Cystic kidney disease: The role of Wnt signaling

Trends in Molecular Medicine

Volumn 16, Issue 8, 2010, Pages 349-360

  Lancaster, Madeline A ^a   Gleeson, Joseph G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; POLYCYSTIN 1; POLYCYSTIN 2; WNT PROTEIN;

ADULT; EUKARYOTIC FLAGELLUM; GENETIC DISORDER; HOMEOSTASIS; HUMAN; KIDNEY DEVELOPMENT; KIDNEY INJURY; KIDNEY POLYCYSTIC DISEASE; MEDULLARY SPONGE KIDNEY; NEPHRONOPHTHISIS; NONHUMAN; REVIEW;

ANIMALS; BETA CATENIN; CELL POLARITY; HUMANS; KIDNEY; KIDNEY DISEASES, CYSTIC; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 77955418239     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2010.05.004     Document Type: Review

References (107)

1. Harris P.C., Torres V.E. Polycystic kidney disease. Annu. Rev. Med. 2009, 60:321-337.
2. Bacallao R.L., McNeill H. Cystic kidney diseases and planar cell polarity signaling. Clin. Genet 2009, 75:107-117.
3. Walz G. Therapeutic approaches in autosomal dominant polycystic kidney disease (ADPKD): is there light at the end of the tunnel?. Nephrol. Dial. Transplant 2006, 21:1752-1757.
4. Reeders S.T. Multilocus polycystic disease. Nat. Genet 1992, 1:235-237.
5. Gonzalez-Perrett S., et al. Polycystin-2, the protein mutated in autosomal dominant polycystic kidney disease (ADPKD), is a Ca2+-permeable nonselective cation channel. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1182-1187.
6. Nauli S.M., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet 2003, 33:129-137.
7. Hanaoka K., et al. Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 2000, 408:990-994.
8. Wang S., et al. Fibrocystin/polyductin, found in the same protein complex with polycystin-2, regulates calcium responses in kidney epithelia. Mol. Cell. Biol. 2007, 27:3241-3252.
9. Bissler J.J., et al. Glomerulocystic kidney disease. Pediatr. Nephrol. 2010, 10.1007/s00467-009-1416-2.
10. Sharp C.K., et al. Dominantly transmitted glomerulocystic kidney disease: a distinct genetic entity. J. Am. Soc. Nephrol. 1997, 8:77-84.
11. Hildebrandt F., et al. Nephronophthisis: disease mechanisms of a ciliopathy. J. Am. Soc. Nephrol. 2009, 20:23-35.
12. Lancaster M.A., Gleeson J.G. The primary cilium as a cellular signaling center: lessons from disease. Curr. Opin. Genet Dev. 2009, 19:220-229.
13. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10:468-477.
14. Petersen C.P., Reddien P.W. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
15. MacDonald B.T., et al. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
16. Kim E., et al. The polycystic kidney disease 1 gene product modulates Wnt signaling. J. Biol. Chem. 1999, 274:4947-4953.
17. Zhang K., et al. PKD1 inhibits cancer cells migration and invasion via Wnt signaling pathway in vitro. Cell Biochem. Funct. 2007, 25:767-774.
18. Zheng R., et al. Polycystin-1 induced apoptosis and cell cycle arrest in G0/G1 phase in cancer cells. Cell Biol. Int. 2008, 32:427-435.
19. Xiao Z., et al. Conditional disruption of Pkd1 in osteoblasts results in osteopenia due to direct impairment of bone formation. J. Biol. Chem. 2010, 285:1177-1187.
20. Lal M., et al. Polycystin-1 C-terminal tail associates with beta-catenin and inhibits canonical Wnt signaling. Hum. Mol. Genet 2008, 17:3105-3117.
21. Kim I., et al. Conditional mutation of Pkd2 causes cystogenesis and upregulates beta-catenin. J. Am. Soc. Nephrol. 2009, 20:2556-2569.
22. Lantinga-van Leeuwen I.S., et al. Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease. Hum. Mol. Genet 2004, 13:3069-3077.
23. Torres V.E., Harris P.C. Mechanisms of disease: autosomal dominant and recessive polycystic kidney diseases. Nat. Clin. Pract. Nephrol. 2006, 2:40-55.
24. Thivierge C., et al. Overexpression of PKD1 causes polycystic kidney disease. Mol. Cell. Biol. 2006, 26:1538-1548.
25. Kurbegovic A., et al. Pkd1 transgenic mice: adult model of polycystic kidney disease with extrarenal and renal phenotypes. Hum. Mol. Genet 2010, 19:1174-1189.
26. Ward C.J., et al. Polycystin, the polycystic kidney disease 1 protein, is expressed by epithelial cells in fetal, adult, and polycystic kidney. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:1524-1528.
27. Saadi-Kheddouci S., et al. Early development of polycystic kidney disease in transgenic mice expressing an activated mutant of the beta-catenin gene. Oncogene 2001, 20:5972-5981.
28. Qian C.N., et al. Cystic renal neoplasia following conditional inactivation of apc in mouse renal tubular epithelium. J. Biol. Chem. 2005, 280:3938-3945.
29. Marose T.D., et al. Beta-catenin is necessary to keep cells of ureteric bud/Wolffian duct epithelium in a precursor state. Dev. Biol. 2008, 314:112-126.
30. Pinson K.I., et al. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000, 407:535-538.
31. Simons M., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet 2005, 37:537-543.
32. Bergmann C., et al. Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am. J. Hum. Genet 2008, 82:959-970.
33. Lancaster M.A., et al. Impaired Wnt-beta-catenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat. Med. 2009, 15:1046-1054.
34. Louie, C.M. and Gleeson, J.G. (2005) Genetic basis of Joubert syndrome and related disorders of cerebellar development. Hum. Mol. Genet 14 Spec No. 2, R235-242.
35. Wiens C.J., et al. Bardet-Biedl syndrome-associated small GTPase ARL6 (BBS3) functions at or near the ciliary gate and modulates Wnt signaling. J. Biol. Chem. 2010, 285:16218-16230.
36. Gerdes J.M., et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet 2007, 39:1350-1360.
37. Marion V., et al. Transient ciliogenesis involving Bardet-Biedl syndrome proteins is a fundamental characteristic of adipogenic differentiation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1820-1825.
38. Axelrod J.D. Progress and challenges in understanding planar cell polarity signaling. Semin. Cell Dev. Biol. 2009, 20:964-971.
39. Zhou W., et al. Nephrocystin-3 is required for ciliary function in zebrafish embryos. Am. J. Physiol. Renal Physiol. 2010, 10.1152/ajprenal.00043.2010.
40. Ross A.J., et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet 2005, 37:1135-1140.
41. Happe H., et al. Toxic tubular injury in kidneys from Pkd1-deletion mice accelerates cystogenesis accompanied by dysregulated planar cell polarity and canonical Wnt signaling pathways. Hum. Mol. Genet 2009, 18:2532-2542.
42. Ferrante M.I., et al. Convergent extension movements and ciliary function are mediated by ofd1, a zebrafish orthologue of the human oral-facial-digital type 1 syndrome gene. Hum. Mol. Genet 2009, 18:289-303.
43. Fischer E., et al. Defective planar cell polarity in polycystic kidney disease. Nat. Genet 2006, 38:21-23.
44. Saburi S., et al. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet 2008, 40:1010-1015.
45. Sopko R., McNeill H. The skinny on Fat: an enormous cadherin that regulates cell adhesion, tissue growth, and planar cell polarity. Curr. Opin. Cell Biol. 2009, 21:717-723.
46. Nikolaidou K.K., Barrett K. Getting to know your neighbours; a new mechanism for cell intercalation. Trends Genet 2005, 21:70-73.
47. Simons M., Walz G. Polycystic kidney disease: cell division without a c(l)ue?. Kidney Int. 2006, 70:854-864.
48. Karner C.M., et al. Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet 2009, 41:793-799.
49. Nishio S., et al. Loss of oriented cell division does not initiate cyst formation. J. Am. Soc. Nephrol. 2010, 21:295-302.
50. Fliegauf M., et al. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell. Biol. 2007, 8:880-893.
51. Mokrzan E.M., et al. Differences in renal tubule primary cilia length in a mouse model of Bardet-Biedl syndrome. Nephron. Exp. Nephrol. 2007, 106:e88-96.
52. Cardenas-Rodriguez M., Badano J.L. Ciliary biology: understanding the cellular and genetic basis of human ciliopathies. Am. J. Med. Genet C. Semin. Med. Genet 2009, 151C:263-280.
53. Nigg E.A., Raff J.W. Centrioles, centrosomes, and cilia in health and disease. Cell 2009, 139:663-678.
54. Berbari N.F., et al. The primary cilium as a complex signaling center. Curr. Biol. 2009, 19:R526-535.
55. Pazour G.J., et al. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 2000, 151:709-718.
56. Yoder B.K., et al. Insertional mutagenesis and molecular analysis of a new gene associated with polycystic kidney disease. Proc. Assoc. Am. Physicians 1995, 107:314-323.
57. Otto E.A., et al. 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.
58. Nakaya M.A., et al. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 2005, 132:5425-5436.
59. Thoma C.R., et al. pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nat. Cell Biol. 2007, 9:588-595.
60. Schermer B., et al. The von Hippel-Lindau tumor suppressor protein controls ciliogenesis by orienting microtubule growth. J. Cell Biol. 2006, 175:547-554.
61. Voronina V.A., et al. Inactivation of Chibby affects function of motile airway cilia. J. Cell Biol. 2009, 185:225-233.
62. Karcher C., et al. Lack of a laterality phenotype in Pkd1 knock-out embryos correlates with absence of polycystin-1 in nodal cilia. Differentiation 2005, 73:425-432.
63. Corbit K.C., et al. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 2008, 10:70-76.
64. McDermott K.M., et al. Primary cilia regulate branching morphogenesis during mammary gland development. Curr. Biol. 2010, 20:731-737.
65. Ocbina P.J., et al. Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS One 2009, 4:e6839.
66. Huang P., Schier A.F. Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 2009, 136:3089-3098.
67. Kishimoto N., et al. Cystic kidney gene seahorse regulates cilia-mediated processes and Wnt pathways. Dev. Cell 2008, 14:954-961.
68. Bonnet C.S., et al. Defects in cell polarity underlie TSC and ADPKD-associated cystogenesis. Hum. Mol. Genet 2009, 18:2166-2176.
69. Oishi I., et al. Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet 2006, 38:1316-1322.
70. Park T.J., et al. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet 2006, 38:303-311.
71. Park T.J., et al. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet 2008, 40:871-879.
72. Hashimoto M., et al. Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 2010, 12:170-176.
73. Tamm S.L., et al. The role of cortical orientation in the control of the direction of ciliary beat in Paramecium. J. Cell Biol. 1975, 64:98-112.
74. Antic D., et al. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One 2010, 5:e8999.
75. Mitchell B., et al. The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr. Biol. 2009, 19:924-929.
76. Maisonneuve C., et al. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 2009, 136:3019-3030.
77. Jones C., et al. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat. Genet 2008, 40:69-77.
78. Jonassen J.A., et al. Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J. Cell Biol. 2008, 183:377-384.
79. Mitchell B., et al. A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 2007, 447:97-101.
80. Piontek K., et al. A critical developmental switch defines the kinetics of kidney cyst formation after loss of Pkd1. Nat. Med. 2007, 13:1490-1495.
81. Schmidt-Ott K.M., et al. beta-catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development 2007, 134:3177-3190.
82. Schmidt-Ott K.M., Barasch J. WNT/beta-catenin signaling in nephron progenitors and their epithelial progeny. Kidney Int. 2008, 74:1004-1008.
83. Schedl A. Renal abnormalities and their developmental origin. Nat. Rev. Genet 2007, 8:791-802.
84. Carroll T.J., et al. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev. Cell 2005, 9:283-292.
85. Park J.S., et al. Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 2007, 134:2533-2539.
86. Yu J., et al. A Wnt7b-dependent pathway regulates the orientation of epithelial cell division and establishes the cortico-medullary axis of the mammalian kidney. Development 2009, 136:161-171.
87. Calvet J.P. Injury and development in polycystic kidney disease. Curr. Opin. Nephrol. Hypertens. 1994, 3:340-348.
88. Takakura A., et al. Renal injury is a third hit promoting rapid development of adult polycystic kidney disease. Hum. Mol. Genet 2009, 18:2523-2531.
89. Patel V., et al. Acute kidney injury and aberrant planar cell polarity induce cyst formation in mice lacking renal cilia. Hum. Mol. Genet 2008, 17:1578-1590.
90. Patel V., et al. Advances in the pathogenesis and treatment of polycystic kidney disease. Curr. Opin. Nephrol. Hypertens. 2009, 18:99-106.
91. Lin S.L., et al. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4194-4199.
92. Davenport J.R., et al. Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr. Biol. 2007, 17:1586-1594.
93. Kottgen M., et al. TRPP2 and TRPV4 form a polymodal sensory channel complex. J. Cell Biol. 2008, 182:437-447.
94. Moch H. Cystic renal tumors: new entities and novel concepts. Adv. Anat. Pathol. 2010, 17:209-214.
95. Bonsib S.M. Renal cystic diseases and renal neoplasms: a mini-review. Clin. J. Am. Soc. Nephrol. 2009, 4:1998-2007.
96. Wong S.Y., et al. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat. Med. 2009, 15:1055-1061.
97. Han Y.G., et al. Dual and opposing roles of primary cilia in medulloblastoma development. Nat. Med. 2009, 15:1062-1065.
98. Deschaseaux F., et al. Mechanisms of bone repair and regeneration. Trends Mol. Med. 2009, 15:417-429.
99. Chen Y., et al. Beta-catenin signaling plays a disparate role in different phases of fracture repair: implications for therapy to improve bone healing. PLoS Med. 2007, 4:e249.
100. Flozak A.S., et al. Beta-catenin/T-cell factor signaling is activated during lung injury and promotes the survival and migration of alveolar epithelial cells. J. Biol. Chem. 2010, 285:3157-3167.
101. Jagasia R., et al. New regulators in adult neurogenesis and their potential role for repair. Trends Mol. Med. 2006, 12:400-405.
102. Apte U., et al. Beta-catenin activation promotes liver regeneration after acetaminophen-induced injury. Am. J. Pathol. 2009, 175:1056-1065.
103. Ravine D., et al. An ultrasound renal cyst prevalence survey: specificity data for inherited renal cystic diseases. Am. J. Kidney Dis. 1993, 22:803-807.
104. Kim Y.S., et al. The Kruppel-like zinc finger protein Glis2 functions as a negative modulator of the Wnt/beta-catenin signaling pathway. FEBS Lett. 2007, 581:858-864.
105. Chitalia V.C., et al. Jade-1 inhibits Wnt signalling by ubiquitylating beta-catenin and mediates Wnt pathway inhibition by pVHL. Nat. Cell Biol. 2008, 10:1208-1216.
106. Lokmane L., et al. vHNF1 functions in distinct regulatory circuits to control ureteric bud branching and early nephrogenesis. Development 2010, 137:347-357.
107. Ma D., et al. Fidelity in planar cell polarity signalling. Nature 2003, 421:543-547.