Analysis of coding variants identified from exome sequencing resources for association with diabetic and non-diabetic nephropathy in African Americans

Human Genetics

Volumn 133, Issue 6, 2014, Pages 769-779

  Cooke Bailey, Jessica N ^a   Palmer, Nicholette D ^a   Ng, Maggie C Y ^a   Bonomo, Jason A ^a   Hicks, Pamela J ^a   Hester, Jessica M ^a   Langefeld, Carl D ^a   Freedman, Barry I ^a   Bowden, Donald W ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AFRICAN AMERICAN; APOL1 GENE; APOL2 GENE; APOL3 GENE; ARTICLE; C6ORF167 GENE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; END STAGE RENAL DISEASE; EUROPEAN AMERICAN; EXOME; FEMALE; GENE; GENE FREQUENCY; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; LIMK2 GENE; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OR2AK2 GENE; OR2L13 GENE; OR2L8 GENE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AFRICAN AMERICANS; AGED; APOLIPOPROTEINS; DATABASES, GENETIC; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; EXOME; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; HUMANS; KIDNEY FAILURE, CHRONIC; LIPOPROTEINS, HDL; MALE; MIDDLE AGED; OPEN READING FRAMES; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; UNITED STATES;

EID: 84901231205     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-013-1415-z     Document Type: Article

References (46)

1. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265
2. Behar DM, Rosset S, Tzur S, Selig S, Yudkovsky G, Bercovici S, Kopp JB, Winkler CA, Nelson GW, Wasser WG, Skorecki K (2010) African ancestry allelic variation at the MYH9 gene contributes to increased susceptibility to non-diabetic end-stage kidney disease in Hispanic Americans. Hum Mol Genet 19:1816-1827
3. Boldyrev AA (2000) Problems and perspectives in studying the biological role of carnosine. Biochemistry (Mosc) 65:751-756
4. Bowden DW, Freedman BI (2012) The challenging search for diabetic nephropathy genes. Diabetes 61:1923-1924
5. Bustamante CD, Burchard EG, De la Vega FM (2011) Genomics for the world. Nature 475:163-165
6. Cooke JN, Bostrom MA, Hicks PJ, Ng MC, Hellwege JN, Comeau ME, Divers J, Langefeld CD, Freedman BI, Bowden DW (2012) Polymorphisms in MYH9 are associated with diabetic nephropathy in European Americans. Nephrol Dial Transplant 27:1505-1511
7. de Boer IH, Rue TC, Hall YN, Heagerty PJ, Weiss NS, Himmelfarb J (2011) Temporal trends in the prevalence of diabetic kidney disease in the United States. JAMA 305:2532-2539
8. Freedman BI, Hicks PJ, Sale MM, Pierson ED, Langefeld CD, Rich SS, Xu J, McDonough C, Janssen B, Yard BA, van der Woude FJ, Bowden DW (2007) A leucine repeat in the carnosinase gene CNDP1 is associated with diabetic end-stage renal disease in European Americans. Nephrol Dial Transplant 22:1131-1135
9. Freedman BI, Hicks PJ, Bostrom MA, Comeau ME, Divers J, Bleyer AJ, Kopp JB, Winkler CA, Nelson GW, Langefeld CD, Bowden DW (2009a) Non-muscle myosin heavy chain 9 gene MYH9 associations in African Americans with clinically diagnosed type 2 diabetes mellitus-associated ESRD. Nephrol Dial Transplant 24:3366-3371
10. Freedman BI, Hicks PJ, Bostrom MA, Cunningham ME, Liu Y, Divers J, Kopp JB, Winkler CA, Nelson GW, Langefeld CD, Bowden DW (2009b) Polymorphisms in the non-muscle myosin heavy chain 9 gene (MYH9) are strongly associated with end-stage renal disease historically attributed to hypertension in African Americans. Kidney Int 75:736-745
11. Freedman BI, Kopp JB, Winkler CA, Nelson GW, Rao DC, Eckfeldt JH, Leppert MF, Hicks PJ, Divers J, Langefeld CD, Hunt SC (2009c) Polymorphisms in the nonmuscle myosin heavy chain 9 gene (MYH9) are associated with albuminuria in hypertensive African Americans: the HyperGEN study. Am J Nephrol 29:626-632
12. Freedman BI, Kopp JB, Langefeld CD, Genovese G, Friedman DJ, Nelson GW, Winkler CA, Bowden DW, Pollak MR (2010) The apolipoprotein L1 (APOL1) gene and nondiabetic nephropathy in African Americans. J Am Soc Nephrol 21:1422-1426
13. Freedman BI, Langefeld CD, Lu L, Divers J, Comeau ME, Kopp JB, Winkler CA, Nelson GW, Johnson RC, Palmer ND, Hicks PJ, Bostrom MA, Cooke JN, McDonough CW, Bowden DW (2011) Differential effects of MYH9 and APOL1 risk variants on FRMD3 association with diabetic ESRD in African Americans. PLoS Genet 7:e1002150
14. Freedman BI, Langefeld CD, Turner J, Nunez M, High KP, Spainhour M, Hicks PJ, Bowden DW, Reeves-Daniel AM, Murea M, Rocco MV, Divers J (2012) Association of APOL1 variants with mild kidney disease in the first-degree relatives of African American patients with non-diabetic end-stage renal disease. Kidney Int 82(7):805-811
15. Genovese G, Friedman DJ, Ross MD, Lecordier L, Uzureau P, Freedman BI, Bowden DW, Langefeld CD, Oleksyk TK, Uscinski Knob AL, Bernhardy AJ, Hicks PJ, Nelson GW, Vanhollebeke B, Winkler CA, Kopp JB, Pays E, Pollak MR (2010) Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329:841-845
16. Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, Yu F, Gibbs RA, Bustamante CD (2011) Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA 108:11983-11988
17. Hipkiss AR, Preston JE, Himsworth DT, Worthington VC, Keown M, Michaelis J, Lawrence J, Mateen A, Allende L, Eagles PA, Abbott NJ (1998) Pluripotent protective effects of carnosine, a naturally occurring dipeptide. Ann NY Acad Sci 854:37-53
18. Janssen B, Hohenadel D, Brinkkoetter P, Peters V, Rind N, Fischer C, Rychlik I, Cerna M, Romzova M, de Heer E, Baelde H, Bakker SJ, Zirie M, Rondeau E, Mathieson P, Saleem MA, Meyer J, Koppel H, Sauerhoefer S, Bartram CR, Nawroth P, Hammes HP, Yard BA, Zschocke J, van der Woude FJ (2005) Carnosine as a protective factor in diabetic nephropathy: association with a leucine repeat of the carnosinase gene CNDP1. Diabetes 54:2320-2327
19. Kao WH, Klag MJ, Meoni LA, Reich D, Berthier-Schaad Y, Li M, Coresh J, Patterson N, Tandon A, Powe NR, Fink NE, Sadler JH, Weir MR, Abboud HE, Adler SG, Divers J, Iyengar SK, Freedman BI, Kimmel PL, Knowler WC, Kohn OF, Kramp K, Leehey DJ, Nicholas SB, Pahl MV, Schelling JR, Sedor JR, Thornley-Brown D, Winkler CA, Smith MW, Parekh RS (2008) MYH9 is associated with nondiabetic end-stage renal disease in African Americans. Nat Genet 40:1185-1192
20. Karter AJ, Ferrara A, Liu JY, Moffet HH, Ackerson LM, Selby JV (2002) Ethnic disparities in diabetic complications in an insured population. JAMA 287:2519-2527
21. Keene KL, Mychaleckyj JC, Leak TS, Smith SG, Perlegas PS, Divers J, Langefeld CD, Freedman BI, Bowden DW, Sale MM (2008) Exploration of the utility of ancestry informative markers for genetic association studies of African Americans with type 2 diabetes and end stage renal disease. Hum Genet 124:147-154
22. King GL, Loeken MR (2004) Hyperglycemia-induced oxidative stress in diabetic complications. Histochem Cell Biol 122:333-338
23. Kopp JB, Smith MW, Nelson GW, Johnson RC, Freedman BI, Bowden DW, Oleksyk T, McKenzie LM, Kajiyama H, Ahuja TS, Berns JS, Briggs W, Cho ME, Dart RA, Kimmel PL, Korbet SM, Michel DM, Mokrzycki MH, Schelling JR, Simon E, Trachtman H, Vlahov D, Winkler CA (2008) MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat Genet 40:1175-1184
24. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, Willer CJ, Jackson AU, Vedantam S, Raychaudhuri S, Ferreira T, Wood AR, Weyant RJ, Segre AV, Speliotes EK, Wheeler E, Soranzo N, Park JH, Yang J, Gudbjartsson D, Heard-Costa NL, Randall JC, Qi L, Vernon Smith A, Magi R, Pastinen T, Liang L, Heid IM, Luan J, Thorleifsson G, Winkler TW, Goddard ME, Sin Lo K, Palmer C, Workalemahu T, Aulchenko YS, Johansson A, Zillikens MC, Feitosa MF, Esko T, Johnson T, Ketkar S, Kraft P, Mangino M, Prokopenko I, Absher D, Albrecht E, Ernst F, Glazer NL, Hayward C, Hottenga JJ, Jacobs KB, Knowles JW, Kutalik Z, Monda KL, Polasek O, Preuss M, Rayner NW, Robertson NR, Steinthorsdottir V, Tyrer JP, Voight BF, Wiklund F, Xu J, Zhao JH, Nyholt DR, Pellikka N, Perola M, Perry JR, Surakka I, Tammesoo ML, Altmaier EL, Amin N, Aspelund T, Bhangale T, Boucher G, Chasman DI, Chen C, Coin L, Cooper MN, Dixon AL, Gibson Q, Grundberg E, Hao K, Juhani Junttila M, Kaplan LM, Kettunen J, Konig IR, Kwan T, Lawrence RW, Levinson DF, Lorentzon M, McKnight B, Morris AP, Muller M, Suh Ngwa J, Purcell S, Rafelt S, Salem RM, Salvi E et al (2010) Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467:832-838
25. Lipworth L, Mumma MT, Cavanaugh KL, Edwards TL, Ikizler TA, Tarone RE, McLaughlin JK, Blot WJ (2012) Incidence and predictors of end stage renal disease among low-income blacks and whites. PLoS ONE 7:e48407
26. Maeda S, Kobayashi MA, Araki S, Babazono T, Freedman BI, Bostrom MA, Cooke JN, Toyoda M, Umezono T, Tarnow L, Hansen T, Gaede P, Jorsal A, Ng DP, Ikeda M, Yanagimoto T, Tsunoda T, Unoki H, Kawai K, Imanishi M, Suzuki D, Shin HD, Park KS, Kashiwagi A, Iwamoto Y, Kaku K, Kawamori R, Parving HH, Bowden DW, Pedersen O, Nakamura Y (2010) A single nucleotide polymorphism within the acetyl-coenzyme A carboxylase beta gene is associated with proteinuria in patients with type 2 diabetes. PLoS Genet 6:e1000842
27. Malnic B, Godfrey PA, Buck LB (2004) The human olfactory receptor gene family. Proc Natl Acad Sci USA 101:2584-2589
28. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, McCarroll SA, Visscher PM (2009) Finding the missing heritability of complex diseases. Nature 461:747-753
29. McDonough CW, Hicks PJ, Lu L, Langefeld CD, Freedman BI, Bowden DW (2009) The influence of carnosinase gene polymorphisms on diabetic nephropathy risk in African-Americans. Hum Genet 126:265-275
30. McDonough CW, Palmer ND, Hicks PJ, Roh BH, An SS, Cooke JN, Hester JM, Wing MR, Bostrom MA, Rudock ME, Lewis JP, Talbert ME, Blevins RA, Lu L, Ng MC, Sale MM, Divers J, Langefeld CD, Freedman BI, Bowden DW (2011) A genome-wide association study for diabetic nephropathy genes in African Americans. Kidney Int 79:563-572
31. O'Seaghdha CM, Parekh RS, Hwang SJ, Li M, Kottgen A, Coresh J, Yang Q, Fox CS, Kao WH (2011) The MYH9/APOL1 region and chronic kidney disease in European-Americans. Hum Mol Genet 20:2450-2456
32. Pattaro C, Aulchenko YS, Isaacs A, Vitart V, Hayward C, Franklin CS, Polasek O, Kolcic I, Biloglav Z, Campbell S, Hastie N, Lauc G, Meitinger T, Oostra BA, Gyllensten U, Wilson JF, Pichler I, Hicks AA, Campbell H, Wright AF, Rudan I, van Duijn CM, Riegler P, Marroni F, Pramstaller PP (2009) Genome-wide linkage analysis of serum creatinine in three isolated European populations. Kidney Int 76(3):297-306
33. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575
34. Ripke S, Sanders AR, Kendler KS, Levinson DF, Sklar P, Holmans PA, Lin DY, Duan J, Ophoff RA, Andreassen OA, Scolnick E, Cichon S, St Clair D, Corvin A, Gurling H, Werge T, Rujescu D, Blackwood DH, Pato CN, Malhotra AK, Purcell S, Dudbridge F, Neale BM, Rossin L, Visscher PM, Posthuma D, Ruderfer DM, Fanous A, Stefansson H, Steinberg S, Mowry BJ, Golimbet V, De Hert M, Jonsson EG, Bitter I, Pietilainen OP, Collier DA, Tosato S, Agartz I, Albus M, Alexander M, Amdur RL, Amin F, Bass N, Bergen SE, Black DW, Borglum AD, Brown MA, Bruggeman R, Buccola NG, Byerley WF, Cahn W, Cantor RM, Carr VJ, Catts SV, Choudhury K, Cloninger CR, Cormican P, Craddock N, Danoy PA, Datta S, de Haan L, Demontis D, Dikeos D, Djurovic S, Donnelly P, Donohoe G, Duong L, Dwyer S, Fink-Jensen A, Freedman R, Freimer NB, Friedl M, Georgieva L, Giegling I, Gill M, Glenthoj B, Godard S, Hamshere M, Hansen M, Hansen T, Hartmann AM, Henskens FA, Hougaard DM, Hultman CM, Ingason A, Jablensky AV, Jakobsen KD, Jay M, Jurgens G, Kahn RS, Keller MC, Kenis G, Kenny E, Kim Y, Kirov GK, Konnerth H, Konte B, Krabbendam L, Krasucki R et al (2011) Genome-wide association study identifies five new schizophrenia loci. Nat Genet 43:969-976
35. Sauerhofer S, Yuan G, Braun GS, Deinzer M, Neumaier M, Gretz N, Floege J, Kriz W, van der Woude F, Moeller MJ (2007) L-carnosine, a substrate of carnosinase-1, influences glucose metabolism. Diabetes 56:2425-2432
36. Sklar P, Ripke S, Scott LJ, Andreassen OA, Cichon S, Craddock N, Edenberg HJ, Nurnberger JI Jr, Rietschel M, Blackwood D, Corvin A, Flickinger M, Guan W, Mattingsdal M, McQuillin A, Kwan P, Wienker TF, Daly M, Dudbridge F, Holmans PA, Lin D, Burmeister M, Greenwood TA, Hamshere ML, Muglia P, Smith EN, Zandi PP, Nievergelt CM, McKinney R, Shilling PD, Schork NJ, Bloss CS, Foroud T, Koller DL, Gershon ES, Liu C, Badner JA, Scheftner WA, Lawson WB, Nwulia EA, Hipolito M, Coryell W, Rice J, Byerley W, McMahon FJ, Schulze TG, Berrettini W, Lohoff FW, Potash JB, Mahon PB, McInnis MG, Zollner S, Zhang P, Craig DW, Szelinger S, Barrett TB, Breuer R, Meier S, Strohmaier J, Witt SH, Tozzi F, Farmer A, McGuffin P, Strauss J, Xu W, Kennedy JL, Vincent JB, Matthews K, Day R, Ferreira MA, O'Dushlaine C, Perlis R, Raychaudhuri S, Ruderfer D, Hyoun PL, Smoller JW, Li J, Absher D, Thompson RC, Meng FG, Schatzberg AF, Bunney WE, Barchas JD, Jones EG, Watson SJ, Myers RM, Akil H, Boehnke M, Chambert K, Moran J, Scolnick E, Djurovic S, Melle I, Morken G, Gill M, Morris D, Quinn E, Muhleisen TW, Degenhardt FA, Mattheisen M et al (2011) Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat Genet 43:977-983
37. Tang H, Peng J, Wang P, Risch NJ (2005) Estimation of individual admixture: analytical and study design considerations. Genet Epidemiol 28:289-301
38. Teer JK, Mullikin JC (2010) Exome sequencing: the sweet spot before whole genomes. Hum Mol Genet 19:R145-R151
39. Tennessen JA, Bigham AW, O'Connor TD, Fu W, Kenny EE, Gravel S, McGee S, Do R, Liu X, Jun G, Kang HM, Jordan D, Leal SM, Gabriel S, Rieder MJ, Abecasis G, Altshuler D, Nickerson DA, Boerwinkle E, Sunyaev S, Bustamante CD, Bamshad MJ, Akey JM (2012) Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337:64-69
40. Teufel M, Saudek V, Ledig JP, Bernhardt A, Boularand S, Carreau A, Cairns NJ, Carter C, Cowley DJ, Duverger D, Ganzhorn AJ, Guenet C, Heintzelmann B, Laucher V, Sauvage C, Smirnova T (2003) Sequence identification and characterization of human carnosinase and a closely related non-specific dipeptidase. J Biol Chem 278:6521-6531
41. USRDS (2009) USRDS 2009 Annual data report: atlas of chronic kidney disease and end-stage renal disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, 2009
42. USRDS (2011) USRDS 2011 Annual data report: atlas of chronic kidney disease and end-stage renal disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, 2011
43. Wessman M, Forsblom C, Kaunisto MA, Soderlund J, Ilonen J, Sallinen R, Hiekkalinna T, Parkkonen M, Maxwell AP, Tarnow L, Parving HH, Hadjadj S, Marre M, Peltonen L, Groop PH (2011) Novel susceptibility locus at 22q11 for diabetic nephropathy in type 1 diabetes. PLoS ONE 6:e24053
44. WHO (2011) WHO Diabetes Fact sheet N°312
45. Yang J, Ferreira T, Morris AP, Medland SE, Madden PA, Heath AC, Martin NG, Montgomery GW, Weedon MN, Loos RJ, Frayling TM, McCarthy MI, Hirschhorn JN, Goddard ME, Visscher PM (2012) Conditional and joint multiple-SNP analysis of GWAS summary statistics identifies additional variants influencing complex traits. Nat Genet 44(369-75):S1-S3
46. Zeggini E (2011) Next-generation association studies for complex traits. Nat Genet 43:287-288