ApoE gene and exceptional longevity: Insights from three independent cohorts

Experimental Gerontology

Volumn 53, Issue , 2014, Pages 16-23

  Garatachea, Nuria ^a,j   Emanuele, Enzo ^b   Calero, Miguel ^c   Fuku, Noriyuki ^d   Arai, Yasumichi ^e   Abe, Yukiko ^e   Murakami, Haruka ^f   Miyachi, Motohiko ^f   Yvert, Thomas ^g   Verde, Zoraida ^g   Zea, Ma Ascensión ^c   Venturini, Letizia ^b   Santiago, Catalina ^g   Santos Lozano, Alejandro ^h,j   Rodríguez Romo, Gabriel ⁱ   Ricevuti, Giovanni ^b   Hirose, Nobuyoshi ^e   Rábano, Alberto ^c   Lucia, Alejandro ^g,j  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b UNIVERSITY OF PAVIA   (Italy)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f NATIONAL INSTITUTE OF HEALTH AND NUTRITION   (Japan)

^g UNIVERSIDAD EUROPEA DE MADRID   (Spain)

^h UNIVERSITY OF LEÓN   (Spain)

ⁱ UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^j HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

more..

Author keywords

ApoE; Case control study; Centenarians; Genetics; Longevity

Indexed keywords

APOLIPOPROTEIN E;

ADULT; AGED; ALLELE; APOE GENE; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; COMPARATIVE GENE MAPPING; CONTROLLED STUDY; ETHNIC DIFFERENCE; EXCEPTIONAL LONGEVITY; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; GEOGRAPHIC ORIGIN; HUMAN; ITALY; JAPAN; LONGEVITY; MAXIMUM LIKELIHOOD METHOD; PREVALENCE; PRIORITY JOURNAL; SPAIN; VERY ELDERLY; AGING; CLINICAL TRIAL; GENETICS; GENOTYPE; MIDDLE AGED; MULTICENTER STUDY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; AGING; APOLIPOPROTEINS E; CASE-CONTROL STUDIES; COHORT STUDIES; GENE FREQUENCY; GENOTYPE; HUMANS; LONGEVITY; MIDDLE AGED; YOUNG ADULT;

EID: 84894652561     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.02.004     Document Type: Article

References (45)

1. Asada T., Kariya T., Yamagata Z., Kinoshita T., Asaka A. Apolipoprotein E allele in centenarians. Neurology 1996, 46:1484.
2. Beekman M., Blanche H., Perola M., Hervonen A., Bezrukov V., Sikora E., Flachsbart F., Christiansen L., De Craen A.J., Kirkwood T.B., Rea I.M., Poulain M., Robine J.M., Valensin S., Stazi M.A., Passarino G., Deiana L., Gonos E.S., Paternoster L., Sorensen T.I., Tan Q., Helmer Q., van den Akker E.B., Deelen J., Martella F., Cordell H.J., Ayers K.L., Vaupel J.W., Tornwall O., Johnson T.E., Schreiber S., Lathrop M., Skytthe A., Westendorp R.G., Christensen K., Gampe J., Nebel A., Houwing-Duistermaat J.J., Slagboom P.E., Franceschi C., consortium G. Genome-wide linkage analysis for human longevity: genetics of healthy aging study. Aging cell. 2013, 12:184-193.
3. Bennet A.M., Di Angelantonio E., Ye Z., Wensley F., Dahlin A., Ahlbom A., Keavney B., Collins R., Wiman B., de Faire U., Danesh J. Association of apolipoprotein E genotypes with lipid levels and coronary risk. JAMA 2007, 298:1300-1311.
4. Blanche H., Cabanne L., Sahbatou M., Thomas G. A study of French centenarians: are ACE and APOE associated with longevity?. C. R. Acad. Sci. III 2001, 324:129-135.
5. Calero O., Hortigüela R., Bullido M.J., Calero M. Apolipoprotein E genotyping method by real time PCR, a fast and cost-effective alternative to the TaqMan and FRET assays. J. Neurosci. Methods 2009, 183:238-240.
6. Capurso C., Solfrizzi V., D'Introno A., Colacicco A.M., Capurso S.A., Semeraro C., Capurso A., Panza F. Interleukin 6-174G/C promoter gene polymorphism in centenarians: no evidence of association with human longevity or interaction with apolipoprotein E alleles. Exp. Gerontol. 2004, 39:1109-1114.
7. Castro E., Ogburn C.E., Hunt K.E., Tilvis R., Louhija J., Penttinen R., Erkkola R., Panduro A., Riestra R., Piussan C., Deeb S.S., Wang L., Edland S.D., Martin G.M., Oshima J. Polymorphisms at the Werner locus: I. Newly identified polymorphisms, ethnic variability of 1367Cys/Arg, and its stability in a population of Finnish centenarians. Am. J. Med. Genet. 1999, 82:399-403.
8. Christensen K., Johnson T.E., Vaupel J.W. The quest for genetic determinants of human longevity: challenges and insights. Nat. Rev. Genet. 2006, 7:436-448.
9. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
10. Dallongeville J., Lussier-Cacan S., Davignon J. Modulation of plasma triglyceride levels by apoE phenotype: a meta-analysis. J. Lipid Res. 1992, 33:447-454.
11. Drenos F., Kirkwood T.B. Selection on alleles affecting human longevity and late-life disease: the example of apolipoprotein E. PLoS One 2010, 5:e10022.
12. Emanuele E., Fontana J.M., Minoretti P., Geroldi D. Preliminary evidence of a genetic association between chromosome 9p21.3 and human longevity. Rejuvenation Res. 2010, 13:23-26.
13. Feng J., Xiang L., Wan G., Qi K., Sun L., Huang Z., Zheng C., Lv Z., Hu C., Yang Z. Is APOE epsilon3 a favourable factor for the longevity: an association study in Chinese population. J. Genet. 2011, 90:343-347.
14. Fried L.P., Tangen C.M., Walston J., Newman A.B., Hirsch C., Gottdiener J., Seeman T., Tracy R., Kop W.J., Burke G., McBurnie M.A. Frailty in older adults: evidence for a phenotype. J. Gerontol. A Biol. Sci. Med. Sci. 2001, 56:M146-M156.
15. Gerdes L.U., Jeune B., Ranberg K.A., Nybo H., Vaupel J.W. Estimation of apolipoprotein E genotype-specific relative mortality risks from the distribution of genotypes in centenarians and middle-aged men: apolipoprotein E gene is a "frailty gene," not a "longevity gene". Genet. Epidemiol. 2000, 19:202-210.
16. Gomez-Isla T., West H.L., Rebeck G.W., Harr S.D., Growdon J.H., Locascio J.J., Perls T.T., Lipsitz L.A., Hyman B.T. Clinical and pathological correlates of apolipoprotein E epsilon 4 in Alzheimer's disease. Ann. Neurol. 1996, 39:62-70.
17. Gondo Y., Hirose N., Arai Y., Inagaki H., Masui Y., Yamamura K., Shimizu K., Takayama M., Ebihara Y., Nakazawa S., Kitagawa K. Functional status of centenarians in Tokyo, Japan: developing better phenotypes of exceptional longevity. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:305-310.
18. Hallman D.M., Boerwinkle E., Saha N., Sandholzer C., Menzel H.J., Csazar A., Utermann G. The apolipoprotein E polymorphism: a comparison of allele frequencies and effects in nine populations. Am. J. Hum. Genet. 1991, 49:338-349.
19. Hashimoto T., Serrano-Pozo A., Hori Y., Adams K.W., Takeda S., Banerji A.O., Mitani A., Joyner D., Thyssen D.H., Bacskai B.J., Frosch M.P., Spires-Jones T.L., Finn M.B., Holtzman D.M., Hyman B.T. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid beta peptide. J. Neurosci. 2012, 32:15181-15192.
20. Hixson J.E., Vernier D.T. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J. Lipid Res. 1990, 31:545-548.
21. Hjelmborg J.V., Iachine I., Skytthe A., Vaupel J.W., McGue M., Koskenvuo M., Kaprio J., Pedersen N.L., Christensen K. Genetic influence on human lifespan and longevity. Hum. Genet. 2006, 119:312-321.
22. Jacobsen R., Martinussen T., Christiansen L., Jeune B., Andersen-Ranberg K., Vaupel J.W., Christensen K. Increased effect of the ApoE gene on survival at advanced age in healthy and long-lived Danes: two nationwide cohort studies. Aging Cell 2010, 9:1004-1009.
23. Kolovou G., Yiannakouris N., Hatzivassiliou M., Malakos J., Daskalova D., Hatzigeorgiou G., Cariolou M.A., Cokkinos D.V. Association of apolipoprotein E polymorphism with myocardial infarction in Greek patients with coronary artery disease. Curr. Med. Res. Opin. 2002, 18:118-124.
24. Kumar N.T., Liestol K., Loberg E.M., Reims H.M., Brorson S.H., Maehlen J. The apolipoprotein E polymorphism and cardiovascular diseases-an autopsy study. Cardiovasc. Pathol. 2012, 21:461-469.
25. Lewis S.J., Brunner E.J. Methodological problems in genetic association studies of longevity-the apolipoprotein E gene as an example. Int. J. Epidemiol. 2004, 33:962-970.
26. Lindahl-Jacobsen R., Tan Q., Mengel-From J., Christensen K., Nebel A., Christiansen L. Effects of the APOE ε2 allele on mortality and cognitive function in the oldest. J. Gerontol. A Biol. Sci. Med. Sci. 2013, 68:389-394.
27. Liu C.C., Kanekiyo T., Xu H., Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 2013, 9:106-118.
28. Louhija J., Miettinen H.E., Kontula K., Tikkanen M.J., Miettinen T.A., Tilvis R.S. Aging and genetic variation of plasma apolipoproteins. Relative loss of the apolipoprotein E4 phenotype in centenarians. Arterioscler. Thromb. 1994, 14:1084-1089.
29. Louhija J., Viitanen M., Aguero-Torres H., Tilvis R. Survival in Finnish centenarians in relation to apolipoprotein E polymorphism. J. Am. Geriatr. Soc. 2001, 49:1007-1008.
30. Maruszak A., Peplonska B., Safranow K., Chodakowska-Zebrowska M., Barcikowska M., Zekanowski C. TOMM40 rs10524523 polymorphism's role in late-onset Alzheimer's disease and in longevity. J. Alzheimers Dis. 2012, 28:309-322.
31. Nebel A., Kleindorp R., Caliebe A., Nothnagel M., Blanche H., Junge O., Wittig M., Ellinghaus D., Flachsbart F., Wichmann H.E., Meitinger T., Nikolaus S., Franke A., Krawczak M., Lathrop M., Schreiber S. A genome-wide association study confirms APOE as the major gene influencing survival in long-lived individuals. Mech. Ageing Dev. 2011, 132:324-330.
32. Panza F., Solfrizzi V., Torres F., Mastroianni F., Del Parigi A., Colacicco A.M., Basile A.M., Capurso C., Noya R., Capurso A. Decreased frequency of apolipoprotein E epsilon4 allele from Northern to Southern Europe in Alzheimer's disease patients and centenarians. Neurosci. Lett. 1999, 277:53-56.
33. Panza F., Solfrizzi V., Colacicco A.M., Basile A.M., D'Introno A., Capurso C., Sabba M., Capurso S., Capurso A. Apolipoprotein E (APOE) polymorphism influences serum APOE levels in Alzheimer's disease patients and centenarians. Neuroreport 2003, 14:605-608.
34. Pinós T., Fuku N., Cámara Y., Arai Y., Abe Y., Rodríguez-Romo G., Garatachea N., Santos-Lozano A., Miro-Casas E., Ruiz-Meana M., Otaegui I., Murakami H., Miyachi M., Garcia-Dorado D., Hinohara K., Andreu A.L., Kimura A., Hirose N., Lucia A. The rs1333049 polymorphism on locus 9p21.3 and extreme longevity in Spanish and Japanese cohorts. Age 2014, (in press). 10.1007/s11357-013-9593-0.
35. Rebeck G.W., Reiter J.S., Strickland D.K., Hyman B.T. Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 1993, 11:575-580.
36. Sadigh-Eteghad S., Talebi M., Farhoudi M. Association of apolipoprotein E epsilon 4 allele with sporadic late onset Alzheimer's disease. A meta-analysis. Neurosciences (Riyadh) 2012, 17:321-326.
37. Schachter F., Faure-Delanef L., Guenot F., Rouger H., Froguel P., Lesueur-Ginot L., Cohen D. Genetic associations with human longevity at the APOE and ACE loci. Nat. Genet. 1994, 6:29-32.
38. Seripa D., Franceschi M., Matera M.G., Panza F., Kehoe P.G., Gravina C., Orsitto G., Solfrizzi V., Di Minno G., Dallapiccola B., Pilotto A. Sex differences in the association of apolipoprotein E and angiotensin-converting enzyme gene polymorphisms with healthy aging and longevity: a population-based study from Southern Italy. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61:918-923.
39. Singh P.P., Singh M., Mastana S.S. APOE distribution in world populations with new data from India and the UK. Ann. Hum. Biol. 2006, 33:279-308.
40. Slooter A.J., Cruts M., Van Broeckhoven C., Hofman A., van Duijin C.M. Apolipoprotein E and longevity: the Rotterdam Study. J. Am. Geriatr. Soc. 2001, 49:1258-1259.
41. Smith J.D. Apolipoproteins and aging: emerging mechanisms. Ageing Res. Rev. 2002, 1:345-365.
42. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., Roses A.D. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:1977-1981.
43. Takayama M., Hirose N., Arai Y., Gondo Y., Shimizu K., Ebihara Y., Yamamura K., Nakazawa S., Inagaki H., Masui Y., Kitagawa K. Morbidity of Tokyo-area centenarians and its relationship to functional status. J. Gerontol. A Biol. Sci. Med. Sci. 2007, 62:774-782.
44. Verghese P.B., Castellano J.M., Garai K., Wang Y., Jiang H., Shah A., Bu G., Frieden C., Holtzman D.M. ApoE influences amyloid-beta (Abeta) clearance despite minimal apoE/Abeta association in physiological conditions. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E1807-E1816.
45. Wu H.Y., Hudry E., Hashimoto T., Kuchibhotla K., Rozkalne A., Fan Z., Spires-Jones T., Xie H., Arbel-Ornath M., Grosskreutz C.L., Bacskai B.J., Hyman B.T. Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J. Neurosci. 2010, 30:2636-2649.