Acute kidney injury and aberrant planar cell polarity induce cyst formation in mice lacking renal cilia

Human Molecular Genetics

Volumn 17, Issue 11, 2008, Pages 1578-1590

  Patel, Vishal ^a   Li, Ling ^a   Cobo stark, Patricia ^a   Shao, Xinli ^a   Somlo, Stefan ^c   Lin, Fangming ^a,b   Igarashi, Peter ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN 2; PROTEIN KIF3A; TAMOXIFEN;

ACUTE DISEASE; AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL LOSS; CELL POLARITY; CELL PROLIFERATION; CELL REGENERATION; CILIATED EPITHELIUM; CONTROLLED STUDY; DISEASE EXACERBATION; EMBRYO; FEMALE; GENE INACTIVATION; GENE TARGETING; HENLE LOOP; KIDNEY CYST; KIDNEY INJURY; KIDNEY POLYCYSTIC DISEASE; MALE; MOUSE; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TISSUE SPECIFICITY; TUMOR LOCALIZATION;

ACUTE DISEASE; ANIMALS; CELL POLARITY; CILIA; CYSTS; HUMANS; KIDNEY DISEASES; KINESIN; LOOP OF HENLE; MICE; MICE, TRANSGENIC; POLYCYSTIC KIDNEY DISEASES;

MAMMALIA; MUS;

EID: 44349116202     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn045     Document Type: Article

References (36)

1. Igarashi, P. and Somlo, S. (2002) Genetics and pathogenesis of polycystic kidney disease. J. Am. Soc. Nephrol., 13, 2384-2398.
2. Lin, F. and Satlin, L.M. (2004) Polycystic kidney disease: The cilium as a common pathway in cystogenesis. Curr. Opin. Pediatr., 16, 171-176.
3. Hiesberger, T. and Igarashi, P. (2005) Elucidating the function of primary cilia by conditional gene inactivation. Curr. Opin. Nephrol. Hypertesns., 14, 373-377.
4. Davenport, J.R. and Yoder, B.K. (2005) An incredible decade for the primary cilium: A look at a once-forgotten organelle. Am. J. Physiol. Renal Physiol., 289, F1159-F1169.
5. Praetorius, H.A. and Spring, K.R. (2003) The renal cell primary cilium functions as a flow sensor. Curr. Opin. Nephrol. Hypertens., 12 517-520.
6. Germino, G.G. (2005) Linking cilia to Wnts. Nat. Genet., 37, 455-457.
7. Hildebrandt, F. and Zhou, W. (2007) Nephronophthisis-associated ciliopathies. J. Am. Soc. Nephrol., 18, 1855-1871.
8. Badano, J.L., Mitsuma, N., Beales, P.L. and Katsanis, N. (2006) The ciliopathies: An emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet., 7, 125-148.
9. Nauli, S.M., Alenghat, F.J., Lou, Y., Williams, E., Vassilev, P., Li, X., Elia, A.E., Lu, W., Brown, E.M., Quinn, S.J. et al. (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet., 33, 129-137.
10. Eggenschwiler, J.T. and Anderson, K.V. (2006) Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol, 23, 345-373.
11. Scholey, J.M. and Anderson, K.V. (2006) Intraflagellar transport and cilium-based signaling. Cell, 125, 439-442.
12. Takeda, S., Yonekawa, Y., Tanaka, Y., Okada, Y., Nonaka, S. and Hirokawa, N. (1999) Left-right asymmetry and kinesin superfamily protein KIF3A: New insights in determination of laterality and mesoderm induction by kif3a mice analysis. J. Cell Biol., 145, 825-836.
13. Marszalek, J.R., Ruiz-Lozano, P., Roberts, E., Chien, K.R. and Goldstein, L.S. (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl Acad. Sci. USA, 96, 5043-5048.
14. Lin, F., Hiesberger, T., Cordes, K., Sinclair, A.M., Goldstein, L.S., 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.
15. Murcia, N.S., Richards, W.G., Yoder, B.K., Mucenski, M.L., Dunlap, J.R. and Woychik, R.P. (2000) The Oak Ridge Polycystic Kidney (orpk) disease gene is required for lett-right axis determination. Development, 127, 2347-2355.
16. Feil, R., Wagner, J., Metzger, D. and Chambon, P. (1997) Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun., 237, 752-757.
17. Shao, X., Johnson, J.E., Richardson, J.A., Hiesberger, T. and Igarashi, P. (2002) A minimal Ksp-cadherin promoter linked to a green fluorescent protein reporter gene exhibits tissue-specific expression in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol., 13, 1824-1836.
18. Shao, X., Somlo, S. and Igarashi, P. (2002) Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol., 13, 1837-1846.
19. Lantinga-van Leeuwen, I.S., Leonhard, W.N., van de Wal, A., Breuning, M.H., Verbeek, S., de Heer, E. and Peters, D.J. (2006) Transgenic mice expressing tamoxifen-inducible Cre for somatic gene modification in renal epithelial cells. Genesis, 44, 225-232.
20. Srinivas, S., Watanabe, T., Lin, C.S., William, C.M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol., 1, 4.
21. Marszalek, JR., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S. and Goldstein, L.S. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102, 175-187.
22. Duffield., J.S., Park, K.M., Hsiao, L.L., Kelley, V.R., Scadden, D.T., Ichimura, T. and Bonventre, J.V. (2005) Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J. Clin. Invest., 115, 1743-1755.
23. Lin, F., Moran, A. and Igarashi, P. (2005) Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J. Clin. Invest., 115, 1756-1764.
24. Fischer, E., Legue, E., Doyen, A., Nato, F., Nicolas, J.F., Torres, V., Yaniv, M. and Pontoglio, M. 2006 Defective planar cell polarity in polycystic kidney disease. Nat. Genet., 38, 21-23.
25. Davenport, J.R., Watts, A.J., Roper, V.C., Croyle, M.J., van Groen, T., Wyss, J.M., Nagy, T.R., Kesteron, R.A. and Yoder, B.K. (2007) Disruption of intraflagellar transport in adult mice leads to obesity and slow-onse cystic kidney disease. Curr. Biol., 17, 1586-1594.
26. Piontek, K., Menezes, L.F., Garcia-Gonzalez, M.A., Huso, D.L. and Germino, G.G. (2007) A critical developmental switch defines the kinetics of kidney cyst formation after loss of Pkd1. Nat. Med., 13, 1490-1495.
27. Cha, J.H., Kim, Y.H., Jung, J.Y., Han, K.H., Madsen, K.M. and Kim, J. (2001) Cell proliferation in the loop of henle in the developing rat kidney. J. Am. Soc. Nephrol., 12, 1410-1421.
28. Rankin, C.A., Grantham, J.J. and Calvet, J.P. (1992) c-Fos expression is hypersensitive to serum-stimulation in cultured cystic kidney cells from the C57BL/6J-cpk mouse. J. Cell. Physiol., 152, 578-586.
29. Calvet, J.P. (1994) Injury and development in polycystic kidney disease. Curr. Opin. Nephrol. Hypertens., 3, 340-348.
30. Karner, C., Wharton, K.A., Jr. and and Carroll, T.J. (2006) Planar cell polarity and vertebrate organogenesis. Semin. Cell Dev. Biol., 17, 194-203.
31. Park, T.J., Haigo, S.L. and Wallingford, J.B. (2006) Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet., 38, 303-311.
32. Mitchell, B. Jacobs, R. Li, J., Chien, S. and Kintner, C. (2007) A positive feedback mechanism governs the polarity and motion of motile cilia. Nature, 447, 97-101.
33. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O.A. Jenny, A. et al. (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet., 37, 537-543.
34. Simons, M. and Walz, G. (2006) Polycystic kidney disease: Cell division without a c(l)ue? Kidney. Int., 70, 854-864.
35. Kaimori, J.Y., Nagasawa, Y., Menezes, L.F., Garcia-Gonzalez, M.A., Deng, J., Imai, E., Onuchic, L.F., Guay-Woodford, L. M. and Germino, G.G. (2007) Polyductin undergoes notch-like processing and regulated release from primary cilia. Hum. Mol. Genet., 16, 942-956.
36. Hiesberger, T., Bai, Y., Shao, X., McNally, B.T., Sinclair, A.M., Tian, X., Somlo, S. and Igarashi, P. (2004) Mutation of hepatocyte nuclear factor-1beta inhibits Pkhd1 Rene expression and produces renal cysts in mice. J. Clin. Invest., 113, 814-825.