APOL1-G1 in nephrocytes induces hypertrophy and accelerates cell death

Journal of the American Society of Nephrology

Volumn 28, Issue 4, 2017, Pages 1106-1116

  Fu, Yulong ^a   Zhu, Jun Yi ^a   Richman, Adam ^a   Zhang, Yi ^a,b   Xie, Xuefang ^b   Das, Jharna R ^b,c,d   Li, Jinliang ^b,d   Ray, Patricio E ^b,c,d   Han, Zhe ^a,d  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

^b Center for Nutrition Genetics & Health   (United States)

^c CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN; SILVER NITRATE; APOL1 PROTEIN, HUMAN; APOLIPOPROTEIN; HIGH DENSITY LIPOPROTEIN;

ACIDIFICATION; ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOL1 G1 GENE; ARTICLE; CELL CULTURE; CELL DEATH; CELL ORGANELLE; CELL SIZE; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; HEMOLYMPH; HUMAN; HUMAN CELL; HYPERTROPHY; KIDNEY CELL; KIDNEY DISEASE; MALE; MOLECULAR BIOLOGY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENE; TRANSGENIC DROSOPHILA; UPREGULATION; ANIMAL; DISEASE COURSE; DISEASE MODEL; DROSOPHILA; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOLIPOPROTEINS; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DROSOPHILA; GENE EXPRESSION REGULATION; HUMANS; HYPERTROPHY; KIDNEY; KIDNEY DISEASES; LIPOPROTEINS, HDL;

EID: 85021848759     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2016050550     Document Type: Article

References (55)

1. Tzur S, Rosset S, Shemer R, Yudkovsky G, 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
2. GenoveseG, FriedmanDJ, 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
3. Friedman DJ, Pollak MR: Genetics of kidney failure and the evolving story of APOL1. J Clin Invest 121: 3367-3374, 2011
4. Friedman DJ, Pollak MR: Apolipoprotein L1 and kidney disease in African Americans. Trends Endocrinol Metab 27: 204-215, 2016
5. Limou S, Nelson GW, Kopp JB, Winkler CA: APOL1 kidney risk alleles: Population genetics and disease associations. Adv Chronic Kidney Dis 21: 426-433, 2014
6. Chen TK, Estrella MM, Parekh RS: The evolving science of apolipoprotein-L1 and kidney disease. Curr Opin Nephrol Hypertens 25: 217-225, 2016
7. Vanhamme L, Paturiaux-Hanocq F, Poelvoorde P, Nolan DP, Lins L, Van Den Abbeele J, Pays A, Tebabi P, Van Xong H, Jacquet A, Moguilevsky N, DieuM, Kane JP, De Baetselier P, Brasseur R, Pays E: Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422: 83-87, 2003
8. 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, Smith MC, Trachtman H, Michel DM, Schelling JR, Vlahov D, Pollak M, Winkler CA: APOL1 genetic variants in focal segmental glomerulosclerosis andHIV-associated nephropathy. J Am Soc Nephrol 22: 2129-2137, 2011
9. Tzur S, Rosset S, Skorecki K, Wasser WG: APOL1 allelic variants are associated with lower age of dialysis initiation and thereby increased dialysis vintage in African and Hispanic Americans with non-diabetic end-stage kidney disease. Nephrol Dial Transplant 27: 1498-1505, 2012
10. Ulasi II, Tzur S, Wasser WG, Shemer R, Kruzel E, Feigin E, Ijoma CK, Onodugo OD, Okoye JU, Arodiwe EB, Ifebunandu NA, Chukwuka CJ, OnyedumCC, Ijoma UN, Nna E, OnuigboM, Rosset S, Skorecki K:High population frequencies of APOL1 risk variants are associated with increased prevalence of non-diabetic chronic kidney disease in the Igbo people from south-eastern Nigeria. Nephron Clin Pract 123: 123-128, 2013
11. Thomson R, Genovese G, Canon C, Kovacsics D, Higgins MK, CarringtonM, Winkler CA, Kopp J, Rotimi C, Adeyemo A, Doumatey A, Ayodo G, Alper SL, Pollak MR, Friedman DJ, Raper J: Evolution of the primate trypanolytic factor APOL1. Proc Natl Acad Sci USA 111: E2130-E2139, 2014
12. Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, Gibbs RA, Hurles ME, McVean GA; 1000 Genomes Project Consortium: A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073, 2010
13. 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
14. Freedman BI, Langefeld CD, Andringa KK, Croker JA, Williams AH, Garner NE, BirminghamDJ, Hebert LA, Hicks PJ, SegalMS, 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
15. 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 associatedwith sickle cell disease nephropathy. Br JHaematol 155: 386-394, 2011
16. Lipkowitz MS, Freedman BI, Langefeld CD, Comeau ME, Bowden DW, Kao WH, Astor BC, Bottinger EP, Iyengar SK, Klotman PE, Freedman RG, Zhang W, Parekh RS, Choi MJ, Nelson GW, Winkler CA, Kopp JB; SK Investigators: Apolipoprotein L1 gene variants associate with hypertension-attributed nephropathy and the rate of kidney function decline in African Americans. Kidney Int 83: 114-120, 2013
17. 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
18. BostromMA, KaoWH, LiM, Abboud HE, Adler SG, Iyengar SK, Kimmel PL, Hanson RL, Nicholas SB, Rasooly RS, Sedor JR, Coresh J, Kohn OF, Leehey DJ, Thornley-Brown D, Bottinger EP, Lipkowitz MS, Meoni LA, Klag MJ, Lu L, Hicks PJ, Langefeld CD, Parekh RS, Bowden DW, Freedman BI; Family Investigation of Nephropathy andDiabetes (FIND) Research Group: Genetic association and gene-gene interaction analyses in African American dialysis patients with nondiabetic nephropathy. Am J Kidney Dis 59: 210-221, 2012
19. 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
20. 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
21. Lee BT, Kumar V, Williams TA, Abdi R, Bernhardy A, Dyer C, Conte S, Genovese G, Ross MD, Friedman DJ, Gaston R, Milford E, Pollak MR, Chandraker A: The APOL1 genotype of African American kidney transplant recipients does not impact 5-year allograft survival. Am. J. Transplant. 12: 1924-1928, 2012.
22. 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 associated with renal allograft failure. Am. J. Transplant. 15: 1615-1622, 2015.
23. Reeves-Daniel AM, DePalma JA, Bleyer AJ, Rocco MV, Murea M, Adams PL, Langefeld CD, Bowden DW, Hicks PJ, Stratta RJ, Lin JJ, Kiger DF, GautreauxMD, Divers J, Freedman BI: The APOL1 gene and allograft survival after kidney transplantation. Am. J. Transplant. 11: 1025-1030, 2011.
24. 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
25. Khatua AK, Cheatham AM, Kruzel ED, Singhal PC, Skorecki K, PopikW: Exon 4-encoded sequence is a major determinant of cytotoxicity of apolipoprotein L1. Am J Physiol Cell Physiol 309: C22-C37, 2015
26. OlabisiOA, Zhang JY, 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 USA 113: 830-837, 2016
27. Lan X, Jhaveri A, Cheng K, Wen H, SaleemMA, Mathieson PW, Mikulak J, Aviram S, Malhotra A, Skorecki K, Singhal PC: APOL1 risk variants enhance podocyte necrosis through compromising lysosomal membrane permeability. Am J Physiol Renal Physiol 307: F326-F336, 2014
28. Bruggeman LA, Wu Z, Luo L, Madhavan SM, Konieczkowski M, Drawz PE, Thomas DB, Barisoni L, Sedor JR, O'Toole JF: APOL1-G0 or APOL1-G2 transgenic models develop preeclampsia but not kidney disease [published online ahead of print March 29, 2016]. J Am Soc Nephrol doi: 10.1681/ASN.2015111220
29. Ashraf S, Gee HY, Woerner S, Xie LX, Vega-Warner V, Lovric S, Fang H, Song X, Cattran DC, Avila-Casado C, Paterson AD, Nitschké P, Bole-Feysot C, Cochat P, Esteve-Rudd J, Haberberger B, Allen SJ, Zhou W, Airik R, Otto EA, BaruaM, Al-HamedMH, Kari JA, Evans J, Bierzynska A, Saleem MA, Böckenhauer D, Kleta R, El Desoky S, Hacihamdioglu DO, Gok F, Washburn J, Wiggins RC, Choi M, Lifton RP, Levy S, Han Z, Salviati L, Prokisch H, Williams DS, Pollak M, Clarke CF, Pei Y, Antignac C, Hildebrandt F: ADCK4 mutations promote steroid-resistant nephrotic syndrome through CoQ10 biosynthesis disruption. JClin Invest 123: 5179-5189, 2013
30. Gee HY, Saisawat P, Ashraf S, Hurd TW, Vega-Warner V, Fang H, Beck BB, Gribouval O, Zhou W, Diaz KA, Natarajan S, Wiggins RC, Lovric S, Chernin G, Schoeb DS, Ovunc B, Frishberg Y, Soliman NA, Fathy HM, Goebel H, Hoefele J, Weber LT, Innis JW, Faul C, Han Z, Washburn J, Antignac C, Levy S, Otto EA, Hildebrandt F: ARHGDIAmutations cause nephrotic syndrome via defective RHO GTPase signaling. J Clin Invest 123: 3243-3253, 2013
31. GeeHY, Zhang F, Ashraf S, Kohl S, Sadowski CE, Vega-Warner V, ZhouW, Lovric S, Fang H, Nettleton M, Zhu JY, Hoefele J, Weber LT, Podracka L, Boor A, Fehrenbach H, Innis JW, Washburn J, Levy S, Lifton RP, Otto EA, Han Z, Hildebrandt F: KANK deficiency leads to podocyte dysfunction and nephrotic syndrome. J Clin Invest 125: 2375-2384, 2015
32. Zhang F, Zhao Y, Han Z: An in vivo functional analysis system for renal gene discovery in Drosophila pericardial nephrocytes. J Am Soc Nephrol 24: 191-197, 2013
33. Zhang F, Zhao Y, Chao Y, Muir K, Han Z: Cubilin and amnionless mediate protein reabsorption in Drosophila nephrocytes. J Am Soc Nephrol 24: 209-216, 2013
34. Weavers H, Prieto-Sánchez S, Grawe F, Garcia-López A, Artero R, Wilsch-Bräuninger M, Ruiz-Gómez M, Skaer H, Denholm B: The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature 457: 322-326, 2009
35. Simons M, Huber TB: Flying podocytes. Kidney Int 75: 455-457, 2009
36. Na J, Cagan R: The Drosophila nephrocyte: Back on stage. J Am Soc Nephrol 24: 161-163, 2013
37. Zhuang S, Shao H, Guo F, Trimble R, Pearce E, Abmayr SM: Sns and Kirre, theDrosophila orthologs of Nephrin andNeph1, direct adhesion, fusion and formation of a slit diaphragm-like structure in insect nephrocytes. Development 136: 2335-2344, 2009
38. Cagan RL: The Drosophila nephrocyte. Curr Opin Nephrol Hypertens 20: 409-415, 2011
39. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta C(T)) method. Methods 25: 402-408, 2001
40. Xie X, Colberg-Poley AM, Das JR, Li J, Zhang A, Tang P, Jerebtsova M, Gutkind JS, Ray PE: The basic domain of HIV-tat transactivating protein is essential for its targeting to lipid rafts and regulating fibroblast growth factor-2 signaling in podocytes isolated from children with HIV-1-associated nephropathy. J Am Soc Nephrol 25: 1800-1813, 2014
41. Brand AH, Perrimon N: Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415, 1993
42. Gullaud M, Delanoue R, Silber J: A Drosophila model to study the functions of TWIST orthologs in apoptosis and proliferation. Cell Death Differ 10: 641-651, 2003
43. Esposito T, Lea RA, Maher BH, Moses D, Cox HC, Magliocca S, Angius A, Nyholt DR, Titus T, Kay T, Gray NA, Rastaldi MP, Parnham A, Gianfrancesco F, Griffiths LR: Unique X-linked familial FSGS with cosegregating heart block disorder is associated with a mutation in the NXF5 gene. Hum Mol Genet 22: 3654-3666, 2013
44. Lan X, Wen H, Lederman R, Malhotra A, Mikulak J, Popik W, Skorecki K, Singhal PC: Protein domains of APOL1 and its risk variants. Exp Mol Pathol 99: 139-144, 2015
45. Akilesh S, Huber TB, Wu H, Wang G, Hartleben B, Kopp JB, Miner JH, Roopenian DC, Unanue ER, Shaw AS: Podocytes use FcRn to clear IgG fromthe glomerular basementmembrane. ProcNatl Acad Sci USA105: 967-972, 2008
46. Soda K, Ishibe S: The function of endocytosis in podocytes. Curr Opin Nephrol Hypertens 22: 432-438, 2013
47. Schieppati A, Remuzzi G: The June 2003 Barry M. Brenner Comgan lecture. The future of renoprotection: Frustration and promises. Kidney Int 64: 1947-1955, 2003
48. Okamura K, Dummer P, Kopp J, Qiu L, Levi M, Faubel S, Blaine J: Endocytosis of albumin by podocytes elicits an inflammatory response and induces apoptotic cell death. PLoS One 8: E54817, 2013
49. Mallipattu SK, He JC: A new mechanism for albuminuria-induced podocyte injury. J Am Soc Nephrol 24: 1709-1711, 2013
50. Schießl IM, Hammer A, Kattler V, Gess B, Theilig F, Witzgall R, Castrop H: Intravital imaging reveals angiotensin II-induced transcytosis of albumin by podocytes. J Am Soc Nephrol 27: 731-744, 2016
51. Han Z, Olson EN: Hand is a direct target of Tinman and GATA factors during Drosophila cardiogenesis and hematopoiesis. Development 132: 3525-3536, 2005
52. Han Z, Yi P, Li X, Olson EN: Hand, an evolutionarily conserved bHLH transcription factor required for Drosophila cardiogenesis and hematopoiesis. Development 133: 1175-1182, 2006
53. Yi P, Han Z, Li X, Olson EN: The mevalonate pathway controls heart formation in Drosophila by isoprenylation of Ggamma1. Science 313: 1301-1303, 2006
54. Schell C, Baumhakl L, Salou S, Conzelmann AC, Meyer C, Helmstädter M, Wrede C, Grahammer F, Eimer S, Kerjaschki D, Walz G, Snapper S, Huber TB: N-wasp is required for stabilization of podocyte foot processes. J Am Soc Nephrol 24: 713-721, 2013
55. Kim JM, Wu H, Green G, Winkler CA, Kopp JB, Miner JH, Unanue ER, Shaw AS: CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 300: 1298-1300, 2003