Progressive development of polycystic kidney disease in the mouse model expressing Pkd1 extracellular domain

Human Molecular Genetics

Volumn 22, Issue 12, 2013, Pages 2361-2375

  Kurbegovic, Almira ^a   Trudel, Marie ^a  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCYSTIN 1; POLYCYSTIN 2; TUBERIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HISTOPATHOLOGY; HOMOLOGOUS RECOMBINATION; KIDNEY FUNCTION; KIDNEY POLYCYSTIC DISEASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PATHOPHYSIOLOGY; PHENOTYPE; PKD1 GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; TRANSCRIPTION REGULATION; TRANSGENE; URINARY EXCRETION;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; KIDNEY; MALE; MICE; MICE, TRANSGENIC; MUTATION; POLYCYSTIC KIDNEY DISEASES; PROTEIN STRUCTURE, TERTIARY; TRPP CATION CHANNELS;

MUS MUSCULUS;

EID: 84878472559     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt081     Document Type: Article

References (62)

1. European Chromosome 16 Tuberous Sclerosis Consortium (1993) Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell, 75, 1305-1315.
2. The European Polycystic Kidney Disease Consortium (1994) The polycystic kidney disease 1 gene encodes a 14 kb transcript and lies within a duplicated region on chromosome 16. Cell, 77, 881-894.
3. Burn, T.C., Connors, T.D., Dackowski, W.R., Petry, L.R., Van Raay, T.J., Millholland, J.M., Venet, M., Miller, G., Hakim, R.M., Landes, G.M. et al. (1995) Analysis of the genomic sequence for the autosomal dominant polycystic kidney disease (PKD1) gene predicts the presence of a leucine-rich repeat. Hum. Mol. Genet., 4, 575-582.
4. The International Polycystic Kidney Disease Consortium (1995) Polycystic kidney disease: the complete structure of the PKD1 gene and its protein. Cell, 81, 289-298.
5. Qian, F., Boletta, A., Bhunia, A.K., Xu, H., Liu, L., Ahrabi, A.K., Watnick, T.J., Zhou, F. and Germino, G.G. (2002) Cleavage of polycystin-1 requires the receptor for egg jelly domain and is disrupted by human autosomal-dominant polycystic kidney disease 1-associated mutations. Proc. Natl Acad. Sci. USA, 99, 16981-16986.
6. Arac, D., Boucard, A.A., Bolliger, M.F., Nguyen, J., Soltis, S.M., Sudhof, T.C. and Brunger, A.T. (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J., 31, 1364-1378.
7. Bateman, A. and Sandford, R. (1999) The PLAT domain: a new piece in the PKD1 puzzle. Curr. Biol., 9, R588-R590. 8. van Tilbeurgh, H., Egloff, M.P., Martinez, C., Rugani, N., Verger, R. and Cambillau, C. (1993) Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature, 362, 814-820.
8. van Tilbeurgh, H., Egloff, M.P., Martinez, C., Rugani, N., Verger, R. and Cambillau, C. (1993) Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature,362,814-820
9. Gillmor, S.A., Villasenor, A., Fletterick, R., Sigal, E. and Browner, M.F. (1998) The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity. Nat. Struct. Biol., 4, 1003-1009.
10. Naylor, C.E., Eaton, J.T., Howells, A., Justin, N., Moss, D.S., Titball, R.W. and Basak, A.K. (1998) Structure of the key toxin in gas gangrene. Nat. Struct. Biol., 5, 738-746.
11. Peral, B., Gamble, V., Stron, C., Ong, A.C.M., Sloane-Stanley, J., Zerres, K., Winearls, C.G. and Harris, P.C. (1997) Identification of mutations in the duplicated region of the polycystic kidney disease 1 gene (PKD1) by a novel approach. Am. J. Hum. Genet., 60, 1399-1410.
12. Rossetti, S., Chauveau, D., Walker, D., Saggar-Malik, A., Winearls, C.G., Torres, V.E. and Harris, P.C. (2002) A complete mutation screen of the ADPKD genes by DHPLC. Kidney Int., 61, 1588-1599.
13. Thomas, R., McConnell, R., Whittacker, J., Kirkpatrick, P., Bradley, J. and Sandford, R. (1999) Identification of mutations in the repeated part of the autosomal dominant polycystic kidney disease type 1 gene, PKD1, by long-range PCR. Am. J. Hum. Genet., 65, 39-49.
14. Brook-Carter, P.T., Peral, B., Ward, C.J., Thompson, P., Hughes, J., Maheshwar, M.M., Nellist, M., Gamble, V., Harris, P.C. and Sampson J.R. (1994) Deletion of the TSC2 and PKD1 genes associated with severe infantile polycystic kidney disease - a contiguous gene syndrome. Nat. Genet., 8, 328-332.
15. Ward, C.J., Turley, H., Ong, A.C.M., Comley, M., Biddolph, S., Chetty, R., Ratcliffe, P.J., Gatter, K. and Harris, P.C. (1996) Polycystin, the polycystic kidney disease 1 protein, is expressed by epithelial cells in fetal, adult and polycystic kidney. Proc. Natl Acad. Sci. USA, 93, 1524-1528.
16. Ong, A.C.M., Harris, P.C., Davies, D.R., Pritchard, L., Rossetti, S., Biddolph, S., Vaux, D.J.T., Migone, N. and Ward, C.J. (1999) Polycystin-1 expression in PKD1, early onset PKD1 and TSC2/PKD1 cystic tissue: implications for understanding cystogenesis. Kidney Int., 56, 1324-1333.
17. Qian, F., Watnick, T.J., Onuchic, L.F. and Germino, G.G. (1996) The molecular basis of focal cyst formation in human autosomal dominant polycystic kidney disease type I. Cell, 87, 979-987.
18. Brasier, J.L. and Henske, E.P. (1997) Loss of the polycystic kidney disease (PKD1) region of chromosome 16p13 in renal cyst cells supports a loss-of-function model for cyst pathogenesis. J. Clin. Invest., 99, 194-199.
19. Koptides, M., Constantinides, R., Kyriakides, G., Hadjigavriel, M., Patsalis, P.C., Pierides, A. and Deltas, C.C. (1998) Loss of heterozygosity in polycystic kidney disease with a missense mutation in the repeated region of PKD1. Hum. Genet., 103, 709-717.
20. Rossetti, S., Kubly, V.J., Consugar, M.B., Hopp, K., Roy, S., Horsley, S.W., Chauveau, D., Rees, L., Barratt, T.M., van't Hoff, W.G. et al. (2009) Incompletely penetrant PKD1 alleles suggest a role for gene dosage in cyst initiation in polycystic kidney disease. Kidney Int., 75, 848-855.
21. Lanoix, J., D'Agati, V., Szabolcs, M. and Trudel, M. (1996) Dysregulation of cellular proliferation and apoptosis mediates human autosomal dominant polycystic kidney disease (ADPKD). Oncogene, 13, 1153-1160.
22. Ong, A.C.M., Ward, C.J., Butler, R.J., Biddolph, S., Bowker, C., Torra, R., Pei, Y. and Harris, P.C. (1999) Coordinate expression of the autosomal dominant polycystic kidney disease proteins, polycystin-2 and polycystin-1, in normal and cystic tissue. Am. J. Pathol., 154, 1721-1729.
23. Pritchard, L., Sloane-Stanley, J.A., Sharpe, J.A., Aspinwall, R., Lu, W., Buckle, V., Strmecki, L., Walker, D., Ward, C.J., Alpers, C.E. et al. (2000) A human PKD1 transgene generates functional polycystin-1 in mice and is associated with a cystic phenotype. Hum. Mol. Genet., 9, 2617-2627.
24. Boulter, C., Mulroy, S., Webb, S., Fleming, S., Brindle, K. and Sandford, R. (2001) Cardiovascular, skeletal, and renal defects in mice with a targeted disruption of the Pkd1 gene. Proc. Natl Acad. Sci. USA, 98, 12174-12179.
25. Kim, K., Drummond, I., Ibraghimov-Beskrovnaya, O., Klinger, K. and Arnaout, M.A. (2000) Polycystin 1 is required for the structural integrity of blood vessels. Proc. Natl Acad. Sci. USA, 97, 1731-1736.
26. Lu, W., Peissel, B., Babakhanlou, H., Pavlova, A., Geng, L., Fan, X., Larson, C., Brent, G. and Zhou, J. (1997) Perinatal lethality with kidney and pancreas defects in mice with a targetted PKD1 mutation. Nat. Genet., 17, 179-181.
27. Lu, W., Shen, X., Pavlova, A., Lakkis, M., Watrd, C.J., Pritchard, L., Harris, P.C., Genest, D.R., Perez-Atayde, A.R. and Zhou, J. (2001) Comparison of Pkd1-targeted mutants reveals that loss of polycystin-1 causes cystogenesis and bone defects. Hum. Mol. Genet., 10, 2385-2396.
28. Muto, S., Aiba, A., Saito, Y., Nakao, K., Nakamura, K., Tomita, K., Kitamura, T., Kurabayashi, M., Nagai, R., Higashihara, E. et al. (2002) Pioglitazone improves the phenotype and molecular defects of a targeted Pkd1 mutant. Hum. Mol. Genet., 11, 1731-1742.
29. Wu, G., Tian, X., Nishimura, S., Markowitz, G.S., D'Agati, V., Park, J.H., Yao, L., Li, L., Geng, L., Zhao, H. et al. (2002) Trans-heterozygous Pkd1 and Pkd2 mutations modify expression of polycystin kidney disease. Hum. Mol. Genet., 11, 1845-1854.
30. Lantinga-van Leeuwen, I.S., Dauwerse, J.G., Baelde, H.J., Leonhard, W.N., van de Wal, A., Ward, C.J., Verbeek, S., Deruiter, M.C., Breuning, M.H., de Heer, E. et al. (2004) Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease. Hum. Mol. Genet., 13, 3069-3077.
31. Thivierge, C., Kurbegovic, A., Couillard, M., Guillaume, R., Cote, O. and Trudel, M. (2006) Overexpression of PKD1 causes polycystic kidney disease. Mol. Cell. Biol., 26, 1538-1548.
32. Kurbegovic, A., Cote, O., Couillard, M., Ward, C.J., Harris, P.C. and Trudel, M. (2010) Pkd1 transgenic mice: adult model of polycystic kidney disease with extrarenal and renal phenotypes. Hum. Mol. Genet., 19, 1174-1189.
33. Phakdeekitcharoen, B., Watnick, T.J. and Germino, G.G. (2001) Mutation analysis of the entire replicated portion of PKD1 using genomic DNA samples. J. Am. Soc. Nephrol., 12, 955-963.
34. Kobayashi, T., Minowa, O., Kuno, J., Mitani, H., Hino, O. and Noda, T. (1999) Renal carcinogenesis, hepatic hemangiomatosis, and embryonic lethality caused by a germ-line Tsc2 mutation in mice. Cancer Res., 59, 1206-1211.
35. Onda, H., Lueck, A., Marks, P.W., Warren, H.B. and Kwiatkowski, D.J. (1999) Tsc2+/2 mice develop tumors in multiple sites that express gelsolin and are influenced by genetic background. J. Clin. Invest., 104, 687-698.
36. Cheadle, J.P., Reeve, M.P., Sampson, J.R. and Kwiatkowski, D.J. (2000) Molecular genetic advances in tuberous sclerosis. Hum. Genet., 107, 97-114.
37. Van Adelsberg, J. (1999) Peptides from the PKD repeats of polycystin, the PKD1 gene product, modulate pattern formation in the developing kidney. Dev. Gen., 24, 299-308.
38. Mao, Y., Mulvaney, J., Zakaria, S., Yu, T., Morgan, K.M., Allen, S., Basson, M.A., Francis-West, P. and Irvine, K.D. (2011) Characterization of a Dchs1 mutant mouse reveals requirements for Dchs1-Fat4 signaling during mammalian development. Development, 138, 947-957.
39. Couillard, M. and Trudel, M. (2009) C-myc as a modulator of renal stem/ progenitor cell population. Dev. Dyn., 238, 405-414.
40. Trudel, M., D'Agati, V. and Costantini, F. (1991) C-myc as an inducer of polycystic kidney disease in transgenic mice. Kidney Int., 39, 665-671.
41. Wu, Q., D'Agati, V., Cai, Y., Markowitz, G., Park, J.H., Reynolds, D.M., Maeda, Y., Le, T.C., Hou, H. Jr, Kucherlapati, R. et al. (1998) Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell, 93, 177-188.
42. Ahrabi, A.K., Terryn, S., Valenti, G., Caron, N., Serradeil-Le Gal, C., Raufaste, D., Nielsen, S., Horie, S., Verbavatz, J.M. and Devuyst, O. (2007) PKD1 haploinsufficiency causes a syndrome of inappropriate antidiuresis in mice. J. Am. Soc. Nephrol., 18, 1740-1753.
43. Lu, W., Fan, X., Basora, N., Babakhanlou, H., Law, T., Rifai, N., Harris, P.C., Perez-Atayde, A.R., Rennke, H.G. and Zhou, J. (1999) Late onset of renal and hepatic cysts in Pkd1-targeted heterozygotes. Nat. Genet., 21, 160-161.
44. Tsiokas, L., Kim, E., Arnould, T., Sukhatme, V.P. and Walz, G. (1997) Homo- and heterodimeric interactions between the gene product of PKD1 and PKD2. Proc. Natl Acad. Sci. USA, 94, 6965-6970.
45. Qian, F., Germino, F.J., Cai, Y., Zhang, X., Somlo, S. and Germino, G.G. (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat. Genet., 16, 179-183.
46. Newby, L.J., Streets, A.J., Zhao, Y., Harris, P.C., Ward, C.J. and Ong, A.C. (2002) Identification, characterization, and localization of a novel kidney polycystin-1-polycystin-2 complex. J. Biol. Chem., 277, 20763-20773.
47. Hanaoka, K., Qian, F., Boletta, A., Bhunia, A.K., Plontek, K., Tslokas, L., Sukhatme, V.P., Guggino, W.B. and Germino, G.G. (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature, 408, 990-994.
48. Chapin, H.C., Rajendran, V. and Caplan, M.J. (2010) Polycystin-1 surface localization is stimulated by polycystin-2 and cleavage at the G protein-coupled receptor proteolytic site. Mol. Biol. Cell, 21, 4338-4348.
49. Wu, G., Markowitz, G.S., D'Agati, V.D., Factor, S.M., Geng, L., Tibara, S., Tuchman, J., Cai, Y., Park, J.H., van Adelsberg, J. et al. (2000) Cardiac defects and renal failure in mice with targeted mutations in PKD2. Nat. Gen., 24, 75-78.
50. Park, E.Y., Sung, Y.H., Yang, M.H., Noh, J.Y., Park, S.Y., Lee, T.Y., Yook, Y.J., Yoo, K.H., Roh, K.J., Kim, I. et al. (2009) Cyst formation in kidney via B-Raf signaling in the PKD2 transgenic mice. J. Biol. Chem., 284, 7214-7222.
51. Burtey, S., Riera, M., Ribe, E., Pennekamp, P., Passage, E., Rance, R., Dworniczak, B. and Fontes, M. (2008) Overexpression of PKD2 in the mouse is associated with renal tubulopathy. Nephrol. Dial. Transplant., 23, 1157-1165.
52. Ahn, K., Herman, S.B. and Fahnoe, D.C. (1998) Soluble human endothelinconverting enzyme-1: expression, purification, and demonstration of pronounced pH sensitivity. Arch. Biochem. Biophys., 359, 258-268.
53. Horan, T.P., Simonet, L., Jacobsen, R., Mann, M., Haniu, M., Wen, J., Arakawa, T., Kuwamoto, M. and Martin, F. (1998) Coexpression of G-CSF with an unglycosylated G-CSF receptor mutant results in secretion of a stable complex. Protein Expr. Purif., 14, 45-53.
54. Okamoto, T., Sekiyama, N., Otsu, M., Shimada, Y., Sato, A., Nakanishi, S. and Jingami, H. (1998) Expression and purification of the extracellular ligand binding region of metabotropic glutamate receptor subtype 1. J. Biol. Chem.,
55. Robbins, M.J., Ciruela, F., Rhodes, A. and McIlhinney, R.A. (1999) Characterization of the dimerization of metabotropic glutamate receptors using an N-terminal truncation of mGluR1alpha. J. Neurochem., 72, 2539-2547.
56. Kleymenova, E., Ibraghimov-Beskrovnaya, O., Kugoh, H., Everitt, J., Xu, H., Kiguchi, K., Landes, G., Harris, P. and Walker, C. (2001) Tuberin-dependent membrane localization of polycystin-1: a functional link between polycystic kidney disease and the TSC2 tumor suppressor gene. Mol. Cell, 7, 823-832.
57. Hogan, M.C., Manganelli, L., Woollard, J.R., Masyuk, A.I., Masyuk, T.V., Tammachote, R., Huang, B.Q., Leontovich, A.A., Beito, T.G., Madden, B.J. et al. (2009) Characterization of PKD protein-positive exosome-like vesicles. J. Am. Soc. Nephrol., 20, 278-288.
58. Gong, S., Yang, X.W., Li, C. and Heintz, N. (2002) Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6Kg origin of replication. Genome Res., 12, 1992-1998.
59. De Paepe, M.E. and Trudel, M. (1994) The transgenic SAD mouse: a model of human sickle cell glomerulopathy. Kidney Int., 46, 1337-1345.
60. Couillard, M., Guillaume, R., Tanji, N., D'Agati, V. and Trudel, M. (2002) c-myc-induced apoptosis in polycystic kidney disease is independent of FasL/Fas interaction. Cancer Res., 62, 2210-2214.
61. Trudel, M., Lanoix, J., Barisoni, L., Blouin, M.-J., Desforges, M., L'Italien, C. and D'Agati, V. (1997) C-myc-induced apoptosis in polycystic kidney disease is Bcl-2 and p53 independent. J. Exp. Med., 186, 1873-1884.
62. Guillaume, R., D'Agati, V., Daoust, M. and Trudel, M. (1999) Murine Pkd1 is a developmentally regulated gene from morula to adulthood: role in tissue condensation and patterning. Dev. Dyn., 214, 337-348.