Aquaporin 2 (AQP2) and vasopressin type 2 receptor (V2R) endocytosis in kidney epithelial cells: AQP2 is located in ‘endocytosis‐resistant’ membrane domains after vasopressin treatment

Biology of the Cell - Tập 98 Số 4 - Trang 215-232 - 2006
Richard Bouley1,2, Gayle Hawthorn1,2, Leileata M. Russo1,2, Herbert Y. Lin1,2, Dennis A. Ausiello1,2, Dennis Brown1,2
1Harvard Medical School, Boston, MA 02114, U.S.A.
2Program in Membrane Biology and Renal Unit, Massachusetts General Hospital, Charlestown, MA 02129, U.S.A.

Tóm tắt

Background information. Aquaporin 2 (AQP2) plays an important, VP (vasopressin)‐regulated role in water reabsorption by the kidney. The amount of AQP2 expressed at the surface of principal cells results from an equilibrium between the AQP2 in intracellular vesicles and the AQP2 on the plasma membrane. VP shifts the equilibrium in favour of the plasma membrane and this allows osmotic equilibration to occur between the collecting duct lumen and the interstitial space. Membrane accumulation of AQP2 could result from a VP‐induced increase in exocytosis, a decrease in endocytosis, or both. In the present study, we further investigated AQP2 accumulation at the cell surface, and compared it with V2R (VP type 2 receptor) trafficking using cells that express epitope‐tagged AQP2 and V2R.

Results. Endocytosis of V2R and of AQP2 are independent events that can be separated temporally and spatially. The burst of endocytosis seen after VP addition to target cells, when AQP2 accumulates at the cell surface, is primarily due to internalization of the V2R. Increased endocytosis is not induced by forskolin, which also induces membrane accumulation of AQP2 by direct stimulation of adenylate cyclase. This indicates that cAMP elevation is not the primary cause of the initial, VP‐induced endocytic process. After VP exposure, AQP2 is not located in endosomes with internalized V2R. Instead, it remains at the cell surface in ‘endocytosis‐resistant’ membrane domains, visualized by confocal imaging. After VP washout, AQP2 is progressively internalized with the fluid‐phase marker FITC—dextran, indicating that VP washout releases an endocytotic block that maintains AQP2 at the cell surface. Finally, polarized application of VP to filter‐grown cells shows that apical VP can induce basolateral endocytosis and V2R down‐regulation, and vice versa.

Conclusions. After VP stimulation of renal epithelial cells, AQP2 accumulates at the cell surface, while the V2R is actively internalized. This endocytotic block may involve a reduced capacity of phosphorylated AQP2 to interact with components of the endocytotic machinery. In addition, a complex cross‐talk exists between the apical and basolateral plasma‐membrane domains with respect to endocytosis and V2R down‐regulation. This may be of physiological significance in down‐regulating the VP response in the kidney in vivo.

Từ khóa


Tài liệu tham khảo

10.1073/pnas.92.18.8328

10.1016/S0008-6363(01)00328-5

Baylis P.H., 1987, Osmoregulation and control of vasopressin secretion in healthy humans, Am. J. Physiol., 253, R671

10.1152/ajpcell.00477.2002

10.1152/ajpcell.00353.2004

10.1124/mol.59.6.1395

10.1152/ajprenal.00387.2002

Brown D., 2000, The Kidney, 575

10.1152/physrev.1996.76.1.245

Brown D., 1985, Lack of intramembranous particle clusters in collecting ducts of mice with nephrogenic diabetes insipidus, Am. J. Physiol. Renal Physiol., 249, F582, 10.1152/ajprenal.1985.249.4.F582

Brown D., 1988, Vasopressin stimulates endocytosis in kidney collecting duct principal cells, Eur. J. Cell Biol., 46, 336

10.1007/BF01463929

Champigneulle A., 1993, V2‐like vasopressin receptor mobilizes intracellular Ca2+ in rat medullary collecting tubules, Am. J. Physiol. Renal Physiol., 265, F35, 10.1152/ajprenal.1993.265.1.F35

10.1083/jcb.200205086

10.1074/jbc.M005552200

10.1152/ajprenal.2000.279.5.F874

10.1038/nature01451

Deen P.M., 2001, Aquaporins: Current Topics in Membranes, 235

Deen P.M., 1997, Aquaporin‐2 transfection of Madin‐Darby canine kidney cells reconstitutes vasopressin‐regulated transcellular osmotic water transport, J. Am. Soc. Nephrol, 8, 1493, 10.1681/ASN.V8101493

10.1152/ajprenal.0168.2001

10.1210/endo-108-2-399

10.1038/361549a0

Fushimi K., 1994, Functional characterization and cell immunolocalization of AQP‐CD water channel in kidney collecting duct, Am. J. Physiol. Renal. Physiol., 267, F573, 10.1152/ajprenal.1994.267.4.F573

10.1074/jbc.272.23.14800

10.1034/j.1600-0854.2001.020105.x

Glanzer K., 1984, Measurement of 8‐arginine‐vasopressin by radioimmunoassay. Development and application to urine and plasma samples using one extraction method, Acta Endocrinol. (Copenh.), 106, 317

10.1152/ajprenal.2000.278.2.F317

Hammer M., 1980, Relationship between plasma osmolality and plasma vasopressin in human subjects, Am. J. Physiol., 238, E313

10.1093/oxfordjournals.ndt.a027350

10.1016/S0006-291X(05)81558-X

Imbert‐Teboul M., 1995, Functional expression of vasopressin receptors V1a and V2 along the mammalian nephron, C.R. Seances Soc. Biol. Fil., 189, 151

10.3109/10799899909036654

10.1159/000066651

10.1073/pnas.92.16.7212

Katsura T., 1996, Direct demonstration of aquaporin‐2 water channel recycling in stably transfected LLC‐PK1 epithelial cells, Am. J. Physiol. Renal Physiol., 270, F548, 10.1152/ajprenal.1996.270.3.F548

10.1152/ajprenal.1997.272.6.F816

10.3109/10799899409067001

10.1007/BFb0119577

10.1074/jbc.M010270200

Knepper M.A., 1993, Kinetic model of water and urea permeability regulation by vasopressin in collecting duct, Am. J. Physiol., 265, F214

10.1007/s004670100051

10.1034/j.1600-0854.2002.30801.x

10.1152/ajpcell.1990.259.6.C920

10.1083/jcb.111.2.379

Lu H., 2003, Heat shock protein 70 (Hsp70/Hsc70) is an aquaporin‐2 interacting protein and is involved in AQp2 endocytosis, J. Am. Soc. Nephrol, 14, 31A

10.1152/ajprenal.00179.2003

10.1074/jbc.M308285200

10.1146/annurev.physiol.63.1.607

10.1042/bj20031000

10.1124/mol.65.6.1507

10.1146/annurev.cellbio.19.110701.161425

10.1152/ajprenal.00291.2004

10.1074/jbc.M407351200

10.1073/pnas.90.24.11663

10.1073/pnas.92.4.1013

10.1152/physrev.00024.2001

10.1172/JCI118222

10.1074/jbc.274.45.32248

10.1006/excr.1998.4159

10.1096/fj.02-0870fje

10.1091/mbc.E04-04-0337

Russo L.M., 2004, Redistribution of aquaporin‐2 in the isolated perfused kidney following treatment with methyl beta cyclodextrin, J. Am. Soc. Nephrol, 15, 302A

10.1007/BF00233445

10.1091/mbc.01-08-0403

10.1093/ndt/gfh172

10.1093/ndt/15.suppl_6.21

10.1126/science.1063866

10.1172/JCI113534

10.1007/BF01871929

10.1152/ajprenal.00257.2001

10.1152/ajprenal.0091.2001

10.1083/jcb.200309175

10.1074/jbc.271.40.24365

Valenti G., 2000, The phosphatase inhibitor okadaic acid induces AQP2 translocation independently from AQP2 phosphorylation in renal collecting duct cells, J. Cell Sci., 113, 1985, 10.1242/jcs.113.11.1985

10.1074/jbc.M207525200

10.1074/jbc.M207339200

Yamamoto T., 1995, Localization and expression of a collecting duct water channel, aquaporin, in hydrated and dehydrated rats, Exp. Nephrol, 3, 193

10.1152/ajprenal.2000.278.3.F388

Thông tin
Thông tin xuất bản

Biology of the Cell

Tập 98 Số 4

215-232

Thông tin tác giả