Nephronophthisis and related syndromes

Current Opinion in Pediatrics

Volumn 27, Issue 2, 2015, Pages 201-211

  Wolf, Matthias T F ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

ciliopathy; Jeune syndrome; Joubert syndrome; nephronophthisis

Indexed keywords

CELL ORGANELLE; CILIARY MOTILITY; END STAGE RENAL DISEASE; GENE EXPRESSION; GENE IDENTIFICATION; GENE PRODUCT; HUMAN; INTRACELLULAR SIGNALING; JOUBERT SYNDROME; LIVER FIBROSIS; MAMMAL CELL; MECKEL SYNDROME; NEPHRONOPHTHISIS; NONHUMAN; PATHOGENESIS; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; SKELETON MALFORMATION; ADOLESCENT; CHILD; COMPLICATION; EUKARYOTIC FLAGELLUM; GENETICS; KIDNEY; KIDNEY DISEASES, CYSTIC; KIDNEY FAILURE, CHRONIC; METABOLISM; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; RECESSIVE GENE; SIGNAL TRANSDUCTION;

MEMBRANE PROTEIN; NPHP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADOLESCENT; CHILD; CILIA; GENES, RECESSIVE; HUMANS; KIDNEY; KIDNEY DISEASES, CYSTIC; KIDNEY FAILURE, CHRONIC; MEMBRANE PROTEINS; MUTATION; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 84922263988     PISSN: 10408703     EISSN: 1531698X     Source Type: Journal    
DOI: 10.1097/MOP.0000000000000194     Document Type: Review

References (91)

1. Fanconi G, Hanhart E, Von Albertini A,. et al. [Familial, juvenile nephronophthisis (idiopathic parenchymal contracted kidney)]. Helv Paediatr Acta 1951; 6: 1-49
2. Hurd TW, Hildebrandt F. Mechanisms of nephronophthisis and related ciliopathies. Nephron Exp Nephrol 2011; 118: e9-14
3. Wolf MT, Hildebrandt F. Nephronophthisis. Pediatr Nephrol 2011; 26: 181-194
4. Simms RJ, Hynes AM, Eley L, Sayer JA. Nephronophthisis: a genetically diverse ciliopathy. Int J Nephrol 2011; 2011: 527137
5. Benzing T, Schermer B. Clinical spectrum and pathogenesis of nephronophthisis. Curr Opin Nephrol Hypertens 2012; 21: 272-278
6. Hildebrandt F, Strahm B, Nothwang HG,. et al. Molecular genetic identification of families with juvenile nephronophthisis type 1: rate of progression to renal failure. APN Study Group. Arbeitsgemeinschaft fur Padiatrische Nephrologie. Kidney Int 1997; 51: 261-269
7. Gagnadoux MF, Bacri JL, Broyer M, Habib R. Infantile chronic tubulo-interstitial nephritis with cortical microcysts: variant of nephronophthisis or new disease entity?. Pediatr Nephrol 1989; 3: 50-55
8. Omran H, Fernandez C, Jung M,. et al. Identification of a new gene locus for adolescent nephronophthisis, on chromosome 3q22 in a large Venezuelan pedigree. Am J Hum Genet 2000; 66: 118-127
9. Ala-Mello S, Kivivuori SM, Ronnholm KA,. et al. Mechanism underlying early anaemia in children with familial juvenile nephronophthisis. Pediatr Nephrol 1996; 10: 578-581
10. Blowey DL, Querfeld U, Geary D,. et al. Ultrasound findings in juvenile nephronophthisis. Pediatr Nephrol 1996; 10: 22-24
11. Salomon R, Saunier S, Niaudet P. Nephronophthisis. Pediatr Nephrol 2009; 24: 2333-2344
12. Waldherr R, Lennert T, Weber HP,. et al. The nephronophthisis complex. A clinicopathologic study in children. Virchows Arch A Pathol Anat Histol 1982; 394: 235-254
13. Haider NB, Carmi R, Shalev H,. et al. A Bedouin kindred with infantile nephronophthisis demonstrates linkage to chromosome 9 by homozygosity mapping. Am J Hum Genet 1998; 63: 1404-1410
14. Gee HY, Otto EA, Hurd TW,. et al. Whole-exome resequencing distinguishes cystic kidney diseases from phenocopies in renal ciliopathies. Kidney Int 2014; 85: 880-88
15. Hildebrandt F, Otto E, Rensing C,. et al. A novel gene encoding an SH3 domain protein is mutated in nephronophthisis type 1. Nat Genet 1997; 17: 149-153
16. Saunier S, Calado J, Heilig R,. et al. A novel gene that encodes a protein with a putative src homology 3 domain is a candidate gene for familial juvenile nephronophthisis. Hum Mol Genet 1997; 6: 2317-2323
17. Otto EA, Schermer B, Obara T,. et al. Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat Genet 2003; 34: 413-420
18. Olbrich H, Fliegauf M, Hoefele J,. et al. Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis. Nat Genet 2003; 34: 455-459
19. Mollet G, Salomon R, Gribouval O,. et al. The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat Genet 2002; 32: 300-305
20. Otto E, Hoefele J, Ruf R,. et al. A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am J Hum Genet 2002; 71: 1161-1167
21. Otto EA, Loeys B, Khanna H,. et al. Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat Genet 2005; 37: 282-288
22. Sayer JA, Otto EA, OToole JF,. et al. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet 2006; 38: 674-681
23. Attanasio M, Uhlenhaut NH, Sousa VH,. et al. Loss of GLIS2 causes nephronophthisis in humans and mice by increased apoptosis and fibrosis. Nat Genet 2007; 39: 1018-1024
24. Delous M, Baala L, Salomon R,. et al. The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome. Nat Genet 2007; 39: 875-881
25. Wolf MT, Saunier S, OToole JF,. et al. Mutational analysis of the RPGRIP1L gene in patients with Joubert syndrome and nephronophthisis. Kidney Int 2007; 72: 1520-1526
26. Otto EA, Trapp ML, Schultheiss UT,. et al. NEK8 mutations affect ciliary and centrosomal localization and may cause nephronophthisis. J Am Soc Nephrol 2008; 19: 587-592
27. Otto EA, Hurd TW, Airik R,. et al. Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy. Nat Genet 2010; 42: 840-850
28. Otto EA, Tory K, Attanasio M,. et al. Hypomorphic mutations in meckelin (MKS3/TMEM67) cause nephronophthisis with liver fibrosis (NPHP11). J Med Genet 2009; 46: 663-670
29. Davis EE, Zhang Q, Liu Q,. et al. TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum. Nat Genet 2011; 43: 189-196
30. Fehrenbach H, Decker C, Eisenberger T,. et al. Mutations in WDR19 encoding the intraflagellar transport component IFT144 cause a broad spectrum of ciliopathies. Pediatr Nephrol 2014; 29: 1451-1456
31. Bredrup C, Saunier S, OudMM,. et al. Ciliopathies with skeletal anomalies and renal insufficiency due to mutations in the IFT-A gene WDR19. Am J Hum Genet 2011; 895: 634-643
32. Chaki M, Airik R, Ghosh AK,. et al. Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling. Cell 2012; 150: 533-548
33. Taskiran EZ, Korkmaz E, Gucer S,. et al. Mutations in ANKS6 cause a nephronophthisis-like phenotype with ESRD. J Am Soc Nephrol 2014; 25: 1653-166
34. Hoff S, Halbritter J, Epting D,. et al. ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3. Nat Genet 2013; 45: 951-956
35. Halbritter J, Bizet AA, Schmidts M,. et al. Defects in the IF T-B component IFT172 cause Jeune and Mainzer-Saldino syndromes in humans. Am J Hum Genet 2013; 93: 915-925
36. Failler M, Gee HY, Krug P,. et al. Mutations of CEP83 cause infantile nephronophthisis and intellectual disability. Am J Hum Genet 2014; 94: 905-914
37. OToole JF, Liu Y, Davis EE,. et al. Individuals with mutations in XPNPEP3, which encodes a mitochondrial protein, develop a nephronophthisis-like nephropathy. J Clin Invest 2010; 120: 791-802
38. Hurd TW, Otto EA, Mishima E,. et al. Mutation of the Mg2 transporter SLC41A1 results in a nephronophthisis-like phenotype. J Am Soc Nephrol 2013; 24: 967-977
39. Halbritter J, Porath JD, Diaz KA,. et al. Identification of 99 novel mutations in a worldwide cohort of 1, 056 patients with a nephronophthisis-related ciliopathy. Hum Genet 2013; 132: 865-884
40. Hildebrandt F, Attanasio M, Otto E. Nephronophthisis: disease mechanisms of a ciliopathy. J Am Soc Nephrol 2009; 20: 23-35
41. Betz R, Rensing C, Otto E,. et al. Children with ocular motor apraxia type Cogan carry deletions in the gene (NPHP1) for juvenile nephronophthisis. J Pediatr 2000; 136: 828-831
42. Ronquillo CC, Bernstein PS, Baehr W. Senior-Loken syndrome: a syndromic form of retinal dystrophy associated with nephronophthisis. Vision Res 2012; 75: 88-97
43. Wang J, Deretic D. Molecular complexes that direct rhodopsin transport to primary cilia. Prog Retin Eye Res 2014; 38: 1-19
44. Romani M, Micalizzi A, Valente EM. Joubert syndrome: congenital cerebellar ataxia with the molar tooth. Lancet Neurol 2013; 12: 894-905
45. Barker AR, Thomas R, Dawe HR. Meckel-Gruber syndrome and the role of primary cilia in kidney, skeleton, and central nervous system development. Organogenesis 2014; 10: 96-107
46. Gunay-Aygun M. Liver and kidney disease in ciliopathies. Am J Med Genet C Semin Med Genet 2009; 151C: 296-306
47. Huber C, Cormier-Daire V. Ciliary disorder of the skeleton. Am J Med Genet C Semin Med Genet 2012; 160C: 165-174
48. Arts H, Knoers N. Cranioectodermal dysplasia. Seattle, WA: NCBI Bookshelf; 1993-2014
49. Baujat G, Huber C, El Hokayem J,. et al. Asphyxiating thoracic dysplasia: clinical and molecular review of 39 families. J Med Genet 2013; 50: 91-98
50. Hildebrandt F, Benzing T, Katsanis N. Ciliopathies. N Engl J Med 2011; 364: 1533-1543
51. Hildebrandt F, Otto E. Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease?. Nat Rev Genet 2005; 6: 928-940
52. Omran H. NPHP proteins: gatekeepers of the ciliary compartment. J Cell Biol 2010; 190: 715-717
53. Wolf MT, Lee J, Panther F,. et al. Expression and phenotype analysis of the nephrocystin-1 and nephrocystin-4 homologs in Caenorhabditis elegans. J Am Soc Nephrol 2005; 16: 676-687
54. Buisson J, Chenouard N, Lagache T,. et al. Intraflagellar transport proteins cycle between the flagellum and its base. J Cell Sci 2013; 126: 327-338
55. Taschner M, Bhogaraju S, Lorentzen E. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 2012; 83: S12-S22
56. Chang B, Khanna H, Hawes N,. et al. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 2006; 15: 1847-1857
57. den Hollander AI, Koenekoop RK, Yzer S,. et al. Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am J Hum Genet 2006; 79: 556-561
58. Fliegauf M, Horvath J, Von Schnakenburg C,. et al. Nephrocystin specifically localizes to the transition zone of renal and respiratory cilia and photoreceptor connecting cilia. J Am Soc Nephrol 2006; 17: 2424-2433
59. Murga-Zamalloa CA, Desai NJ, Hildebrandt F, Khanna H. Interaction of ciliary disease protein retinitis pigmentosa GTPase regulator with nephronophthisisassociated proteins in mammalian retinas. Mol Vis 2010; 16: 1373-1381
60. Collin GB, Won J, Hicks WL,. et al. Meckelin is necessary for photoreceptor intraciliary transport and outer segment morphogenesis. Invest Ophthalmol Vis Sci 2012; 53: 967-974
61. Khanna H, Davis EE, Murga-Zamalloa CA,. et al. A common allele in RPGRIP1L is a modifier of retinal degeneration in ciliopathies. Nat Genet 2009; 41: 739-745
62. Scherft JP, Daems WT. Single cilia in chondrocytes. J Ultrastruct Res 1967; 19: 546-555
63. Beales PL, Bland E, Tobin JL,. et al. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat Genet 2007; 39: 727-729
64. Arts HH, Bongers EM, Mans DA,. et al. C14ORF179 encoding IFT43 is mutated in Sensenbrenner syndrome. J Med Genet 2011; 48: 390-395
65. Mill P, Lockhart PJ, Fitzpatrick E,. et al. Human and mouse mutations in WDR35 cause short-rib polydactyly syndromes due to abnormal ciliogenesis. Am J Hum Genet 2011; 88: 508-515
66. Walczak-Sztulpa J, Eggenschwiler J, Osborn D,. et al. Cranioectodermal dysplasia, Sensenbrenner syndrome, is a ciliopathy caused by mutations in the IFT122 gene. Am J Hum Genet 2010; 86: 949-956
67. Schmidts M, Frank V, Eisenberger T,. et al. Combined NGS approaches identify mutations in the intraflagellar transport gene IFT140 in skeletal ciliopathies with early progressive kidney disease. Hum Mutat 2013; 34: 714-724
68. Perrault I, Saunier S, Hanein S,. et al. Mainzer-Saldino syndrome is a ciliopathy caused by IFT140 mutations. Am J Hum Genet 2012; 90: 864-870
69. Gilissen C, Arts HH, Hoischen A,. et al. Exome sequencing identifies WDR35 variants involved in Sensenbrenner syndrome. Am J Hum Genet 2010; 87: 418-423
70. Seo S, Baye LM, Schulz NP,. et al. BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc Natl Acad Sci U S A 2010; 107: 1488-1493
71. Sang L, Miller JJ, Corbit KC,. et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011; 145: 513-528
72. Simons M, Gloy J, Ganner A,. et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 2005; 37: 537-543
73. Bergmann C, Fliegauf M, Bruchle NO,. et al. Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am J Hum Genet 2008; 82: 959-970
74. Burckle C, Gaude HM, Vesque C,. et al. Control of the Wnt pathways by nephrocystin-4 is required for morphogenesis of the zebrafish pronephros. Hum Mol Genet 2011; 20: 2611-2627
75. Mollet G, Silbermann F, Delous M,. et al. Characterization of the nephrocystin/nephrocystin-4 complex and subcellular localization of nephrocystin-4 to primary cilia and centrosomes. Hum Mol Genet 2005; 14: 645-656
76. Hynes AM, Giles RH, Srivastava S,. et al. Murine Joubert syndrome reveals Hedgehog signaling defects as a potential therapeutic target for nephronophthisis. Proc Natl Acad Sci U S A 2014; 111: 9893-9898
77. Whitfield JF. The solitary (primary) cilium - a mechanosensory toggle switch in bone and cartilage cells. Cell Signal 2008; 20: 1019-1024
78. Habbig S, Bartram MP, Muller RU,. et al. NPHP4, a cilia-associated protein, negatively regulates the Hippo pathway. J Cell Biol 2011; 193: 633-642
79. Habbig S, Bartram MP, Sagmuller JG,. et al. The ciliopathy disease protein NPHP9 promotes nuclear delivery and activation of the oncogenic transcriptional regulator TAZ. Hum Mol Genet 2012; 21: 5528-5538
80. Frank V, Habbig S, Bartram MP,. et al. Mutations in NEK8 link multiple organ dysplasia with altered Hippo signalling and increased c-MYC expression. Hum Mol Genet 2013; 22: 2177-2185
81. Choi HJ, Lin JR, Vannier JB,. et al. NEK8 links the ATR-regulated replication stress response and S phase CDK activity to renal ciliopathies. Mol Cell 2013; 51: 423-439
82. Katsanis N, Ansley SJ, Badano JL,. et al. Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder. Science 2001; 293: 2256-2259
83. Baala L, Audollent S, Martinovic J,. et al. Pleiotropic effects of CEP290 (NPHP6) mutations extend to Meckel syndrome. Am J Hum Genet 2007; 81: 170-179
84. Frank V, den Hollander AI, Bruchle NO,. et al. Mutations of the CEP290 gene encoding a centrosomal protein cause Meckel-Gruber syndrome. Hum Mutat 2008; 29: 45-52
85. Helou J, Otto EA, Attanasio M,. et al. Mutation analysis of NPHP6/CEP290 in patients with Joubert syndrome and Senior-Loken syndrome. J Med Genet 2007; 44: 657-663
86. Leitch CC, Zaghloul NA, Davis EE,. et al. Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat Genet 2008; 40: 443-448
87. Louie CM, Caridi G, Lopes VS,. et al. AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis. Nat Genet 2010; 42: 175-180
88. Zhang Y, Seo S, Bhattarai S,. et al. BBS mutations modify phenotypic expression of CEP290-related ciliopathies. Hum Mol Genet 2014; 23: 40-51
89. Hoefele J, Wolf MT, OToole JF,. et al. Evidence of oligogenic inheritance in nephronophthisis. J Am Soc Nephrol 2007; 18: 2789-2795
90. Badano JL, Kim JC, Hoskins BE,. et al. Heterozygous mutations in BBS1, BBS2 and BBS6 have a potential epistatic effect on Bardet-Biedl patients with two mutations at a second BBS locus. Hum Mol Genet 2003; 12: 1651-1659
91. Tory K, Lacoste T, Burglen L,. et al. High NPHP1 and NPHP6 mutation rate in patients with Joubert syndrome and nephronophthisis: potential epistatic effect of NPHP6 and AHI1 mutations in patients with NPHP1 mutations. J Am Soc Nephrol 2007; 18: 1566-1575