Urinary concentration defects and mechanisms underlying nephronophthisis

Kidney and Blood Pressure Research

Volumn 31, Issue 3, 2008, Pages 152-162

  Krishnan, Rajesh ^a   Eley, Lorraine ^a   Sayer, John A ^a,b  

^a INSTITUTE OF HUMAN GENETICS   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Adherens junction; Aquaporin; Cilia; Collecting duct; Cystic kidney; Nephronophthisis; Urinary concentration defect; Vasopressin receptor

Indexed keywords

CYSTINE; NEPHROCYSTIN; VASOPRESSIN;

GENE MUTATION; GENETIC ANALYSIS; HUMAN; KIDNEY CONCENTRATING CAPACITY; KIDNEY DISEASE; NEPHRONOPHTHISIS; PATHOPHYSIOLOGY; POLYURIA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW;

AQUAPORINS; HUMANS; KIDNEY DISEASES, CYSTIC; URINARY TRACT PHYSIOLOGY; URINE; VASOPRESSINS;

EID: 44149119089     PISSN: 14204096     EISSN: None     Source Type: Journal    
DOI: 10.1159/000129648     Document Type: Review

References (72)

1. Otto E, Kispert A, Schätzle S, Lescher B, Rensing C, Hildebrandt F: Nephrocystin: gene expression and sequence conservation between human, mouse, and Caenorhabditis elegans. J Am Soc Nephrol 2000;11:270-282.
2. Hildebrandt F, Otto E: Molecular genetics of nephronophthisis and medullary cystic kidney disease. J Am Soc Nephrol 2000;11:1753-1761.
3. Gardner KD Jr: Juvenile nephronophthisis and renal medullary cystic disease. Perspect Nephrol Hypertens 1976;4:173-185.
4. Zhai XY, Fenton RA, Andreasen A, Thomsen JS, Christensen EI: Aquaporin-1 is not expressed in descending thin limbs of short-loop nephrons. J Am Soc Nephrol 2007;18:2937-2944.
5. Pisitkun T, Shen RF, Knepper MA: Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004;101:13368-13373.
6. Tamma G, Klussmann E, Oehlke J, Krause E, Rosenthal W, Svelto M, Valenti G: Actin remodeling requires ERM function to facilitate AQP2 apical targeting. J Cell Sci 2005;118:3623-3630.
7. Kokko JP, Rector FC Jr: Countercurrent multiplication system without active transport in inner medulla. Kidney Int 1972;2:214-223.
8. Sasaki S: Nephrogenic diabetes insipidus: update of genetic and clinical aspects. Nephrol Dial Transplant 2004;19:1351-1353.
9. Ward DT, Hammond TG, Harris HW: Modulation of vasopressin-elicited water transport by trafficking of aquaporin2-containing vesicles. Annu Rev Physiol 1999;61:683-697.
10. Marples D, Frøkiaer J, Dørup J, Knepper MA, Nielsen S: Hypokalemia-induced downregulation of aquaporin-2 water channel expression in rat kidney medulla and cortex. J Clin Invest 1996;97:1960-1968.
11. Sands JM, Flores FX, Kato A, Baum MA, Brown EM, Ward DT, Hebert SC, Harris HW: Vasopressin-elicited water and urea permeabilities are altered in IMCD in hypercalcemic rats. Am J Physiol 1998;274:F978-F985.
12. Frøkiaer J, Marples D, Knepper MA, Nielsen S: Bilateral ureteral obstruction downregulates expression of vasopressin-sensitive AQP-2 water channel in rat kidney. Am J Physiol 1996;270:F657-F668.
13. Marples D, Christensen S, Christensen EL, Ottosen PD, Nielsen S: Lithium-induced downregulating of aquaporin-2 water channel expression in rat kidney medulla. J Clin Invest 1995;95:1838-1845.
14. Feldman BJ, Rosenthal SM, Vargas GA, Fenwick RG, Huang EA, Matsuda-Abedini M, Lustig RG: Nephrogenic syndrome of inappropriate antidiuresis. N Engl J Med 2005;352:1884-1890.
15. Gabow PA, Kaehny WD, Johnson AM, Duley IT, Manco-Johnson M, Lezotte DC, Schrier RW: The clinical utility of renal concentrating capacity in polycystic kidney disease. Kidney Int 1989;35:675-680.
16. Dalgaard OZ: Bilateral polycystic disease of the kidneys: a follow-up of two hundred and eighty-four patients and their families. Acta Med Scand Suppl 1957;328:1-255.
17. Martinez-Maldonado M, Yium JJ, Eknoyan G, Suki WN: Adult polycystic kidney disease: studies of the defect in urine concentration. Kidney Int 1972;2:107-113.
18. Bodaghi E, Honarmand MT, Ahmadi M: Infantile nephronophthisis. Int J Pediatr Nephrol 1987;8:207-210.
19. Scolari F, Caridi G, Rampoldi L, Tardanico R, Izzi C, Pirulli D, Amoroso A, Casari G, Ghiggeri GM: Uromodulin storage diseases: clinical aspects and mechanisms. Am J Kidney Dis 2004;44:987-999.
20. Ucar B, Yakut A, Kural N, Büyükasik F, Vardareli E: Renal involvement in the Laurence-Moon-Bardet-Biedl syndrome: report of five cases. Pediatr Nephrol 1997;11:31-35.
21. Hildebrandt F, Sayer JA, Jungers P, Grunfeld JP: Nephronophthisis, medullary cystic and medullary sponge kidney disease; in Schrier RW (ed): Diseases of the Kidney and Urinary Tract. Philadelphia, Lippincott Williams & Wilkins, 2001.
22. Gardner KD Jr: Evolution of clinical signs in adult-onset cystic disease of the renal medulla. Ann Intern Med 1971;74:47-54.
23. Brouhard BH, Srivastava RN, Travis LB, Kay MI, Beathard GA, Dodge WF, Lorentz WB Jr: Nephronophthisis. Renal function and histologic studies in a family. Nephron 1977;19:99-112.
24. Giselson N, Heinegard D, Holmberg CG, Lindberg LG, Lindstedt E, Lindstedt G, Schersten B: Renal medullary cystic disease or familial juvenile nephronophthisis: a renal tubular disease. Biochemical findings in two siblings. Am J Med 1970;48:174-184.
25. Broberger O, Winberg J, Zetterström R: Juvenile nephronophthisis. 1. A genetically determined nephropathy with hypotonic polyuria and azotaemia. Acta Paediatr 1960;49:470-479.
26. Gattone VH 2nd, Wang X, Harris PC, Torres VE: Inhibition of renal cystic disease development and progression by a vasopressin V2 receptor antagonist. Nat Med 2003;9:1323-1326.
27. Frøkiaer J, Marples D, Valtin H, Morris JF, Knepper MA, Nielsen S: Low aquaporin-2 levels in polyuric DI+/+ severe mice with constitutively high cAMP-phosphodiesterase activity. Am J Physiol Renal Physiol 1999;45:F179-F190.
28. Wang X, Gattone V 2nd, Harris PC, Torres VE: Effectiveness of vasopressin V2 receptor antagonists OPC-31260 and OPC-41061 on polycystic kidney disease development in the PCK rat. J Am Soc Nephrol 2005;16:846-851.
29. Torres VE, Wang X, Qian Q, Somlo S, Harris PC, Gattone VH 2nd: Effective treatment of an orthologous model of autosomal dominant polycystic kidney disease. Nat Med 2004;10:363-364.
30. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J: Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 2003;33:129-137.
31. Yamaguchi T, Wallace DP, Magenheimer BS, Hempson SJ, Grantham JJ, Calvet JP: Calcium restriction allows cAMP activation of the B-Raf/ERK pathway, switching cells to a cAMP-dependent growth-stimulated phenotype. J Biol Chem 2004;279:40419-40430.
32. Yamaguchi T, Hempson SJ, Reif GA, Hedge AM, Wallace DP: Calcium restores a normal proliferation phenotype in human polycystic kidney disease epithelial cells. J Am Soc Nephrol 2006;17:178-187.
33. Nagao S, Nishii K, Katsuyama M, Kurahashi H, Marunouchi T, Takahashi H, Wallace DP: Increased water intake decreases progression of polycystic kidney disease in the PCK rat. J Am Soc Nephrol 2006;17:2220-2227.
34. Wang X, Wu Y, Ward CJ, Harris PC, Torres VE: Vasopressin directly regulates cyst growth in polycystic kidney disease. J Am Soc Nephrol 2008;19:102-108.
35. Ding GH, Franki N, Condeelis J, Hays RM: Vasopressin depolymerizes F-actin in toad bladder epithelial cells. Am J Physiol 1991;260:C9-C16.
36. Gattone VH 2nd, Maser RL, Tian C, Rosenberg JM, Branden MG: Developmental expression of urine concentration-associated genes and their altered expression in murine infantile-type polycystic kidney disease. Dev Genet 1999;24:309-318.
37. Hayashi M, Yamaji Y, Monkawa T, Yoshida T, Tsuganezawa H, Sasamura H, Kitajima W, Sasaki S, Ishibashi K, Maurmo F, Saruta T: Expression and localization of the water channels in human autosomal dominant polycystic kidney disease. Nephron 1997;75:321-326.
38. Wilson PD: Polycystic kidney disease: new understanding in the pathogenesis. Int J Biochem Cell Biol 2004;36:1868-1873.
39. Hildebrandt F, Omram H: New insights: nephronophthisis-medullary cystic kidney disease. Pediatr Nephrol 2001;16:168-176.
40. Ashizawa M, Miyazaki M, Furusu A, Abe K, Kanamoto Y, Iwanaga N, Ozono Y, Harada T, Taguchi T, Kohno S: Nephronophthisis in two siblings. Clin Exp Nephrol 2005;9:320-325.
41. Zollinger HU, Mihatsch MJ, Edefonti A, Gaboardi F, Imbasciati E, Lennert T: Nephronophthisis (medullary cystic disease of the kidney). A study using electron microscopy, immunofluorescence, and a review of the morphological findings. Helv Paediatr Acta 1980;35:509-530.
42. Antignac C, Arduy CH, Beckmann JS, Benessy F, Gros F, Medhioub M, Hildebrandt F, Dufier JL, Kleinknecht C, Broyer M, et al: A gene for familial juvenile nephronophthisis (recessive medullary cystic kidney disease) maps to chromosome 2p. Nat Genet 1993;3:342-345.
43. Sherman FE, Studnicki FM, Fetterman G: Renal lesions of familial juvenile nephronophthisis examined by microdissection. Am J Clin Pathol 1971;55:391-400.
44. Phillips CL, Miller KJ, Filson AJ, Nürnberger J, Clendenon JL, Cook GW, Dunn KW, Overbeek PA, Gattone VH 2nd, Bacallao RL: Renal cysts of inv/inv mice resemble early infantile nephronophthisis. J Am Soc Nephrol 2004;15:1744-1755.
45. Hildebrandt F, Otto E: Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease? Nat Rev Genet 2005;6:928-940.
46. Attanasio M, Uhlenhaut NH, Sousa VH, O'Toole JF, Otto E, Anlag K, Klugmann C, Treier AC, Helou J, Sayer JA, Seelow D, Nürnberg G, Becker C, Chudley AE, Nürnberg P, Hildebrandt F, Treier M: Loss of GLIS2 causes nephronophthisis in humans and mice by increased apoptosis and fibrosis. Nat Genet 2007;39:1018-1024.
47. Sayer JA, Otto EA, O'Toole JF, Nürnberg G, Kennedy MA, Becker C, Hennies HC, Helou J, Attanasio M, Fausett BV, Utsch B, Khanna H, Liu Y, Drummond I, Kawakami I, Kusakabe T, Tsuda M, Ma L, Lee H, Larson RG, Allen SJ, Wilkinson CJ, Nigg EA, Shou C, Lillo C, Williams DS, Hoppe B, Kemper MJ, Neuhaus T, Parisi MA, Glass IA, Petry M, Kispert A, Gloy J, Ganner A, Walz G, Zhu X, Goldman D, Nürnberg P, Swaroop A, Leroux MR, Hildebrandt F: The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet 2006;38:674-681.
48. Utsch B, Sayer JA, Attanasio M, Pereira RR, Eccles M, Hennies HC, Otto EA, Hildebrandt F: Identification of the first AHI1 gene mutations in nephronophthisis-associated Joubert syndrome. Pediatr Nephrol 2006;21:32-35.
49. Saunier S, Salomon R, Antignac C: Nephronophthisis. Curr Opin Genet Dev 2005;15:324-331.
50. Otto EA, Schermer B, Obara T, O'Toole JF, Hiller KS, Mueller AM, Ruf RG, Hoefele J, Beekmann F, Landau D, Foreman JW, Goodship JA, Strachan T, Kispert A, Wolf MT, Gagnadoux MF, Nivet H, Antignac C, Walz G, Drummond IA, Benzing T, Hildebrandt F: 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.
51. Donaldson JC, Dempsey PJ, Reddy S, Bouton AH, Coffey RJ, Hanks SK: Crk-associated substrate p130(Cas) interacts with nephrocystin and both proteins localize to cell-cell contacts of polarized epithelial cells. Exp Cell Res 2000;256:168-178.
52. Benzing T, Gerke P, Höpker K, Hildebrandt F, Kim E, Walz G: Nephrocystin interacts with Pyk2, p130(Cas), and tensin and triggers phosphorylation of Pyk2. Proc Natl Acad Sci USA 2001;98:9784-9789.
53. Olbrich H, Fliegauf M, Hoefele J, Kispert A, Otto E, Volz A, Wolf MT, Sasmaz G, Trauer U, Reinhardt R, Sudbrak R, Antignac C, Gretz N, Walz G, Schermer B, Benzing T, Hildebrandt F, Omran H: Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapeto-retinal degeneration and hepatic fibrosis. Nat Genet 2003;34:455-459.
54. Mollet G, Silbermann F, Delous M, Salomon R, Antignac C, Saunier S: 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.
55. Mollet G, Salomon R, Gribouval O, Silbermann F, Bacq D, Landthaler G, Milford D, Nayir A, Rizzoni G, Antignac C, Saunier S: The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat Genet 2002;32:300-305.
56. Otto E, Hoefele J, Ruf R, Mueller AM, Hiller KS, Wolf MT, Schuermann MJ, Becker A, Birkenhager R, Sudbrak R, Hennies HC, Nürnberg P, Hildebrandt F: A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am J Hum Genet 2002;71:1161-1167.
57. Sayer JA, Otto EA, Hildebrandt F: Protein interaction partners of nephrocystin-1 using yeast-2-hybrid analysis. J Am Soc Nephrol 2006;17:517A.
58. Watnick T, Germino G: From cilia to cyst. Nat Genet 2003;34:355-356.
59. Morgan D, Goodship J, Essner JJ, Vogan KJ, Turnpenny L, Yost HJ, Tabin CJ, Strachan T: The left-right determinant inversin has highly conserved ankyrin repeat and IQ domains and interacts with calmodulin. Hum Genet 2002;110:377-384.
60. Morgan D, Turnpenny L, Goodship J, Dai W, Majumder K, Matthews L, Gardner A, Schuster G, Vien L, Harrison W, Elder FF, Penman-Splitt M, Overbeek P, Strachan T: Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat Genet 1998;20:149-156.
61. Morgan D, Eley L, Sayer JA, Strachan T, Yates LM, Craighead AS, Goodship JA: Expression analyses and interaction with the anaphase promoting complex protein Apc2 suggest a role for inversin in primary cilia and involvement in the cell cycle. Hum Mol Genet 2002;11:3345-3350.
62. Eley L, Turnpenny L, Yates LM, Craighead AS, Morgan D, Whistler C, Goodship JA, Strachan T: A perspective on inversin. Cell Biol Int 2004;28:119-124.
63. Nürnberger J, Kribben A, Opazo Saez A, Heusch G, Philipp T, Phillips CL: The Invs gene encodes a microtubule-associated protein. J Am Soc Nephrol 2004;15:1700-1710.
64. Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Krönig C, Schermer B, Benzing T, Cabello OA, Jenny A, Mlodzik M, Polok B, Driever W, Obara T, Walz G: Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 2005;37:537-543.
65. Germino GG: Linking cilia to Wnts. Nat Genet 2005;37:455-457.
66. Arts HH, Doherty D, van Beersum SE, Parisi MA, Letteboer SJ, Gorden NT, Peters TA, Märker T, Voesenek K, Kartono A, Ozyurek H, Farin FM, Kroes HY, Wolfrum U, Brunner HG, Cremers FP, Glass IA, Knoers NV, Roepman R: Mutations in the gene encoding the basal body protein RPGRIP1L, a nephrocystin-4 interactor, cause Joubert syndrome. Nat Genet 2007;39:882-888.
67. Otto EA, Loeys B, Khanna H, Hellemans J, Sudbrak R, Fan S, Muerb U, O'Toole JF, Helou J, Attanasio M, Utsch B, Sayer JA, Lillo C, Jimeno D, Coucke P, De Paepe A, Reinhardt R, Klages S, Tsuda M, Kawakami I, Kusakabe T, Omran H, Imm A, Tippens M, Raymond PA, Hill J, Beales P, He S, Kispert A, Margolis B, Williams DS, Swaroop A, Hildebrandt F: 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.
68. Ferland RJ, Eyaid W, Collura RV, Tully LD, Hill RS, Al-Nouri D, Al-Rumayyan A, Topcu M, Gascon G, Bodell A, Shugart YY, Ruvolo M, Walsh CA: Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nat Genet 2004;36:1008-1013.
69. Dixon-Salazar T, Silhavy JL, Marsh SE, Louie CM, Scott LC, Gururaj A, Al-Gazali L, Al-Tawari AA, Kayserili H, Sztriha L, Gleeson JG: Mutations in the AHI1 gene, encoding jouberin, cause Joubert syndrome with cortical polymicrogyria. Am J Hum Genet 2004;75:979-987.
70. Eley L, Gabrielides C, Adams M, Johnson CA, Hildebrandt F, Sayer JA: Characterization of jouberin reveals a direct interaction with nephrocystin-1, and a collecting duct localization. Kidney Int, submitted.
71. Verkman AS: Renal concentrating and diluting function in deficiency of specific aquaporin genes. Exp Nephrol 2002;10:235-240.
72. Cohen AH, Hoyer JR: Nephronophthisis. A primary tubular basement membrane defect. Lab Invest 1986;55:564-572.