Characterization of PKD protein-positive exosome-like vesicles

Journal of the American Society of Nephrology

Volumn 20, Issue 2, 2009, Pages 278-288

  Hogan, Marie C ^a   Manganelli, Luca ^a,e   Woollard, John R ^a   Masyuk, Anatoliy I ^b   Masyuk, Tatyana V ^b   Tammachote, Rachaneekorn ^a   Huang, Bing Q ^b   Leontovich, Alexey A ^c   Beito, Thomas G ^d   Madden, Benjamin J ^d   Charlesworth, M Cristine ^d   Torres, Vicente E ^a   Larusso, Nicholas F ^b   Harris, Peter C ^a   Ward, Christopher J ^a,d  

^a Division of Nephrology and Hypertension   (United States)

^b Center for Basic Research in Digestive Diseases   (United States)

^c Bioinformatics Core Facility   (United States)

^d MAYO CLINIC   (United States)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; AQUAPORIN 2; CYSTINE; FIBROCYSTIN; PODOCIN; POLYCYSTIN 1; POLYCYSTIN 2; SERINE PROTEINASE; SMOOTHENED PROTEIN; TAMM HORSFALL GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BARDET BIEDL SYNDROME; CELL VACUOLE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; EXOSOME; HUMAN; HUMAN CELL; KIDNEY EPITHELIUM; KIDNEY POLYCYSTIC DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEOMICS; RAT; SIGNAL TRANSDUCTION;

EID: 59949104184     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2008060564     Document Type: Article

References (46)

1. Torres V, Holley K, Offord K. Epidemiology. In: Problems in Diagnosis and Management of Polycystic Kidney Disease, edited by Grantham JJ, Kansas City: PKR Foundation Kansas City, 1985, pp 349-369
2. Wilson PD: Polycystic kidney disease. N Engl J Med 350: 151-164,2004
3. The polycystic kidney disease 1 gene encodes a 14 kb transcript and lies within a duplicated region on chromosome 16. The European Polycystic Kidney Disease Consortium. Cell 77: 881-894, 1994
4. Polycystic kidney disease: The complete structure of the PKD1 gene and its protein. The International Polycystic Kidney Disease Consortium. Cell 81: 289-298, 1995
5. Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, Millan JL, Gamble V, Harris PC: The polycystic kidney disease 1(PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151-160, 1995
6. Mochizuki T, Wu G, Hayashi T, Xenophontos SL, Veldhuisen B, Saris JJ, Reynolds DM, Cai Y, Gabow PA, Pierides A, Kimberling WJ, Breuning MH, Deltas CC, Peters DJ, Somlo S: PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272: 1339-1342, 1996
7. Ward CJ, Hogan MC, Rossetti S, Walker D, Sneddon T, Wang X, Kubly V, Cunningham JM, Bacallao R, Ishibashi M, Milliner DS, Torres VE, Harris PC: The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein. Nat Genet 30: 259 -269, 2002
8. Onuchic LF, Furu L, Nagasawa Y, Hou X, Eggermann T, Ren Z, Bergmann C, Senderek J, Esquivel E, Zeltner R, Rudnik-Schoneborn S, Mrug M, Sweeney W, Avner ED, Zerres K, Guay-Woodford LM, Somlo S, Germino GG: 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, 2002
9. Ward CJ, Yuan D, Masyuk TV, Wang X, Punyashthiti R, Whelan S, Bacallao R, Torra R, LaRusso NF, Torres VE, Harris PC: Cellular and subcellular localization of the ARPKD protein; fibrocystin is expressed on primary cilia. Hum Mol Genet 12: 2703-2710, 2003
10. Yoder BK, Hou X, Guay-Woodford LM: The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 13: 2508-2516, 2002
11. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J: Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33: 129-137, 2003
12. Wang S, Zhang J, Nauli SM, Li X, Starremans PG, Luo Y, Roberts KA, Zhou J: Fibrocystin/polyductin, found in the same protein complex with polycystin-2, regulates calcium responses in kidney epithelia. Mol Cell Biol 27: 3241-3252, 2007
13. Wu Y, Dai X-Q, Li Q, Chen CX, Mai W, Hussain Z, Long W, Montalbetti N, Li G, Glynne R, Wang S, Cantiello HF, Wu G, Chen X-Z: Kinesin-2 mediates physical and functional interactions between polycystin-2 and fibrocystin. Hum Mol Genet 15: 3280-3292, 2006
14. Pisitkun T, Shen R-F, Knepper MA: Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 101: 13368-13373, 2004
15. Zhou H, Yuen PST, Pisitkun T, Gonzales PA, Yasuda H, DearJW, Gross P, Knepper MA, Star RA: Collection, storage, preservation, and normalization of human urinary exosomes for biomarker discovery. Kidney Int 69: 1471-1476, 2006
16. Tanaka Y, Okada Y, Hirokawa N: FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435: 172-177, 2005
17. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J, Blum M, Dworniczak B: The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12: 938 -943, 2002
18. McGrath J, Somlo S, Makova S, Tian X, Brueckner M: Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61-73, 2003
19. Woollard JR, Punyashtiti R, Richardson S, Masyuk TV, Whelan S, Huang BQ, Lager DJ, vanDeursen J, Torres VE, Gattone VH, LaRusso NF, Harris PC, Ward CJ: A mouse model of autosomal recessive polycystic kidney disease with biliary duct and proximal tubule dilatation. Kidney Int 72: 328-336, 2007
20. Ong AC, Harris PC, Davies DR, Pritchard L, Rossetti S, Biddolph S, Vaux DJ, Migone N, Ward CJ: Polycystin-1 expression in PKD1, early-onset PKD1, and TSC2/PKD1 cystic tissue. Kidney Int 56: 1324-1333, 1999
21. Cai Y, Maeda Y, Cedzich A, Torres VE, Wu G, Hayashi T, Mochizuki T, Park JH, Witzgall R, Somlo S: Identification and characterization of polycystin-2, the PKD2 gene product. J Biol Chem 274: 28557-28565, 1999
22. Lehtonen S, Ora A, Olkkonen VM, Geng L, Zerial M, Somlo S, Lehtonen E: In vivo interaction of the adapter protein CD2-associated protein with the type 2 polycystic kidney disease protein, polycystin-2. J Biol Chem 275: 32888 -32893, 2000
23. Li Q, Montalbetti N, Shen PY, Dai X-Q, Cheeseman CI, Karpinski E, Wu G, Cantiello HF, Chen X-Z: Alpha-actinin associates with polycystin-2 and regulates its channel activity. Hum Mol Genet 14: 1587-1603, 2005
24. Zatti A, Chauvet V, Rajendran V, Kimura T, Pagel P, Caplan MJ: The C-terminal tail of the polycystin-1 protein interacts with the Na,K-ATPase alpha-subunit. Mol Biol Cell 16: 5087-5093, 2005
25. Parnell SC, Magenheimer BS, Maser RL, Rankin CA, Smine A, Oka moto T, Calvet JP: The polycystic kidney disease-1 protein, polycystin-1, binds and activates heterotrimeric G-proteins in vitro. Biochem Biophys Res Commun 251: 625-631, 1998
26. Parnell SC, Magenheimer BS, Maser RL, Zien CA, Frischauf A-M, Calvet JP: Polycystin-1 activation of c-Jun N-terminal kinase and AP-1 is mediated by heterotrimeric G proteins. J Biol Chem 277: 19566 -19572, 2002
27. Kaimori J-Y, Nagasawa Y, Menezes LF, Garcia-Gonzalez MA, Deng J, Imai E, Onuchic LF, Guay-Woodford LM, Germino GG: Polyductin undergoes notch-like processing and regulated release from primary cilia. Hum Mol Genet 16: 942-956, 2007
28. Ponting CP, Hofmann K, Bork P: A latrophilin/CL-1-like GPS domain in polycystin-1. Curr Biol 9: R585-R588, 1999
29. Qian F, Boletta A, Bhunia AK, Xu H, Liu L, Ahrabi AK, Watnick TJ, Zhou F, Germino GG: 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, 2002
30. Hou X, Mrug M, Yoder BK, Lefkowitz EJ, Kremmidiotis G, D'Eustachio P, Beier DR, Guay-Woodford LM: Cystin, a novel cilia-associated protein, is disrupted in the cpk mouse model ofpolycystic kidney disease. J Clin Invest 109: 533-540, 2002
31. Chiang AP, Nishimura D, Searby C, Elbedour K, Carmi R, Ferguson AL, Secrist J, Braun T, Casavant T, Stone EM, Sheffield VC: Comparative genomic analysis identifies an ADP-ribosylation factor-like gene as the cause of Bardet-Biedl syndrome(BBS3). Am J Hum Genet 75: 475-484, 2004
32. Fan Y, Esmail MA, Ansley SJ, Blacque OE, Boroevich K, Ross AJ, Moore SJ, Badano JL, May-Simera H, Compton DS, Green JS, Lewis RA, van Haelst MM, Parfrey PS, Baillie DL, Beales PL, Katsanis N, Davidson WS, Leroux MR: Mutations in a member of the Ras super-family of small GTP-binding proteins causes Bardet-Biedl syndrome. Nat Genet 36: 989-993, 2004
33. Adachi J, Kumar C, Zhang Y, Olsen JV, Mann M: The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins. Genome Biol 7: R80, 2006
34. Sohara E, Luo Y, Zhang J, Manning DK, Beier DR, Zhou J: Nek8 regulates the expression and localization of polycystin-1 and polycystin-2. J Am Soc Nephrol 19: 469 -476, 2008
35. Follit JA, Tuft RA, Fogarty KE, Pazour GJ: The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 17: 3781-3792, 2006
36. Marzesco A-M, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB: Release of extracellular membrane particles carrying the stem cell marker prominin-1(CD133) from neural progenitors and other epithelial cells. J Cell Sci 118: 2849-2858, 2005
37. Fonseca AV, Bauer N, Corbeil D: The stem cell marker CD133 meets the endosomal compartment: New insights into te cell division of hematopoietic stem cells. Blood Cells Mol Dis 41: 194-195, 2008
38. Jing H, Takagi J, Liu J-h, Lindgren S, Zhang R-g, Joachimiak A, Wang J-h, Springer TA: Archaeal surface layer proteins contain beta propeller PKD, and beta helix domains and are related to metazoan cell surface proteins. Structure 10: 1453-1464, 2002
39. Rigden DJ, Mello LV, Galperin MY: The PA14 domain, a conserved all-beta domain in bacterial toxins, enzymes, adhesins and signaling molecules. Trends Biochem Sci 29: 335-339, 2004
40. de Groot PW, Klis FM: The conserved PA14 domain of cell wall associated fungal adhesins governs their glycan-binding specificity. Mol Microbiol 68: 535-537, 2008
41. Praetorius HA, Frokiaer J, Nielsen S, Spring KR: Bending the primary cilium opens Ca2+-sensitive intermediate-conductance K+ channels in MDCK cells. J Membr Biol 191: 193-200, 2003
42. Wang X, li VG, Harris PC, Torres VE: Effectiveness of vasopressin V2 receptor antagonists OPC-31260 and OPC-41061 on polycystic kidney disease development in the PCK rat. J Am Soc Nephrol 16: 846-851, 2005
43. Masyuk TV, Masyuk Al, Torres VE, Harris PC, Larusso NF: Octreotide inhibits hepatic cystogenesis in a rodent model of polycystic liver disease by reducing cholangiocyte adenosine 3′,5′-cyclic monophosphate. Gastroenterology 132: 1104-1116, 2007
44. Rohatgi R, Milenkovic L, Scott MP: Patched1 regulates hedgehog signaling at the primary cilium. Science 317: 372-376, 2007
45. Krishna MM, Hoang L, Lin Y, Englander SW: Hydrogen exchange methods to study protein folding. Methods 34: 51-64, 2004
46. Roberts SK, Kuntz SM, Gores GJ, LaRusso NF: Regulation of bicarbonate-dependent ductular bile secretion assessed by lumenal micropuncture of isolated rodent intrahepatic bile ducts. Proc Natl Acad Sci USA 90: 9080-9084, 1993