde J., Bertelsen S., Jeng A.T., Cooper B., Skorupa T., Carrell D., Levitch D., Hsu S., Choi J., Ryten M., Hardy J., Trabzuni D., Weale M.E., Ramasamy A., Smith C., Sassi C., Bras J., Gibbs J.R., Hernandez D.G., Lupton M.K., Powell J., Forabosco P., Ridge P.G., Corcoran C.D., Tschanz J.T., Norton M.C., Munger R.G., Schmutz C., Leary M., Demirci F.Y., Bamne M.N., Wang X., Lopez O.L., Ganguli M., Medway C., Turton J., Lord J., Braae A., Barber I., Brown K., Passmore P., Craig D., Johnston J., McGuinness B., Todd S., Heun R., Kolsch H., Kehoe P.G., Hooper N.M., Vardy E.R., Mann D.M., Pickering-Brown S., Kalsheker N., Lowe J., Morgan K., David Smith A., Wilcock G., Warden D., Holmes C., Pastor P., Lorenzo-Betancor O., Brkanac Z., Scott E., Topol E., Rogaeva E., Singleton A.B., Kamboh M.I., St George-Hyslop P., Cairns N., Morris J.C., Kauwe J.S., Goate A.M. Rare coding variants in the phospholipase D3 gene confer risk for Alzheimer's disease. Nature 2014, 505:550-554.
9. Di Rienzo A., Hudson R.R. An evolutionary framework for common diseases: the ancestral-susceptibility model. Trends Genet. 2005, 21:596-601.
10. DuBoff B., Feany M., Gotz J. Why size matters - balancing mitochondrial dynamics in Alzheimer's disease. Trends Neurosci. 2013, 36:325-335.
11. Ellouze S., Augustin S., Bouaita A., Bonnet C., Simonutti M., Forster V., Picaud S., Sahel J.A., Corral-Debrinski M. Optimized allotopic expression of the human mitochondrial ND4 prevents blindness in a rat model of mitochondrial dysfunction. Am. J. Hum. Genet. 2008, 83:373-387.
12. Falkenberg M., Larsson N.G., Gustafsson C.M. DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem. 2007, 76:679-699.
13. Fan L., Yao Y.G. An update to MitoTool: using a new scoring system for faster mtDNA haplogroup determination. Mitochondrion 2013, 13:360-363.
14. Fesahat F., Houshmand M., Panahi M.S., Gharagozli K., Mirzajani F. Do haplogroups H and U act to increase the penetrance of Alzheimer's disease?. Cell Mol. Neurobiol. 2007, 27:329-334.
15. Gauderman W.J. Sample size requirements for matched case-control studies of gene-environment interaction. Stat. Med. 2002, 21:35-50.
16. Ghezzi D., Marelli C., Achilli A., Goldwurm S., Pezzoli G., Barone P., Pellecchia M.T., Stanzione P., Brusa L., Bentivoglio A.R., Bonuccelli U., Petrozzi L., Abbruzzese G., Marchese R., Cortelli P., Grimaldi D., Martinelli P., Ferrarese C., Garavaglia B., Sangiorgi S., Carelli V., Torroni A., Albanese A., Zeviani M. Mitochondrial DNA haplogroup K is associated with a lower risk of Parkinson's disease in Italians. Eur. J. Hum. Genet. 2005, 13:748-752.
17. Guo H., Zhuang X.Y., Zhang A.M., Zhang W., Yuan Y., Guo L., Yu D., Liu J., Yang D.K., Yao Y.G. Presence of mutation m.14484T>C in a Chinese family with maternally inherited essential hypertension but no expression of LHON. Biochim. Biophys. Acta 2012, 1822:1535-1543.
18. Hsu P.P., Sabatini D.M. Cancer cell metabolism: Warburg and beyond. Cell 2008, 134:703-707.
19. Huang Y., Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148:1204-1222.
20. Hudson G., Sims R., Harold D., Chapman J., Hollingworth P., Gerrish A., Russo G., Hamshere M., Moskvina V., Jones N., Thomas C., Stretton A., Holmans P.A., O'Donovan M.C., Owen M.J., Williams J., Chinnery P.F. No consistent evidence for association between mtDNA variants and Alzheimer disease. Neurology 2012, 78:1038-1042.
21. Ji F., Sharpley M.S., Derbeneva O., Alves L.S., Qian P., Wang Y., Chalkia D., Lvova M., Xu J., Yao W., Simon M., Platt J., Xu S., Angelin A., Davila A., Huang T., Wang P.H., Chuang L.M., Moore L.G., Qian G., Wallace D.C. Mitochondrial DNA variant associated with Leber hereditary optic neuropathy and high-altitude Tibetans. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7391-7396.
22. Ji Y., Zhang A.-M., Jia X., Zhang Y.-P., Xiao X., Li S., Guo X., Bandelt H.-J., Zhang Q., Yao Y.-G. Mitochondrial DNA haplogroups M7b1'2 and M8a affect clinical expression of leber hereditary optic neuropathy in Chinese families with the m.11778G>A mutation. Am. J. Hum. Genet. 2008, 83:760-768.
23. Jonsson T., Stefansson H., Steinberg S., Jonsdottir I., Jonsson P.V., Snaedal J., Bjornsson S., Huttenlocher J., Levey A.I., Lah J.J., Rujescu D., Hampel H., Giegling I., Andreassen O.A., Engedal K., Ulstein I., Djurovic S., Ibrahim-Verbaas C., Hofman A., Ikram M.A., van Duijn C.M., Thorsteinsdottir U., Kong A., Stefansson K. Variant of TREM2 Associated with the risk of Alzheimer's Disease. N.Engl. J. Med. 2013, 368:107-116.
24. Kaltimbacher V., Bonnet C., Lecoeuvre G., Forster V., Sahel J.A., Corral-Debrinski M. mRNA localization to the mitochondrial surface allows the efficient translocation inside the organelle of a nuclear recoded ATP6 protein. RNA 2006, 12:1408-1417.
25. Karch C.M., Cruchaga C., Goate A.M. Alzheimer's disease genetics: from the bench to the clinic. Neuron 2014, 83:11-26.
26. Krishnan K.J., Ratnaike T.E., De Gruyter H.L., Jaros E., Turnbull D.M. Mitochondrial DNA deletions cause the biochemical defect observed in Alzheimer's disease. Neurobiol. Aging 2012, 33:2210-2214.
27. Lakatos A., Derbeneva O., Younes D., Keator D., Bakken T., Lvova M., Brandon M., Guffanti G., Reglodi D., Saykin A., Weiner M., Macciardi F., Schork N., Wallace D.C., Potkin S.G. Association between mitochondrial DNA variations and Alzheimer's disease in the ADNI cohort. Neurobiol. Aging 2010, 31:1355-1363.
28. Lambert J.C., Ibrahim-Verbaas C.A., Harold D., Naj A.C., Sims R., Bellenguez C., DeStafano A.L., Bis J.C., Beecham G.W., Grenier-Boley B., Russo G., Thorton-Wells T.A., Jones N., Smith A.V., Chouraki V., Thomas C., Ikram M.A., Zelenika D., Vardarajan B.N., Kamatani Y., Lin C.F., Gerrish A., Schmidt H., Kunkle B., Dunstan M.L., Ruiz A., Bihoreau M.T., Choi S.H., Reitz C., Pasquier F., Cruchaga C., Craig D., Amin N., Berr C., Lopez O.L., De Jager P.L., Deramecourt V., Johnston J.A., Evans D., Lovestone S., Letenneur L., Moron F.J., Rubinsztein D.C., Eiriksdottir G., Sleegers K., Goate A.M., Fievet N., Huentelman M.W., Gill M., Brown K., Kamboh M.I., Keller L., Barberger-Gateau P., McGuiness B., Larson E.B., Green R., Myers A.J., Dufouil C., Todd S., Wallon D., Love S., Rogaeva E., Gallacher J., St George-Hyslop P., Clarimon J., Lleo A., Bayer A., Tsuang D.W., Yu L., Tsolaki M., Bossu P., Spalletta G., Proitsi P., Collinge J., Sorbi S., Sanchez-Garcia F., Fox N.C., Hardy J., Deniz Naranjo M.C., Bosco P., Clarke R., Brayne C., Galimberti D., Mancuso M., Matthews F., Moebus S., Mecocci P., Del Zompo M., Maier W., Hampel H., Pilotto A., Bullido M., Panza F., Caffarra P., Nacmias B., Gilbert J.R., Mayhaus M., Lannefelt L., Hakonarson H., Pichler S., Carrasquillo M.M., Ingelsson M., Beekly D., Alvarez V., Zou F., Valladares O., Younkin S.G., Coto E., Hamilton-Nelson K.L., Gu W., Razquin C., Pastor P., Mateo I., Owen M.J., Faber K.M., Jonsson P.V., Combarros O., O'Donovan M.C., Cantwell L.B., Soininen H., Blacker D., Mead S., Mosley T.H., Bennett D.A., Harris T.B., Fratiglioni L., Holmes C., de Bruijn R.F., Passmore P., Montine T.J., Bettens K., Rotter J.I., Brice A., Morgan K., Foroud T.M., Kukull W.A., Hannequin D., Powell J.F., Nalls M.A., Ritchie K., Lunetta K.L., Kauwe J.S., Boerwinkle E., Riemenschneider M., Boada M., Hiltuenen M., Martin E.R., Schmidt R., Rujescu D., Wang L.S., Dartigues J.F., Mayeux R., Tzourio C., Hofman A., Nothen M.M., Graff C., Psaty B.M., Jones L., Haines J.L., Holmans P.A., Lathrop M., Pericak-Vance M.A., Launer L.J., Farrer L.A., van Duijn C.M., Van Broeckhoven C., Moskvina V., Seshadri S., Williams J., Schellenberg G.D., Amouyel P. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat. Genet. 2013, 45:1452-1458.
29. Liang W.S., Reiman E.M., Valla J., Dunckley T., Beach T.G., Grover A., Niedzielko T.L., Schneider L.E., Mastroeni D., Caselli R., Kukull W., Morris J.C., Hulette C.M., Schmechel D., Rogers J., Stephan D.A. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4441-4446.
30. Mancuso M., Calsolaro V., Orsucci D., Siciliano G., Murri L. Is there a primary role of the mitochondrial genome in Alzheimer's disease?. J.Bioenerg. Biomembr. 2009, 41:411-416.
31. Manfredi G., Fu J., Ojaimi J., Sadlock J.E., Kwong J.Q., Guy J., Schon E.A. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat. Genet. 2002, 30:394-399.
32. Maruszak A., Canter J.A., Styczynska M., Zekanowski C., Barcikowska M. Mitochondrial haplogroup H and Alzheimer's disease-is there a connection?. Neurobiol. Aging 2009, 30:1749-1755.
33. Maruszak A., Safranow K., Branicki W., Gaweda-Walerych K., Pospiech E., Gabryelewicz T., Canter J.A., Barcikowska M., Zekanowski C. The impact of mitochondrial and nuclear DNA variants on late-onset Alzheimer's disease risk. J.Alzheimers Dis. 2011, 27:197-210.
34. Mattson M.P., Gleichmann M., Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766.
35. Mishmar D., Ruiz-Pesini E., Golik P., Macaulay V., Clark A.G., Hosseini S., Brandon M., Easley K., Chen E., Brown M.D., Sukernik R.I., Olckers A., Wallace D.C. Natural selection shaped regional mtDNA variation in humans. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:171-176.
36. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N.Engl. J. Med. 2010, 362:329-344.
37. Rhein V., Song X., Wiesner A., Ittner L.M., Baysang G., Meier F., Ozmen L., Bluethmann H., Drose S., Brandt U., Savaskan E., Czech C., Gotz J., Eckert A. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20057-20062.
38. Ridge P.G., Koop A., Maxwell T.J., Bailey M.H., Swerdlow R.H., Kauwe J.S., Honea R.A. Mitochondrial haplotypes associated with biomarkers for Alzheimer's disease. PLoS One 2013, 8:e74158.
39. Ruiz-Pesini E., Mishmar D., Brandon M., Procaccio V., Wallace D.C. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 2004, 303:223-226.
40. Santoro A., Balbi V., Balducci E., Pirazzini C., Rosini F., Tavano F., Achilli A., Siviero P., Minicuci N., Bellavista E., Mishto M., Salvioli S., Marchegiani F., Cardelli M., Olivieri F., Nacmias B., Chiamenti A.M., Benussi L., Ghidoni R., Rose G., Gabelli C., Binetti G., Sorbi S., Crepaldi G., Passarino G., Torroni A., Franceschi C. Evidence for sub-haplogroup h5 of mitochondrial DNA as a risk factor for late onset Alzheimer's disease. PLoS One 2010, 5:e12037.
41. Schmidt C., Lepsverdize E., Chi S.L., Das A.M., Pizzo S.V., Dityatev A., Schachner M. Amyloid precursor protein and amyloid beta-peptide bind to ATP synthase and regulate its activity at the surface of neural cells. Mol. Psychiatry 2008, 13:953-969.
42. Swerdlow R.H., Burns J.M., Khan S.M. The Alzheimer's disease mitochondrial cascade hypothesis: progress and perspectives. Biochim. Biophys. Acta 2014, 1842:1219-1231.
43. Tanzi R.E. The genetics of Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2.
44. Tranah G.J., Nalls M.A., Katzman S.M., Yokoyama J.S., Lam E.T., Zhao Y., Mooney S., Thomas F., Newman A.B., Liu Y., Cummings S.R., Harris T.B., Yaffe K. Mitochondrial DNA sequence variation associated with dementia and cognitive function in the elderly. J.Alzheimers Dis. 2012, 32:357-372.
45. Tranah G.J., Yokoyama J.S., Katzman S.M., Nalls M.A., Newman A.B., Harris T.B., Cesari M., Manini T.M., Schork N.J., Cummings S.R., Liu Y., Yaffe K. Mitochondrial DNA sequence associations with dementia and amyloid-beta in elderly African Americans. Neurobiol. Aging 2014, 35:442.e441-442.e448.
46. van der Walt J.M., Dementieva Y.A., Martin E.R., Scott W.K., Nicodemus K.K., Kroner C.C., Welsh-Bohmer K.A., Saunders A.M., Roses A.D., Small G.W., Schmechel D.E., Murali Doraiswamy P., Gilbert J.R., Haines J.L., Vance J.M., Pericak-Vance M.A. Analysis of European mitochondrial haplogroups with Alzheimer disease risk. Neurosci. Lett. 2004, 365:28-32.
47. van Oven M., Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 2009, 30:E386-E394.
48. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
49. Yao J., Irwin R.W., Zhao L., Nilsen J., Hamilton R.T., Brinton R.D. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14670-14675.
50. Yao Y.G., Kong Q.P., Bandelt H.J., Kivisild T., Zhang Y.P. Phylogeographic differentiation of mitochondrial DNA in Han Chinese. Am. J. Hum. Genet. 2002, 70:635-651.
51. Zhang A.-M., Jia X., Bi R., Salas A., Li S., Xiao X., Wang P., Guo X., Kong Q.-P., Zhang Q., Yao Y.-G. Mitochondrial DNA haplogroup background affects LHON, but not suspected LHON, in Chinese patients. PLoS One 2011, 6:e27750.
52. Zhang W., Tang J., Zhang A.M., Peng M.S., Xie H.B., Tan L., Xu L., Zhang Y.P., Chen X., Yao Y.G. Amatrilineal genetic legacy from the last glacial maximum confers susceptibility to schizophrenia in Han Chinese. J.Genet. Genomics 2014, 41:397-407.