Polycystin-1: A master regulator of intersecting cystic pathways

Trends in Molecular Medicine

Volumn 20, Issue 5, 2014, Pages 251-260

  Fedeles, Sorin V ^a   Gallagher, Anna Rachel ^a   Somlo, Stefan ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chaperone therapy; Cyst progression; Polycystic kidney disease; Polycystic liver disease; Polycystin 1 dosage; Protein biogenesis

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1BETA; POLYCYSTIN 1; STRESS ACTIVATED PROTEIN KINASE; VASOPRESSIN V2 RECEPTOR; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIN;

AMINO ACID SEQUENCE; AUTOSOMAL DOMINANT POLYCYSTIC LIVER DISEASE; DISEASE SEVERITY; GENE DOSAGE; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOSITY; HUMAN; KIDNEY CYST; KIDNEY POLYCYSTIC DISEASE; LIVER POLYCYSTIC DISEASE; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; PROTEIN FUNCTION; REVIEW; TISSUE SPECIFICITY; ANIMAL; CYST; GENETICS; METABOLISM;

ANIMALS; CYSTS; HUMANS; POLYCYSTIC KIDNEY DISEASES; TRPP CATION CHANNELS;

EID: 84899977205     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.01.004     Document Type: Review

References (86)

1. Guay-Woodford L.M. Renal cystic diseases: diverse phenotypes converge on the cilium/centrosome complex. Pediatr. Nephrol. 2006, 21:1369-1376.
2. Hughes J., et al. The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat. Genet. 1995, 10:151-160.
3. Mochizuki T., et al. PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 1996, 272:1339-1342.
4. Nauli S.M., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33:129-137.
5. Qian F., et al. The molecular basis of focal cyst formation in human autosomal dominant polycystic kidney disease type I. Cell 1996, 87:979-987.
6. Wu G., et al. Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell 1998, 93:177-188.
7. Torra R., et al. A loss-of-function model for cystogenesis in human autosomal dominant polycystic kidney disease type 2. Am. J. Hum. Genet. 1999, 65:345-352.
8. Brasier J.L., Henske E.P. 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. 1997, 99:194-199.
9. Pei Y., et al. Somatic PKD2 mutations in individual kidney and liver cysts support a 'two-hit' model of cystogenesis in type 2 autosomal dominant polycystic kidney disease. J. Am. Soc. Nephrol. 1999, 10:1524-1529.
10. Watnick T.J., et al. Somatic mutation in individual liver cysts supports a two-hit model of cystogenesis in autosomal dominant polycystic kidney disease. Mol. Cell 1998, 2:247-251.
11. Nishio S., et al. Pkd1 regulates immortalized proliferation of renal tubular epithelial cells through p53 induction and JNK activation. J. Clin. Invest. 2005, 115:910-918.
12. 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.
13. Pei Y., et al. Bilineal disease and trans-heterozygotes in autosomal dominant polycystic kidney disease. Am. J. Hum. Genet. 2001, 68:355-363.
14. Wu G., et al. Trans-heterozygous Pkd1 and Pkd2 mutations modify expression of polycystic kidney disease. Hum. Mol. Genet. 2002, 11:1845-1854.
15. 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.
16. Jiang S.T., et al. Defining a link with autosomal-dominant polycystic kidney disease in mice with congenitally low expression of Pkd1. Am. J. Pathol. 2006, 168:205-220.
17. Rossetti S., et al. Incompletely penetrant PKD1 alleles suggest a role for gene dosage in cyst initiation in polycystic kidney disease. Kidney Int. 2009, 75:848-855.
18. Wang E., et al. Progressive renal distortion by multiple cysts in transgenic mice expressing artificial microRNAs against Pkd1. J. Pathol. 2010, 222:238-248.
19. Hopp K., et al. Functional polycystin-1 dosage governs autosomal dominant polycystic kidney disease severity. J. Clin. Invest. 2012, 122:4257-4273.
20. Fedeles S.V., et al. A genetic interaction network of five genes for human polycystic kidney and liver diseases defines polycystin-1 as the central determinant of cyst formation. Nat. Genet. 2011, 43:639-647.
21. Nims N., et al. Transmembrane domain analysis of polycystin-1, the product of the polycystic kidney disease-1 (PKD1) gene: evidence for 11 membrane-spanning domains. Biochemistry 2003, 42:13035-13048.
22. Yoder B.K., et al. The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J. Am. Soc. Nephrol. 2002, 13:2508-2516.
23. Foggensteiner L., et al. Cellular and subcellular distribution of polycystin-2, the protein product of the PKD2 gene. J. Am. Soc. Nephrol. 2000, 11:814-827.
24. Scheffers M.S., et al. Polycystin-1, the product of the polycystic kidney disease 1 gene, co-localizes with desmosomes in MDCK cells. Hum. Mol. Genet. 2000, 9:2743-2750.
25. Berbari N.F., et al. The primary cilium as a complex signaling center. Curr. Biol. 2009, 19:R526-R535.
26. Veland I.R., et al. Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol. 2009, 111:39-53.
27. Wu J., Mlodzik M. A quest for the mechanism regulating global planar cell polarity of tissues. Trends Cell Biol. 2009, 7:295-305.
28. Cai Y., et al. Identification and characterization of polycystin-2, the PKD2 gene product. J. Biol. Chem. 1999, 274:28557-28565.
29. Celic A., et al. Domain mapping of the polycystin-2 C-terminal tail using de novo molecular modeling and biophysical analysis. J. Biol. Chem. 2008, 283:28305-28312.
30. 2+-dependent regulation of polycystin-2 channel activity. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:9176-9181.
31. Geng L., et al. Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J. Cell Sci. 2006, 119:1383-1395.
32. Casuscelli J., et al. Analysis of the cytoplasmic interaction between polycystin-1 and polycystin-2. Am. J. Physiol. Renal Physiol. 2009, 297:F1310-F1315.
33. Celic A.S., et al. Calcium-induced conformational changes in C-terminal tail of polycystin-2 are necessary for channel gating. J. Biol. Chem. 2012, 287:17232-17240.
34. Ferreira F.M., et al. Macromolecular assembly of polycystin-2 intracytosolic C-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9833-9838.
35. Gallagher A.R., et al. Molecular advances in autosomal dominant polycystic kidney disease. Adv. Chronic Kidney Dis. 2010, 17:118-130.
36. Harris P.C., Torres V.E. Polycystic kidney disease. Annu. Rev. Med. 2009, 60:321-337.
37. Ma M., et al. Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease. Nat. Genet. 2013, 45:1004-1012.
38. Ward C.J., et al. The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein. Nat. Genet. 2002, 30:259-269.
39. Onuchic L.F., et al. PKHD1, the polycystic kidney and hepatic disease 1 gene, encodes a novel large protein containing multiple immunoglobulin-like plexin-transcription-factor domains and parallel beta-helix 1 repeats. Am. J. Hum. Genet. 2002, 70:1305-1317.
40. Furu L., et al. Milder presentation of recessive polycystic kidney disease requires presence of amino acid substitution mutations. J. Am. Soc. Nephrol. 2003, 14:2004-2014.
41. Zhang D., et al. Exome sequencing identifies compound heterozygous PKHD1 mutations as a cause of autosomal recessive polycystic kidney disease. Chin. Med. J. (Engl.) 2012, 125:2482-2486.
42. Nagasawa Y., et al. Identification and characterization of Pkhd1, the mouse orthologue of the human ARPKD gene. J. Am. Soc. Nephrol. 2002, 13:2246-2258.
43. Bakeberg J.L., et al. Epitope-tagged Pkhd1 tracks the processing, secretion, and localization of fibrocystin. J. Am. Soc. Nephrol. 2011, 22:2266-2277.
44. Menezes L.F., et al. Polyductin, the PKHD1 gene product, comprises isoforms expressed in plasma membrane, primary cilium, and cytoplasm. Kidney Int. 2004, 66:1345-1355.
45. Wang S., et al. The autosomal recessive polycystic kidney disease protein is localized to primary cilia, with concentration in the basal body area. J. Am. Soc. Nephrol. 2004, 15:592-602.
46. Zhang M.Z., et al. PKHD1 protein encoded by the gene for autosomal recessive polycystic kidney disease associates with basal bodies and primary cilia in renal epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2311-2316.
47. Gallagher A.R., et al. Biliary and pancreatic dysgenesis in mice harboring a mutation in Pkhd1. Am. J. Pathol. 2008, 172:417-429.
48. Fischer E., et al. Defective planar cell polarity in polycystic kidney disease. Nat. Genet. 2006, 38:21-23.
49. Nishio S., et al. Loss of oriented cell division does not initiate cyst formation. J. Am. Soc. Nephrol. 2010, 21:295-302.
50. Fedeles S., Gallagher A.R. Cell polarity and cystic kidney disease. Pediatr. Nephrol. 2013, 28:1161-1172.
51. Reynolds D.M., et al. Identification of a locus for autosomal dominant polycystic liver disease, on chromosome 19p13.2-13.1. Am. J. Hum. Genet. 2000, 67:1598-1604.
52. Li A., et al. Mutations in PRKCSH cause isolated autosomal dominant polycystic liver disease. Am. J. Hum. Genet. 2003, 72:691-703.
53. Drenth J.P., et al. Germline mutations in PRKCSH are associated with autosomal dominant polycystic liver disease. Nat. Genet. 2003, 33:345-347.
54. Davila S., et al. Mutations in SEC63 cause autosomal dominant polycystic liver disease. Nat. Genet. 2004, 36:575-577.
55. Trombetta E.S., et al. Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J. Biol. Chem. 1996, 271:27509-27516.
56. Stigliano I.D., et al. Glucosidase II beta subunit modulates N-glycan trimming in fission yeasts and mammals. Mol. Biol. Cell 2009, 17:3974-3984.
57. Skowronek M.H., et al. Molecular characterization of a novel mammalian DnaJ-like Sec63p homolog. Biol. Chem. 1999, 380:1133-1138.
58. Hanein D., et al. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 1996, 87:721-732.
59. Lang S., et al. Differential effects of Sec61alpha-, Sec62- and Sec63-depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J. Cell Sci. 2012, 125:1958-1969.
60. Mades A., et al. Role of human sec63 in modulating the steady-state levels of multi-spanning membrane proteins. PLoS ONE 2012, 7:e49243.
61. Alder N.N., et al. The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. J. Cell Biol. 2005, 168:389-399.
62. Blau M., et al. ERj1p uses a universal ribosomal adaptor site to coordinate the 80S ribosome at the membrane. Nat. Struct. Mol. Biol. 2005, 12:1015-1016.
63. Waanders E., et al. Secondary and tertiary structure modeling reveals effects of novel mutations in polycystic liver disease genes PRKCSH and SEC63. Clin. Genet. 2010, 78:47-56.
64. Zimmermann R., et al. Protein transport into the endoplasmic reticulum: mechanisms and pathologies. Trends Mol. Med. 2006, 12:567-573.
65. Janssen M.J., et al. Secondary, somatic mutations might promote cyst formation in patients with autosomal dominant polycystic liver disease. Gastroenterology 2011, 141:2056-2063.
66. Janssen M.J., et al. Loss of heterozygosity is present in SEC63 germline carriers with polycystic liver disease. PLoS ONE 2012, 7:e50324.
67. Watnick T., et al. Mutations of PKD1 in ADPKD2 cysts suggest a pathogenic effect of trans-heterozygous mutations. Nat. Genet. 2000, 25:143-144.
68. 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.
69. Takakura A., et al. Pkd1 inactivation induced in adulthood produces focal cystic disease. J. Am. Soc. Nephrol. 2008, 19:2351-2363.
70. 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.
71. 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.
72. Bastos A.P., et al. Pkd1 haploinsufficiency increases renal damage and induces microcyst formation following ischemia/reperfusion. J. Am. Soc. Nephrol. 2009, 20:2389-2402.
73. Sharma N., et al. Proximal tubule proliferation is insufficient to induce rapid cyst formation after cilia disruption. J. Am. Soc. Nephrol. 2013, 24:456-464.
74. Pritchard L., et al. A human PKD1 transgene generates functional polycystin-1 in mice and is associated with a cystic phenotype. Hum. Mol. Genet. 2000, 9:2617-2627.
75. Bergmann C., Weiskirchen R. It's not all in the cilium, but on the road to it: genetic interaction network in polycystic kidney and liver diseases and how trafficking and quality control matter. J. Hepatol. 2011, 56:1201-1203.
76. Torres V.E., et al. Tolvaptan in patients with autosomal dominant polycystic kidney disease. N. Engl. J. Med. 2012, 367:2407-2418.
77. Audrezet M.P., et al. Autosomal dominant polycystic kidney disease: comprehensive mutation analysis of PKD1 and PKD2 in 700 unrelated patients. Hum. Mutat. 2012, 33:1239-1250.
78. Cornec-Le Gall E., et al. Type of PKD1 mutation influences renal outcome in ADPKD. J. Am. Soc. Nephrol. 2013, 24:1006-1013.
79. Vujic M., et al. Incompletely penetrant PKD1 alleles mimic the renal manifestations of ARPKD. J. Am. Soc. Nephrol. 2010, 21:1097-1102.
80. Bergmann C., et al. Mutations in multiple PKD genes may explain early and severe polycystic kidney disease. J. Am. Soc. Nephrol. 2011, 22:2047-2056.
81. Kleffmann J., et al. Dosage-sensitive network in polycystic kidney and liver disease: multiple mutations cause severe hepatic and neurological complications. J. Hepatol. 2012, 57:476-477.
82. Gresh L., et al. A transcriptional network in polycystic kidney disease. EMBO J. 2004, 23:1657-1668.
83. Garcia-Gonzalez M.A., et al. Genetic interaction studies link autosomal dominant and recessive polycystic kidney disease in a common pathway. Hum. Mol. Genet. 2007, 16:1940-1950.
84. Hampton R.Y., Sommer T. Finding the will and the way of ERAD substrate retrotranslocation. Curr. Opin. Cell Biol. 2012, 24:460-466.
85. Belcher C.N., Vij N. Protein processing and inflammatory signaling in cystic fibrosis: challenges and therapeutic strategies. Curr. Mol. Med. 2010, 10:82-94.
86. Valle C.W., Vij N. Can correcting the δF508-CFTR proteostasis-defect rescue CF lung disease?. Curr. Mol. Med. 2012, 12:860-871.