SNX31: A Novel sorting nexin associated with the uroplakin-degrading multivesicular bodies in terminally differentiated urothelial cells

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Vieira, Neide ^a   Deng, Fang Ming ^b   Liang, Feng Xia ^a   Liao, Yi ^a   Chang, Jennifer ^a   Zhou, Ge ^a   Zheng, Weiyue ^a   Simon, Jean Pierre ^a   Ding, Mingxiao ^c   Wu, Xue Ru ^a,b,d   Romih, Rok ^e   Kreibich, Gert ^a   Sun, Tung Tien ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PEKING UNIVERSITY   (China)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

UROPLAKIN; BIOLOGICAL MARKER; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; POLYPHOSPHOINOSITIDE; PROTEIN BINDING; SORTING NEXIN;

ARTICLE; ANIMAL; BIOLOGICAL MODEL; BOVINAE; C57BL MOUSE; CELL DIFFERENTIATION; CELL MEMBRANE; CYTOLOGY; DOG; ENDOCYTOSIS; ENDOSOME; ENZYMOLOGY; GENE INACTIVATION; MDCK CELL LINE; METABOLISM; MULTIVESICULAR BODY; ULTRACENTRIFUGATION; ULTRASTRUCTURE; UROTHELIUM;

ANIMALS; BIOLOGICAL MARKERS; CATTLE; CELL DIFFERENTIATION; CELL MEMBRANE; DOGS; ENDOCYTOSIS; ENDOSOMES; GENE KNOCKOUT TECHNIQUES; MADIN DARBY CANINE KIDNEY CELLS; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MULTIVESICULAR BODIES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; SORTING NEXINS; ULTRACENTRIFUGATION; UROPLAKINS; UROTHELIUM;

EID: 84902668546     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099644     Document Type: Article

References (75)

1. Negrete HO, Lavelle JP, Berg J, Lewis SA, Zeidel ML (1996) Permeability properties of the intact mammalian bladder epithelium. American Journal of Physiology-Renal Physiology 40: F886-F894.
2. Hicks RM (1975) The mammalian urinary bladder: an accommodating organ. Biol Rev Camb Philos Soc 50: 215-246.
3. Khandelwal P, Abraham SN, Apodaca G (2009) Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol 297: F1477-1501.
4. Lewis SA (2000) Everything you wanted to know about the bladder epithelium but were afraid to ask. Am J Physiol Renal Physiol 278: F867-874.
5. Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT (2009) Uroplakins in urothelial biology, function, and disease. Kidney Int 75: 1153-1165.
6. Wu XR, Lin JH, Walz T, Haner M, Yu J, et al. (1994) Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins. Journal of Biological Chemistry 269: 13716-13724.
7. Kachar B, Liang F, Lins U, Ding M, Wu XR, et al. (1999) Three-dimensional analysis of the 16 nm urothelial plaque particle: luminal surface exposure, preferential head-to-head interaction, and hinge formation. J Mol Biol 285: 595-608. (Pubitemid 29041795)
8. Desalle R, Chicote JU, Sun TT, Garcia-Espana A (2014) Generation of divergent uroplakin tetraspanins and their partners during vertebrate evolution: identification of novel uroplakins. BMC Evol Biol 14: 13.
9. Hu CC, Bachmann T, Zhou G, Liang FX, Ghiso J, et al. (2008) Assembly of a membrane receptor complex: roles of the uroplakin II prosequence in regulating uroplakin bacterial receptor oligomerization. Biochem J 414: 195-203.
10. Hu P, Deng FM, Liang FX, Hu CM, Auerbach AB, et al. (2000) Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J Cell Biol 151: 961-972.
11. Hu P, Meyers S, Liang FX, Deng FM, Kachar B, et al. (2002) Role of membrane proteins in permeability barrier function: uroplakin ablation elevates urothelial permeability. Am J Physiol Renal Physiol 283: F1200-1207. (Pubitemid 35332650)
12. Kong XT, Deng FM, Hu P, Liang FX, Zhou G, et al. (2004) Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J Cell Biol 167: 1195-1204. (Pubitemid 40066633)
13. Wu XR, Sun T-T, Medina JJ (1996) In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proceedings of the National Academy of Sciences of the United States of America 93: 9630-9635. (Pubitemid 26296659)
14. Zhou G, Mo WJ, Sebbel P, Min G, Neubert TA, et al. (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci 114: 4095-4103. (Pubitemid 33115030)
15. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000) Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proceedings of the National Academy of Sciences of the United States of America 97: 8829-8835. (Pubitemid 30626633)
16. Hannan TJ, Totsika M, Mansfield KJ, Moore KH, Schembri MA, et al. (2012) Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS microbiology reviews 36: 616-648.
17. Mysorekar IU, Hultgren SJ (2006) Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proceedings of the National Academy of Sciences of the United States of America 103: 14170-14175. (Pubitemid 44452998)
18. Yu J, Lin JH, Wu XR, Sun T-T (1994) Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. Journal of Cell Biology 125: 171-182. (Pubitemid 24100047)
19. Lin JH, Wu XR, Kreibich G, Sun T-T (1994) Precursor sequence, processing, and urothelium-specific expression of a major 15-kDa protein subunit of asymmetric unit membrane. Journal of Biological Chemistry 269: 1775-1784. (Pubitemid 24035374)
20. Wu XR, Sun T-T (1993) Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein. Journal of Cell Science 106: 31-43.
21. Liang FX, Riedel I, Deng FM, Zhou G, Xu C, et al. (2001) Organization of uroplakin subunits: transmembrane topology, pair formation and plaque composition. Biochem J 355: 13-18. (Pubitemid 32304230)
22. Tu L, Sun TT, Kreibich G (2002) Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol Biol Cell 13: 4221-4230. (Pubitemid 35471180)
23. Wu XR, Medina JJ, Sun T-T (1995) Selective interactions of UPIa and UPIb, two members of the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells. Journal of Biological Chemistry 270: 29752-29759. (Pubitemid 26001642)
24. Hu CC, Liang FX, Zhou G, Tu L, Tang CH, et al. (2005) Assembly of urothelial plaques: tetraspanin function in membrane protein trafficking. Mol Biol Cell 16: 3937-3950. (Pubitemid 41262868)
25. Min G, Stolz M, Zhou G, Liang F, Sebbel P, et al. (2002) Localization of uroplakin Ia, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particle. J Mol Biol 317: 697-706. (Pubitemid 34722158)
26. Min G, Wang H, Sun TT, Kong XP (2006) Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J Cell Biol 173: 975-983.
27. Severs NJ, Hicks RM (1979) Analysis of membrane structure in the transitional epithelium of rat urinary bladder. 2. The discoidal vesicles and Golgi apparatus: their role in luminal membrane biogenesis. J Ultrastruct Res 69: 279-296. (Pubitemid 10158856)
28. Hudoklin S, Jezernik K, Neumuller J, Pavelka M, Romih R (2011) Urothelial plaque formation in post-Golgi compartments. PLoS One 6: e23636.
29. Hudoklin S, Jezernik K, Neumuller J, Pavelka M, Romih R (2012) Electron tomography of fusiform vesicles and their organization in urothelial cells. PLoS One 7: e32935.
30. Thumbikat P, Berry RE, Zhou G, Billips BK, Yaggie RE, et al. (2009) Bacteria-induced uroplakin signaling mediates bladder response to infection. PLoS Pathog 5: e1000415.
31. Khandelwal P, Ruiz WG, Apodaca G (2010) Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J 29: 1961-1975.
32. Romih R, Jezernik K (1994) Endocytosis during postnatal differentiation in superficial cells of the mouse urinary bladder epithelium. Cell biology international 18: 663-668. (Pubitemid 24239842)
33. Truschel ST, Wang E, Ruiz WG, Leung SM, Rojas R, et al. (2002) Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol Biol Cell 13: 830-846. (Pubitemid 34250349)
34. Lewis SA, Demoura JLC (1982) Incorporation of Cytoplasmic Vesicles into Apical Membrane of Mammalian Urinary-Bladder Epithelium. Nature 297: 685-688. (Pubitemid 12096191)
35. Amano O, Kataoka S, Yamamoto TY (1991) Turnover of asymmetric unit membranes in the transitional epithelial superficial cells of the rat urinary bladder. Anat Rec 229: 9-15.
36. Zhang SX, Seguchi H (1994) The fate of the luminal asymmetric unit membrane of the superficial cell of the rat transitional epithelium. Histology and histopathology 9: 315-323. (Pubitemid 24148886)
37. Derganc J, Antonny B, Copic A (2013) Membrane bending: the power of protein imbalance. Trends Biochem Sci 38: 576-584.
38. Deng FM, Ding M, Lavker RM, Sun TT (2001) Urothelial function reconsidered: a role in urinary protein secretion. Proc Natl Acad Sci U S A 98: 154-159. (Pubitemid 32095879)
39. Teasdale RD, Collins BM (2012) Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: structures, functions and roles in disease. The Biochemical journal 441: 39-59.
40. Cullen PJ (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 9: 574-582.
41. Surya B, Yu J, Manabe M, Sun TT (1990) Assessing the differentiation state of cultured bovine urothelial cells: elevated synthesis of stratification-related K5 and K6 keratins and persistent expression of uroplakin I. Journal of cell science 97 (Pt 3): 419-432. (Pubitemid 20374483)
42. Veranic P, Jezernik K (2002) Trajectorial organisation of cytokeratins within the subapical region of umbrella cells. Cell Motil Cytoskeleton 53: 317-325. (Pubitemid 35332730)
43. Wu XR, Manabe M, Yu J, Sun T-T (1990) Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. Journal of Biological Chemistry 265: 19170-19179.
44. Guo X, Tu L, Gumper I, Plesken H, Novak EK, et al. (2009) Involvement of vps33a in the fusion of uroplakin-degrading multivesicular bodies with lysosomes. Traffic 10: 1350-1361.
45. Zhou G, Liang FX, Romih R, Wang Z, Liao Y, et al. (2012) MAL facilitates the incorporation of exocytic uroplakin-delivering vesicles into the apical membrane of urothelial umbrella cells. Mol Biol Cell 23: 1354-1366.
46. Leuchowius KJ, Weibrecht I, Soderberg O (2011) In situ proximity ligation assay for microscopy and flow cytometry. Curr Protoc Cytom Chapter 9: Unit 9 36.
47. Xu Y, Hortsman H, Seet L, Wong SH, Hong W (2001) SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P. Nat Cell Biol 3: 658-666. (Pubitemid 32624422)
48. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657. (Pubitemid 44564702)
49. Seet LF, Hong W (2006) The Phox (PX) domain proteins and membrane traffic. Biochimica et biophysica acta 1761: 878-896.
50. Carlton J, Bujny M, Rutherford A, Cullen P (2005) Sorting nexins - unifying trends and new perspectives. Traffic 6: 75-82.
51. Yu Z, Mannik J, Soto A, Lin KK, Andersen B (2009) The epidermal differentiation-associated Grainyhead gene Get1/Grhl3 also regulates urothelial differentiation. EMBO J 28: 1890-1903.
52. Sun T-T (2006) Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. American J Physiology (Renal Physiology) 291: F9-F21.
53. Romih R, Korosec P, de Mello W Jr, Jezernik K (2005) Differentiation of epithelial cells in the urinary tract. Cell Tissue Res 320: 259-268. (Pubitemid 40684752)
54. Truschel ST, Ruiz WG, Shulman T, Pilewski J, Sun TT, et al. (1999) Primary uroepithelial cultures. A model system to analyze umbrella cell barrier function. J Biol Chem 274: 15020-15029.
55. Kreft ME, Robenek H (2012) Freeze-fracture replica immunolabelling reveals urothelial plaques in cultured urothelial cells. PLoS One 7: e38509.
56. Ghai R, Mobli M, Norwood SJ, Bugarcic A, Teasdale RD, et al. (2011) Phox homology band 4.1/ezrin/radixin/moesin-like proteins function as molecular scaffolds that interact with cargo receptors and Ras GTPases. Proceedings of the National Academy of Sciences of the United States of America 108: 7763-7768.
57. Knauth P, Schluter T, Czubayko M, Kirsch C, Florian V, et al. (2005) Functions of sorting nexin 17 domains and recognition motif for P-selectin trafficking. Journal of molecular biology 347: 813-825. (Pubitemid 40357922)
58. Burden JJ, Sun XM, Garcia AB, Soutar AK (2004) Sorting motifs in the intracellular domain of the low density lipoprotein receptor interact with a novel domain of sorting nexin-17. The Journal of biological chemistry 279: 16237-16245. (Pubitemid 38509317)
59. Lee J, Retamal C, Cuitino L, Caruano-Yzermans A, Shin JE, et al. (2008) Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes. The Journal of biological chemistry 283: 11501-11508.
60. Bottcher RT, Stremmel C, Meves A, Meyer H, Widmaier M, et al. (2012) Sorting nexin 17 prevents lysosomal degradation of beta1 integrins by binding to the beta1-integrin tail. Nature cell biology 14: 584-592.
61. Steinberg F, Heesom KJ, Bass MD, Cullen PJ (2012) SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways. The Journal of cell biology 197: 219-230.
62. Valdes JL, Tang J, McDermott MI, Kuo JC, Zimmerman SP, et al. (2011) Sorting nexin 27 protein regulates trafficking of a p21-activated kinase (PAK) interacting exchange factor (beta-Pix)-G protein-coupled receptor kinase interacting protein (GIT) complex via a PDZ domain interaction. The Journal of biological chemistry 286: 39403-39416.
63. Hayashi H, Naoi S, Nakagawa T, Nishikawa T, Fukuda H, et al. (2012) Sorting nexin 27 interacts with multidrug resistance-associated protein 4 (MRP4) and mediates internalization of MRP4. The Journal of biological chemistry 287: 15054-15065.
64. Hicks RM (1966) The function of the golgi complex in transitional epithelium. Synthesis of the thick cell membrane. J Cell Biol 30: 623-643.
65. Jezernik K, Sterle M (1992) Multivesicular bodies in the transitional epithelium of the neonatal mouse urinary border. Cell biology international reports 16: 1219-1228. (Pubitemid 23052133)
66. Piper RC, Katzmann DJ (2007) Biogenesis and function of multivesicular bodies. Annual review of cell and developmental biology 23: 519-547.
67. Hanson PI, Cashikar A (2012) Multivesicular Body Morphogenesis. Annual review of cell and developmental biology.
68. Pisitkun T, Shen RF, Knepper MA (2004) Identification and proteomic profiling of exosomes in human urine. Proceedings of the National Academy of Sciences of the United States of America 101: 13368-13373. (Pubitemid 39209672)
69. Babst M (2011) MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Current opinion in cell biology 23: 452-457.
70. Davies BA, Lee JR, Oestreich AJ, Katzmann DJ (2009) Membrane protein targeting to the MVB/lysosome. Chem Rev 109: 1575-1586.
71. Hurley JH (2008) ESCRT complexes and the biogenesis of multivesicular bodies. Current opinion in cell biology 20: 4-11.
72. Katzmann DJ (2006) No ESCRT to the melanosome: MVB sorting without ubiquitin. Dev Cell 10: 278-280.
73. Reggiori F, Pelham HR (2001) Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20: 5176-5186. (Pubitemid 32910912)
74. Liang F, Kachar B, Ding M, Zhai Z, Wu XR, et al. (1999) Urothelial hinge as a highly specialized membrane: detergent- insolubility, urohingin association, and in vitro formation. Differentiation 65: 59-69. (Pubitemid 29361267)
75. Wang H, Min G, Glockshuber R, Sun TT, Kong XP (2009) Uropathogenic E. coli adhesin-induced host cell receptor conformational changes: implications in transmembrane signaling transduction. J Mol Biol 392: 352-361.