Novel functional complexity of polycystin-1 by GPS cleavage in vivo: Role in polycystic kidney disease

Molecular and Cellular Biology

Volumn 34, Issue 17, 2014, Pages 3341-3353

  Kurbegovic, Almira ^a   Kim, Hyunho ^b   Xu, Hangxue ^b   Yu, Shengqiang ^b,e   Cruanès, Julie ^a   Maser, Robin L ^c   Boletta, Alessandra ^d   Trudel, Marie ^a   Qian, Feng ^b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PEPTIDE FRAGMENT; POLYCYSTIN 1; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CELL MEMBRANE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; COVALENT BOND; EMBRYO; ENDOPLASMIC RETICULUM; GENETIC COMPLEMENTATION; IN VIVO STUDY; KIDNEY POLYCYSTIC DISEASE; KIDNEY TUBULE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; REGULATORY MECHANISM; SECRETORY PATHWAY; ACTIVE TRANSPORT; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; C57BL MOUSE; CHEMISTRY; GENETICS; GOLGI COMPLEX; HUMAN; KNOCKOUT MOUSE; METABOLISM; MUTATION; TRANSGENIC MOUSE;

ANIMALS; BINDING SITES; BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE; GENETIC COMPLEMENTATION TEST; GOLGI APPARATUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTATION; PEPTIDE FRAGMENTS; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; RECEPTORS, G-PROTEIN-COUPLED; TRPP CATION CHANNELS;

EID: 84915779680     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00687-14     Document Type: Article

References (65)

1. Gabow PA. 1993. Autosomal dominant polycystic kidney disease. N. Engl. J. Med. 329:332-342. http://dx.doi.org/10.1056/NEJM199307293290508.
2. Ahrabi AK, Jouret F, Marbaix E, Delporte C, Horie S, Mulroy S, Boulter C, Sandford R, Devuyst O. 2010. Glomerular and proximal tubule cysts as early manifestations of Pkd1 deletion. Nephrol. Dial. Transplant. 25:1067-1078. http://dx.doi.org/10.1093/ndt/gfp611.
3. Lu W, Shen X, Pavlova A, Lakkis M, Ward CJ, Pritchard L, Harris PC, Genest DR, Perez-Atayde AR, 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. http://dx.doi.org/10.1093/hmg/10.21.2385.
4. Piontek KB, Huso DL, Grinberg A, Liu L, Bedja D, Zhao H, Gabrielson K, Qian F, Mei C, Westphal H, Germino GG. 2004. A functional floxed allele of Pkd1 that can be conditionally inactivated in vivo. J. Am. Soc. Nephrol. 15:3035-3043. http://dx.doi.org/10.1097/01.ASN.0000144204.01352.86.
5. Piontek K, Menezes LF, Garcia-Gonzalez MA, Huso DL, Germino GG. 2007 A critical developmental switch defines the kinetics of kidney cyst formation after loss of Pkd1. Nat. Med. 13:1490-1495. http://dx.doi.org/10.1038/nm1675.
6. Kim K, Drummond I, Ibraghimov-Beskrovnaya O, Klinger K, Arnaout MA. 2000. Polycystin 1 is required for the structural integrity of blood vessels. Proc. Natl. Acad. Sci. U. S. A. 97:1731-1736. http://dx.doi.org/10.1073/pnas.040550097.
7. Chauvet V, Qian F, Boute N, Cai Y, Phakdeekitacharoen B, Onuchic LF, Attie-Bitach T, Guicharnaud L, Devuyst O, Germino GG, Gubler MC. 2002. Expression of PKD1 and PKD2 transcripts and proteins in human embryo and during normal kidney development. Am. J. Pathol. 160:973-983. http://dx.doi.org/10.1016/S0002-9440(10)64919-X.
8. Foggensteiner L, Bevan AP, Thomas R, Coleman N, Boulter C, Bradley J, Ibraghimov-Beskrovnaya O, Klinger K, Sandford R. 2000. Cellular and subcellular distribution of polycystin-2, the protein product of the PKD2 gene. J. Am. Soc. Nephrol. 11:814-827.
9. Guillaume R, D'Agati V, Daoust M, 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. http://dx.doi.org/10.1002/(SICI)1097-0177(199904)214:4<337::AID-AJA6>3.0.CO;2-O.
10. Guillaume R, Trudel M. 2000. Distinct and common developmental expression patterns of the murine Pkd2 and Pkd1 genes. Mech. Dev. 93: 179-183. http://dx.doi.org/10.1016/S0925-4773(00)00257-4.
11. Van Adelsberg J, Chamberlain S, D'Agati V. 1997. Polycystin expression is temporally and spatially regulated during renal development. Am. J. Physiol. 272:F602-F609.
12. Geng L, Segal Y, Peissel B, Deng N, Pei Y, Carone F, Rennke HG, Glucksmann-Kuis AM, Schneider MC, Ericsson M, Reeders ST, Zhou J. 1996 Identification and localization of polycystin, the PKD1 gene product. J. Clin. Invest. 98:2674-2682. http://dx.doi.org/10.1172/JCI119090.
13. Palsson R, Sharma CP, Kim K, McLaughlin M, Brown D, Arnaout MA. 1996 Characterization and cell distribution of polycystin, the product of autosomal dominant polycystic kidney disease gene 1. Mol. Med. 2:702-711.
14. Geng L, Segal Y, Pavlova A, Barros EJ, Lohning C, Lu W, Nigam SK, Frischauf AM, Reeders ST, Zhou J. 1997. Distribution and developmen-tally regulated expression of murine polycystin. Am. J. Physiol. 272:F451-F459.
15. Kleymenova E, Ibraghimov-Beskrovnaya O, Kugoh H, Everitt J, Xu H, Kiguchi K, Landes G, Harris P, Walker C. 2001. Tuberin-dependent membrane localization of polycystin-1: a functional link between polycystic kidney disease and the TSC2 tumor suppressor gene. Mol. Cell 7:823-832 http://dx.doi.org/10.1016/S1097-2765(01)00226-X.
16. Boletta A, Qian F, Onuchic LF, Bragonzi A, Cortese M, Deen PM, Courtoy PJ, Soria MR, Devuyst O, Monaco L, Germino GG. 2001. Biochemical characterization of bona fide polycystin-1 in vitro and in vivo. Am. J. Kidney Dis. 38:1421-1429. http://dx.doi.org/10.1053/ajkd.2001.29282.
17. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J. 2003. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33:129-137. http://dx.doi.org/10.1038/ng1076.
18. Yoder BK, Hou X, Guay-Woodford LM. 2002. The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are colocalized in renal cilia. J. Am. Soc. Nephrol. 13:2508-2516. http://dx.doi.org/10.1097/01.ASN.0000029587.47950.25.
19. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millan JL, Gamble V, Harris PC. 1995. The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat. Genet. 10:151-160. http://dx.doi.org/10.1038/ng0695-151.
20. Ponting CP, Hofmann K, Bork P. 1999. A latrophilin/CL-1-like GPS domain in polycystin-1. Curr. Biol. 9:R585-R588. http://dx.doi.org/10.1016/S0960-9822(99)80379-0.
21. Wei W, Hackmann K, Xu H, Germino G, 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. http://dx.doi.org/10.1074/jbc.M703218200.
22. Qian F, Boletta A, Bhunia AK, Xu H, Liu L, Ahrabi AK, Watnick TJ, Zhou F, Germino GG. 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. U. S. A. 99:16981-16986. http://dx.doi.org/10.1073/pnas.252484899.
23. Arac D, Boucard AA, Bolliger MF, Nguyen J, Soltis SM, Sudhof TC, Brunger AT. 2012. A novel evolutionarily conserved domain of celladhesion GPCRs mediates autoproteolysis. EMBO J. 31:1364-1378. http://dx.doi.org/10.1038/emboj.2012.26.
24. Garcia-Gonzalez MA, Jones JG, Allen SK, Palatucci CM, Batish SD, Seltzer WK, Lan Z, Allen E, Qian F, Lens XM, Pei Y, Germino GG, Watnick TJ. 2007. Evaluating the clinical utility of a molecular genetic test for polycystic kidney disease. Mol. Genet. Metab. 92:160-167. http://dx.doi.org/10.1016/j.ymgme.2007.05.004.
25. Qian F. 2012. Polycystin-1, p 3728-3736. In Rawlings ND, Salvesen G (ed), The handbook of proteolytic enzymes, 3rd ed. Academic Press, San Diego, CA.
26. Yu S, Hackmann K, Gao J, He X, Piontek K, Garcia-Gonzalez MA, Menezes LF, Xu H, Germino GG, Zuo J, Qian F. 2007. Essential role of cleavage of polycystin-1 at G protein-coupled receptor proteolytic site for kidney tubular structure. Proc. Natl. Acad. Sci. U. S. A. 104:18688-18693. http://dx.doi.org/10.1073/pnas.0708217104.
27. Fredriksson R, Lagerstrom MC, Hoglund PJ, Schioth HB. 2002. Novel human G protein-coupled receptors with long N-terminals containing GPS domains and Ser/Thr-rich regions. FEBS Lett. 531:407-414. http://dx.doi.org/10.1016/S0014-5793(02)03574-3.
28. Lin HH, Stacey M, Yona S, Chang GW. 2010. GPS proteolytic cleavage of adhesion-GPCRs. Adv. Exp. Med. Biol. 706:49-58. http://dx.doi.org/10.1007/978-1-4419-7913-1_4.
29. Sugita S, Ichtchenko K, Khvotchev M, Sudhof TC. 1998.-Latrotoxin receptor CIRL/latrophilin 1 (CL1) defines an unusual family of ubiquitous G-protein-linked receptors. G-protein coupling not required for triggering exocytosis. J. Biol. Chem. 273:32715-32724.
30. Abe J, Fukuzawa T, Hirose S. 2002. Cleavage of Ig-Hepta at a "SEA" module and at a conservedGprotein-coupled receptor proteolytic site. J. Biol. Chem. 277:23391-23398. http://dx.doi.org/10.1074/jbc.M110877200.
31. Gray JX, Haino M, Roth MJ, Maguire JE, Jensen PN, Yarme A, Stetler-Stevenson MA, Siebenlist U, Kelly K. 1996. CD97 is a processed, seventransmembrane, heterodimeric receptor associated with inflammation. J. Immunol. 157:5438-5447.
32. Krasnoperov VG, Bittner MA, Beavis R, Kuang Y, Salnikow KV, Chepurny OG, Little AR, Plotnikov AN, Wu D, Holz RW, Petrenko AG. 1997 alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18:925-937. http://dx.doi.org/10.1016/S0896-6273(00)80332-3.
33. Lin HH, Chang GW, Davies JQ, Stacey M, Harris J, Gordon S. 2004. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J. Biol. Chem. 279:31823-31832 http://dx.doi.org/10.1074/jbc.M402974200.
34. Hsiao CC, Chen HY, Chang GW, Lin HH. 2011. GPS autoproteolysis is required for CD97 to up-regulate the expression of N-cadherin that promotes homotypic cell-cell aggregation. FEBS Lett. 585:313-318. http://dx.doi.org/10.1016/j.febslet.2010.12.005.
35. Paavola KJ, Stephenson JR, Ritter SL, Alter SP, Hall RA. 2011. The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J. Biol. Chem. 286:28914-28921. http://dx.doi.org/10.1074/jbc.M111.247973.
36. Promel S, Frickenhaus M, Hughes S, Mestek L, Staunton D, Woollard A, Vakonakis I, Schoneberg T, Schnabel R, Russ AP, Langenhan T. 2012 The GPS motif is a molecular switch for bimodal activities of adhesion class G protein-coupled receptors. Cell Rep. 2:321-331. http://dx.doi.org/10.1016/j.celrep.2012.06.015.
37. Ward Y, Lake R, Yin JJ, Heger CD, Raffeld M, Goldsmith PK, Merino M, Kelly K. 2011. LPA receptor heterodimerizes with CD97 to amplify LPAinitiated RHO-dependent signaling and invasion in prostate cancer cells. Cancer Res. 71:7301-7311. http://dx.doi.org/10.1158/0008-5472.CAN-11-2381.
38. Paavola KJ, Hall RA. 2012. Adhesion G protein-coupled receptors: signaling, pharmacology, and mechanisms of activation. Mol. Pharmacol. 82:777-783. http://dx.doi.org/10.1124/mol.112.080309.
39. Promel S, Langenhan T, Arac D. 2013. Matching structure with function: the GAIN domain of Adhesion-GPCR and PKD1-like proteins. Trends Pharmacol. Sci. 34:470-478. http://dx.doi.org/10.1016/j.tips.2013.06.002.
40. Kaur B, Brat DJ, Devi NS, Van Meir EG. 2005. Vasculostatin, a proteolytic fragment of brain angiogenesis inhibitor 1, is an antiangiogenic and antitumorigenic factor. Oncogene 24:3632-3642. http://dx.doi.org/10.1038/sj.onc.1208317.
41. Kaur B, Cork SM, Sandberg EM, Devi NS, Zhang Z, Klenotic PA, Febbraio M, Shim H, Mao H, Tucker-Burden C, Silverstein RL, Brat DJ, Olson JJ, Van Meir EG. 2009. Vasculostatin inhibits intracranial glioma growth and negatively regulates in vivo angiogenesis through a CD36-dependent mechanism. Cancer Res. 69:1212-1220. http://dx.doi.org/10.1158/0008-5472.CAN-08-1166.
42. Herron BJ, Lu W, Rao C, Liu S, Peters H, Bronson RT, Justice MJ, McDonald JD, Beier DR. 2002. Efficient generation and mapping of recessive developmental mutations using ENU mutagenesis. Nat. Genet. 30:185-189. http://dx.doi.org/10.1038/ng812.
43. Kurbegovic A, Cote O, Couillard M, Ward CJ, Harris PC, Trudel M. 2010 Pkd1 transgenic mice: adult model of polycystic kidney disease with extrarenal and renal phenotypes. Hum. Mol. Genet. 19:1174-1189. http://dx.doi.org/10.1093/hmg/ddp588.
44. Kurbegovic A, Trudel M. 2013. Progressive development of polycystic kidney disease in the mouse model expressing Pkd1 extracellular domain. Hum. Mol. Genet. 22:2361-2375. http://dx.doi.org/10.1093/hmg/ddt081.
45. Wodarczyk C, Rowe I, Chiaravalli M, Pema M, Qian F, Boletta A. 2009. A novel mouse model reveals that polycystin-1 deficiency in ependyma and choroid plexus results in dysfunctional cilia and hydrocephalus. PLoS One 4:e7137. http://dx.doi.org/10.1371/journal.pone.0007137.
46. Thivierge C, Kurbegovic A, Couillard M, Guillaume R, Cote O, Trudel M. 2006. Overexpression of PKD1 causes polycystic kidney disease. Mol. Cell. Biol. 26:1538-1548. http://dx.doi.org/10.1128/MCB.26.4.1538-1548.2006.
47. Couillard M, Trudel M. 2009. C-myc as a modulator of renal stem/progenitor cell population. Dev. Dyn. 238:405-414. http://dx.doi.org/10.1002/dvdy.21841.
48. Ong AC, Harris PC, Davies DR, Pritchard L, Rossetti S, Biddolph S, Vaux DJ, Migone N, Ward CJ. 1999. Polycystin-1 expression in PKD1, early-onset PKD1, and TSC2/PKD1 cystic tissue. Kidney Int. 56:1324-1333 http://dx.doi.org/10.1046/j.1523-1755.1999.00659.x.
49. Freeze HH. 2001. Use of glycosidases to study protein trafficking. Curr. Protoc. Cell Biol. Chapter 15:Unit 15.2. http://dx.doi.org/10.1002/0471143030.cb1502s03.
50. Kornfeld R, Kornfeld S. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664. http://dx.doi.org/10.1146/annurev.bi.54.070185.003215.
51. Stanley P. 2011. Golgi glycosylation. Cold Spring Harb. Perspect. Biol. 3:a005199. http://dx.doi.org/10.1101/cshperspect.a005199.
52. Chapin HC, Rajendran V, Caplan MJ. 2010. Polycystin-1 surface localization is stimulated by polycystin-2 and cleavage at theGprotein-coupled receptor proteolytic site. Mol. Biol. Cell 21:4338-4348. http://dx.doi.org/10.1091/mbc.E10-05-0407.
53. Krasnoperov V, Lu Y, Buryanovsky L, Neubert TA, Ichtchenko K, Petrenko AG. 2002. Post-translational proteolytic processing of the calcium-independent receptor of alpha-latrotoxin (CIRL), a natural chimera of the cell adhesion protein and the G protein-coupled receptor. Role of the G protein-coupled receptor proteolysis site (GPS) motif. J. Biol. Chem. 277:46518-46526. http://dx.doi.org/10.1074/jbc.M206415200.
54. - Co-transporter-dependent cystic dilation. J. Am. Soc. Nephrol. 17: 3424-3437. http://dx.doi.org/10.1681/ASN.2006030295.
55. Xu H, Shen J, Walker CL, Kleymenova E. 2001. Tissue-specific expression and splicing of the rat polycystic kidney disease 1 gene. DNA Seq. 12:361-366.
56. Butscheid Y, Chubanov V, Steger K, Meyer D, Dietrich A, Gudermann T. 2006. Polycystic kidney disease and receptor for egg jelly is a plasma membrane protein of mouse sperm head. Mol. Reprod. Dev. 73:350-360. http://dx.doi.org/10.1002/mrd.20410.
57. Jin Z, Tietjen I, Bu L, Liu-Yesucevitz L, Gaur SK, Walsh CA, Piao X. 2007 Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum. Mol. Genet. 16:1972-1985. http://dx.doi.org/10.1093/hmg/ddm144.
58. Kim H, Jeong W, Ahn K, Ahn C, Kang S. 2004. Siah-1 interacts with the intracellular region of polycystin-1 and affects its stability via the ubiquitin-proteasome pathway. J. Am. Soc. Nephrol. 15:2042-2049. http://dx.doi.org/10.1097/01.ASN.0000133490.00348.59.
59. Low SH, Vasanth S, Larson CH, Mukherjee S, Sharma N, Kinter MT, Kane ME, Obara T, Weimbs T. 2006. Polycystin-1, STAT6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Dev. Cell 10:57-69. http://dx.doi.org/10.1016/j.devcel.2005.12.005.
60. Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G. 1997. Homo-and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc. Natl. Acad. Sci. U. S. A. 94:6965-6970. http://dx.doi.org/10.1073/pnas.94.13.6965.
61. Chauvet V, Tian X, Husson H, Grimm DH, Wang T, Hiesberger T, Igarashi P, Bennett AM, Ibraghimov-Beskrovnaya O, Somlo S, Caplan MJ. 2004. Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J. Clin. Invest. 114:1433-1443. http://dx.doi.org/10.1172/JCI21753.
62. Woodward OM, Li Y, Yu S, Greenwell P, Wodarczyk C, Boletta A, Guggino WB, Qian F. 2010. Identification of a polycystin-1 cleavage product, P100, that regulates store operatedCaentry through interactions with STIM1. PLoS One 5:e12305. http://dx.doi.org/10.1371/journal.pone.0012305.
63. Porter JA, Young KE, Beachy PA. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255-259 http://dx.doi.org/10.1126/science.274.5285.255.
64. Volynski KE, Silva JP, Lelianova VG, Atiqur Rahman M, Hopkins C, Ushkaryov YA. 2004. Latrophilin fragments behave as independent proteins that associate and signal on binding of LTX(N4C). EMBO J. 23: 4423-4433. http://dx.doi.org/10.1038/sj.emboj.7600443.
65. Cornec-Le Gall E, Audrezet MP, Chen JM, Hourmant M, Morin MP, Perrichot R, Charasse C, Whebe B, Renaudineau E, Jousset P, Guillodo MP, Grall-Jezequel A, Saliou P, Ferec C, Le Meur Y. 2013. Type of PKD1 Mutation Influences Renal Outcome in ADPKD. J. Am. Soc. Nephrol. 24:1006-1013. http://dx.doi.org/10.1681/ASN.2012070650.