APOL1 renal-risk variants induce mitochondrial dysfunction

Journal of the American Society of Nephrology

Volumn 28, Issue 4, 2017, Pages 1093-1105

  Ma, Lijun ^a   Chou, Jeff W ^a   Snipes, James A ^a   Bharadwaj, Manish S ^a   Craddock, Ann L ^a   Cheng, Dongmei ^a   Weckerle, Allison ^a   Petrovic, Snezana ^a   Hicks, Pamela J ^a   Hemal, Ashok K ^a   Hawkins, Gregory A ^a   Miller, Lance D ^a   Molina, Anthony J A ^a   Langefeld, Carl D ^a   Murea, Mariana ^a   Parks, John S ^a   Freedman, Barry I ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; APOLIPOPROTEIN; APOLIPOPROTEIN L1; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE SUBUNIT 4; DOXYCYCLINE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINATE PHOSPHORIBOSYLTRANSFERASE; POTASSIUM; PROTEIN; SMAD INTERACTING PROTEIN 1; TRANSFER RNA; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; ZINC FINGER E BOX BINDING HOMEOBOX 2; APOL1 PROTEIN, HUMAN; HIGH DENSITY LIPOPROTEIN;

ADULT; ARTICLE; BIOSYNTHESIS; CELL RESPIRATION; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE CONTROL; GENE EXPRESSION PROFILING; GENOTYPE; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; MALE; MIDDLE AGED; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; OXYGEN CONSUMPTION; POTASSIUM CELL LEVEL; POTASSIUM DEPLETION; PRIORITY JOURNAL; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; TGF BETA SIGNALING; BLACK PERSON; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; KIDNEY DISEASE; RISK FACTOR;

AFRICAN CONTINENTAL ANCESTRY GROUP; APOLIPOPROTEINS; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; KIDNEY DISEASES; LIPOPROTEINS, HDL; MALE; MIDDLE AGED; MITOCHONDRIAL DISEASES; RISK FACTORS;

EID: 85021848543     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2016050567     Document Type: Article

References (37)

1. Genovese G, Friedman DJ, RossMD, 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: Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329: 841-845, 2010
2. Tzur S, Rosset S, Shemer R, YudkovskyG, Selig S, Tarekegn A, Bekele E, Bradman N, WasserWG, Behar DM, Skorecki K: Missense mutations in the APOL1 gene are highly associated with end stage kidney disease risk previously attributed to theMYH9 gene. HumGenet 128: 345-350, 2010
3. Freedman BI, Kopp JB, Langefeld CD, Genovese G, Friedman DJ, Nelson GW, Winkler CA, Bowden DW, Pollak MR: The apolipoprotein L1 (APOL1) gene and nondiabetic nephropathy in African Americans. J Am Soc Nephrol 21: 1422-1426, 2010
4. Larsen CP, Beggs ML, Saeed M, Walker PD: Apolipoprotein L1 risk variants associate with systemic lupus erythematosus-associated collapsing glomerulopathy. J Am Soc Nephrol 24: 722-725, 2013
5. Freedman BI, Langefeld CD, Andringa KK, Croker JA, Williams AH, Garner NE, BirminghamDJ, Hebert LA, Hicks PJ, Segal MS, Edberg JC, Brown EE, Alarcón GS, Costenbader KH, Comeau ME, Criswell LA, Harley JB, James JA, Kamen DL, Lim SS, Merrill JT, Sivils KL, Niewold TB, Patel NM, Petri M, Ramsey-Goldman R, Reveille JD, Salmon JE, Tsao BP, Gibson KL, Byers JR, Vinnikova AK, Lea JP, Julian BA, Kimberly RP; Lupus Nephritis-End-Stage Renal Disease Consortium: End-stage renal disease in African Americans with lupus nephritis is associated with APOL1. Arthritis Rheumatol 66: 390-396, 2014
6. Ashley-Koch AE, Okocha EC, Garrett ME, Soldano K, De Castro LM, Jonassaint JC, Orringer EP, Eckman JR, Telen MJ: MYH9 and APOL1 are both associated with sickle cell disease nephropathy. Br J Haematol 155: 386-394, 2011
7. Weckerle A, Snipes JA, Cheng D, Gebre AK, Reisz JA, Murea M, Shelness GS, Hawkins GA, Furdui CM, Freedman BI, Parks JS, Ma L: Characterization of circulating APOL1 protein complexes in African Americans. J Lipid Res 57: 120-130, 2016
8. Bruggeman LA, O'Toole JF, Ross MD, Madhavan SM, Smurzynski M, Wu K, Bosch RJ, Gupta S, Pollak MR, Sedor JR, Kalayjian RC: Plasma apolipoprotein L1 levels do not correlate with CKD. J Am Soc Nephrol 25: 634-644, 2014
9. Reeves-Daniel AM, DePalma JA, Bleyer AJ, Rocco MV, Murea M, Adams PL, Langefeld CD, Bowden DW, Hicks PJ, Stratta RJ, Lin J-J, Kiger DF, GautreauxMD, Divers J, Freedman BI: The APOL1 gene and allograft survival after kidney transplantation. Am J Transplant 11: 1025-1030, 2011
10. Freedman BI, Julian BA, Pastan SO, Israni AK, Schladt D, Gautreaux MD, Hauptfeld V, Bray RA, Gebel HM, Kirk AD, Gaston RS, Rogers J, Farney AC, Orlando G, Stratta RJ, Mohan S, Ma L, Langefeld CD, Hicks PJ, Palmer ND, Adams PL, Palanisamy A, Reeves-Daniel AM, Divers J: Apolipoprotein L1 gene variants in deceased organ donors are associatedwith renal allograft failure. AmJ Transplant 15: 1615-1622, 2015
11. Freedman BI, Pastan SO, Israni AK, Schladt D, Julian BA, Gautreaux MD, Hauptfeld V, Bray RA, Gebel HM, Kirk AD, Gaston RS, Rogers J, Farney AC, Orlando G, Stratta RJ, Mohan S, Ma L, Langefeld CD, Bowden DW, Hicks PJ, Palmer ND, Palanisamy A, Reeves-Daniel AM, Brown WM, Divers J: APOL1 Genotype and Kidney Transplantation Outcomes From Deceased African American Donors. Transplantation 100: 194-202, 2016
12. Ma L, Shelness GS, Snipes JA, Murea M, Antinozzi PA, Cheng D, Saleem MA, Satchell SC, Banas B, Mathieson PW, Kretzler M, Hemal AK, Rudel LL, Petrovic S, Weckerle A, Pollak MR, Ross MD, Parks JS, Freedman BI: Localization of APOL1 protein and mRNA in the human kidney: nondiseased tissue, primary cells, and immortalized cell lines. J Am Soc Nephrol 26: 339-348, 2015
13. Madhavan SM, O'Toole JF, Konieczkowski M, Ganesan S, Bruggeman LA, Sedor JR: APOL1 localization in normal kidney and nondiabetic kidney disease. J Am Soc Nephrol 22: 2119-2128, 2011
14. Hara N, Yamada K, Shibata T, Osago H, Hashimoto T, TsuchiyaM: Elevation of cellular NAD levels by nicotinic acid and involvement of nicotinic acid phosphoribosyltransferase in human cells. J Biol Chem 282: 24574-24582, 2007
15. Hipkiss AR: Aging, Proteotoxicity, Mitochondria, Glycation, NAD and Carnosine: Possible Inter-Relationships and Resolution of the Oxygen Paradox. Front Aging Neurosci 2: 10, 2010
16. Kawakami T, Gomez IG, Ren S, Hudkins K, Roach A, Alpers CE, Shankland SJ, D'Agati VD, Duffield JS: Deficient Autophagy Results in Mitochondrial Dysfunction and FSGS. J Am Soc Nephrol 26: 1040-1052, 2015
17. OlabisiOA, Zhang J-Y, VerPlank L, ZahlerN, DiBartolo S 3rd, Heneghan JF, Schlöndorff JS, Suh JH, Yan P, Alper SL, Friedman DJ, Pollak MR: APOL1 kidney disease risk variants cause cytotoxicity by depleting cellular potassium and inducing stress-activated protein kinases. Proc Natl Acad Sci U S A 113: 830-837, 2016
18. ChengD, Weckerle A, Yu Y, MaL, Zhu X, MureaM, Freedman BI, Parks JS, Shelness GS: Biogenesis and cytotoxicity of APOL1 renal risk variant proteins in hepatocytes and hepatoma cells. J LipidRes 56: 1583-1593, 2015
19. Schweikert E-M, Devarajan A, Witte I, Wilgenbus P, Amort J, Förstermann U, Shabazian A, Grijalva V, Shih DM, Farias-Eisner R, Teiber JF, Reddy ST, Horke S: PON3 is upregulated in cancer tissues and protects against mitochondrial superoxide-mediated cell death. Cell Death Differ 19: 1549-1560, 2012
20. Benarroch EE: Na+, K+-ATPase: Functions in the nervous system and involvement in neurologic disease. Neurology 76: 287-293, 2011
21. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, Epstein CJ, Huang TT, Richardson A: Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am J Physiol Heart Circ Physiol 281: H1422-H1432, 2001
22. Kokoszka JE, Coskun P, Esposito LA, Wallace DC: Increased mitochondrial oxidative stress in the Sod2 (+/-) mouse results in the agerelated decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci U S A 98: 2278-2283, 2001
23. Vanwalleghem G, Fontaine F, Lecordier L, Tebabi P, Klewe K, Nolan DP, Yamaryo-Botté Y, Botté C, Kremer A, Burkard GS, Rassow J, Roditi I, Pérez-Morga D, Pays E: Coupling of lysosomal and mitochondrial membrane permeabilization in trypanolysis by APOL1. Nat Commun 6: 8078, 2015
24. Espinosa-Parrilla Y, Amiel J, Augé J, Encha-Razavi F, Munnich A, Lyonnet S, Vekemans M, Attié-Bitach T: Expression of the SMADIP1 gene during early human development. Mech Dev 114: 187-191, 2002
25. Böttinger EP: TGF-beta in renal injury and disease. Semin Nephrol 27: 309-320, 2007
26. Hagler MA, Hadley TM, Zhang H, Mehra K, Roos CM, Schaff HV, Suri RM, Miller JD: TGF-b signalling and reactive oxygen species drive fibrosis andmatrix remodelling in myxomatous mitral valves. Cardiovasc Res 99: 175-184, 2013
27. Jain M, Rivera S, Monclus EA, Synenki L, Zirk A, Eisenbart J, Feghali-Bostwick C, Mutlu GM, Budinger GRS, Chandel NS: Mitochondrial reactive oxygen species regulate transforming growth factor-b signaling. J Biol Chem 288: 770-777, 2013
28. Yoon Y-S, Lee J-H, Hwang S-C, Choi KS, Yoon G: TGF beta1 induces prolongedmitochondrial ROS generation through decreased complex IV activity with senescent arrest in Mv1Lu cells. Oncogene 24: 1895-1903, 2005
29. Freedman BI, Skorecki K: Gene-gene and gene-environment interactions in apolipoprotein L1 gene-associated nephropathy. Clin J AmSoc Nephrol 9: 2006-2013, 2014
30. Anderson BR, HowellDN, Soldano K, GarrettME, KatsanisN, TelenMJ, Davis EE, Ashley-Koch AE: In vivo Modeling Implicates APOL1 in Nephropathy: Evidence for Dominant Negative Effects and Epistasis under Anemic Stress. PLoS Genet 11: E1005349, 2015
31. Kopp JB, Nelson GW, Sampath K, Johnson RC, Genovese G, An P, Friedman D, Briggs W, Dart R, Korbet S, Mokrzycki MH, Kimmel PL, Limou S, Ahuja TS, Berns JS, Fryc J, Simon EE, SmithMC, Trachtman H, Michel DM, Schelling JR, Vlahov D, Pollak M, Winkler CA: APOL1 genetic variants in focal segmental glomerulosclerosis and HIV-associated nephropathy. J Am Soc Nephrol 22: 2129-2137, 2011
32. Divers J, Núñez M, High KP, Murea M, Rocco MV, Ma L, Bowden DW, Hicks PJ, Spainhour M, Ornelles DA, Kleiboeker SB, Duncan K, Langefeld CD, Turner J, Freedman BI: JC polyoma virus interacts with APOL1 in African Americans with nondiabetic nephropathy. Kidney Int 84: 1207-1213, 2013
33. Ohta A, Nishiyama Y: Mitochondria and viruses. Mitochondrion 11: 1-12, 2011
34. Nichols B, JogP, LeeJH, BlacklerD, WilmotM, D'AgatiV, Markowitz G, Kopp JB, Alper SL, Pollak MR, Friedman DJ: Innate immunity pathways regulate the nephropathy gene Apolipoprotein L1. Kidney Int 87: 332-342, 2015
35. Leishangthem BD, Sharma A, Bhatnagar A: Role of altered mitochondria functions in the pathogenesis of systemic lupus erythematosus. Lupus 25: 272-281, 2016
36. Sampson MG, Robertson CC, Martini S, Mariani LH, Lemley KV, Gillies CE, Otto EA, Kopp JB, Randolph A, Vega-Warner V, Eichinger F, Nair V, Gipson DS, Cattran DC, Johnstone DB, O'Toole JF, Bagnasco SM, Song PX, Barisoni L, Troost JP, Kretzler M, Sedor JR; Nephrotic Syndrome Study Network: Integrative Genomics Identifies Novel Associations with APOL1 Risk Genotypes in Black NEPTUNE Subjects. J Am Soc Nephrol 27: 814-823, 2016
37. Freedman BI, Langefeld CD, Turner J, NúñezM, High KP, Spainhour M, Hicks PJ, BowdenDW, Reeves-Daniel AM, MureaM, RoccoMV, Divers J: Association of APOL1 variants with mild kidney disease in the firstdegree relatives of African American patients with non-diabetic endstage renal disease. Kidney Int 82: 805-811, 2012