Mosaic Loss of Chromosome y in Blood Is Associated with Alzheimer Disease

American Journal of Human Genetics

Volumn 98, Issue 6, 2016, Pages 1208-1219

  Dumanski, Jan P ^a   Lambert, Jean Charles ^b   Rasi, Chiara ^a   Giedraitis, Vilmantas ^c   Davies, Hanna ^a   Grenier Boley, Benjamin ^b   Lindgren, Cecilia M ^d,e   Campion, Dominique ^f   Dufouil, Carole ^g   Pasquier, Florence ^b,h   Amouyel, Philippe ^b   Lannfelt, Lars ^c   Ingelsson, Martin ^c   Kilander, Lena ^c   Lind, Lars ^a   Forsberg, Lars A ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIV LILLE   (France)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f ROUEN UNIVERSITY HOSPITAL   (France)

^g INSERM   (France)

^h LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE; AGED; ALZHEIMER DISEASE; APOLIPOPROTEIN E GENE; ARTICLE; BLOOD CELL; BLOOD SAMPLING; CONTROLLED STUDY; FEMALE; FOLLOW UP; GENE; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; HUMAN; IMMUNOSURVEILLANCE; MAJOR CLINICAL STUDY; MALE; MOSAICISM; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; RISK FACTOR; SMOKING; Y CHROMOSOME; BLOOD; CASE CONTROL STUDY; COMPARATIVE STUDY; GENETICS; LONGITUDINAL STUDY; MIDDLE AGED; PROGNOSIS; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; SINGLE NUCLEOTIDE POLYMORPHISM; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; CASE-CONTROL STUDIES; CHROMOSOMES, HUMAN, Y; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MOSAICISM; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS; PROSPECTIVE STUDIES; RISK FACTORS;

EID: 84971569993     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.05.014     Document Type: Article

References (62)

1. K. Bettens, K. Sleegers, and C. Van Broeckhoven Genetic insights in Alzheimer's disease Lancet Neurol. 12 2013 92 104
2. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
3. M. Gatz, C.A. Reynolds, L. Fratiglioni, B. Johansson, J.A. Mortimer, S. Berg, A. Fiske, and N.L. Pedersen Role of genes and environments for explaining Alzheimer disease Arch. Gen. Psychiatry 63 2006 168 174
4. E. Genin, D. Hannequin, D. Wallon, K. Sleegers, M. Hiltunen, O. Combarros, M.J. Bullido, S. Engelborghs, P. De Deyn, C. Berr, and et al. APOE and Alzheimer disease: a major gene with semi-dominant inheritance Mol. Psychiatry 16 2011 903 907
5. J.C. Lambert, C.A. Ibrahim-Verbaas, D. Harold, A.C. Naj, R. Sims, C. Bellenguez, A.L. DeStafano, J.C. Bis, G.W. Beecham, B. Grenier-Boley, et al. European Alzheimer's Disease Initiative (EADI) Genetic and Environmental Risk in Alzheimer's Disease Alzheimer's Disease Genetic Consortium Cohorts for Heart and Aging Research in Genomic Epidemiology Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease Nat. Genet. 45 2013 1452 1458
6. V. Escott-Price, C. Bellenguez, L.S. Wang, S.H. Choi, D. Harold, L. Jones, P. Holmans, A. Gerrish, A. Vedernikov, A. Richards, et al. United Kingdom Brain Expression Consortium Cardiovascular Health Study (CHS) Gene-wide analysis detects two new susceptibility genes for Alzheimer's disease PLoS ONE 9 2014 e94661
7. R. Guerreiro, A. Wojtas, J. Bras, M. Carrasquillo, E. Rogaeva, E. Majounie, C. Cruchaga, C. Sassi, J.S. Kauwe, S. Younkin, et al. Alzheimer Genetic Analysis Group TREM2 variants in Alzheimer's disease N. Engl. J. Med. 368 2013 117 127
8. J.C. Lambert, B. Grenier-Boley, D. Harold, D. Zelenika, V. Chouraki, Y. Kamatani, K. Sleegers, M.A. Ikram, M. Hiltunen, C. Reitz, and et al. Genome-wide haplotype association study identifies the FRMD4A gene as a risk locus for Alzheimer's disease Mol. Psychiatry 18 2013 461 470
9. B.A. Benitez, S.C. Jin, R. Guerreiro, R. Graham, J. Lord, D. Harold, R. Sims, J.C. Lambert, J.R. Gibbs, J. Bras, et al. 3C Study Group EADI consortium Alzheimer's Disease Genetic Consortium (ADGC) Alzheimer's Disease Neuroimaging Initiative (ADNI) GERAD Consortium Missense variant in TREML2 protects against Alzheimer's disease Neurobiol. Aging 35 2014 1510.e19 1510.e26
10. International Genomics of Alzheimer's Disease Consortium (IGAP) Convergent genetic and expression data implicate immunity in Alzheimer's disease Alzheimers Dement. 11 2014 658 671
11. J. Chapman, E. Rees, D. Harold, D. Ivanov, A. Gerrish, R. Sims, P. Hollingworth, A. Stretton, P. Holmans, M.J. Owen, et al. GERAD1 Consortium A genome-wide study shows a limited contribution of rare copy number variants to Alzheimer's disease risk Hum. Mol. Genet. 22 2013 816 824
12. L.A. Forsberg, D. Absher, and J.P. Dumanski Non-heritable genetics of human disease: spotlight on post-zygotic genetic variation acquired during lifetime J. Med. Genet. 50 2013 1 10
13. L.A. Forsberg, C. Rasi, H.R. Razzaghian, G. Pakalapati, L. Waite, K.S. Thilbeault, A. Ronowicz, N.E. Wineinger, H.K. Tiwari, D. Boomsma, and et al. Age-related somatic structural changes in the nuclear genome of human blood cells Am. J. Hum. Genet. 90 2012 217 228
14. K.B. Jacobs, M. Yeager, W. Zhou, S. Wacholder, Z. Wang, B. Rodriguez-Santiago, A. Hutchinson, X. Deng, C. Liu, M.J. Horner, and et al. Detectable clonal mosaicism and its relationship to aging and cancer Nat. Genet. 44 2012 651 658
15. C.C. Laurie, C.A. Laurie, K. Rice, K.F. Doheny, L.R. Zelnick, C.P. McHugh, H. Ling, K.N. Hetrick, E.W. Pugh, C. Amos, and et al. Detectable clonal mosaicism from birth to old age and its relationship to cancer Nat. Genet. 44 2012 642 650
16. G. Genovese, A.K. Kähler, R.E. Handsaker, J. Lindberg, S.A. Rose, S.F. Bakhoum, K. Chambert, E. Mick, B.M. Neale, M. Fromer, and et al. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence N. Engl. J. Med. 371 2014 2477 2487
17. S. Jaiswal, P. Fontanillas, J. Flannick, A. Manning, P.V. Grauman, B.G. Mar, R.C. Lindsley, C.H. Mermel, N. Burtt, A. Chavez, and et al. Age-related clonal hematopoiesis associated with adverse outcomes N. Engl. J. Med. 371 2014 2488 2498
18. J. Score, A. Chase, L.A. Forsberg, L. Feng, K. Waghorn, A.V. Jones, C. Rasi, D.C. Linch, J.P. Dumanski, R.E. Gale, and N.C. Cross Detection of leukemia-associated mutations in peripheral blood DNA of hematologically normal elderly individuals Leukemia 29 2015 1600 1602
19. A. Bonnefond, B. Skrobek, S. Lobbens, E. Eury, D. Thuillier, S. Cauchi, O. Lantieri, B. Balkau, E. Riboli, M. Marre, and et al. Association between large detectable clonal mosaicism and type 2 diabetes with vascular complications Nat. Genet. 45 2013 1040 1043
20. C.M. de Carvalho, and F.R. Santos Human Y-chromosome variation and male dysfunction J. Mol. Genet. Med. 1 2005 63 75
21. J.F. Hughes, and S. Rozen Genomics and genetics of human and primate y chromosomes Annu. Rev. Genomics Hum. Genet. 13 2012 83 108
22. P.A. Jacobs, M. Brunton, W.M. Court Brown, R. Doll, and H. Goldstein Change of human chromosome count distribution with age: evidence for a sex differences Nature 197 1963 1080 1081
23. R.V. Pierre, and H.C. Hoagland Age-associated aneuploidy: loss of Y chromosome from human bone marrow cells with aging Cancer 30 1972 889 894
24. G.P. Nowinski, D.L. Van Dyke, B.C. Tilley, G. Jacobsen, V.R. Babu, M.J. Worsham, G.N. Wilson, and L. Weiss The frequency of aneuploidy in cultured lymphocytes is correlated with age and gender but not with reproductive history Am. J. Hum. Genet. 46 1990 1101 1111
25. United Kingdom Cancer Cytogenetics Group (UKCCG) Loss of the Y chromosome from normal and neoplastic bone marrows Genes Chromosomes Cancer 5 1992 83 88
26. A. Wiktor, B.A. Rybicki, Z.S. Piao, M. Shurafa, B. Barthel, K. Maeda, and D.L. Van Dyke Clinical significance of Y chromosome loss in hematologic disease Genes Chromosomes Cancer 27 2000 11 16
27. A.K. Wong, B. Fang, L. Zhang, X. Guo, S. Lee, and R. Schreck Loss of the Y chromosome: an age-related or clonal phenomenon in acute myelogenous leukemia/myelodysplastic syndrome? Arch. Pathol. Lab. Med. 132 2008 1329 1332
28. A.E. Wiktor, D.L. Van Dyke, J.M. Hodnefield, J. Eckel-Passow, and C.A. Hanson The significance of isolated Y chromosome loss in bone marrow metaphase cells from males over age 50 years Leuk. Res. 35 2011 1297 1300
29. P.A. Jacobs, V. Maloney, R. Cooke, J.A. Crolla, A. Ashworth, and A.J. Swerdlow Male breast cancer, age and sex chromosome aneuploidy Br. J. Cancer 108 2013 959 963
30. L.A. Forsberg, C. Rasi, N. Malmqvist, H. Davies, S. Pasupulati, G. Pakalapati, J. Sandgren, T. Diaz de Ståhl, A. Zaghlool, V. Giedraitis, and et al. Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer Nat. Genet. 46 2014 624 628
31. J.P. Dumanski, C. Rasi, M. Lönn, H. Davies, M. Ingelsson, V. Giedraitis, L. Lannfelt, P.K. Magnusson, C.M. Lindgren, A.P. Morris, and et al. Mutagenesis. Smoking is associated with mosaic loss of chromosome Y Science 347 2015 81 83
32. L.J. Zhang, E.S. Shin, Z.X. Yu, and S.B. Li Molecular genetic evidence of Y chromosome loss in male patients with hematological disorders Chin. Med. J. (Engl.) 120 2007 2002 2005
33. N.O. Bianchi Y chromosome structural and functional changes in human malignant diseases Mutat. Res. 682 2009 21 27
34. L.C.S. Veiga, N.A. Bérgamo, P.P. Reis, L.P. Kowalski, and S.R. Rogatto Loss of Y-chromosome does not correlate with age at onset of head and neck carcinoma: a case-control study Braz. J. Med. Biol. Res. 45 2012 172 178
35. P.H. Duijf, N. Schultz, and R. Benezra Cancer cells preferentially lose small chromosomes Int. J. Cancer 132 2013 2316 2326
36. C. Ganster, D. Kämpfe, K. Jung, F. Braulke, K. Shirneshan, S. Machherndl-Spandl, S. Suessner, C.P. Bramlage, T.J. Legler, M.J. Koziolek, and et al. New data shed light on Y-loss-related pathogenesis in myelodysplastic syndromes Genes Chromosomes Cancer 54 2015 717 724
37. P. Noveski, S. Madjunkova, E. Sukarova Stefanovska, N. Matevska Geshkovska, M. Kuzmanovska, A. Dimovski, and D. Plaseska-Karanfilska Loss of Y Chromosome in Peripheral Blood of Colorectal and Prostate Cancer Patients PLoS ONE 11 2016 e0146264
38. L. Persani, M. Bonomi, A. Lleo, S. Pasini, F. Civardi, I. Bianchi, I. Campi, P. Finelli, M. Miozzo, C. Castronovo, and et al. Increased loss of the Y chromosome in peripheral blood cells in male patients with autoimmune thyroiditis J. Autoimmun. 38 2012 J193 J196
39. A. Lleo, S. Oertelt-Prigione, I. Bianchi, L. Caliari, P. Finelli, M. Miozzo, R. Lazzari, A. Floreani, F. Donato, M. Colombo, and et al. Y chromosome loss in male patients with primary biliary cirrhosis J. Autoimmun. 41 2013 87 91
40. J.C. Lambert, S. Heath, G. Even, D. Campion, K. Sleegers, M. Hiltunen, O. Combarros, D. Zelenika, M.J. Bullido, B. Tavernier, et al. European Alzheimer's Disease Initiative Investigators Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease Nat. Genet. 41 2009 1094 1099
41. 3C Study Group Vascular factors and risk of dementia: design of the Three-City Study and baseline characteristics of the study population Neuroepidemiology 22 2003 316 325
42. H. Hedstrand A study of middle-aged men with particular reference to risk factors for cardiovascular disease Ups. J. Med. Sci. Suppl. 19 1975 1 61
43. L. Lind, N. Fors, J. Hall, K. Marttala, and A. Stenborg A comparison of three different methods to evaluate endothelium-dependent vasodilation in the elderly: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study Arterioscler. Thromb. Vasc. Biol. 25 2005 2368 2375
44. G. McKhann, D. Drachman, M. Folstein, R. Katzman, D. Price, and E.M. Stadlan 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 34 1984 939 944
45. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
46. V. Boeva, T. Popova, K. Bleakley, P. Chiche, J. Cappo, G. Schleiermacher, I. Janoueix-Lerosey, O. Delattre, and E. Barillot Control-FREEC: a tool for assessing copy number and allelic content using next-generation sequencing data Bioinformatics 28 2012 423 425
47. R Development Core Team R: A language and environment for statistical computing 2012 R Foundation for Statistical Computing Vienna, Austria
48. J.K. Cataldo, J.J. Prochaska, and S.A. Glantz Cigarette smoking is a risk factor for Alzheimer's Disease: an analysis controlling for tobacco industry affiliation J. Alzheimers Dis. 19 2010 465 480
49. S. Norton, F.E. Matthews, D.E. Barnes, K. Yaffe, and C. Brayne Potential for primary prevention of Alzheimer's disease: an analysis of population-based data Lancet Neurol. 13 2014 788 794
50. P. Jha, C. Ramasundarahettige, V. Landsman, B. Rostron, M. Thun, R.N. Anderson, T. McAfee, and R. Peto 21st-century hazards of smoking and benefits of cessation in the United States N. Engl. J. Med. 368 2013 341 350
51. A.R. Simard, D. Soulet, G. Gowing, J.P. Julien, and S. Rivest Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease Neuron 49 2006 489 502
52. M. Schwartz, and R. Shechter Protective autoimmunity functions by intracranial immunosurveillance to support the mind: The missing link between health and disease Mol. Psychiatry 15 2010 342 354
53. S.S. Ousman, and P. Kubes Immune surveillance in the central nervous system Nat. Neurosci. 15 2012 1096 1101
54. P. Maheshwari, and G.D. Eslick Bacterial infection and Alzheimer's disease: a meta-analysis J. Alzheimers Dis. 43 2015 957 966
55. H. Lovheim, J. Gilthorpe, A. Johansson, S. Eriksson, G. Hallmans, and F. Elgh Herpes simplex infection and the risk of Alzheimer's disease-A nested case-control study Alzheimers Dement. 11 2015 587 592
56. T. Arendt Cell cycle activation and aneuploid neurons in Alzheimer's disease Mol. Neurobiol. 46 2012 125 135
57. M.J. McConnell, M.R. Lindberg, K.J. Brennand, J.C. Piper, T. Voet, C. Cowing-Zitron, S. Shumilina, R.S. Lasken, J.R. Vermeesch, I.M. Hall, and F.H. Gage Mosaic copy number variation in human neurons Science 342 2013 632 637
58. L.K. Case, E.H. Wall, J.A. Dragon, N. Saligrama, D.N. Krementsov, M. Moussawi, J.F. Zachary, S.A. Huber, E.P. Blankenhorn, and C. Teuscher The Y chromosome as a regulatory element shaping immune cell transcriptomes and susceptibility to autoimmune disease Genome Res. 23 2013 1474 1485
59. B.D. James, S.E. Leurgans, L.E. Hebert, P.A. Scherr, K. Yaffe, and D.A. Bennett Contribution of Alzheimer disease to mortality in the United States Neurology 82 2014 1045 1050
60. A.S. Ahmad, N. Ormiston-Smith, and P.D. Sasieni Trends in the lifetime risk of developing cancer in Great Britain: comparison of risk for those born from 1930 to 1960 Br. J. Cancer 112 2015 943 947
61. B. Blatt Kalben Why Men Die Younger N. Am. Actuar. J. 4 2000 83 111
62. Central Intelligence Agency The World Factbook 2013-14 2013 Central Intelligence Agency Washington, DC