Depolymerization of cortical actin inhibits UT-A1 urea transporter endocytosis but promotes forskolin-stimulated membrane trafficking

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 7, 2012, Pages

  Xu, Gang ^a,c   Su, Hua ^a   Carter, Conner B ^a   Fröhlich, Otto ^b   Chen, Guangping ^a  

^a Renal Division   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Cytoskeletal protein; Latrunculin; Membrane protein; Urea transport

Indexed keywords

ALANINE; CARRIER PROTEIN; CYTOSKELETON PROTEIN; F ACTIN; FORSKOLIN; LATRUNCULIN B; MEMBRANE PROTEIN; SERINE; UNCLASSIFIED DRUG; UREA TRANSPORTER A1;

ACTIN FILAMENT; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; DEPOLYMERIZATION; ENDOCYTOSIS; GENE DISRUPTION; LIPID RAFT; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; REGULATORY MECHANISM; TWO HYBRID SYSTEM;

ACTINS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BINDING SITES; CAVEOLIN 1; CELLS, CULTURED; CLATHRIN; CYTOPLASM; DOGS; ENDOCYTOSIS; FORSKOLIN; KIDNEY TUBULES, COLLECTING; MEMBRANE MICRODOMAINS; MEMBRANE TRANSPORT PROTEINS; OOCYTES; PROTEIN BINDING; PROTEIN TRANSPORT; THIAZOLIDINES; XENOPUS LAEVIS; YEASTS;

EID: 84859456955     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00440.2011     Document Type: Article

References (44)

1. Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2: 149-159, 2001.
2. Bresnick AR, Warren V, Condeelis J. Identification of a short sequence essential for actin binding by Dictyostelium ABP-120. J Biol Chem 265: 9236-9240, 1990.
3. Chen G, Froehlich O, Yang Y, Klein JD, Sands JM. Loss of N-linked glycosylation reduces urea transporter UT-A1 response to vasopressin. J Biol Chem 281: 27436-27442, 2006.
4. Chen G, Howe AG, Xu G, Fröhlich O, Klein JD, Sands JM. Mature N-linked glycans facilitate UT-A1 urea transporter lipid raft compartmentalization. FASEB J 25: 4531-4539, 2011.
5. Chen G, Huang H, Fröhlich O, Yang Y, Klein JD, Price SR, Sands JM. MDM2 E3 ubiquitin ligase mediates UT-A1 urea transporter ubiquitination and degradation. Am J Physiol Renal Physiol 295: F1528-F1534, 2008.
6. 2 exchanger. Am J Physiol Cell Physiol 290: C691-C701, 2006.
7. Ding GH, Franki N, Condeelis J, Hays RM. Vasopressin depolymerizes F-actin in toad bladder epithelial cells. Am J Physiol Cell Physiol 260: C9-C16, 1991.
8. Fechheimer M, Daiss JL, Cebra JJ. Interaction of immunoglobulin with actin. Mol Immunol 16: 881-888, 1979.
9. Feng X, Huang H, Yang Y, Fröhlich 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.
10. Fenton RA, Chou CL, Stewart GS, Smith CP, Knepper MA. Urinary concentrating defect in mice with selective deletion of phloretin-sensitive urea transporters in the renal collecting duct. Proc Natl Acad Sci USA 101: 7469-7474, 2004.
11. Ferguson SM, Raimondi A, Paradise S, Shen H, Mesaki K, Ferguson A, Destaing O, Ko G, Takasaki J, Cremona O, O' Toole E, De Camilli P. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 17: 811-822, 2009.
12. Fröhlich O, Klein JD, Smith PM, Sands JM, Gunn RB. Urea transport in MDCK cells that are stably transfected with UT-A1. Am J Physiol Cell Physiol 286: C1264-C1270, 2004.
13. Galletta BJ, Mooren OL, Cooper JA. Actin dynamics and endocytosis in yeast and mammals. Curr Opin Biotechnol 21: 604-610, 2010.
14. Gormley K, Dong Y, Sagnella GA. Regulation of the epithelial sodium channel by accessory proteins. Biochem J 371: 1-14, 2003.
15. Huang H, Feng X, Zhuang J, Fröhlich O, Klein JD, Cai H, Sands JM, Chen G. Internalization of UT-A1 urea transporter is dynamin dependent and mediated by both caveolae-and clathrin-coated pit pathways. Am J Physiol Renal Physiol 299: F1389-F1395, 2010.
16. Hyman T, Shmuel M, Altschuler Y. Actin is required for endocytosis at the apical surface of Madin-Darby canine kidney cells where ARF6 and clathrin regulate the actin cytoskeleton. Mol Biol Cell 17: 427-437, 2006.
17. Ikari A, Harada H, Takagi K. Role of actin in the cAMP-dependent activation of sodium/glucose cotransporter in renal epithelial cells. Biochim Biophys Acta 1711: 20-24, 2005.
18. Kanzaki M, Pessin JE. Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling. J Biol Chem 276: 42436-42444, 2001.
19. Klein JD, Fröhlich O, Blount MA, Martin CF, Smith TD, Sands JM. Vasopressin increases plasma membrane accumulation of urea transporter UT-A1 in rat inner medullary collecting ducts. J Am Soc Nephrol 17: 2680-2686, 2006.
20. Liedtke CM, Hubbard M, Wang X. Stability of actin cytoskeleton and PKC-delta binding to actin regulate NKCC1 function in airway epithelial cells. Am J Physiol Cell Physiol 284: C487-C496, 2003.
21. Mazzochi C, Bubien JK, Smith PR, Benos DJ. The carboxyl terminus of the alpha-subunit of the amiloride-sensitive epithelial sodium channel binds to F-actin. J Biol Chem 281: 6528-6538, 2006.
22. McCarthy AM, Spisak KO, Brozinick JT, Elmendorf JS. Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport. Am J Physiol Cell Physiol 291: C860-C868, 2006.
23. Mistry AC, Mallick R, Fröhlich O, Klein JD, Rehm A, Chen G, Sands JM. The UT-A1 urea transporter interacts with snapin, a SNARE-associated protein. J Biol Chem 282: 30097-30106, 2007.
24. Mistry AC, Mallick R, Klein JD, Weimbs T, Sands JM, Fröhlich O. Syntaxin specificity of aquaporins in the inner medullary collecting duct. Am J Physiol Renal Physiol 297: F292-F300, 2009.
25. Morales M, Colicos MA, Goda Y. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27: 539-550, 2000.
26. Nielsen S, Terris J, Smith CP, Hediger MA, Ecelbarger CA, Knepper MA. Cellular and subcellular localization of the vasopressin-regulated urea transporter in rat kidney. Proc Natl Acad Sci USA 93: 5495-5500, 1996.
27. Noda Y, Sasaki S. Regulation of aquaporin-2 trafficking and its binding protein complex. Biochim Biophys Acta 1758: 1117-1125, 2006.
28. Noda Y, Horikawa S, Katayama Y, Sasaki S. Water channel aqua-porin-2 directly binds to actin. Biochem Biophys Res Commun 322: 740-745, 2004.
29. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 101: 13368-13373, 2004.
30. Prat AG, Bertorello AM, Ausiello DA, Cantiello HF. Activation of epithelial Na channels by protein kinase A requires actin filaments. Am J Physiol Cell Physiol 265: C224-C233, 1993.
31. Prat AG, Cunningham CC, Jackson GR Jr, Borkan SC, Wang Y, Ausiello DA, Cantiello HF. Actin filament organization is required for proper cAMP-dependent activation of CFTR. Am J Physiol Cell Physiol 277: C1160-C1169, 1999.
32. Robertson AS, Smythe E, Ayscough KR. Functions of actin in endocytosis. Cell Mol Life Sci 66: 2049-2065, 2009.
33. 2channel by the actin-binding proteins-actinin and dystrophin. Am J Physiol Cell Physiol 282: C1502-C1511, 2002.
34. Sands JM. Molecular mechanisms of urea transport. J Membr Biol 191: 149-163, 2003.
35. Simon H, Gao Y, Franki N, Hays RM. Vasopressin depolymerizes apical F-actin in rat inner medullary collecting duct. Am J Physiol Cell Physiol 265: C757-C762, 1993.
36. Smith PR, Saccomani G, Joe EH, Angelides KJ, Benos DJ. Amiloridesensitive sodium channel is linked to the cytoskeleton in renal epithelial cells. Proc Natl Acad Sci USA 88: 6971-6975, 1991.
37. Tamma G, Klussmann E, Maric K, Aktories K, Svelto M, Rosenthal W, Valenti G. Rho inhibits cAMP-induced translocation of aquaporin-2 into the apical membrane of renal cells. Am J Physiol Renal Physiol 281: F1092-F1101, 2001.
38. Valenti G, Procino G, Tamma G, Carmosino M, Svelto M. Minireview: aquaporin 2 trafficking. Endocrinology 146: 5063-5070, 2005.
39. Vandekerckhove JS, Kaiser DA, Pollard TD. Acanthamoeba actin and profilin can be cross-linked between glutamic acid 364 of actin and lysine 115 of profilin. J Cell Biol 109: 619-626, 1989.
40. Wang Y, Klein JD, Blount MA, Martin CF, Kent KJ, Pech V, Wall SM, Sands JM. Epac regulates UT-A1 to increase urea transport in inner medullary collecting ducts. J Am Soc Nephrol 20: 2018-2024, 2009.
41. Watts 3rd BA, George T, Good DW. The basolateral NHE1 Na /H exchanger regulates transepithelial HCO3 absorption through actin cytoskeleton remodeling in renal thick ascending limb. J Biol Chem 280: 11439-11447, 2005.
42. Yarar D, Waterman-Storer CM, Schmid SL. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16: 964-975, 2005.
43. Zhang C, Sands JM, Klein JD. Vasopressin rapidly increases phosphorylation of UT-A1 urea transporter in rat IMCDs through PKA. Am J Physiol Renal Physiol 282: F85-F90, 2002.
44. Zou S, Jha S, Kim EY, Dryer SE. A novel actin-binding domain on Slo1 calcium-activated potassium channels is necessary for their expression in the plasma membrane. Mol Pharmacol 73: 359-368, 2008.