Linking Alzheimer's disease and type 2 diabetes: Novel shared susceptibility genes detected by cFDR approach

Journal of the Neurological Sciences

Volumn 380, Issue , 2017, Pages 262-272

  Wang, Xia Fang ^a   Lin, Xu ^a   Li, Ding You ^b   Zhou, Rou ^a   Greenbaum, Jonathan ^c   Chen, Yuan Cheng ^a   Zeng, Chun Ping ^a   Peng, Lin Ping ^a   Wu, Ke Hao ^c   Ao, Zeng Xin ^a   Lu, Jun Min ^a   Guo, Yan Fang ^d   Shen, Jie ^a   Deng, Hong Wen ^a,c  

^a THE THIRD AFFILIATED HOSPITAL OF SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; ccFDR; cFDR; Susceptibility gene; Type 2 diabetes

Indexed keywords

ALZHEIMER DISEASE; ARTICLE; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENOME-WIDE ASSOCIATION STUDY; HUMAN; META ANALYSIS (TOPIC); MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; EUROPE; FEMALE; GENETIC PREDISPOSITION; GENETICS; GENOMICS; MALE; META ANALYSIS;

CARRIER PROTEIN; CYTOKINE; HEAT SHOCK PROTEIN; MITOCHONDRIAL PROTEIN; NDUFAF6 PROTEIN, HUMAN; PLEIOTROPHIN; TOMM40 PROTEIN, HUMAN; TP53INP1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; CARRIER PROTEINS; CYTOKINES; DIABETES MELLITUS, TYPE 2; EUROPE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; HEAT-SHOCK PROTEINS; HUMANS; MALE; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 85027869449     PISSN: 0022510X     EISSN: 18785883     Source Type: Journal    
DOI: 10.1016/j.jns.2017.07.044     Document Type: Article

References (90)

1. World Alzheimer Report, http://www.worldalzreport2015.org/, 2015.
2. Tamayo, T., Rosenbauer, J., Wild, S.H., et al. Diabetes in Europe: an update. Diabetes Res. Clin. Pr. 103:2 (2014), 206–217.
3. Garcia-Casares, N., Jorge, R.E., Garcia-Arnes, J.A., et al. Cognitive dysfunctions in middle-aged type 2 diabetic patients and neuroimaging correlations: a cross-sectional study. J. Alzheimers Dis. 42:4 (2014), 1337–1346.
4. Fei, M., Yan Ping, Z., Ru Juan, M., et al. Risk factors for dementia with type 2 diabetes mellitus among elderly people in China. Age Ageing 42:3 (2013), 398–400.
5. Arvanitakis, Z., Wilson, R.S., Bienias, J.L., et al. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch. Neurol. 61:5 (2004), 661–666.
6. Mittal, K., Katare, D.P., Shared links between type 2 diabetes mellitus and Alzheimer's disease: a review. Diabetes & Metab. Syndr. 10:2 (2016), 144–149.
7. Golpich, M., Amini, E., Mohamed, Z., et al. Mitochondrial dysfunction and biogenesis in neurodegenerative diseases: pathogenesis and treatment. CNS Neurosci. Ther. 23:1 (2017), 5–22.
8. Willette, A.A., Bendlin, B.B., Starks, E.J., et al. Association of insulin resistance with cerebral glucose uptake in late middle–aged adults at risk for Alzheimer disease. JAMA Neurol. 72:9 (2015), 1013–1020.
9. Hoscheidt, S.M., Starks, E.J., Oh, J.M., et al. Insulin resistance is associated with increased Alzheimer's disease pathology and reduced memory function in at-risk healthy middle-aged adults. J. Alzheimers Dis. 52:4 (2016), 1373–1383.
10. Ahmed, S., Mahmood, Z., Zahid, S., Linking insulin with Alzheimer's disease: emergence as type III diabetes. Neurol. Sci. 36:10 (2015), 1763–1769.
11. Herder, C., Roden, M., Genetics of type 2 diabetes: pathophysiologic and clinical relevance. Eur. J. Clin. Investig. 41:6 (2011), 679–692.
12. Gatz, M., Reynolds, C.A., Fratiglioni, L., et al. Role of genes and environments for explaining Alzheimer disease. Arch. Gen. Psychiatry 63:2 (2006), 168–174.
13. He, Q., Lin, D.Y., A variable selection method for genome-wide association studies. Bioinformatics 27:1 (2010), 1–8.
14. Shi, H., Belbin, O., Medway, C., et al. Genetic variants influencing human aging from late-onset Alzheimer's disease (LOAD) genome-wide association studies (GWAS). Neurobiol. Aging 33:8 (2012), 1845–1849.
15. Nolan, C.J., Damm, P., Prentki, M., Type 2 diabetes across generations: from pathophysiology to prevention and management. Lancet 378:9786 (2011), 169–181.
16. Gao, L., Cui, Z., Shen, L., Ji, H.F., Shared genetic etiology between type 2 diabetes and Alzheimer's disease identified by bioinformatics analysis. J. Alzheimers Dis. 50:1 (2016), 13–17.
17. Hao, K., Di Narzo, A.F., Ho, L., et al. Shared genetic etiology underlying Alzheimer's disease and type 2 diabetes. Mol. Asp. Med. 43–44 (2015), 66–76.
18. Liley, J., Wallace, C., A pleiotropy-informed Bayesian false discovery rate adapted to a shared control design finds new disease associations from GWAS summary statistics. PLoS Genet., 11(2), 2015, e1004926.
19. Andreassen, O.A., Thompson, W.K., Schork, A.J., et al. Improved detection of common variants associated with schizophrenia and bipolar disorder using pleiotropy-informed conditional false discovery rate. PLoS Genet., 9(4), 2013, e1005544.
20. Andreassen, O.A., McEvoy, L.K., Thompson, W.K., et al. Identifying common genetic variants in blood pressure due to polygenic pleiotropy with associated phenotypes. Hypertension 63:4 (2014), 819–826.
21. Andreassen, O.A., Djurovic, S., Thompson, W.K., et al. Improved detection of common variants associated with schizophrenia by leveraging pleiotropy with cardiovascular-disease risk factors. Am. J. Hum. Genet. 92:2 (2013), 197–209.
22. Desikan, R.S., Schork, A.J., Wang, Y., et al. Polygenic overlap between C-reactive protein, plasma lipids, and Alzheimer disease. Circulation 131:23 (2015), 2061–2069.
23. Lambert, J., Ibrahim-Verbaas, C.A., Harold, D., et al. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat. Genet. 45:12 (2013), 1452–1458.
24. Morris, A.P., Voight, B.F., Teslovich, T.M., et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat. Genet. 44:9 (2012), 981–990.
25. Devlin, B., Roeder, K., Genomic control for association studies. Biometrics 55:4 (1999), 997–1004.
26. Greenbaum, J., Wu, K., Zhang, L., et al. Increased detection of genetic loci associated with risk predictors of osteoporotic fracture using a pleiotropic cFDR method. Bone 99 (2017), 62–68.
27. Efron, B., Size, power and false discovery rates. Ann. Stat. 35:4 (2007), 1351–1377.
28. Zeng, C.P., Chen, Y.C., Lin, X., et al. Increased identification of novel variants in type 2 diabetes, birth weight and their pleiotropic loci. J Diabetes, 2016, 10.1111/1753-0407.12510.
29. http://www.alzgene.org.
30. Yokoyama, J.S., Wang, Y., Schork, A.J., et al. Association between genetic traits for immune-mediated diseases and Alzheimer disease. JAMA Neurol. 73:6 (2016), 691–697.
31. Szymanski, M., Wang, R., Bassett, S.S., Avramopoulos, D., Alzheimer's risk variants in the clusterin gene are associated with alternative splicing. Transl. Psychiatry, 1(7), 2011, e18.
32. Rosenthal, S.L., Barmada, M.M., Wang, X., et al. Connecting the dots: potential of data integration to identify regulatory SNPs in late-onset Alzheimer's disease GWAS findings. PLoS One, 9(4), 2014, e95152.
33. Lu, H., Zhu, X.C., Wang, H.F., et al. Lack of association between SLC24A4 polymorphism and late-onset Alzheimer's disease in Han Chinese. Curr. Neurovasc. Res. 13:3 (2016), 239–243.
34. Perez-Palma, E., Bustos, B.I., Villaman, C.F., et al. Overrepresentation of glutamate signaling in Alzheimer's disease: network-based pathway enrichment using meta-analysis of genome-wide association studies. PLoS One, 9(4), 2014, e95413.
35. Andres, D.A., Milatovich, A., Ozcelik, T., et al. cDNA cloning of the two subunits of human CAAX farnesyltransferase and chromosomal mapping of FNTA and FNTB loci and related sequences. Genomics 18:1 (1993), 105–112.
36. Cheng, S., Cao, D., Hottman, D.A., et al. Farnesyltransferase haplodeficiency reduces neuropathology and rescues cognitive function in a mouse model of Alzheimer disease. J. Biol. Chem. 288:50 (2013), 35952–35960.
37. Lecompte, S., Pasquetti, G., Hermant, X., et al. Genetic and molecular insights into the role of PROX1 in glucose metabolism. Diabetes 62:5 (2013), 1738–1745.
38. Salem, S.D., Saif-Ali, R., Ismail, I.S., et al. IGF2BP2 alternative variants associated with glutamic acid decarboxylase antibodies negative diabetes in Malaysian subjects. PLoS One, 7(9), 2012, e45573.
39. Franks, P.W., Rolandsson, O., Debenham, S.L., et al. Replication of the association between variants in WFS1 and risk of type 2 diabetes in European populations. Diabetologia 51:3 (2008), 458–463.
40. Yamakawa-Kobayashi, K., Natsume, M., Aoki, S., et al. The combined effect of the T2DM susceptibility genes is an important risk factor for T2DM in non-obese Japanese: a population based case-control study. BMC Med. Genet., 13, 2012, 11.
41. Cooper, J.D., Walker, N.M., Healy, B.C., et al. Analysis of 55 autoimmune disease and type II diabetes loci: further confirmation of chromosomes 4q27, 12q13.2 and 12q24.13 as type I diabetes loci, and support for a new locus, 12q13.3–q14.1. Genes Immun. 10 (2009), 95–120 suppl 1.
42. Gamboa-Melendez, M.A., Huerta-Chagoya, A., Moreno-Macias, H., et al. Contribution of common genetic variation to the risk of type 2 diabetes in the Mexican Mestizo population. Diabetes 61:12 (2012), 3314–3321.
43. Mahajan, A., Go, M.J., Zhang, W., et al. Genome-wide trans-ancestry meta-analysis provides insight into the genetic architecture of type 2 diabetes susceptibility. Nat. Genet. 46:3 (2014), 234–244.
44. Hanson, R.L., Guo, T., Muller, Y.L., et al. Strong parent-of-origin effects in the association of KCNQ1 variants with type 2 diabetes in American Indians. Diabetes 62:8 (2013), 2984–2991.
45. Wu, L., Rabe, K.G., Petersen, G.M., Do variants associated with susceptibility to pancreatic cancer and type 2 diabetes reciprocally affect risk?. PLoS One, 10(2), 2015, e117230.
46. Ohshige, T., Iwata, M., Omori, S., et al. Association of new loci identified in European genome-wide association studies with susceptibility to type 2 diabetes in the Japanese. PLoS One, 6(10), 2011, e26911.
47. Rees, S.D., Hydrie, M.Z., O'Hare, J.P., et al. Effects of 16 genetic variants on fasting glucose and type 2 diabetes in South Asians: ADCY5 and GLIS3 variants may predispose to type 2 diabetes. PLoS One, 6(9), 2011, e24710.
48. Qian, Y., Lu, F., Dong, M., et al. Genetic variants of IDE-KIF11-HHEX at 10q23.33 associated with type 2 diabetes risk: a fine-mapping study in Chinese population. PLoS One, 7(4), 2012, e35060.
49. Cornelis, M.C., Tchetgen Tchetgen, E.J., Liang, L., et al. Gene-environment interactions in genome-wide association studies: a comparative study of tests applied to empirical studies of type 2 diabetes. Am. J. Epidemiol. 175:3 (2012), 191–202.
50. Voight, B.F., Scott, L.J., Steinthorsdottir, V., et al. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat. Genet. 42:7 (2010), 579–589.
51. Zhu, Z., Tong, X., Zhu, Z., et al. Development of GMDR-GPU for gene-gene interaction analysis and its application to WTCCC GWAS data for type 2 diabetes. PLoS One, 8(4), 2013, e61943.
52. Grant, S.F., Thorleifsson, G., Reynisdottir, I., et al. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat. Genet. 38:3 (2006), 320–323.
53. Palmer, N.D., Hester, J.M., An, S.S., et al. Resequencing and analysis of variation in the TCF7L2 gene in African Americans suggests that SNP rs7903146 is the causal diabetes susceptibility variant. Diabetes 60:2 (2011), 662–668.
54. Meigs, J.B., Manning, A.K., Fox, C.S., et al. Genome-wide association with diabetes-related traits in the Framingham Heart Study. BMC Med. Genet.(8 Suppl 1), 2007, S16.
55. Langenberg, C., Sharp, S.J., Franks, P.W., et al. Gene-lifestyle interaction and type 2 diabetes: the EPIC interact case-cohort study. PLoS Med., 11(5), 2014, e1001647.
56. Timpson, N.J., Lindgren, C.M., Weedon, M.N., et al. Adiposity-related heterogeneity in patterns of type 2 diabetes susceptibility observed in genome-wide association data. Diabetes 58:2 (2009), 505–510.
57. McCormack, S., Grant, S.F., Genetics of obesity and type 2 diabetes in African Americans. J. Obes., 2013, 2013, 396416.
58. Almawi, W.Y., Nemr, R., Keleshian, S.H., et al. A replication study of 19 GWAS-validated type 2 diabetes at-risk variants in the Lebanese population. Diabetes Res. Clin. Pr. 102:2 (2013), 117–122.
59. Mercader, J.M., Puiggros, M., Segre, A.V., et al. Identification of novel type 2 diabetes candidate genes involved in the crosstalk between the mitochondrial and the insulin signaling systems. PLoS Genet., 8(12), 2012, e1003046.
60. Rees, S.D., Hydrie, M.Z.I., Shera, A.S., et al. Replication of 13 genome-wide association (GWA)-validated risk variants for type 2 diabetes in Pakistani populations. Diabetologia 54:6 (2011), 1368–1374.
61. Ng, M.C., Shriner, D., Chen, B.H., et al. Meta-analysis of genome-wide association studies in African Americans provides insights into the genetic architecture of type 2 diabetes. PLoS Genet., 10(8), 2014, e1004517.
62. Qi, L., Cornelis, M.C., Kraft, P., et al. Genetic variants at 2q24 are associated with susceptibility to type 2 diabetes. Hum. Mol. Genet. 19:13 (2010), 2706–2715.
63. Cook, J.P., Morris, A.P., Multi-ethnic genome-wide association study identifies novel locus for type 2 diabetes susceptibility. Eur. J. Hum. Genet. 24:8 (2016), 1175–1180.
64. Zee, R.Y.L., Ridker, P.M., Chasman, D.I., Genetic variants of 11 telomere-pathway gene loci and the risk of incident type 2 diabetes mellitus: the Women's Genome Health Study. Atherosclerosis 218:1 (2011), 144–146.
65. Torkamandi, S., Bastami, M., Ghaedi, H., et al. MAP3K1 may be a promising susceptibility gene for type 2 diabetes mellitus in an Iranian population. Int. J. Mol. Cell Med. 5:3 (2016), 134–140.
66. Yeung, E., Qi, L., Hu, F.B., Zhang, C., Novel abdominal adiposity genes and the risk of type 2 diabetes: findings from two prospective cohorts. Int. J. Mol. Epidemiol. Genet. 2:2 (2011), 138–144.
67. Harder, M.N., Appel, E.V., Grarup, N., et al. The type 2 diabetes risk allele of TMEM154-rs6813195 associates with decreased beta cell function in a study of 6,486 Danes. PLoS One, 10(3), 2015, e120890.
68. Dridi, L., Seyrantepe, V., Fougerat, A., et al. Positive regulation of insulin signaling by neuraminidase 1. Diabetes 62:7 (2013), 2338–2346.
69. Escott-Price, V., Bellenguez, C., Wang, L.S., et al. Gene-wide analysis detects two new susceptibility genes for Alzheimer's disease. PLoS One, 9(6), 2014, e94661.
70. Huang, H., Zhao, J., Xu, B., et al. The TOMM40 gene rs2075650 polymorphism contributes to Alzheimer's disease in Caucasian, and Asian populations. Neurosci. Lett. 628 (2016), 142–146.
71. Chung, D., Yang, C., Li, C., et al. GPA: a statistical approach to prioritizing GWAS results by integrating pleiotropy and annotation. PLoS Genet., 10(11), 2014, e1004787.
72. Cichonska, A., Rousu, J., Marttinen, P., et al. metaCCA: summary statistics-based multivariate meta-analysis of genome-wide association studies using canonical correlation analysis. Bioinformatics 32:13 (2016), 1981–1989.
73. Smith, E.N., Bloss, C.S., Badner, J.A., et al. Genome-wide association study of bipolar disorder in European American and African American individuals. Mol. Psychiatry 14:8 (2009), 755–763.
74. Chen, S., Zhang, B., Wang, Y., et al. Neuroprotective effects of salidroside through PI3K/Akt pathway activation in Alzheimers disease models. Drug Design, Development and Therapy 10 (2016), 1335–1343.
75. Ma, Y., Wu, D., Zhang, W., et al. Investigation of PI3K/PKB/mTOR/S6K1 signaling pathway in relationship of type 2 diabetes and Alzheimer's disease. Int. J. Clin. Exp. Med. 8:10 (2015), 18581–18590.
76. Lu, F., Guan, H., Gong, B., et al. Genetic variants in PVRL2-TOMM40-APOE region are associated with human longevity in a Han Chinese population. PLoS One, 9(6), 2014, e995806.
77. Seux, M., Peuget, S., Montero, M.P., et al. TP53INP1 decreases pancreatic cancer cell migration by regulating SPARC expression. Oncogene 30:27 (2011), 3049–3061.
78. Sándor, N., Schilling-Tóth, B., Kis, E., et al. TP53inp1 gene is implicated in early radiation response in human fibroblast cells. Int. J. Mol. Sci. 16:10 (2015), 25450–25465.
79. Seillier, M., Pouyet, L., N'Guessan, P., et al. Defects in mitophagy promote redox-driven metabolic syndrome in the absence of TP53INP1. EMBO Mol. Med. 7:6 (2015), 802–818.
80. Humphries, A.D., Streimann, I.C., Stojanovski, D., et al. Dissection of the mitochondrial import and assembly pathway for human Tom40. J. Biol. Chem. 280:12 (2005), 11535–11543.
81. Ferencz, B., Karlsson, S., Kalpouzos, G., Promising genetic biomarkers of preclinical Alzheimer's disease: the influence of APOE and TOMM40 on brain integrity. Int. J. Alzheimers Dis., 2012, 2012, 421452.
82. Caselli, R.J., Dueck, A.C., Huentelman, M.J., et al. Longitudinal modeling of cognitive aging and the TOMM40 effect. Alzheimers Dement. 8:6 (2012), 490–495.
83. Zurita Rendon, O., Shoubridge, E.A., Early complex I assembly defects result in rapid turnover of the ND1 subunit. Hum. Mol. Genet. 21:17 (2012), 3815–3824.
84. Andreazza, A.C., Shao, L., Wang, J.F., Young, L.T., Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch. Gen. Psychiatry 67:4 (2010), 360–368.
85. Zhang, L., Zhang, S., Maezawa, I., et al. Modulation of mitochondrial complex I activity averts cognitive decline in multiple animal models of familial Alzheimer's Disease. EBioMedicine 2:4 (2015), 294–305.
86. Zhu, X., Perry, G., Moreira, P.I., et al. Mitochondrial abnormalities and oxidative imbalance in Alzheimer disease. J. Alzheimers Dis. 9:2 (2006), 147–153.
87. Jeong, E.M., Chung, J., Liu, H., et al. Role of mitochondrial oxidative stress in glucose tolerance, insulin resistance, and cardiac diastolic dysfunction. J. Am. Heart Assoc., 5(5), 2016, e3046.
88. Manczak, M., Jung, Y., Park, B.S., et al. Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J. Neurochem. 92:3 (2005), 494–504.
89. Swerdlow, R.H., Burns, J.M., Khan, S.M., The Alzheimer's Disease mitochondrial cascade hypothesis. J. Alzheimers Dis. 20:s2 (2010), S265–279.
90. Petersen, K.F., Dufour, S., Befroy, D., et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350:7 (2004), 664–671.