Polyductin undergoes notch-like processing and regulated release from primary cilia

Human Molecular Genetics

Volumn 16, Issue 8, 2007, Pages 942-956

  Kaimori, Jun ya ^a   Nagasawa, Yasuyuki ^b   Menezes, Luis F ^a   Garcia Gonzalez, Miguel A ^a   Deng, Jie ^a   Imai, Enyu ^b   Onuchic, Luiz F ^c   Guay Woodford, Lisa M ^d   Germino, Gregory G ^a,e  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e Division of Nephrology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ALPHA SECRETASE; DISULFIDE; FIBROCYSTIN; GENE PRODUCT; SERINE PROTEINASE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVATION; EUKARYOTIC FLAGELLUM; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY CELL; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SECRETION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CILIA; DISULFIDES; DOGS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RECEPTORS, NOTCH; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 34447308769     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm039     Document Type: Article

References (38)

1. Zerres, K., Mucher, G., Becker, J., Steinkamm, C., Rudnik-Schoneborn, S., Heikkila, P., Rapola, J., Salonen, R., Germino, G.G., Onuchic, L. et al. (1998) Prenatal diagnosis of autosomal recessive polycystic kidney disease (ARPKD): Molecular genetics, clinical experience, and fetal morphology. Am. J. Med. Genet., 76, 137-144.
2. Guay-Woodford, L.M. and Desmond, R.A. (2003) Autosomal recessive polycystic kidney disease: The clinical experience in North America. Pediatrics, 111, 1072-1080.
3. Fonck, C., Chauveau, D., Gagnadoux, M.F., Pirson, Y. and Grunfeld, J.P. (2001) Autosomal recessive polycystic kidney disease in adulthood. Nephrol. Dial. Transplant, 16, 1648-1652.
4. Guay-Woodford, L. (1996) Autosomal recessive disease:cLinical and genetic profiles. Watson, M.L. and Torres, V.E. (Eds), Polycystic Kidney Disease, Oxford University Press, Oxford, UK.
5. Zerres, K., Mucher, G., Bachner, L., Deschennes, G., Eggermann, T., Kaariainen, H., Knapp, M., Lennert, T., Misselwitz, J., von Muhlendahl, K.E. et al. (1994) Mapping of the gene for autosomal recessive polycystic kidney disease (ARPKD) to chromosome 6p21-cen. Nat. Genet. 7, 429-432.
6. Onuchic, L.F., Furu, L., Nagasawa, Y., Hou, X., Eggermann, T., Ren, Z., Bergmann, C., Senderek, J., Esquivel, E., Zeltner, R. et al. (2002) 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., 70, 1305-1317.
7. Ward, C.J., Hogan, M.C., Rossetti, S., Walker, D., Sneddon, T., Wang, X., Kubly, V., Cunningham, J.M., Bacallao, R., Ishibashi, M. et al. (2002) The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein. Nat. Genet., 30 259-269.
8. Xiong, H., Chen, Y., Yi, Y., Tsuchiya, K., Moeckel, G., Cheung, J., Liang, D., Tham, K., Xu, X., Chen, X.Z. et al. (2002) A novel gene encoding a TIG multiple domain protein is a positional candidate for autosomal recessive polycystic kidney disease. Genomics, 80, 96-104.
9. Nagasawa, Y., Matthiesen, S., Onuchic. L.F., Hou, X., Bergmann, C., Esquivel, E., Senderek, J., Ren, Z., Zeltner, R., Furu, L. et al. (2002) Identification and characterization of Pkhd1, the mouse orthologue of the human ARPKD gene. J. Am. Soc. Nephrol., 13 2246-2258.
10. Bergmann, C., Senderek, J., Windelen, E., Kupper, F., Middeldorf, I., Schneider, F., Dornia, C., Rudnik-Schoneborn, S., Konrad, M, Schmitt, C.P. et al. (2005) Clinical consequences of PKHD1 mutations in 164 patients with autosomal-recessive polycystic kidney disease (ARPKD). Kidney Int., 67, 829-848.
11. Sharp, A.M., Messiaen, L.M., Page, G. Antignac, C., Gubler, M.C., Onuchic, L.F., Somlo, S., Germino, G.G. and Guay-Woodford, L.M. (2005) Comprehensive genomic analysis of PKHD1 mutations in ARPKD cohorts. J. Med. Genet., 42, 336-349.
12. Furu, L., Onuchic, L.F., Gharavi, A., Hou, X., Esquivel, E.L., Nagasawa, Y., Bergmann, C., Senderek, J., Avner, E., Zerres, K. et al. (2003) Milder presentation of recessive polycystic kidney disease requires presence of amino acid substitution mutations. J. Am. Soc. Nephrol., 14, 2004-2014.
13. Ward, C.J., Yuan, D., Masyuk, T.V., Wang, X., Punyashthiti, R., Whelan, S., Bacallao, R., Torra, R., LaRusso, N.F., Torres, V.E. et al. (2003) Cellular and subcellular localization of the ARPKD protein; fibrocystin is expressed on primary cilia. Hum. Mol. Genet., 12 2703-2710.
14. Li, J.B., Gerdes, J.M., Haycraft, C.J., Fan, Y., Teslovich, T.M., May-Simera, H., Li, H., Blacque, O.E., Li, L., Leitch, C.C. et al. (2004) Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell, 117 541-552.
15. 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.
16. Menezes, L.F., Cai, Y., Nagasawa, Y., Silva, A.M., Watkins, M.L., Da Silva, A.M., Somlo, S., Guay-Woodford, L.M., Germino, G.G. and Onuchic, L.F. (2004) Polyductin, the PKHD1 gene product, comprises isoforms expressed in plasma membrane, primary cilium, and cytoplasm. Kidney Int., 66, 1345-1355.
17. Wang, S., Luo, Y., Wilson, P.D., Witman, G.B. and Zhou, J. (2004) The autosomal recessive polycystic kidney disease protein is localized to primary cilia, with concentration in the basal body area. J. Am. Soc. Nephrol., 15, 592-602.
18. 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.
19. Mai, W., Chen, D., Ding, T., Kim, I., Park, S., Cho, S.Y., Chu, J.S., Liang, D., Wang, N., Wu, D. et al. (2005) Inhibition of Pkhd1 impairs tubulomorphogenesis of cultured IMCD cells. Mol. Biol. Cell 16, 4398-4409.
20. Duckert, P., Brunak, S. and Blom, N. (2004) Prediction of proprotein convertase cleavage sites. Protein Eng. Des. Sel., 17, 107-112.
21. Nakayama, K. (1997) Furin: A mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J., 327 (Pt 3), 625-635.
22. Henrich, S., Cameron, A., Bourenkov, G.P., Kiefersauer, R., Huber, R., Lindberg, L, Bode, W. and Than, M.E. (2003) The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol., 10, 520-526.
23. Bergmann, C., Senderek, J., Kupper, F., Schneider, F., Dornia, C., Windelen, E., Eggermann, T., Rudnik-Schoneborn, S., Kirfel, J., Furu, L. et al. (2004) PKHD1 mutations in autosomal recessive polycystic kidney disease (ARPKD). Hum. Mutat., 23, 453-463.
24. Huovila, A,P., Turner, A.J., Pelto-Huikko, M., Karkkainen, I. and Ortiz, R.M. (2005) Shedding light on ADAM metalloproteinases. Trends Biochem. Sci., 30, 413-422.
25. Wilhelmsen, K. and van der Geer, P. (2004) Phorbol 12-myristate 13-acetate-induced release of the colony-stimulating factor 1 receptor cytoplasmic domain into the cytosol involves two separate cleavage events. Mol. Cell. Biol., 24, 454-464.
26. Fan, S., Hurd, T.W., Liu, C.J., Straight, S.W., Weimbs, T., Hurd, E.A., Domino, S.E. and Margolis, B. (2004) Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol., 14 1451-1461.
27. Geng, L., Okuhara, D., Yu, Z., Tian, X., Cai, Y., Shibazaki, S. and Somlo, S. (2006) Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J. Cell Sci., 119, 1383-1395.
28. Ross, A.J., May-Simera, H., Eichers, E.R., Kai, M., Hill, J., Jagger, D.J., Leitch, C.C., Chapple, J.P., Munro, P.M., Fisher, S. et al. (2005) Disruption of BardetBiedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet., 37, 1135-1140.
29. De Strooper, B., Annaert, W., Cupers, P., Saftig, P., Craessaerts, K., Mumm, J.S., Schroeter, E.H., Schrijvers, V., Wolfe, M.S., Ray, W.J. et al. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature, 398, 518-522.
30. Schroeter, E.H., Kisslinger, J.A. and Kopan, R. (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature, 393, 382-386.
31. Rauchman, M.I., Nigam, S.Y., Delpire, E. and Gullans, S.R. (1993) An osmotically tolerant inner medullary collecting duct cell line from an SV40 transgenic mouse. Am. J. Physiol., 265, F416-F424.
32. Hiesberger, T., Gourley, E., Erickson, A., Koulen, P., Ward, C.J., Masyuk, T.V., Larusso, N.F., Harris, P.C. and Igarashi, P. (2006) Proteolytic cleavage and nuclear translocation of fibrocystin is regulated by intracellular Ca2+ and activation of protein kinase C. J. Biol. Chem., 281, 34357-34364.
33. Harper, J.A., Yuan, J.S., Tan, J.B., Visan, I. and Guidos, C.J. (2003) Notch signaling in development and disease. Clin. Genet., 64 461-472.
34. Schweisguth, F. (2004) Notch signaling activity. Curr. Biol., 14, R129-R138.
35. Iwamoto, R. and Mekada, E. (2000) Heparin-binding EGF-like growth factor: A juxtacrine growth factor. Cytokine Growth Factor Rev., 11, 335-344.
36. 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.
37. Akhter, S., Cavet, M.E., Tse, C.M. and Donowitz, M. (2000) C-terminal domains of Na(+)/H(+) exchanger isoform 3 are involved in the basal and serum-stimulated membrane trafficking of the exchanger. Biochemistry 39, 1990-2000.
38. Weimbrs, T., Low, S.H., Li, X. and Kreitzer, G. (2003) SNAREs and epithelial cells. Methods, 30, 191-197.