A truncated polycystin-2 protein causes polycystic kidney disease and retinal degeneration in transgenic rats

Journal of the American Society of Nephrology

Volumn 17, Issue 10, 2006, Pages 2719-2730

  Gallagher, Anna Rachel ^a,c   Hoffmann, Sigrid ^b   Brown, Nelson ^a,d   Cedzich, Anna ^a,b,e   Meruvu, Sujatha ^a   Podlich, Dirk ^b   Feng, Yuxi ^b   Könecke, Vera ^a   De Vries, Uwe ^a   Hammes, Hans Peter ^b   Gretz, Norbert ^b   Witzgall, Ralph ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOXYCYCLINE; IONOMYCIN; MESSENGER RNA; POLYCYSTIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT DISORDER; BRUSH BORDER; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EPITOPE MAPPING; GENE; GENE FREQUENCY; GENE MUTATION; GENETIC TRANSFECTION; INHERITANCE; KIDNEY POLYCYSTIC DISEASE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE EPITHELIUM; MOLECULAR CLONING; NONHUMAN; PATHOPHYSIOLOGY; PKD1 GENE; PKD2 GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; RAT; RECESSIVE INHERITANCE; RETINA DEGENERATION; SOMATIC MUTATION; TRANSGENICS; VALIDATION PROCESS;

EID: 33749268006     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005090979     Document Type: Article

References (67)

1. Dalgaard OZ: Bilateral polycystic disease of the kidneys. A follow-up of two hundred and eighty-four patients and their families. Acta Med Scand 328[Suppl]: 2-31, 1957
2. Iglesias CG, Torres VE, Offord KP, Holley KE, Beard CM, Kurland LT: Epidemiology of adult polycystic kidney disease, Olmsted County, Minnesota: 1935-1980. Am J Kidney Dis 2: 630-639, 1983
3. Churchill DN, Bear JC, Morgan J, Payne RH, McManamon PJ, Gault MH: Prognosis of adult onset polycystic kidney disease re-evaluated. Kidney Int 26: 190-193, 1984
4. Parfrey PS, Bear JC, Morgan J, Cramer BC, McManamon PJ, Gault MH, Churchill DN, Singh M, Hewitt R, Somlo S, Reeders ST: The diagnosis and prognosis of autosomal dominant polycystic kidney disease. N Engl J Med 323: 1085-1090, 1990
5. Gabow PA, Johnson AM, Kaehny WD, Kimberling WJ, Lezotte DC, Duley IT, Jones RH: Factors affecting the progression of renal disease in autosomal-dominant polycystic kidney disease. Kidney Int 41: 1311-1319, 1992
6. Gallagher AR, Hidaka S, Gretz N, Witzgall R: Molecular basis of autosomal-dominant polycystic kidney disease. Cell Mol Life Sci 59: 682-693, 2002
7. Peters DJM, Sandkuijl LA: Genetic heterogeneity of polycystic kidney disease in Europe. Contrib Nephrol 97: 128-139, 1992
8. Roscoe JM, Brissenden JE, Williams EA, Chery AL, Silverman M: Autosomal dominant polycystic kidney disease in Toronto. Kidney Int 44: 1101-1108, 1993
9. Wright AF, Teague PW, Pound SE, Pignatelli PM, Macnicol AM, Carothers AD, de Mey RJ, Allan PL, Watson ML: A study of genetic linkage heterogeneity in 35 adult-onset polycystic kidney disease families. Hum Genet 90: 569-571, 1993
10. Torra R, Badenas C, Darnell A, Nicolau C, Volpini V, Revert L, Estivill X: Linkage, clinical features, and prognosis of autosomal dominant polycystic kidney disease types 1 and 2. J Am Soc Nephrol 7: 2142-2151, 1996
11. Mochizuki T, Wu G, Hayashi T, Xenophontos SL, Veldhuisen B, Saris JJ, Reynolds DM, Cai Y, Gabow PA, Pierides A, Kimberling WJ, Breuning MH, Deltas CC, Peters DJM, Somlo S: PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272: 1339-1342, 1996
12. Delmas P, Padilla F, Osorio N, Coste B, Raoux M, Crest M: Polycystins, calcium signaling, and human diseases. Biochem Biophys Res Commun 322: 1374-1383, 2004
13. Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, Germino GG: PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 16: 179-183, 1997
14. Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G: Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci U S A 94: 6965-6970, 1997
15. Li Q, Montalbetti N, Shen PY, Dai X-Q, Cheeseman CI, Karpinski E, Wu G, Cantiello HF, Chen X-Z: Alpha-actinin associates with polycystin-2 and regulates its channel activity. Hum Mol Genet 14: 1587-1603, 2005
16. Lehtonen S, Ora A, Olkkonen VM, Geng L, Zerial M, Somlo S, Lehtonen E: In vivo interaction of the adapter protein CD2-associated protein with the type 2 polycystic kidney disease protein, polycystin-2. J Biol Chem 275: 32888-32893, 2000
17. Rundle DR, Gorbsky G, Tsiokas L: PKD2 interacts and co-localizes with mDia1 to mitotic spindles of dividing cells. Role of mDia1 in PKD2 localization to mitotic spindles. J Biol Chem 279: 29728-29739, 2004
18. Li X, Luo Y, Starremans PG, McNamara CA, Pai Y, Zhou J: Polycystin-1 and polycystin-2 regulate the cell cycle through the helix-loop-helix inhibitor Id2. Nat Cell Biol 7: 1202-1212, 2005
19. Li Y, Wright JM, Qian F, Germino GG, Guggino WB: Polycystin 2 interacts with type I inositol 1,4,5-trisphosphate receptor to modulate intracellular Ca2+ signaling. J Biol Chem 280: 41298-41306, 2005
20. Kottgen M, Benzing T, Simmen T, Tauber R, Buchholz B, Feliciangeli S, Huber TB, Schermer B, Kramer-Zucker A, Hopker K, Simmen KC, Tschucke CC, Sand ford R, Kim E, Thomas g, Walz G: Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J 24: 705-716, 2005
21. Hidaka S, Konecke V, Osten L, Witzgall R: PIGEA-14, a novel coiled-coil protein affecting the intracellular distribution of polycystin-2. J Biol Chem 279: 35009-35016, 2004
22. Li Q, Dai Y, Guo L, Liu Y, Hao C, Wu G, Basora N, Michalak M, Chen X-Z: Polycystin-2 associates with tropomyosin-1, an actin microfilament component. J Mol Biol 325: 949-962, 2003
23. Li Q, Shen PY, Wu G, Chen X-Z: Polycystin-2 interacts with troponin I, an angiogenesis inhibitor. Biochemistry 42: 450-457, 2003
24. Tsiokas L, Arnould T, Zhu C, Kim E, Walz G, Sukhatme VP: Specific association of the gene product of PKD2 with the TRPC1 channel. Proc Natl Acad Sci U S A 96: 3934-3939, 1999
25. Witzgall R: Polycystin-2: An intracellular or plasma membrane channel? Naunyn-Schmiedebergs Arch Pharmacol 371: 342-347, 2005
26. Pazour GJ, San Agustin JT, Follit JA, Rosenbaum JL, Witman GB: Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr Biol 12: R378-R380, 2002
27. Yoder BK, Hou X, Guay-Woodford LM: The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 13: 2508-2516, 2002
28. Pei Y: A 'two-hit' model of cystogenesis in autosomal dominant polycystic kidney disease. Trends Mol Med 7: 151-156, 2001
29. Wu G, D'Agati V, Cai Y, Markowitz G, Park JH, Reynolds DM, Maeda Y, Le TC, Hou H Jr, Kucherlapati R, Edelmann W, Somlo S: Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell 93: 177-188, 1998
30. Thomson RB, Mentone S, Kim R, Earle K, Delpire E, Somlo S, Aronson PS: Histopathological analysis of renal cystic epithelia in the Pkd2WS25/- mouse model of ADPKD. Am J Physiol Renal Physiol 285: F870-F880, 2003
31. Koptides M, Mean R, Demetriou K, Pierides A, Deltas CC: Genetic evidence for a trans-heterozygous model for cystogenesis in autosomal dominant polycystic kidney disease. Hum Mol Genet 9: 447-452, 2000
32. Watnick T, He N, Wang K, Liang Y, Parfrey P, Hefferton D, St. George-Hyslop P, Germino G, Pei Y: Mutations of PKD1 in ADPKD2 cysts suggest a pathogenic effect of transheterozygous mutations. Nat Genet 25: 143-144, 2000
33. Ausubel FA, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology, New York, John Wiley & Sons, 1996
34. Gossen M, Bujard H: Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A 89: 5547-5551, 1992
35. Koulen P, Cai Y, Geng L, Maeda Y, Nishimura S, Witzgall R, Ehrlich BE, Somlo S: Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 4: 191-197, 2002
36. Morgenstern JP, Land H: Advanced mammalian gene transfer: High titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18: 3587-3596, 1990
37. Chen C, Okayama H: High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7: 2745-2752, 1987
38. Cockett MI, Ochalski R, Benwell K, Franco R, Wardwell-Swanson J: Simultaneous expression of multi-subunit proteins in mammalian cells using a convenient set of mammalian cell expression vectors. Biotechniques 23: 402-407, 1997
39. Dong Y, Skoultchi AI, Pollard JW: Efficient DNA transfection of quiescent mammalian cells using poly-L-ornithine. Nucleic Acids Res 21: 771-772, 1993
40. Hartel-Schenk S, Gossrau R, Reutter W: Comparative immunohistochemistry and histochemistry of dipeptidyl peptidase IV in rat organs during development. Histochem J 22: 567-578, 1990
41. Cai Y, Maeda Y, Cedzich A, Torres VE, Wu G, Hayashi T, Mochizuki T, Park JH, Witzgall R, Somlo S: Identification and characterization of polycystin-2, the PKD2 gene product. J Biol Chem 274: 28557-28565, 1999
42. Karniski LP, Lotscher M, Fucentese M, Hilfiker H, Biber J, Murer H: Immunolocalization of sat-1 sulfate/oxalate/bicarbonate anion exchanger in the rat kidney. Am J Physiol 275: F79-F87, 1998
43. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987
44. Zor T, Selinger Z: Linearization of the Bradford protein assay increases its sensitivity: Theoretical and experimental studies. Anal Biochem 236: 302-308, 1996
45. Deltas CC: Mutations of the human polycystic kidney disease 2 (PKD2) gene. Hum Mutat 18: 13-24, 2001
46. Pazour GJ: Intraflagellar transport and cilia-dependent renal disease: The ciliary hypothesis of polycystic kidney disease. J Am Soc Nephrol 15: 2528-2536, 2004
47. Witzgall R: New developments in the field of cystic kidney diseases. Curr Mol Med 5: 455-465, 2005
48. Brown NE, Murcia NS: Delayed cystogenesis and increased ciliogenesis associated with the re-expression of polaris in Tg737 mutant mice. Kidney Int 63: 1220-1229, 2003
49. Standring S: Gray's Anatomy, 39th Ed., Edinburgh, Elsevier Churchill Livingstone, 2005
50. Katsanis N, Beales PL, Woods MO, Lewis RA, Green JS, Parfrey PS, Ansley SJ, Davidson WS, Lupski JR: Mutations in MKKS cause obesity, retinal dystrophy and renal malformations associated with Bardet-Biedl syndrome. Nat Genet 26: 67-70, 2000
51. 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 34: 455-459, 2003
52. 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 37: 282-288, 2005
53. Obermuller N, Gallagher AR, Cai Y, Gassler N, Gretz N, Somlo S, Witzgall R: The rat Pkd2 protein assumes distinct subcellular distributions in different organs. Am J Physiol 277: F914-F925, 1999
54. Wilson PD, Hovater JS, Casey CC, Fortenberry JA, Schwiebert EM: ATP release mechanisms in primary cultures of epithelia derived from the cysts of polycystic kidneys. J Am Soc Nephrol 10: 218-229, 1999
55. Schwiebert EM, Wallace DP, Braunstein GM, King SR, Peti-Peterdi J, Hanaoka K, Guggino WB, Guay-Woodford LM, Bell PD, Sullivan LP, Grantham JJ, Taylor AL: Autocrine extracellular purinergic signaling in epithelial cells derived from polycystic kidneys. Am J Physiol Renal Physiol 282: F763-F775, 2002
56. Hooper KM, Unwin RJ, Sutters M: The isolated C-terminus of polycystin-1 promotes increased ATP-stimulated chloride secretion in a collecting duct cell line. Clin Sci 104: 217-221, 2003
57. Grantham JJ, Geiser JL, Evan AP: Cyst formation and growth in autosomal dominant polycystic kidney disease. Kidney Int 31: 1145-1152, 1987
58. Devuyst O, Burrow CR, Smith BL, Agre P, Knepper MA, Wilson PD: Expression of aquaporins-1 and -2 during nephrogenesis and in autosomal dominant polycystic kidney disease. Am J Physiol 271: F169-F183, 1996
59. Bachinsky DR, Sabolic I, Emmanouel DS, Jefferson DM, Carone FA, Brown D, Perrone RD: Water channel expression in human ADPKD kidneys. Am J Physiol 268: F398-F403, 1995
60. Verani R, Walker P, Silva FG: Renal cystic disease of infancy: Results of histochemical studies. Pediatr Nephrol 3: 37-42, 1989
61. Baert L: Hereditary polycystic kidney disease (adult form): A microdissection study of two cases at an early stage of the disease. Kidney Int 13: 519-525, 1978
62. Avner ED, Studnicki FE, Young MC, Sweeney WE Jr, Piesco NP, Ellis D, Fettermann GH: Congenital murine polycystic kidney disease. I. The ontogeny of tubular cyst formation. Pediatr Nephrol 1: 587-596, 1987
63. Gattone VH II, Calvet JP, Cowley BD Jr, Evan AP, Shaver TS, Helmstadter K, Grantham JJ: Autosomal recessive polycystic kidney disease in a murine model. A gross and microscopic description. Lab Invest 59: 231-238, 1988
64. Lantinga-van Leeuwen IS, Dauwerse JG, Baelde HJ, Leonhard WN, van de Wal A, Ward CJ, Verbeek S, DeRuiter MC, Breuning MH, de Heer E, Peters DJM: Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease. Hum Mol Genet 13: 3069-3077, 2004
65. Jiang S-T, Chiou Y-Y, Wang E, Lin H-K, Lin Y-T, Chi Y-C, Wang C-KL, Tang M-J, Li H: Defining a link with autosomal-dominant polycystic kidney disease in mice with congenitally low expression of Pkd1. Am J Pathol 168: 205-220, 2006
66. Pritchard L, Sloane-Stanley JA, Sharpe JA, Aspinwall R, Lu W, Buckle V, Strmecki L, Walker D, Ward CJ, Alpers CE, Zhou J, Wood WG, Harris PC: A human PKD1 transgene generates functional polycystin-1 in mice and is associated with a cystic phenotype. Hum Mol Genet 9: 2617-2627, 2000
67. Thivierge C, Kurbegovic A, Couillard M, Guillaume R, Cote O, Trudel M: Overexpression of PKD1 causes polycystic kidney disease. Mol Cell Biol 26: 1538-1548, 2006