Sorting it out in endosomes: An emerging concept in renal epithelial cell transport regulation

Physiology

Volumn 25, Issue 5, 2010, Pages 280-292

  Welling, Paul A ^a   Weisz, Ora A ^b  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; CLATHRIN; ESCRT PROTEIN;

CELL MEMBRANE; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; HUMAN; ION TRANSPORT; KIDNEY; LIPOYLATION; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW;

AQUAPORINS; CELL MEMBRANE; CLATHRIN; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; EPITHELIAL CELLS; HUMANS; ION TRANSPORT; KIDNEY; LIPOYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 77958037552     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00022.2010     Document Type: Review

References (102)

1. Abrami L, Leppla SH, van der Goot FG. Receptor palmitoylation and ubiquitination regulate anthrax toxin endocytosis. J Cell Biol 172:309-320, 2006.
2. Apodaca G, Katz LA, Mostov KE. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol 125:67-86, 1994.
3. Benmerah A, Lamaze C. Clathrin-coated pits: vive la difference? Traffic 8:970-982, 2007.
4. Blaine J, Okamura K, Giral H, Breusegem S, Caldas Y, Millard A, Barry N, Levi M. PTH-induced internalization of apical membrane NaPi2a: role of actin and myosin VI. Am J Physiol Cell Physiol 297:C1339-C1346, 2009.
5. Bomberger JM, Barnaby RL, Stanton BA. The deubiquitinating enzyme USP10 regulates the post-endocytic sorting of cystic fibrosis transmembrane conductance regulator in airway epithelial cells. J Biol Chem 284:18778-18789, 2009.
6. Brown PS, Wang E, Aroeti B, Chapin SJ, Mostov KE, Dunn KW. Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 1:124-140, 2000.
7. Butterworth MB, Edinger RS, Ovaa H, Burg D, Johnson JP, Frizzell RA. The deubiquitinating enzyme UCH-L3 regulates the apical membrane recycling of the epithelial sodium channel. J Biol Chem 282:37885-37893, 2007.
8. Carpentier JL, Gorden P, Anderson RG, Goldstein JL, Brown MS, Cohen S, Orci L. Co-localization of 125I-epidermal growth factor and ferritin-low density lipoprotein in coated pits: a quantitative electron microscopic study in normal and mutant human fibroblasts. J Cell Biol 95:73-77, 1982.
9. Cha SK, Wu T, Huang CL. Protein kinase C inhibits caveolae-mediated endocytosis of TRPV5. Am J Physiol Renal Physiol 294:F1212-F1221, 2008.
10. Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P. Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394:793-797, 1998.
11. +-ATPase endocytosis. J Biol Chem 273:8814-8819, 1998.
12. Damke H, Baba T, van der Bliek AM, Schmid SL. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 131:69-80, 1995.
13. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 78:857-902, 2009.
14. Donaldson JG, Porat-Shliom N, Cohen LA. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21:1-6, 2009.
15. +-ATPase α1-subunit phosphorylation signal into binding and activation of phosphoinositide 3-kinase during endocytosis. J Biol Chem 280:16272-16277, 2005.
16. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591-605, 2004.
17. Fakitsas P, Adam G, Daidie D, van Bemmelen MX, Fouladkou F, Patrignani A, Wagner U, Warth R, Camargo SM, Staub O, Verrey F. Early aldosterone-induced gene product regulates the epithelial sodium channel by deubiquitylation. JAm Soc Nephrol 18:1084-1092, 2007.
18. Fang L, Garuti R, Kim BY, Wade JB, Welling PA. The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J Clin Invest 119:3278-3289, 2009.
19. Feng X, Huang H, Yang Y, Frohlich O, Klein JD, Sands JM, Chen G. Caveolin-1 directly interacts with UT-A1 urea transporter: the role of caveolae/lipid rafts in UT-A1 regulation at the cell membrane. Am J Physiol Renal Physiol 296:F1514-F1520, 2009.
20. Folsch H, Mattila PE, Weisz OA. Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells. Traffic 10:972-981, 2009.
21. French AR, Tadaki DK, Niyogi SK, Lauffenburger DA. Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J Biol Chem 270:4334-4340, 1995.
22. Gaidarov I, Santini F, Warren RA, Keen JH. Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1:1-7, 1999.
23. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597-608, 2009.
24. Hayashi T, Thomas GM, Huganir RL. Dual palmitoylation of NR2 subunits regulates NMDA receptor trafficking. Neuron 64:213-226, 2009.
25. He G, Wang HR, Huang SK, Huang CL. Intersectin links WNK kinases to endocytosis of ROMK1. J Clin Invest 117:1078-1087, 2007.
26. Henry L, Sheff DR. Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol Biol Cell 19:2059-2068, 2008.
27. Honing S, Ricotta D, Krauss M, Spate K, Spolaore B, Motley A, Robinson M, Robinson C, Haucke V, Owen DJ. Phosphatidylinositol-(4, 5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 18:519-531, 2005.
28. + exchanger (NHE3) endocytosis via clathrin-coated vesicles: dependence on protein kinase A-mediated NHE3 phosphorylation. J Biol Chem 276:26906-26915, 2001.
29. Huang F, Goh LK, Sorkin A. EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA 104:16904-16909, 2007.
30. Idkowiak-Baldys J, Baldys A, Raymond JR, Hannun YA. Sustained receptor stimulation leads to sequestration of recycling endosomes in a classical protein kinase C-and phospholipase D-dependent manner. J Biol Chem 284:22322-22331, 2009.
31. Irie F, Okuno M, Pasquale EB, Yamaguchi Y. EphrinBEphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nat Cell Biol 7:501-509, 2005.
32. Johannessen LE, Pedersen NM, Pedersen KW, Madshus IH, Stang E. Activation of the epidermal growth factor (EGF) receptor induces formation of EGF receptor-and Grb2-containing clathrin-coated pits. Mol Cell Biol 26:389-401, 2006.
33. Kahle KT, Wilson FH, Leng Q, Lalioti MD, O'Connell AD, Dong K, Rapson AK, MacGregor GG, Giebisch G, Hebert SC, Lifton RP. WNK4 regulates the balance between renal NaCl reabsorption and K+ secretion. Nat Genet 35:372-376, 2003.
34. Kamsteeg EJ, Hendriks G, Boone M, Konings IB, Oorschot V, van der Sluijs P, Klumperman J, Deen PM. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc Natl Acad Sci USA 103:18344-18349, 2006.
35. Keyel PA, Mishra SK, Roth R, Heuser JE, Watkins SC, Traub LM. A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol Biol Cell 17:4300-4317, 2006.
36. Kinlough CL, McMahan RJ, Poland PA, Bruns JB, Harkleroad KL, Stremple RJ, Kashlan OB, Weixel KM, Weisz OA, Hughey RP. Recycling of MUC1 is dependent on its palmitoylation. J Biol Chem 281:12112-12122, 2006.
37. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168:465-476, 2005.
38. Kittler JT, Chen G, Kukhtina V, Vahedi-Faridi A, Gu Z, Tretter V, Smith KR, McAinsh K, Arancibia-Carcamo IL, Saenger W, Haucke V, Yan Z, Moss SJ. Regulation of synaptic inhibition by phospho-dependent binding of the AP2 complex to a YECL motif in the GABAA receptor gamma2 subunit. Proc Natl Acad Sci USA 105:3616-3621, 2008.
39. Kouranti I, Sachse M, Arouche N, Goud B, Echard A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16:1719-1725, 2006.
40. Lakadamyali M, Rust MJ, Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124:997-1009, 2006.
41. Leonard D, Hayakawa A, Lawe D, Lambright D, Bellve KD, Standley C, Lifshitz LM, Fogarty KE, Corvera S. Sorting of EGF and transferrin at the plasma membrane and by cargo-specific signaling to EEA1-enriched endosomes. J Cell Sci 121:3445-3458, 2008.
42. Lin DH, Sterling H, Lerea KM, Welling P, Jin L, Giebisch G, Wang WH. K depletion increases protein tyrosine kinase-mediated phosphorylation of ROMK. Am J Physiol Renal Physiol 283:F671-F677, 2002.
43. Lin DH, Sterling H, Wang Z, Babilonia E, Yang B, Dong K, Hebert SC, Giebisch G, Wang WH. ROMK1 channel activity is regulated by monoubiquitination. Proc Natl Acad Sci USA 102:4306-4311, 2005.
44. Lin DH, Yue P, Pan CY, Sun P, Zhang X, Han Z, Roos M, Caplan M, Giebisch G, Wang WH. POSH stimulates the ubiquitination and the clathrin-in-dependent endocytosis of ROMK1 channels. J Biol Chem 284:29614-29624, 2009.
45. Linder ME, Deschenes RJ. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 8:74-84, 2007.
46. Lundmark R, Doherty GJ, Howes MT, Cortese K, Vallis Y, Parton RG, McMahon HT. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr Biol 18:1802-1808, 2008.
47. Madrid R, Le Maout S, Barrault MB, Janvier K, Benichou S, Merot J. Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J 20:7008-7721, 2001.
48. Marks MS, Woodruff L, Ohno H, Bonifacino JS. Protein targeting by tyrosine-and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 135:341-354, 1996.
49. Maxfield FR, Schlessinger J, Shechter Y, Pastan I, Willingham MC. Collection of insulin, EGF and alpha2-macroglobulin in the same patches on the surface of cultured fibroblasts and common internalization. Cell 14:805-810, 1978.
50. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603-612, 2007.
51. McCormick PJ, Dumaresq-Doiron K, Pluviose AS, Pichette V, Tosato G, Lefrancois S. Palmitoylation controls recycling in lysosomal sorting and trafficking. Traffic 9:1984-1997, 2008.
52. i-coupled Src kinase signaling pathway. J Cell Biol 150:1057-1070, 2000.
53. Moeller HB, Praetorius J, Rutzler MR, Fenton RA. Phosphorylation of aquaporin-2 regulates its endocytosis and protein-protein interactions. Proc Natl Acad Sci USA 107:424-429, 2010.
54. Mundell SJ, Luo J, Benovic JL, Conley PB, Poole AW. Distinct clathrin-coated pits sort different G protein-coupled receptor cargo. Traffic 7:1420-1431, 2006.
55. Nagai J, Christensen EI, Morris SM, Willnow TE, Cooper JA, Nielsen R. Mutually dependent localization of megalin and Dab2 in the renal proximal tubule. Am J Physiol Renal Physiol 289:F569-F576, 2005.
56. Naim HY, Dodds DT, Brewer CB, Roth MG. Apical and basolateral coated pits of MDCK cells differ in their rates of maturation into coated vesicles, but not in the ability to distinguish between mutant hemagglutinin proteins with different internalization signals. J Cell Biol 129:1241-1250, 1995.
57. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 15:3542-3552, 2004.
58. Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrin-and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 14:417-431, 2003.
59. Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH, Hirschberg K, Phair RD, Lippincott-Schwartz J. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 153:529-541, 2001.
60. Okamoto CT, Song W, Bomsel M, Mostov KE. Rapid internalization of the polymeric immunoglobulin receptor requires phosphorylated serine 726. J Biol Chem 269:15676-15682, 1994.
61. Olsen O, Liu H, Wade JB, Merot J, Welling PA. Basolateral membrane expression of the Kir 2.3 channel is coordinated by PDZ interaction with Lin-7/CASK complex. Am J Physiol Cell Physiol 282:C183-C195, 2002.
62. Picciano JA, Ameen N, Grant BD, Bradbury NA. Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator. Am J Physiol Cell Physiol 285:C1009-C1018, 2003.
63. Puthenveedu MA, von Zastrow M. Cargo regulates clathrin-coated pit dynamics. Cell 127:113-124, 2006.
64. Qin XS, Tsukaguchi H, Shono A, Yamamoto A, Kurihara H, Doi T. Phosphorylation of nephrin triggers its internalization by raft-mediated endocytosis. J Am Soc Nephrol 20:2534-2545, 2009.
65. Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458:445-452, 2009.
66. Rappoport JZ, Simon SM. Endocytic trafficking of activated EGFR is AP-2 dependent and occurs through preformed clathrin spots. J Cell Sci 122:1301-1305, 2009.
67. Riquier AD, Lee DH, McDonough AA. Renal NHE3 and NaPi2 partition into distinct membrane domains. Am J Physiol Cell Physiol 296:C900-C910, 2009.
68. Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JR 3rd, Davis NG. Global analysis of protein palmitoylation in yeast. Cell 125:1003-1013, 2006.
69. Rotin D, Kanelis V, Schild L. Trafficking and cell surface stability of ENaC. Am J Physiol Renal Physiol 281:F391-F399, 2001.
70. Sabharanjak S, Sharma P, Parton RG, Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2:411-423, 2002.
71. Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E. Caveolin-1 and-2 in the exocytic pathway of MDCK cells. J Cell Biol 140:795-806, 1998.
72. Schonteich E, Wilson GM, Burden J, Hopkins CR, Anderson K, Goldenring JR, Prekeris R. The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J Cell Sci 121:3824-3833, 2008.
73. Schwake M, Friedrich T, Jentsch TJ. An internalization signal in ClC-5, an endosomal Cl-channel mutated in dent's disease. J Biol Chem 276:12049-12054, 2001.
74. Semerdjieva S, Shortt B, Maxwell E, Singh S, Fonarev P, Hansen J, Schiavo G, Grant BD, Smythe E. Coordinated regulation of AP2 uncoating from clathrin-coated vesicles by rab5 and hRME-6. J Cell Biol 183:499-511, 2008.
75. Sharma M, Pampinella F, Nemes C, Benharouga M, So J, Du K, Bache KG, Papsin B, Zerangue N, Stenmark H, Lukacs GL. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol 164:923-933, 2004.
76. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15:209-219, 2008.
77. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 315:683-696, 2009.
78. Straight SW, Chen L, Karnak D, Margolis B. Interaction with mLin-7 alters the targeting of endocytosed transmembrane proteins in mammalian epithelial cells. Mol Biol Cell 12:1329-1140, 2001.
79. Subramanya AR, Liu J, Ellison DH, Wade JB, Welling PA. WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J Biol Chem 284:18471-18480, 2009.
80. Tebar F, Sorkina T, Sorkin A, Ericsson M, Kirchhausen T. Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J Biol Chem 271:28727-28730, 1996.
81. Tosoni D, Puri C, Confalonieri S, Salcini AE, De Camilli P, Tacchetti C, Di Fiore PP. TTP specifically regulates the internalization of the transferrin receptor. Cell 123:875-888, 2005.
82. Traub LM. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583-596, 2009.
83. Traub LM, Lukacs GL. Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLASPs. J Cell Sci 120:543-553, 2007.
84. Tzaban S, Massol RH, Yen E, Hamman W, Frank SR, Lapierre LA, Hansen SH, Goldenring JR, Blumberg RS, Lencer WI. The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J Cell Biol 185:673-684, 2009.
85. van der Sluijs P, Hull M, Webster P, Male P, Goud B, Mellman I. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70:729-740, 1992.
86. Verkade P, Harder T, Lafont F, Simons K. Induction of caveolae in the apical plasma membrane of Madin-Darby canine kidney cells. J Cell Biol 148:727-739, 2000.
87. Vilhardt F, Nielsen M, Sandvig K, van Deurs B. Urokinase-type plasminogen activator receptor is internalized by different mechanisms in polarized and nonpolarized Madin-Darby canine kidney epithelial cells. Mol Biol Cell 10:179-195, 1999.
88. Wang E, Brown PS, Aroeti B, Chapin SJ, Mostov KE, Dunn KW. Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1:480-493, 2000.
89. Wang H, Traub LM, Weixel KM, Hawryluk MJ, Shah N, Edinger RS, Perry CJ, Kester L, Butterworth MB, Peters KW, Kleyman TR, Frizzell RA, Johnson JP. Clathrin-mediated endocytosis of the epithelial sodium channel. Role of epsin. J Biol Chem 281:14129-14135, 2006.
90. Warren RA, Green FA, Stenberg PE, Enns CA. Distinct saturable pathways for the endocytosis of different tyrosine motifs. J Biol Chem 273:17056-17063, 1998.
91. Weinman EJ, Cunningham R, Wade JB, Shenolikar S. The role of NHERF-1 in the regulation of renal proximal tubule sodium-hydrogen exchanger 3 and sodium-dependent phosphate co-transporter 2a. J Physiol 567:27-32, 2005. (Pubitemid 41167300)
92. Wiemuth D, Ke Y, Rohlfs M, McDonald FJ. Epithelial sodium channel (ENaC) is multi-ubiquitinated at the cell surface. Biochem J 405:147-155, 2007.
93. Wilde A, Beattie EC, Lem L, Riethof DA, Liu SH, Mobley WC, Soriano P, Brodsky FM. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96:677-687, 1999.
94. Wiley HS. Anomalous binding of epidermal growth factor to A431 cells is due to the effect of high receptor densities and a saturable endocytic system. J Cell Biol 107:801-810, 1988.
95. Wilson FH, Disse-Nicodeme S, Choate KA, Ishikawa K, Nelson-Williams C, Desitter I, Gunel M, Milford DV, Lipkin GW, Achard JM, Feely MP, Dussol B, Berland Y, Unwin RJ, Mayan H, Simon DB, Farfel Z, Jeunemaitre X, Lifton RP. Human hypertension caused by mutations in WNK kinases. Science 293:1107-1112, 2001.
96. Wolfe BL, Trejo J. Clathrin-dependent mechanisms of G protein-coupled receptor endocytosis. Traffic 8:462-470, 2007.
97. + transporters during hypertension or PTH: NHE3 to base of microvilli vs. NaPi2 to endosomes. Am J Physiol Renal Physiol 287:F896-F906, 2004.
98. Yang LE, Maunsbach AB, Leong PK, McDonough AA. Redistribution of myosin VI from top to base of proximal tubule microvilli during acute hyper-tension. J Am Soc Nephrol 16:2890-2896, 2005.
99. Yudowski GA, Puthenveedu MA, Henry AG, von Zastrow M. Cargo-mediated regulation of a rapid Rab4-dependent recycling pathway. Mol Biol Cell 20:2774-2784, 2009.
100. Zagorska A, Pozo-Guisado E, Boudeau J, Vitari AC, Rafiqi FH, Thastrup J, Deak M, Campbell DG, Morrice NA, Prescott AR, Alessi DR. Regulation of activity and localization of the WNK1 protein kinase by hyperosmotic stress. J Cell Biol 176:89-100, 2007.
101. Zhou B, Zhuang J, Gu D, Wang H, Cebotaru L, Guggino WB, Cai H. WNK4 enhances the degradation of NCC through a sortilin-mediated lysosomal pathway. J Am Soc Nephrol 21:82-92, 2010.
102. Zhou R, Patel SV, Snyder PM. Nedd4-2 catalyzes ubiquitination and degradation of cell surface ENaC. J Biol Chem 282:20207-20212, 2007.