The annexin 2-S100A10 complex and its association with TRPV6 is regulated by cAMP/PKA/CnA in airway and gut epithelia

Cell Calcium

Volumn 44, Issue 2, 2008, Pages 147-157

  Borthwick, Lee A ^a   Neal, Andy ^a   Hobson, Lynsey ^a   Gerke, Volker ^b   Robson, Louise ^a   Muimo, Richmond ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Annexin 2 S100A10; Calcineurin; Calcium; cAMP; Epithelia; PKA; PP2B; TRPV6

Indexed keywords

CALCINEURIN INHIBITOR; CALCIUM 45; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; FORSKOLIN; LIPOCORTIN 2; PROTEIN S 100; PROTEIN S 100A10; VANILLOID RECEPTOR 6;

ARTICLE; CALCIUM TRANSPORT; CELL STRAIN CACO 2; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPRECIPITATION; INTESTINE EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 45049086296     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2007.11.001     Document Type: Article

References (60)

1. Bradbury N.A., and Bridges R.J. Endocytosis is regulated by protein kinase A, but not protein kinase C in a secretory epithelial cell line. Biochem. Biophys. Res. Commun. 184 (1992) 1173-1180
2. Bradbury N.A., Jilling T., Berta G., Sorscher E.J., Bridges R.J., and Kirk K.L. Regulation of plasma membrane recycling by CFTR. Science 256 (1992) 530-532
3. Singh A.K., Tasken K., Walker W., Frizzell R.A., Watkins S.C., Bridges R.J., and Bradbury N.A. Characterization of PKA isoforms and kinase-dependent activation of chloride secretion in T84 cells. Am. J. Physiol. 275 (1998) C562-C570
4. Li M., McCann J.D., Liedtke C.M., Nairn A.C., Greengard P., and Welsh M.J. Cyclic AMP-dependent protein kinase opens chloride channels in normal but not cystic fibrosis airway epithelium. Nature 331 (1988) 358-360
5. Schoumacher R.A., Shoemaker R.L., Halm D.R., Tallant E.A., Wallace R.W., and Frizzell R.A. Phosphorylation fails to activate chloride channels from cystic fibrosis airway cells. Nature 330 (1987) 752-754
6. Nakamura T., and Gold G.H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325 (1987) 442-444
7. DiFrancesco D., and Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351 (1991) 145-147
8. Bos J.L., de Bruyn K., Enserink J., Kuiperij B., Rangarajan S., Rehmann H., Riedl J., de Rooij J., van Mansfeld F., and Zwartkruis F. The role of Rap1 in integrin-mediated cell adhesion. Biochem. Soc. Trans. 31 (2003) 83-86
9. Takahashi A., Watkins S.C., Howard M., and Frizzell R.A. CFTR-dependent membrane insertion is linked to stimulation of the CFTR chloride conductance. Am. J. Physiol. 271 (1996) C1887-C1894
10. Zhou J., Yi J., Hu N., George Jr. A.L., and Murray K.T. Activation of protein kinase a modulates trafficking of the human cardiac sodium channel in xenopus oocytes. Circ. Res. 87 (2000) 33-38
11. Winklhofer M., Matthias K., Seifert G., Stocker M., Sewing S., Herget T., Steinhauser C., and Saaler-Reinhardt S. Analysis of phosphorylation-dependent modulation of Kv1.1 potassium channels. Neuropharmacology 44 (2003) 829-842
12. Jacob R., Heine M., Eikemeyer J., Frerker N., Zimmer K.P., Rescher U., Gerke V., and Naim H.Y. Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 279 (2004) 3680-3684
13. Rety S., Sopkova J., Renouard M., Osterloh D., Gerke V., Tabaries S., Russo-Marie F., and Lewit-Bentley A. The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat. Struct. Biol. 6 (1999) 89-95
14. Gerke V., and Moss S.E. Annexins: from structure to function. Physiol. Rev. 82 (2002) 331-371
15. Gerke V., Creutz C.E., and Moss S.E. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6 (2005) 449-461
16. Eberhard D.A., Karns L.R., VandenBerg S.R., and Creutz C.E. Control of the nuclear-cytoplasmic partitioning of annexin II by a nuclear export signal and by p11 binding. J. Cell Sci. 114 (2001) 3155-3166
17. Harder T., Kellner R., Parton R.G., and Gruenberg J. Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8 (1997) 533-545
18. Nilius B., Gerke V., Prenen J., Szucs G., Heinke S., Weber K., and Droogmans G. Annexin II modulates volume-activated chloride currents in vascular endothelial cells. J. Biol. Chem. 271 (1996) 30631-30636
19. Girard C., Tinel N., Terrenoire C., Romey G., Lazdunski M., and Borsotto M. p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1. EMBO J. 21 (2002) 4439-4448
20. Okuse K., Malik-Hall M., Baker M.D., Poon W.Y., Kong H., Chao M.V., and Wood J.N. Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature 417 (2002) 653-656
21. van de Graaf S.F., Hoenderop J.G., Gkika D., Lamers D., Prenen J., Rescher U., Gerke V., Staub O., Nilius B., and Bindels R.J. Functional expression of the epithelial Ca(2+) channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex. EMBO J. 22 (2003) 1478-1487
22. Donier E., Rugiero F., Okuse K., and Wood J.N. Annexin II light chain p11 promotes functional expression of acid-sensing ion channel ASIC1a. J. Biol. Chem. 280 (2005) 38666-38672
23. Svenningsson P., Chergui K., Rachleff I., Flajolet M., Zhang X., El Yacoubi M., Vaugeois J.M., Nomikos G.G., and Greengard P. Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 311 (2006) 77-80
24. Renigunta V., Yuan H., Zuzarte M., Rinne S., Koch A., Wischmeyer E., Schlichthorl G., Gao Y., Karschin A., Jacob R., Schwappach B., Daut J., and Preisig-Muller R. The retention factor p11 confers an endoplasmic reticulum-localization signal to the potassium channel TASK-1. Traffic 7 (2006) 168-181
25. Borthwick L.A., McGaw J., Conner G., Taylor C.J., Gerke V., Mehta A., Robson L., and Muimo R. The formation of the cAMP/protein kinase A-dependent Annexin 2 S100A10 complex with cystic fibrosis conductance regulator protein (CFTR) regulates cftr channel function. Mol. Biol. Cell 18 (2007) 3388-3397
26. Thiel C., Osborn M., and Gerke V. The tight association of the tyrosine kinase substrate annexin II with the submembranous cytoskeleton depends on intact p11- and Ca(2+)-binding sites. J. Cell Sci. 103 (1992) 733-742
27. Gruenert D.C., Willems M., Cassiman J.J., and Frizzell R.A. Established cell lines used in cystic fibrosis research. J. Cyst. Fibros. 3 Suppl. 2 (2004) 191-196
28. Taparia S., Fleet J.C., Peng J.B., Wang X.D., and Wood R.J. 1,25-Dihydroxyvitamin D and 25-hydroxyvitamin D-mediated regulation of TRPV6 (a putative epithelial calcium channel) mRNA expression in Caco-2 cells. Eur. J. Nutr. 45 (2006) 196-204
29. Muimo R., Banner S.J., Marshall L.J., and Mehta A. Nucleoside diphosphate kinase and Cl(-)-sensitive protein phosphorylation in apical membranes from ovine airway epithelium. Am. J. Respir. Cell Mol. Biol. 18 (1998) 270-278
30. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
31. Weber K. Annexin II: interaction with p11. In: Moss S.E. (Ed). The Annexins-Portland Press Research Monograph (1992), Portland Press, London & Chapel Hill 61-68
32. Jost M., and Gerke V. Mapping of a regulatory important site for protein kinase C phosphorylation in the N-terminal domain of annexin II. Biochim. Biophys. Acta 1313 (1996) 283-289
33. Johnsson N., Nguyen Van P., Soling H.D., and Weber K. Functionally distinct serine phosphorylation sites of p36, the cellular substrate of retroviral protein kinase; differential inhibition of reassociation with p11. EMBO J. 5 (1986) 3455-3460
34. Hoenderop J.G., De Pont J.J., Bindels R.J., and Willems P.H. Hormone-stimulated Ca2+ reabsorption in rabbit kidney cortical collecting system is cAMP-independent and involves a phorbol ester-insensitive PKC isotype. Kidney Int. 55 (1999) 225-233
35. Nijenhuis T., Hoenderop J.G.J., van der Kemp A.W.C.M., and Bindels R.J.M. Localization and regulation of the epithelial Ca2+ channel TRPV6 in the kidney. J. Am. Soc. Nephrol. 14 (2003) 2731-2740
36. den Dekker E., Hoenderop J.G., Nilius B., and Bindels R.J. The epithelial calcium channels, TRPV5 & TRPV6: from identification towards regulation. Cell Calcium 33 (2003) 497-507
37. Owsianik G., Talavera K., Voets T., and Nilius B. Permeation and selectivity of TRP channels. Annu. Rev. Physiol. 68 (2006) 685-717
38. Chasserot-Golaz S., Vitale N., Sagot I., Delouche B., Dirrig S., Pradel L.A., Henry J.P., Aunis D., and Bader M.F. Annexin II in exocytosis: catecholamine secretion requires the translocation of p36 to the subplasmalemmal region in chromaffin cells. J. Cell Biol. 133 (1996) 1217-1236
39. Massheimer V., Boland R., and de Boland A.R. Rapid 1,25(OH)2-vitamin D3 stimulation of calcium uptake by rat intestinal cells involves a dihydropyridine-sensitive cAMP-dependent pathway. Cell Signal 6 (1994) 299-304
40. Gkika D., Topala C.N., Hoenderop J.G., and Bindels R.J. The immunophilin FKBP52 inhibits the activity of the epithelial Ca2+ channel TRPV5. Am. J. Physiol. Renal Physiol. 290 (2006) F1253-F1259
41. Wissenbach U., Niemeyer B., Himmerkus N., Fixemer T., Bonkhoff H., and Flockerzi V. TRPV6 and prostate cancer: cancer growth beyond the prostate correlates with increased TRPV6 Ca2+ channel expression. Biochem. Biophys. Res. Commun. 322 (2004) 1359-1363
42. Prevarskaya N., Zhang L., and Barritt G. TRP channels in cancer. Biochim. Biophys. Acta 1772 (2007) 937-946
43. Lehen'kyi V., Flourakis M., Skryma R., and Prevarskaya N. TRPV6 channel controls prostate cancer cell proliferation via Ca(2+)/NFAT-dependent pathways. Oncogene (2007)
44. Rescher U., and Gerke V. S100A10/p11: family, friends and functions. Pflug. Arch. (2007)
45. Arniges M., Vazquez E., Fernandez-Fernandez J.M., and Valverde M.A. Swelling-activated Ca2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J. Biol. Chem. 279 (2004) 54062-54068
46. Feschenko M.S., Stevenson E., Nairn A.C., and Sweadner K.J. A novel cAMP-stimulated pathway in protein phosphatase 2A activation. J. Pharmacol. Exp. Ther. 302 (2002) 111-118
47. Webster C.R.L., Blanch C., and Anwer M.S. Role of PP2B in cAMP-induced dephosphorylation and translocation of NTCP. Am. J. Physiol. Gastrointest. Liver Physiol. 283 (2002) G44-G50
48. Klee C.B., Ren H., and Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 273 (1998) 13367-13370
49. Deora A.B., Kreitzer G., Jacovina A.T., and Hajjar K.A. An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J. Biol. Chem. 279 (2004) 43411-43418
50. Matsuda D., Nakayama Y., Horimoto S., Kuga T., Ikeda K., Kasahara K., and Yamaguchi N. Involvement of Golgi-associated Lyn tyrosine kinase in the translocation of annexin II to the endoplasmic reticulum under oxidative stress. Exp. Cell Res. 312 (2006) 1205-1217
51. Mailliard W.S., Haigler H.T., and Schlaepfer D.D. Calcium-dependent binding of S100C to the N-terminal domain of annexin I. J. Biol. Chem. 271 (1996) 719-725
52. Tomas A., and Moss S.E. Calcium- and cell cycle-dependent association of annexin 11 with the nuclear envelope. J. Biol. Chem. 278 (2003) 20210-20216
53. Garbuglia M., Verzini M., and Donato R. Annexin VI binds S100A1 and S100B and blocks the ability of S100A1 and S100B to inhibit desmin and GFAP assemblies into intermediate filaments. Cell Calcium 24 (1998) 177-191
54. Gerke V., and Weber K. The regulatory chain in the p36-kd substrate complex of viral tyrosine-specific protein kinases is related in sequence to the S-100 protein of glial cells. EMBO J. 4 (1985) 2917-2920
55. Jost M., Weber K., and Gerke V. Annexin II contains two types of Ca(2+)-binding sites. Biochem. J. 298 Pt 3 (1994) 553-559
56. Ayala-Sanmartin J., Vincent M., Sopkova J., and Gallay J. Modulation by Ca(2+) and by membrane binding of the dynamics of domain III of annexin 2 (p36) and the annexin 2-p11 complex (p90): implications for their biochemical properties. Biochemistry 39 (2000) 15179-15189
57. Powell M.A., and Glenney J.R. Regulation of calpactin I phospholipid binding by calpactin I light-chain binding and phosphorylation by p60v-src. Biochem. J. 247 (1987) 321-328
58. Konig J., Prenen J., Nilius B., and Gerke V. The annexin II-p11 complex is involved in regulated exocytosis in bovine pulmonary artery endothelial cells. J. Biol. Chem. 273 (1998) 19679-19684
59. Becker T., Weber K., and Johnsson N. Protein-protein recognition via short amphiphilic helices; a mutational analysis of the binding site of annexin II for p11. EMBO J. 9 (1990) 4207-4213
60. Knop M., Aareskjold E., Bode G., and Gerke V. Rab3D and annexin A2 play a role in regulated secretion of vWF, but not tPA, from endothelial cells. EMBO J. 23 (2004) 2982-2992