Genomics in Diabetic Kidney Disease: A 2024 Update

Seaquist, E.R.; Goetz, F.C.; Rich, S.; Barbosa, J. Familial clustering of diabetic kidney disease. Evidence for genetic susceptibility to diabetic nephropathy. N. Engl. J. Med., 1989, 320(18), 1161-1165.
[http://dx.doi.org/10.1056/NEJM198905043201801] [PMID: 2710189]

Satko, S.G.; Sedor, J.R.; Iyengar, S.K.; Freedman, B.I. Familial clustering of chronic kidney disease. Semin. Dial., 2007, 20(3), 229-236.
[http://dx.doi.org/10.1111/j.1525-139X.2007.00282.x] [PMID: 17555489]

Williams, W.W.; Salem, R.M.; McKnight, A.J.; Sandholm, N.; Forsblom, C.; Taylor, A.; Guiducci, C.; McAteer, J.B.; McKay, G.J.; Isakova, T.; Brennan, E.P.; Sadlier, D.M.; Palmer, C.; Söderlund, J.; Fagerholm, E.; Harjutsalo, V.; Lithovius, R.; Gordin, D.; Hietala, K.; Kytö, J.; Parkkonen, M.; Rosengård-Bärlund, M.; Thorn, L.; Syreeni, A.; Tolonen, N.; Saraheimo, M.; Wadén, J.; Pitkäniemi, J.; Sarti, C.; Tuomilehto, J.; Tryggvason, K.; Österholm, A.M.; He, B.; Bain, S.; Martin, F.; Godson, C.; Hirschhorn, J.N.; Maxwell, A.P.; Groop, P.H.; Florez, J.C. Association testing of previously reported variants in a large case-control meta-analysis of diabetic nephropathy. Diabetes, 2012, 61(8), 2187-2194.
[http://dx.doi.org/10.2337/db11-0751] [PMID: 22721967]

Iyengar, S.K.; Sedor, J.R.; Freedman, B.I.; Kao, W.H.L.; Kretzler, M.; Keller, B.J.; Abboud, H.E.; Adler, S.G.; Best, L.G.; Bowden, D.W.; Burlock, A.; Chen, Y.D.I.; Cole, S.A.; Comeau, M.E.; Curtis, J.M.; Divers, J.; Drechsler, C.; Duggirala, R.; Elston, R.C.; Guo, X.; Huang, H.; Hoffmann, M.M.; Howard, B.V.; Ipp, E.; Kimmel, P.L.; Klag, M.J.; Knowler, W.C.; Kohn, O.F.; Leak, T.S.; Leehey, D.J.; Li, M.; Malhotra, A.; März, W.; Nair, V.; Nelson, R.G.; Nicholas, S.B.; O’Brien, S.J.; Pahl, M.V.; Parekh, R.S.; Pezzolesi, M.G.; Rasooly, R.S.; Rotimi, C.N.; Rotter, J.I.; Schelling, J.R.; Seldin, M.F.; Shah, V.O.; Smiles, A.M.; Smith, M.W.; Taylor, K.D.; Thameem, F.; Thornley-Brown, D.P.; Truitt, B.J.; Wanner, C.; Weil, E.J.; Winkler, C.A.; Zager, P.G.; Igo, R.P., Jr; Hanson, R.L.; Langefeld, C.D. Genome-wide association and trans-ethnic meta-analysis for advanced diabetic kidney disease: Family Investigation of Nephropathy and Diabetes (FIND). PLoS Genet., 2015, 11(8), e1005352.
[http://dx.doi.org/10.1371/journal.pgen.1005352] [PMID: 26305897]

Sandholm, N.; Salem, R.M.; McKnight, A.J.; Brennan, E.P.; Forsblom, C.; Isakova, T. New susceptibility loci associated with kidney disease in type 1 diabetes. PLoS Genet., 2012, 8(9), e1002921.
[http://dx.doi.org/10.1371/journal.pgen.1002921]

Salem, R.M.; Todd, J.N.; Sandholm, N.; Valo, E.; Haukka, J.K.; Harjutsalo, V. Genome-wide association study of diabetic kidney disease highlights biology involved in glomerular basement membrane collagen. J. Am. Soc. Nephrol., 2019, 30(10)
[http://dx.doi.org/10.1681/ASN.2019030218]

Xue, D.; Narisu, N.; Taylor, D.L.; Zhang, M.; Grenko, C.; Taylor, H.J.; Yan, T.; Tang, X.; Sinha, N.; Zhu, J.; Vandana, J.J.; Nok Chong, A.C.; Lee, A.; Mansell, E.C.; Swift, A.J.; Erdos, M.R.; Zhong, A.; Bonnycastle, L.L.; Zhou, T.; Chen, S.; Collins, F.S. Functional interrogation of twenty type 2 diabetes-associated genes using isogenic human embryonic stem cell-derived β-like cells. Cell Metab., 2023, 35(11), 1897-1914.e11.
[http://dx.doi.org/10.1016/j.cmet.2023.09.013] [PMID: 37858332]

Wei, L.; Xiao, Y.; Li, L.; Xiong, X.; Han, Y.; Zhu, X.; Sun, L. The susceptibility genes in diabetic nephropathy. Kidney Dis., 2018, 4(4), 226-237.
[http://dx.doi.org/10.1159/000492633] [PMID: 30574499]

Jin, H.; Kim, Y.A.; Lee, Y.; Kwon, S.; Do, A.R.; Seo, S.; Won, S.; Seo, J.H. Identification of genetic variants associated with diabetic kidney disease in multiple Korean cohorts via a genome-wide association study mega-analysis. BMC Med., 2023, 21(1), 16.
[http://dx.doi.org/10.1186/s12916-022-02723-4] [PMID: 36627639]

Tziastoudi, M.; Stefanidis, I.; Zintzaras, E. The genetic map of diabetic nephropathy: Evidence from a systematic review and meta-analysis of genetic association studies. Clin. Kidney J., 2020, 13(5), 768-781.
[http://dx.doi.org/10.1093/ckj/sfaa077] [PMID: 33123356]

Roumeliotis, A.; Roumeliotis, S.; Tsetsos, F.; Georgitsi, M.; Georgianos, P.I.; Stamou, A.; Vasilakou, A.; Kotsa, K.; Tsekmekidou, X.; Paschou, P.; Panagoutsos, S.; Liakopoulos, V. Oxidative stress genes in Diabetes Mellitus Type 2: Association with diabetic kidney disease. Oxid. Med. Cell. Longev., 2021, 2021, 1-10.
[http://dx.doi.org/10.1155/2021/2531062] [PMID: 34545296]

Roumeliotis, S.; Roumeliotis, A.; Stamou, A.; Panagoutsos, S.; Manolopoulos, V.G.; Tsetsos, F.; Georgitsi, M.; Liakopoulos, V. Association of rs11780592 Polymorphism in the Human Soluble Epoxide Hydrolase Gene (EPHX2) with Oxidized LDL and Mortality in Patients with Diabetic Chronic Kidney Disease. Oxid. Med. Cell. Longev., 2021, 2021, 1-8.
[http://dx.doi.org/10.1155/2021/8817502] [PMID: 34040693]

Tsekmekidou, X.; Tsetsos, F.; Koufakis, T.; Karras, S.N.; Georgitsi, M.; Papanas, N.; Papazoglou, D.; Roumeliotis, A.; Panagoutsos, S.; Thodis, E.; Theodoridis, M.; Pasadakis, P.; Maltezos, E.; Paschou, P.; Kotsa, K. Association between CUBN gene variants, type 2 diabetes and vitamin D concentrations in an elderly Greek population. J. Steroid Biochem. Mol. Biol., 2020, 198, 105549.
[http://dx.doi.org/10.1016/j.jsbmb.2019.105549] [PMID: 31770575]

Lindhardt, M.; Persson, F.; Oxlund, C.; Jacobsen, I.A.; Zürbig, P.; Mischak, H.; Rossing, P.; Heerspink, H.J.L. Predicting albuminuria response to spironolactone treatment with urinary proteomics in patients with type 2 diabetes and hypertension. Nephrol. Dial. Transplant., 2018, 33(2), 296-303.
[PMID: 28064163]

Pena, M.J.; Heinzel, A.; Rossing, P.; Parving, H.H.; Dallmann, G.; Rossing, K.; Andersen, S.; Mayer, B.; Heerspink, H.J.L. Serum metabolites predict response to angiotensin II receptor blockers in patients with diabetes mellitus. J. Transl. Med., 2016, 14(1), 203.
[http://dx.doi.org/10.1186/s12967-016-0960-3] [PMID: 27378474]

Andersen, S.; Mischak, H.; Zürbig, P.; Parving, H.H.; Rossing, P. Urinary proteome analysis enables assessment of renoprotective treatment in type 2 diabetic patients with microalbuminuria. BMC Nephrol., 2010, 11(1), 29.
[http://dx.doi.org/10.1186/1471-2369-11-29] [PMID: 21040538]

Winkler, T.W.; Rasheed, H.; Teumer, A.; Gorski, M.; Rowan, B.X.; Stanzick, K.J.; Thomas, L.F.; Tin, A.; Hoppmann, A.; Chu, A.Y.; Tayo, B.; Thio, C.H.L.; Cusi, D.; Chai, J.F.; Sieber, K.B.; Horn, K.; Li, M.; Scholz, M.; Cocca, M.; Wuttke, M.; van der Most, P.J.; Yang, Q.; Ghasemi, S.; Nutile, T.; Li, Y.; Pontali, G.; Günther, F.; Dehghan, A.; Correa, A.; Parsa, A.; Feresin, A.; de Vries, A.P.J.; Zonderman, A.B.; Smith, A.V.; Oldehinkel, A.J.; De Grandi, A.; Rosenkranz, A.R.; Franke, A.; Teren, A.; Metspalu, A.; Hicks, A.A.; Morris, A.P.; Tönjes, A.; Morgan, A.; Podgornaia, A.I.; Peters, A.; Körner, A.; Mahajan, A.; Campbell, A.; Freedman, B.I.; Spedicati, B.; Ponte, B.; Schöttker, B.; Brumpton, B.; Banas, B.; Krämer, B.K.; Jung, B.; Åsvold, B.O.; Smith, B.H.; Ning, B.; Penninx, B.W.J.H.; Vanderwerff, B.R.; Psaty, B.M.; Kammerer, C.M.; Langefeld, C.D.; Hayward, C.; Spracklen, C.N.; Robinson-Cohen, C.; Hartman, C.A.; Lindgren, C.M.; Wang, C.; Sabanayagam, C.; Heng, C.K.; Lanzani, C.; Khor, C.C.; Cheng, C.Y.; Fuchsberger, C.; Gieger, C.; Shaffer, C.M.; Schulz, C.A.; Willer, C.J.; Chasman, D.I.; Gudbjartsson, D.F.; Ruggiero, D.; Toniolo, D.; Czamara, D.; Porteous, D.J.; Waterworth, D.M.; Mascalzoni, D.; Mook-Kanamori, D.O.; Reilly, D.F.; Daw, E.W.; Hofer, E.; Boerwinkle, E.; Salvi, E.; Bottinger, E.P.; Tai, E.S.; Catamo, E.; Rizzi, F.; Guo, F.; Rivadeneira, F.; Guilianini, F.; Sveinbjornsson, G.; Ehret, G.; Waeber, G.; Biino, G.; Girotto, G.; Pistis, G.; Nadkarni, G.N.; Delgado, G.E.; Montgomery, G.W.; Snieder, H.; Campbell, H.; White, H.D.; Gao, H.; Stringham, H.M.; Schmidt, H.; Li, H.; Brenner, H.; Holm, H.; Kirsten, H.; Kramer, H.; Rudan, I.; Nolte, I.M.; Tzoulaki, I.; Olafsson, I.; Martins, J.; Cook, J.P.; Wilson, J.F.; Halbritter, J.; Felix, J.F.; Divers, J.; Kooner, J.S.; Lee, J.J.M.; O’Connell, J.; Rotter, J.I.; Liu, J.; Xu, J.; Thiery, J.; Ärnlöv, J.; Kuusisto, J.; Jakobsdottir, J.; Tremblay, J.; Chambers, J.C.; Whitfield, J.B.; Gaziano, J.M.; Marten, J.; Coresh, J.; Jonas, J.B.; Mychaleckyj, J.C.; Christensen, K.; Eckardt, K.U.; Mohlke, K.L.; Endlich, K.; Dittrich, K.; Ryan, K.A.; Rice, K.M.; Taylor, K.D.; Ho, K.; Nikus, K.; Matsuda, K.; Strauch, K.; Miliku, K.; Hveem, K.; Lind, L.; Wallentin, L.; Yerges-Armstrong, L.M.; Raffield, L.M.; Phillips, L.S.; Launer, L.J.; Lyytikäinen, L.P.; Lange, L.A.; Citterio, L.; Klaric, L.; Ikram, M.A.; Ising, M.; Kleber, M.E.; Francescatto, M.; Concas, M.P.; Ciullo, M.; Piratsu, M.; Orho-Melander, M.; Laakso, M.; Loeffler, M.; Perola, M.; de Borst, M.H.; Gögele, M.; Bianca, M.L.; Lukas, M.A.; Feitosa, M.F.; Biggs, M.L.; Wojczynski, M.K.; Kavousi, M.; Kanai, M.; Akiyama, M.; Yasuda, M.; Nauck, M.; Waldenberger, M.; Chee, M.L.; Chee, M.L.; Boehnke, M.; Preuss, M.H.; Stumvoll, M.; Province, M.A.; Evans, M.K.; O’Donoghue, M.L.; Kubo, M.; Kähönen, M.; Kastarinen, M.; Nalls, M.A.; Kuokkanen, M.; Ghanbari, M.; Bochud, M.; Josyula, N.S.; Martin, N.G.; Tan, N.Y.Q.; Palmer, N.D.; Pirastu, N.; Schupf, N.; Verweij, N.; Hutri-Kähönen, N.; Mononen, N.; Bansal, N.; Devuyst, O.; Melander, O.; Raitakari, O.T.; Polasek, O.; Manunta, P.; Gasparini, P.; Mishra, P.P.; Sulem, P.; Magnusson, P.K.E.; Elliott, P.; Ridker, P.M.; Hamet, P.; Svensson, P.O.; Joshi, P.K.; Kovacs, P.; Pramstaller, P.P.; Rossing, P.; Vollenweider, P.; van der Harst, P.; Dorajoo, R.; Sim, R.Z.H.; Burkhardt, R.; Tao, R.; Noordam, R.; Mägi, R.; Schmidt, R.; de Mutsert, R.; Rueedi, R.; van Dam, R.M.; Carroll, R.J.; Gansevoort, R.T.; Loos, R.J.F.; Felicita, S.C.; Sedaghat, S.; Padmanabhan, S.; Freitag-Wolf, S.; Pendergrass, S.A.; Graham, S.E.; Gordon, S.D.; Hwang, S.J.; Kerr, S.M.; Vaccargiu, S.; Patil, S.B.; Hallan, S.; Bakker, S.J.L.; Lim, S.C.; Lucae, S.; Vogelezang, S.; Bergmann, S.; Corre, T.; Ahluwalia, T.S.; Lehtimäki, T.; Boutin, T.S.; Meitinger, T.; Wong, T.Y.; Bergler, T.; Rabelink, T.J.; Esko, T.; Haller, T.; Thorsteinsdottir, U.; Völker, U.; Foo, V.H.X.; Salomaa, V.; Vitart, V.; Giedraitis, V.; Gudnason, V.; Jaddoe, V.W.V.; Huang, W.; Zhang, W.; Wei, W.B.; Kiess, W.; März, W.; Koenig, W.; Lieb, W.; Gao, X.; Sim, X.; Wang, Y.X.; Friedlander, Y.; Tham, Y.C.; Kamatani, Y.; Okada, Y.; Milaneschi, Y.; Yu, Z.; Thio, C.H.L.; van der Most, P.J.; de Borst, M.H.; Ho, K.; Josyula, N.S.; Pendergrass, S.A.; Rowan, B.X.; Robinson-Cohen, C.; Gaziano, J.M.; Phillips, L.S.; Tao, R.; Hung, A.M.; Stark, K.J.; Stefansson, K.; Böger, C.A.; Hung, A.M.; Kronenberg, F.; Köttgen, A.; Pattaro, C.; Heid, I.M. Differential and shared genetic effects on kidney function between diabetic and non-diabetic individuals. Commun. Biol., 2022, 5(1), 580.
[http://dx.doi.org/10.1038/s42003-022-03448-z] [PMID: 35697829]

Friedman, D.J.; Pollak, M.R. APOL1 nephropathy: From genetics to clinical applications. Clin. J. Am. Soc. Nephrol., 2021, 16(2), 294-303.
[http://dx.doi.org/10.2215/CJN.15161219] [PMID: 32616495]

Parsa, A.; Kao, W.H.L.; Xie, D.; Astor, B.C.; Li, M.; Hsu, C.; Feldman, H.I.; Parekh, R.S.; Kusek, J.W.; Greene, T.H.; Fink, J.C.; Anderson, A.H.; Choi, M.J.; Wright, J.T., Jr; Lash, J.P.; Freedman, B.I.; Ojo, A.; Winkler, C.A.; Raj, D.S.; Kopp, J.B.; He, J.; Jensvold, N.G.; Tao, K.; Lipkowitz, M.S.; Appel, L.J. APOL1 risk variants, race, and progression of chronic kidney disease. N. Engl. J. Med., 2013, 369(23), 2183-2196.
[http://dx.doi.org/10.1056/NEJMoa1310345] [PMID: 24206458]

Bruggeman, L.A.; Sedor, J.R.; O’Toole, J.F. Apolipoprotein L1 and mechanisms of kidney disease susceptibility. Curr. Opin. Nephrol. Hypertens., 2021, 30(3), 317-323.
[http://dx.doi.org/10.1097/MNH.0000000000000704] [PMID: 33767059]

Freedman, B.I.; Pastan, S.O.; Israni, A.K.; Schladt, D.; Julian, B.A.; Gautreaux, M.D.; Hauptfeld, V.; Bray, R.A.; Gebel, H.M.; Kirk, A.D.; Gaston, R.S.; Rogers, J.; Farney, A.C.; Orlando, G.; Stratta, R.J.; Mohan, S.; Ma, L.; Langefeld, C.D.; Bowden, D.W.; Hicks, P.J.; Palmer, N.D.; Palanisamy, A.; Reeves-Daniel, A.M.; Brown, W.M.; Divers, J. APOL1 genotype and kidney transplantation outcomes from deceased African American donors. Transplantation, 2016, 100(1), 194-202.
[http://dx.doi.org/10.1097/TP.0000000000000969] [PMID: 26566060]

Freedman, B.I.; Moxey-Mims, M.M.; Alexander, A.A.; Astor, B.C.; Birdwell, K.A.; Bowden, D.W.; Bowen, G.; Bromberg, J.; Craven, T.E.; Dadhania, D.M.; Divers, J.; Doshi, M.D.; Eidbo, E.; Fornoni, A.; Gautreaux, M.D.; Gbadegesin, R.A.; Gee, P.O.; Guerra, G.; Hsu, C.; Iltis, A.S.; Jefferson, N.; Julian, B.A.; Klassen, D.K.; Koty, P.P.; Langefeld, C.D.; Lentine, K.L.; Ma, L.; Mannon, R.B.; Menon, M.C.; Mohan, S.; Moore, J.B.; Murphy, B.; Newell, K.A.; Odim, J.; Ortigosa-Goggins, M.; Palmer, N.D.; Park, M.; Parsa, A.; Pastan, S.O.; Poggio, E.D.; Rajapakse, N.; Reeves-Daniel, A.M.; Rosas, S.E.; Russell, L.P.; Sawinski, D.; Smith, S.C.; Spainhour, M.; Stratta, R.J.; Weir, M.R.; Reboussin, D.M.; Kimmel, P.L.; Brennan, D.C. APOL1 long-term kidney transplantation outcomes network (APOLLO): Design and rationale. Kidney Int. Rep., 2020, 5(3), 278-288.
[http://dx.doi.org/10.1016/j.ekir.2019.11.022] [PMID: 32154449]

Ali, A.S.; Pham, C.; Morahan, G.; Ekinci, E.I. Genetic risk scores identify people at high risk of developing diabetic kidney disease: A systematic review. J. Clin. Endocrinol. Metab., 2023, 109(5), 1189-1197.
[http://dx.doi.org/10.1210/clinem/dgad704] [PMID: 38039081]