Pkd1 transgenic mice: Adult model of polycystic kidney disease with extrarenal and renal phenotypes

Human Molecular Genetics

Volumn 19, Issue 7, 2010, Pages 1174-1189

  Kurbegovic, Almira ^a   Côté, Olivier ^a   Couillard, Martin ^a   Ward, Christopher J ^b   Harris, Peter C ^b   Trudel, Marie ^a  

^a UNIVERSITY OF MONTREAL   (Canada)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCYSTIN 1;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; GENE OVEREXPRESSION; GENOMICS; KIDNEY CALCIFICATION; KIDNEY CYST; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY POLYCYSTIC DISEASE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HEART; KIDNEY; LIFE EXPECTANCY; LIVER; MICE; MICE, TRANSGENIC; PHENOTYPE; POLYCYSTIC KIDNEY DISEASES; TRPP CATION CHANNELS; UP-REGULATION;

MUS; MUS MUSCULUS;

EID: 77952491724     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp588     Document Type: Article

References (59)

1. Chapman, A.B., Rubinstein, M.D., Hughes, R., Stears, J.C., Earnest, M.P., Johnson, A.M., Gabow, P.A. and Kaehny, W.D. (1992) Intracranial aneurysms in autosomal dominant polycystic kidney disease. N. Engl. J. Med., 327, 916-920.
2. Wei, W., Hackmann, K., Xu, H., Germino, G. and Qian, F. (2007) Characterization of cis-autoproteolysis of polycystin-1, the product of human polycystic kidney disease 1 gene. J. Biol. Chem., 282, 21729-21737.
3. 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.
4. 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.
5. Geng, L., Segal, Y., Peissel, B., Deng, N., Pei, Y., Carone, F., Rennke, H.G., Glücksmann-Kuis, A.M., Schneider, M.C., Ericsson, M. et al. (1996) Identification and localization of polycystin, the PKD1 gene product. J. Clin. Invest., 98, 2674-2682.
6. Ibraghimov-Beskrovnaya, O., Dackowski, W.R., Foggensteiner, L., Coleman, N., Thiru, S., Petry, L.R., Burn, T.C., Connors, T.D., Van Raay, T., Bradley, J. et al. (1997) Polycystin: In vitro synthesis, in vivo tissue expression, and subcellular localization identifies a large membrane-associated protein. Proc. Natl Acad. Sci. USA, 94, 6397-6402.
7. Chauvet, V., Qian, F., Boute, N., Cai, Y., Phakdeekitacharoen, B., Onuchic, L.F., Attie-Bitach, T., Guicharnaud, L., Devuyst, O., Germino, G.G. et al. (2002) Expression of PKD1 and PKD2 Transcripts and Proteins in Human Embryo and during Normal Kidney Development. Am. J. Pathol., 160, 973-983.
8. Peters, D.J.M., Van De Wal, A., Spruit, L., Saris, J.J., Breuning, M.H., Bruijn, J.A. and de Heer, E. (1999) Cellular localization and tissue distribution of polycystin-1. J. Pathol., 188, 439-446.
9. Trudel, M. and Guillaume, R. (2000) Molecular biology of autosomal dominant polycystic kidney disease. Pediatr. Pathol. Mol. Med., 18, 483-499.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. Guillaume, R. and Trudel, M. (2000) Distinct and common developmental expression patterns of the murine PKD2 and PKD1 genes. Mech. Dev., 93, 179-183.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. Starremans, P.G., Li, X., Finnerty, P.E., Guo, L., Takakura, A., Neilson, E.G. and Zhou, J. (2008) A mouse model for polycystic kidney disease through a somatic in-frame deletion in the 5' end of Pkd1. Kidney Int., 73, 1394-1405.
23. Lantinga-van Leeuwen, I.S., Leonhard, W.N., van der Wal, A., Breuning, M.H., de Heer, E. and Peters, D.J.M. (2007) Kidney-specific inactivation of the Pkd1 gene induces rapid cyst formation in developing kidneys and a slow onset of disease in adult mice. Hum. Mol. Genet., 16, 3188-3196.
24. Takakura, A., Contrino, L., Beck, A.W. and Zhou, J. (2008) Pkd1 inactivation induced in adulthood produces focal cystic disease. J. Am. Soc. Nephrol., 19, 2351-2363.
25. 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.
26. 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.
27. 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.
28. 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.
29. Torres, V.E., Erickson, S.B., Smith, L.H., Wilson, D.M., Hattery, R.R. and Segura, J.W. (1988) The association of nephrolithiasis and autosomal dominant polycystic kidney disease. Am. J. Kidney Dis., 11, 318-325.
30. Torres, V.E., Wilson, D.M., Hattery, R.R. and Segura, J.W. (1993) Renal stone disease in autosomal dominant polycystic kidney disease. Am. J. Kidney Dis., 22, 513-519.
31. Levine, E. and Grantham, J.J. (1992) Calcified renal stones and cyst calcifications in autosomal dominant polycystic kidney disease: clinical and CT study in 84 patients. Am. J. Roentgenol., 159, 77-81.
32. Gonzales, P.A., Pisitkun, T., Hoffert, J.D., Tchapyjnikov, D., Star, R.A., Kleta, R., Wang, N.S. and Knepper, M.A. (2009) Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol., 20, 363-379.
33. 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.
34. Adeney, K.L., Siscovick, D.S., Ix, J.H., Seliger, S.L., Shlipak, M.G., Jenny, N.S. and Kestenbaum, B.R. (2009) Association of serum phosphate with vascular and valvular calcification in moderate CKD. J. Am. Soc. Nephrol., 20, 381-387.
35. Yoder, B.K., Hou, X. and Guay-Woodford, L.M. (2002) 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.
36. Pazour, G.J., Dickert, B.L., Vucica, Y., Seeley, E.S., Rosenbaum, J.L., Witman, G.B. and Cole, D.G. (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell. Biol., 151, 709-718.
37. Lin, F., Hiesberger, T., Cordes, K., Sinclair, A.M., Goldstein, L.S.B., Somlo, S. and Igarashi, P. (2003) Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc. Natl Acad. Sci. USA, 100, 5286-5291.
38. Masyuk, T.V., Huang, B.Q., Ward, C.J., Masyuk, A.I., Yuan, D., Splinter, P.L., Punyashthiti, R., Ritman, E.L., Torres, V.E., Harris, P.C. et al. (2003) Defects in cholangiocyte fibrocystin expression and ciliary structure in the PCK rat. Gastroenterology, 125, 1303-1310.
39. Smith, L.A., Bukanov, N.O., Husson, H., Russo, R.J., Barry, T.C., Taylor, A.L., Beier, D.R. and Ibraghimov-Beskrovnaya, O. (2006) Development of polycystic kidney disease in juvenile cystic kidney mice: insights into pathogenesis, ciliary abnormalities, and common features with human disease. J. Am. Soc. Nephrol., 17, 2821-2831.
40. Cadieux, C., Harada, R., Paquet, M., Cote, O., Trudel, M., Nepveu, A. and Bouchard, M. (2008) Polycystic kidneys caused by sustained expression of Cux1 isoform p75. J. Biol. Chem., 283, 13817-13824.
41. Pisitkun, T., Shen, R.F. and Knepper, M.A. (2004) Identification and proteomic profiling of exosomes in human urine. Proc. Natl Acad. Sci. USA, 101, 13368-13373.
42. Jiang, S.-T., Chiou, Y.-Y., Wang, E., Lin, H.-K., Lin, Y.-T., Chi, Y.-C., Wang, C.-K.L., Tang, M.-J. and Li, H. (2006) Defining a link with autosomal-dominant polycystic kidney disease in mice with congenitally low expression of Pkd1. Am. J. Pathol., 168, 205-220.
43. Trudel, M. and D'Agati, V. (1992) A model of polycystic kidney disease in SBM transgenic mice. In Berlyne, G.M. (ed.), Contrib. Nephrol., Karger, S, Basel, Brooklyn, NY, Vol. 97, pp. 47-59.
44. Griffin, M.D., Torres, V.E., Grande, J.P. and Kumar, R. (1996) Immunolocalization of polycystin in human tissues and cultured cells. Proc. Assoc. Am. Physicians, 108, 185-197.
45. Leier, C.V., Baker, P.B., Kilman, J.W. and Wooley, C.F. (1984) Cardiovascular abnormalities associated with adult polycystic kidney disease. Ann. Intern. Med., 100, 683-688.
46. Hossack, K.F., Leddy, C.L., Johnson, A.M., Schrier, R.W. and Gabow, P.A. (1988) Echocardiographic findings in autosomal dominant polycystic kidney disease. New Engl J Med, 319, 907-912.
47. Griffin, M.D., Torres, V.E., Grande, J.P. and Kumar, R. (1997) Vascular expression of polycystin. J. Am. Soc. Nephrol., 8, 616-626.
48. Peters, D.J.M., Spruit, L., Klingel, R., Prins, F., Baelde, H.J.J., Giordano, P.C., Bernini, L.F., de Heer, E., Breuning, M.H. and Bruijn, J.A. (1996) Adult, fetal, and polycystic kidney expression of polycystin, the polycystic kidney disease-1 gene product. Lab. Invest., 75, 221-230.
49. Weston, B.S., Jeffery, S., Jeffrey, I., Sharaf, S.F.A., Carter, N., Saggar-Malik, A. and Price, R.G. (1997) Polycystin expression during embryonic development of human kidney in adult tissues and ADPKD tissue. Histochem. J., 29, 847-856.
50. Palson, R., Sharma, C.P., Kim, K., McLaughlin, M., Brown, D. and Arnaout, M.A. (1996) Characterization and cell distribution of polycystin, the product of autosomal dominant polycystic kidney disease gene 1. Mol. Med., 2, 702-711.
51. 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.
52. 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.
53. 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.
54. 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 R6Kγ origin of replication. Genome Res., 12, 1992-1998.
55. 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.
56. 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.
57. De Paepe, M.E. and Trudel, M. (1994) The transgenic SAD mouse: a model of human sickle cell glomerulopathy. Kidney Int., 46, 1337-1345.
58. Stoyanova, E., Trudel, M., Felfly, H., Garcia, D. and Cloutier, G. (2007) Characterization of circulatory disorders in beta-thalassemic mice by noninvasive ultrasound biomicroscopy. Physiol. Genomics, 29, 84-90.
59. Couillard, M. and Trudel, M. (2009) C-myc as a modulator of renal stem/progenitor cell population. Dev. Dyn., 238, 405-414.