ADCK4 mutations promote steroid-Resistant nephrotic syndrome through CoQ10 biosynthesis disruption

Journal of Clinical Investigation

Volumn 123, Issue 12, 2013, Pages 5179-5189

  Ashraf, Shazia ^a   Gee, Heon Yung ^a   Woerner, Stephanie ^b,c   Xie, Letian X ^d   Vega Warner, Virginia ^e   Lovric, Svjetlana ^a   Fang, Humphrey ^a   Song, Xuewen ^f   Cattran, Daniel C ^f   Avila Casado, Carmen ^f   Paterson, Andrew D ^g   Nitschké, Patrick ^c   Bole Feysot, Christine ^h   Cochat, Pierre ⁱ   Esteve Rudd, Julian ^j   Haberberger, Birgit ^k,l   Allen, Susan J ^e   Zhou, Weibin ^e   Airik, Rannar ^a   Otto, Edgar A ^e   Barua, Moumita ^m   Al Hamed, Mohamed H ⁿ   Kari, Jameela A ^o   Evans, Jonathan ^p   Bierzynska, Agnieszka ^q   Saleem, Moin A ^q   Böckenhauer, Detlef ^r   Kleta, Robert ^r   Desoky, Sherif El ^o   Hacihamdioglu, Duygu O ^s   Gok, Faysal ^s   Washburn, Joseph ^t   Wiggins, Roger C ^e   Choi, Murim ^u,v   Lifton, Richard P ^u,v   Levy, Shawn ^w   Han, Zhe ^x   Salviati, Leonardo ^y   Prokisch, Holger ^k,l   Williams, David S ^j   Pollak, Martin ⁱ   Clarke, Catherine F ^d   Pei, York ^f   Antignac, Corinne ^b,c   Hildebrandt, Friedhelm ^a,u,x   more..

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^f UNIVERSITY HEALTH NETWORK   (Canada)

^g HOSPITAL FOR SICK CHILDREN   (Canada)

^h IMAGINE INSTITUTE   (France)

ⁱ HOSPICES CIVILS DE LYON   (France)

^j JULES STEIN EYE INSTITUTE   (United States)

^k INSTITUTE OF EPIDEMIOLOGY   (Germany)

^l TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^m BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

ⁿ NEWCASTLE UNIVERSITY   (United Kingdom)

^o KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^p NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^q UNIVERSITY OF BRISTOL   (United Kingdom)

^r GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^s GULHANE SCHOOL OF MEDICINE   (Turkey)

^t Biomedical Research Core Facilities   (United States)

^u HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^v YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^w HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^x UNIVERSITY OF MICHIGAN   (United States)

^y UNIVERSITY OF PADOVA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AARF DOMAIN CONTAINING KINASE 4; PROTEIN KINASE; PROTEIN P53; UBIDECARENONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL FRACTIONATION; CHROMOSOME 19; CONGENITAL NEPHROTIC SYNDROME; DROSOPHILA; ENZYME ACTIVITY; FRAMESHIFT MUTATION; GENE SILENCING; GLOMERULOSCLEROSIS; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN GENOME; HUMAN TISSUE; LYMPHOBLAST; MISSENSE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOCYTE; PRIORITY JOURNAL; RAT; ZEBRA FISH;

ADOLESCENT; ADRENAL CORTEX HORMONES; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CHILD; CONSANGUINITY; CONSERVED SEQUENCE; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; DROSOPHILA PROTEINS; DRUG RESISTANCE; EXOME; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; NEPHROTIC SYNDROME; PODOCYTES; PROTEIN KINASES; RATS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUINONE; YOUNG ADULT; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84890038202     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69000     Document Type: Article

References (42)

1. Antignac C. Genetic models: clues for understanding the pathogenesis of idiopathic nephrotic syndrome. J Clin Invest. 2002;109(4):447-449.
2. Hinkes BG, et al. Nephrotic syndrome in the first year of life: two thirds of cases are caused by mutations in 4 genes (NPHS1, NPHS2, WT1, and LAMB2). Pediatrics. 2007;119(4):e907-e919.
3. Kim MS, Stablein D, Harmon WE. Renal transplantation in children with congenital nephrotic syndrome: a report of the North American Pediatric Renal Transplant Cooperative Study (NAPRTCS). Pediatr Transplant. 1998;2(4):305-308.
4. Benoit G, Machuca E, Heidet L, Antignac C. Hereditary kidney diseases: highlighting the importance of classical Mendelian phenotypes. Ann N Y Acad Sci. 2010;1214:83-98.
5. Hildebrandt F. Genetic kidney diseases. Lancet. 2010;375(9722):1287-1295.
6. Ozaltin F, et al. Disruption of PTPRO causes childhood- onset nephrotic syndrome. Am J Hum Genet. 2011;89(1):139-147.
7. Heeringa SF, et al. COQ6 mutations in human patients produce nephrotic syndrome with sensorineural deafness. J Clin Invest. 2011;121(5):2013-2024.
8. Hildebrandt F, et al. A systematic approach to mapping recessive disease genes in individuals from outbred populations. PLoS Genet. 2009; 5(1):e1000353.
9. Otto EA, et al. Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinalrenal ciliopathy. Nat Genet. 2010;42(10):840-850.
10. Halbritter J, et al. High-throughput mutation analysis in patients with a nephronophthisis-associated ciliopathy applying multiplexed barcoded arraybased PCR amplification and next-generation sequencing. J Med Genet. 2012;49(12):756-767.
11. Robu ME, et al. p53 activation by knockdown technologies. PLoS Genet. 2007;3(5):e78.
12. Zhou W, Hildebrandt F. Inducible podocyte injury and proteinuria in transgenic zebrafish. J Am Soc Nephrol. 2012;23(6):1039-1047.
13. Hinkes B, et al. Positional cloning uncovers mutations in PLCE1 responsible for a nephrotic syndrome variant that may be reversible. Nat Genet. 2006;38(12):1397-1405.
14. Zhang F, Zhao Y, Han Z. An in vivo functional analysis system for renal gene discovery in Drosophila pericardial nephrocytes. J Am Soc Nephrol. 2013; 24(2):191-197.
15. Lagier-Tourenne C, et al. ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency. Am J Hum Genet. 2008;82(3):661-672.
16. Quinzii CM, Hirano M. Primary and secondary CoQ10 deficiencies in humans. Biofactors. 2011; 37(5):361-365.
17. Mollet J, et al. Prenyldiphosphate synthase, subunit 1 (PDSS1) and OH-benzoate polyprenyltransferase (COQ2) mutations in ubiquinone deficiency and oxidative phosphorylation disorders. J Clin Invest. 2007;117(3):765-772.
18. Quinzii CM, et al. Coenzyme Q deficiency and cerebellar ataxia associated with an aprataxin mutation. Neurology. 2005;64(3):539-541.
19. López LC, et al. Leigh syndrome with nephropathy and CoQ10 deficiency due to decaprenyl diphosphate synthase subunit 2 (PDSS2) mutations. Am J Hum Genet. 2006;79(6):1125-1129.
20. Quinzii C, et al. A mutation in para-hydroxybenzoate- polyprenyl transferase (COQ2) causes primary coenzyme Q10 deficiency. Am J Hum Genet. 2006; 78(2):345-349.
21. Mollet J, et al. CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures. Am J Hum Genet. 2008;82(3):623-630.
22. Salviati L, et al. Haploinsufficiency of COQ4 causes coenzyme Q10 deficiency. J Med Genet. 2012; 49(3):187-191.
23. Diomedi-Camassei F, et al. COQ2 nephropathy: a newly described inherited mitochondriopathy with primary renal involvement. J Am Soc Nephrol. 2007; 18(10):2773-2780.
24. Lopez-Martin JM, et al. Missense mutation of the COQ2 gene causes defects of bioenergetics and Delinquent novo pyrimidine synthesis. Hum Mol Genet. 2007; 16(9):1091-1097.
25. McCarthy HJ, et al. Simultaneous sequencing of 24 genes associated with steroid-resistant nephrotic syndrome. Clin J Am Soc Nephrol. 2013;8(4):637-648.
26. Salviati L, et al. Infantile encephalomyopathy and nephropathy with CoQ10 deficiency: a CoQ10- responsive condition. Neurology. 2005;65(4):606-608.
27. Multiple-System Atrophy Research Collaboration. Mutations in COQ2 in familial and sporadic multiplesystem atrophy. N Engl J Med. 2013;369(3):233-244.
28. Montini G, Malaventura C, Salviati L. Early coenzyme Q10 supplementation in primary coenzyme Q10 deficiency. N Engl J Med. 2008;358(26):2849-2850.
29. Do TQ, Hsu AY, Jonassen T, Lee PT, Clarke CF. A defect in coenzyme Q biosynthesis is responsible for the respiratory deficiency in Saccharomyces cerevisiae abc1 mutants. J Biol Chem. 2001; 276(21):18161-18168.
30. Xie LX, et al. Expression of the human atypical kinase ADCK3 rescues coenzyme Q biosynthesis and phosphorylation of Coq polypeptides in yeast coq8 mutants. Biochim Biophys Acta. 2011;1811(5):348-360.
31. Tauche A, Krause-Buchholz U, Rödel G. Ubiquinone biosynthesis in Saccharomyces cerevisiae: the molecular organization of O-methylase Coq3p depends on Abc1p/Coq8p. FEMS Yeast Res. 2008; 8(8):1263-1275.
32. Albaqumi M, Soos TJ, Barisoni L, Nelson PJ. Collapsing glomerulopathy. J Am Soc Nephrol. 2006; 17(10):2854-2863.
33. Barisoni L, Madaio MP, Eraso M, Gasser DL, Nelson PJ. The kd/kd mouse is a model of collapsing glomerulopathy. J Am Soc Nephrol. 2005; 16(10):2847-2851.
34. [No authors listed]. Primary nephrotic syndrome in children: Clinical significance of histopathologic variants of minimal change of diffuse mesangial hypercellularity: A Report of the International Study of Kidney Disease in Children. Kidney Int. 1981;20(6):765-771.
35. Gee HY, et al. ARHGDIA mutations cause nephrotic syndrome via defective RHO GTPase signaling. J Clin Invest. 2013;123(8):3243-3253.
36. Abecasis GR, Cherny SS, Cookson WO, Cardon LR. Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet. 2002;30(1):97-101.
37. Saleem MA, et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol. 2002; 13(3):630-638.
38. Amoli MM, Carthy D, Platt H, Ollier WE. EBV Immortalization of human B lymphocytes separated from small volumes of cryo-preserved whole blood. Int J Epidemiol. 2008;37(suppl 1):i41-i45.
39. Falk MJ, et al. Probucol ameliorates renal and metabolic sequelae of primary CoQ deficiency in Pdss2 mutant mice. EMBO Mol Med. 2011;3(7):410-427.
40. Haack TB, et al. Molecular diagnosis in mitochondrial complex I deficiency using exome sequencing. J Med Genet. 2012;49(4):277-283.
41. Zhang F, Zhao Y, Chao Y, Muir K, Han Z. Cubilin and amnionless mediate protein reabsorption in Drosophila nephrocytes. J Am Soc Nephrol. 2013; 24(2):209-216.
42. Han Z, Olson EN. Hand is a direct target of Tinman and GATA factors during Drosophila cardiogenesis and hematopoiesis. Development. 2005; 132(15):3525-3536.