Neurobiology of Aging
Volume 30, Issue 11 , Pages 1749-1755 , November 2009

Mitochondrial haplogroup H and Alzheimer's disease—Is there a connection?

  • Aleksandra Maruszak

      Affiliations

    • Department of Neurodegenerative Disorders, Polish Academy of Sciences Medical Research Center, 5 Pawińskiego Street, 02-106 Warsaw, Poland
    • Corresponding Author InformationCorresponding author. Tel.: +48 22 6086485; fax: +48 22 6685532.
    • ,
  • Jeffrey A Canter

      Affiliations

    • Center for Human Genetics Research, Vanderbilt University Medical Center, Nashville, TN, USA
    • ,
  • Maria Styczyńska

      Affiliations

    • Department of Neurodegenerative Disorders, Polish Academy of Sciences Medical Research Center, 5 Pawińskiego Street, 02-106 Warsaw, Poland
    • ,
  • Cezary Żekanowski

      Affiliations

    • Department of Neurodegenerative Disorders, Polish Academy of Sciences Medical Research Center, 5 Pawińskiego Street, 02-106 Warsaw, Poland
    • ,
  • Maria Barcikowska

      Affiliations

    • Department of Neurodegenerative Disorders, Polish Academy of Sciences Medical Research Center, 5 Pawińskiego Street, 02-106 Warsaw, Poland

Received 7 August 2007 ,Revised 5 December 2007 ,Accepted 5 January 2008.

References 

  1. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drobin J, et al. Sequence and organization of the human mitochondrial genome. Nature. 1981;290:457–465
  2. Beal MF. Mitochondrial dysfunction in neurodegenerative diseases. Biochim. Biophys. Acta. 1998;1366:211–223
  3. Bonilla E, Tanji K, Hirano M, Vu TH, DiMauro S, Schon EA. Mitochondrial involvement in Alzheimer's disease. Biochim. Biophys. Acta. 1999;1410:171–182
  4. Brown MD, Shoffner JM, Kim YL, Jun AS, Graham BH, Cabell MF, et al. Mitochondrial DNA sequence analysis of four Alzheimer's and Parkinson's disease patients. Am. J. Hum. Genet. 1996;61:281–289
  5. Burris TP, Krishnan V. Estrogen: a mitochondrial energizer that keeps on going. Mol. Pharmacol. 2005;68:956–958
  6. Cahill L. Why sex matters for neuroscience. Nat. Rev. Neurosci. 2006;7:477–484
  7. Canter JA, Kallianpur AR, Parl FF, Millikan RC. Mitochondrial DNA G10398A polymorphism and invasive breast cancer in African-American women. Cancer Res. 2005;65:8028–8033
  8. Carelli V, Giordano C, d’Amati G. Pathogenic expression of homoplasmic mtDNA mutations needs a complex nuclear-mitochondrial interaction. Trends Genet. 2003;19:257–262
  9. Carrieri G, Bonafe M, De Luca M, Rose G, Varcasia O, Bruni A, et al. Mitochondrial DNA haplogroups and APOE4 allele are non-independent variables in sporadic Alzheimer's disease. Hum. Genet. 2001;108:194–198
  10. Chagnon P, Gee M, Filion M, Robitaille Y, Belouchi M, Gauvreau D. Phylogenetic analysis of the mitochondrial genome indicates significant differences between patients with Alzheimer disease and controls in a French-Canadian founder population. Am. J. Med. Genet. 1999;85:20–30
  11. Chapman J, Estupinan J, Asherow A. A simple and efficient method for apolipoprotein E genotype determination. Neurology. 1996;46:1484–1485
  12. Chinnery PF, Taylor GA, Howell N, Andrews RM, Morris CM, Taylor RW, et al. Mitochondrial DNA haplogroups and susceptibility to AD and dementia with Lewy bodies. Neurology. 2000;55:302–304
  13. Chisu V, Manca P, Lepore G, Gadau S, Zedda M, Farina V. Testosterone induces neuroprotection from oxidative stress. Effects on catalase activity and 3-nitro-L-tyrosine incorporation into alpha-tubulin in a mouse neuroblastoma cell line. Arch. Ital. Biol. 2006;144:63–73
  14. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, et al. Gene dose of apoliprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 1993;261:921–923
  15. Coskun PE, Beal MF, Wallace DC. Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc. Natl. Acad. Sci. U.S.A. 2004;101:10726–10731
  16. Coskun PE, Ruiz-Pesini E, Wallace DC. Control region mtDNA variants: longevity, climatic adaptation, and a forensic conundrum. Proc. Natl. Acad. Sci. U.S.A. 2003;100:2174–2176
  17. Crispim D, Canani LH, Gross JL, Tschiedel B, Souto KEP, Roisenberg I. The European-specific mitochondrial cluster J/T could confer an increased risk of insulin-resistance and type 2 diabetes: An analysis of the m.4216T>C and m. 4917A>G variants. Ann. Hum. Genet. 2005;69:1–8
  18. Elson JL, Herrnstadt C, Preston G, Thal L, Morris CM, Edwardson JA, et al. Does the mitochondrial genome play a role in the etiology of Alzheimer's disease?. Hum. Genet. 2006;12:1–14
  19. Farrer LA, Cupples LA, Haines JL, Hyman B, Kukull WA, Mayeux R, et al. Effects of age, sex, and ethnicity on the association between apoliprotein E genotype and Alzheimer's disease: a meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA. 1997;278:1349–1356
  20. Felty Q, Roy D. Estrogen, mitochondria, and growth of cancer and non-cancer cells. J. Carcinog. 2005;4:1–18
  21. Fesahat F, Houshmand M, Panahi MS, Gharagozli K, Mirzajani F. Do haplogroup H and U act to increase the penetrance of Alzheimer's disease?. Cell Mol. Neurobiol. 2007;27:329–334
  22. Finnilä S, Lehtonen MS, Majamaa K. Phylogenic network for European mtDNA. Am. J. Hum. Genet. 2001;68:1475–1484
  23. Fukuyama H, Ogawa M, Yamauchi H, Yamaguchi S, Kimura J, Yonekura Y, et al. Altered cerebral energy metabolism in Alzheimer's disease: a PET study. J. Nucl. Med. 1994;35:1–6
  24. Gibson GE, Blass JP, Beal MF, Bunik V. The α-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem. Int. 2000;36:97–112
  25. Gibson GE, Haroutunian V, Zhang H, Park LCH, Shi Q, Lesser M, et al. Mitochondrial damage in Alzheimer's disease varies with apolipoprotein E genotype. Ann. Neurol. 2000;48:297–303
  26. Gibson GE, Sheu KF, Blass JP. Abnormalities of mitochondrial enzymes in Alzheimer disease. J. Neural Transm. 1998;105:855–870
  27. Grazina M, Pratas J, Silva F, Oliveira S, Santana I, Oliveira C. Genetic basis of Alzheimer's dementia: role of mtDNA mutations. Genes Brain Behav. 2006;2(Suppl.):92–107
  28. Hofmann S, Bezold R, Jaksch M, Obermaier-Kusser B, Mertens S, Kaufhold P, et al. Wolfram (DIDMOAD) syndrome and Leber hereditary optic neuropathy (LHON) are associated with distinct mitochondrial haplotypes. Genomics. 1997;39:8–18
  29. Howell N, Elson JL, Chinnery PF, Turnbull DM. mtDNA mutations and common neurodegenerative disorders. Trends Genet. 2005;21:583–584
  30. Kalman B, Lublen FD, Alder H. Mitochondria DNA mutations in multiple sclerosis. Mult. Scler. 1995;1:32–36
  31. Kirchner SC, Hallagan SE, Farin FM, Dilley J, Costa-Mallen P, Smith-Weller T, et al. Mitochondrial ND1 sequence analysis and association of the T4216C mutation with Parkinson's disease. Neurotoxicology. 2000;21:441–446
  32. Mahley RW, Weisgraber KH, Huang Y. Apoliprotein E: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2006;103:5644–5651
  33. Mancuso M, Nardini M, Micheli D, Rocchi A, Nesti C, Giglioli NJ, et al. Lack of association between mtDNA haplogroups and Alzheimer's disease in Tuscany. Neurol. Sci. 2007;28:142–147
  34. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34:939–944
  35. Metspalu M, Kivisild T, Metspalu E, Parik J, Hudjashov G, Kaldma K, et al. Most of the extant mtDNA boundaries in South and Southwest Asia were likely shaped during the initial settlement of Eurasia by anatomically modern humans. BMC Genet. 2004;5:26
  36. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16:1215
  37. Moreira PI, Custodio J, Moreno A, Oliveira CR, Santos MS. Tamoxifen and estradiol interact with the flavin mononucleotide site of complex I leading to mitochondrial failure. J. Biol. Chem. 2006;281:10143–10152
  38. Nunomura A, Perry G, Aliev G, Hirai K, Takeda A, Balraj EK, et al. Oxidative damage is the earliest event in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 2001;60:759–767
  39. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA. Involvement of oxidative stress in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 2006;65:631–641
  40. Parihar MS, Brewer GJ. Mitoenergetic failure in Alzheimer disease. Am. J. Physiol., Cell Physiol. 2007;292:C8–C23
  41. Poirier J, Davignon J, Bouthillier D, Kogan S, Bertrand P, Gauthier S. Apoliprotein E polymorphism and Alzheimer's disease. Lancet. 1993;342:697–699
  42. Raber J, Bongers G, LeFevour A, Buttini M, Mucke L. Androgens protect against apolipoprotein E4-induced cognitive deficits. J. Neurosci. 2002;22:5204–5209
  43. Reddy PH, Beal MF. Are mitochondria critical in the pathogenesis of Alzheimer's disease?. Brain Res. Brain Res. Rev. 2005;49:618–632
  44. Risner ME, Saunders AM, Altman JFB, Ormandy GC, Craft S, Foley IM, et al. Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogen. J. 2006;6:246–254
  45. Roostalu U, Kutuev I, Loogvali EL, Metspalu E, Tambets K, Reidla M, et al. Origin and expansion of haplogroup H, the dominant human mitochondrial DNA lineage in West Eurasia: the near Eastern and Caucasian perspective. Mol. Biol. Evol. 2007;24:436–448
  46. Rosario ER, Carroll JC, Oddo S, LaFerla FM, Pike CJ. Androgens regulate the development of neuropathology a triple transgenic mouse model of Alzheimer's disease. J. Neurosci. 2006;26:13384–13389
  47. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, Montoya J, Alvarez E, et al. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am. J. Hum. Genet. 2000;67:682–696
  48. Sullivan PG, Brown MR. Mitochondrial aging and dysfunction in Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2005;29:407–410
  49. Tanaka M, Takeyasu T, Fuku N, Li-Jun G, Kurata M. Mitochondrial genome single nucleotide polymorphisms and their phenotypes in the Japanese. Ann. N.Y. Acad. Sci. 2004;1011:7–20
  50. Torroni A, Huoponen K, Francalacci P, Petrozzi M, Morelli L, Scozzari R, et al. Classification of European mtDNAs from an analysis of three European populations. Genetics. 1996;144:1835–1850
  51. Torroni A, Lott MT, Cabell MF, Chen Y-S, Lavergne L, Wallace DC. mtDNA and the origin of Caucasians: identification of ancient Caucasian-specific haplogroups, one of which is prone to a recurrent somatic duplication in the D-loop region. Am. J. Hum. Genet. 1994;55:760–776
  52. Torroni A, Petrozzi M, D’Urbano L, Sellitto D, Zeviani M, Carrara F, et al. Haplotype and phylogenetic analyses suggest that one European-specific mtDNA background plays a role in the expression of Leber hereditary optic neuropathy by increasing the penetrance of the primary mutations 11778 and 14484. Am. J. Hum. Genet. 1997;60:1107–1121
  53. van der Walt JM, Dementieva YA, Martin ER, Scott WK, Nicodemus KK, Kroner CC, et al. Analysis of European mitochondrial haplogroups with Alzheimer disease risk. Neurosci. Lett. 2004;365:28–32
  54. van der Walt JM, Nicodemus KK, Martin ER, Scott WK, Nance MA, Watts RL, et al. Mitochondrial polymorphisms significantly reduce the risk of Parkinson disease. Am. J. Hum. Genet. 2003;72:804–811
  55. Wang JM, Irwin RW, Brinton RD. Activation of estrogen receptor α increases and estrogen receptor β decreases apoliprotein E expression in hippocampus in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 2006;103:16983–16988
  56. Yaffe K, Barnes D, Lindquist K, Cauley J, Simonsick EM, Penninx B, et al. Endogenous sex hormone levels and risk of cognitive decline in an older biracial cohort. Neurobiol. Aging. 2007;28:171–178
  57. Yaffe K, Haan M, Byers A, Tangen C, Kuller L. Estrogen use, APOE, and cognitive decline. Neurology. 2000;54:1949–1953

PII: S0197-4580(08)00007-9

doi: 10.1016/j.neurobiolaging.2008.01.004

Neurobiology of Aging
Volume 30, Issue 11 , Pages 1749-1755 , November 2009

Article Tools

* Image Usage & Resolution