CAMP signalling protects proximal tubular epithelial cells from cisplatin-induced apoptosis via activation of Epac

British Journal of Pharmacology

Volumn 165, Issue 4 B, 2012, Pages 1137-1150

  Qin, Yu ^a   Stokman, Geurt ^a   Yan, Kuan ^b   Ramaiahgari, Sreenivasa ^a   Verbeek, Fons ^b   De Graauw, Marjo ^a   Van De Water, Bob ^a   Price, Leo S ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

cAMP signalling; cell apoptosis; cell cell junction; cisplatin nephrotoxicity; Epac Rap activation; proximal tubular epithelium

Indexed keywords

BETA CATENIN; CASPASE 3; CISPLATIN; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; RAP PROTEIN; RAP1 PROTEIN; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL ISOLATION; CELL JUNCTION; CELL MEMBRANE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TIGHT JUNCTION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BETA CATENIN; CASPASE 3; CELL LINE; CELL LINE, TUMOR; CISPLATIN; CYCLIC AMP; EPITHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; KIDNEY TUBULES, PROXIMAL; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PHOSPHOPROTEINS; RAP1 GTP-BINDING PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84856360059     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01594.x     Document Type: Article

References (64)

1. Arany I, Herbert J, Herbert Z, Safirstein RL, (2008). Restoration of CREB function ameliorates cisplatin cytotoxicity in renal tubular cells. Am J Physiol Renal Physiol 294: F577-F581. (Pubitemid 351442228)
2. Atzpodien J, Terfloth K, Fluck M, Reitz M, (2007). Cisplatin, gemcitabine, and treosulfan in relapsed stage IV cutaneous malignant melanoma patients. Br J Cancer 97: 1329-1332. (Pubitemid 350114793)
3. Boettner B, Van Aelst L, (2009). Control of cell adhesion dynamics by Rap1 signaling. Curr Opin Cell Biol 21: 684-693.
4. Bos JL, de Rooij J, Reedquist KA, (2001). Rap1 signalling: adhering to new models. Nat Rev Mol Cell Biol 2: 369-377. (Pubitemid 33674049)
5. Bosl GJ, Motzer RJ, (1997). Testicular germ-cell cancer. N Engl J Med 337: 242-253.
6. Caron E, Self AJ, Hall A, (2000). The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr Biol 10: 974-978.
7. Cheng X, Ji Z, Tsalkova T, Mei F, (2008). Epac and PKA: a tale of two intracellular cAMP receptors. Acta Biochim Biophys Sin (Shanghai) 40: 651-662. (Pubitemid 352009080)
8. Cordes N, (2006). Integrin-mediated cell-matrix interactions for prosurvival and antiapoptotic signaling after genotoxic injury. Cancer Lett 242: 11-19. (Pubitemid 44485301)
9. Decatris MP, Sundar S, O'Byrne KJ, (2004). Platinum-based chemotherapy in metastatic breast cancer: current status. Cancer Treat Rev 30: 53-81. (Pubitemid 38240088)
10. Drubin DG, Nelson WJ, (1996). Origins of cell polarity. Cell 84: 335-344. (Pubitemid 26058559)
11. Dube N, Kooistra MR, Pannekoek WJ, Vliem MJ, Oorschot V, Klumperman J, et al,. (2008). The RapGEF PDZ-GEF2 is required for maturation of cell-cell junctions. Cell Signal 20: 1608-1615.
12. Enserink JM, Christensen AE, de Rooij J, van Triest M, Schwede F, Genieser HG, et al,. (2002). A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 4: 901-906. (Pubitemid 35331366)
13. Enserink JM, Price LS, Methi T, Mahic M, Sonnenberg A, Bos JL, et al,. (2004). The cAMP-Epac-Rap1 pathway regulates cell spreading and cell adhesion to laminin-5 through the alpha3beta1 integrin but not the alpha6beta4 integrin. J Biol Chem 279: 44889-44896. (Pubitemid 39430901)
14. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, et al,. (2005). Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 25: 136-146. (Pubitemid 40039806)
15. de Graauw M, Tijdens I, Cramer R, Corless S, Timms JF, van de Water B, (2005). Heat shock protein 27 is the major differentially phosphorylated protein involved in renal epithelial cellular stress response and controls focal adhesion organization and apoptosis. J Biol Chem 280: 29885-29898. (Pubitemid 41177066)
16. de Graauw M, van Miltenburg MH, Schmidt MK, Pont C, Lalai R, Kartopawiro J, et al,. (2010). Annexin A1 regulates TGF-beta signaling and promotes metastasis formation of basal-like breast cancer cells. Proc Natl Acad Sci USA 107: 6340-6345.
17. Hodkinson PS, Mackinnon AC, Sethi T, (2007). Extracellular matrix regulation of drug resistance in small-cell lung cancer. Int J Radiat Biol 83: 733-741. (Pubitemid 350219111)
18. Hogan C, Serpente N, Cogram P, Hosking CR, Bialucha CU, Feller SM, et al,. (2004). Rap1 regulates the formation of E-cadherin-based cell-cell contacts. Mol Cell Biol 24: 6690-6700. (Pubitemid 38944348)
19. Holz GG, Chepurny OG, Schwede F, (2008). Epac-selective cAMP analogs: new tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell Signal 20: 10-20. (Pubitemid 350138365)
20. Honegger KJ, Capuano P, Winter C, Bacic D, Stange G, Wagner CA, et al,. (2006). Regulation of sodium-proton exchanger isoform 3 (NHE3) by PKA and exchange protein directly activated by cAMP (EPAC). Proc Natl Acad Sci USA 103: 803-808. (Pubitemid 43153106)
21. Imamdi R, de Graauw M, van de Water B, (2004). Protein kinase C mediates cisplatin-induced loss of adherens junctions followed by apoptosis of renal proximal tubular epithelial cells. J Pharmacol Exp Ther 311: 892-903. (Pubitemid 39612693)
22. Iwatsubo K, Minamisawa S, Tsunematsu T, Nakagome M, Toya Y, Tomlinson JE, et al,. (2004). Direct inhibition of type 5 adenylyl cyclase prevents myocardial apoptosis without functional deterioration. J Biol Chem 279: 40938-40945. (Pubitemid 39287693)
23. Jandial DD, Farshchi-Heydari S, Larson CA, Elliott GI, Wrasidlo WJ, Howell SB, (2009). Enhanced delivery of cisplatin to intraperitoneal ovarian carcinomas mediated by the effects of bortezomib on the human copper transporter 1. Clin Cancer Res 15: 553-560.
24. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, et al,. (1998). A family of cAMP-binding proteins that directly activate Rap1. Science 282: 2275-2279. (Pubitemid 29004080)
25. Khuri FR, Nemunaitis J, Ganly I, Arseneau J, Tannock IF, Romel L, et al,. (2000). a controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat Med 6: 879-885. (Pubitemid 30644745)
26. Knox AL, Brown NH, (2002). Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 295: 1285-1288. (Pubitemid 34157618)
27. Kooistra MR, Corada M, Dejana E, Bos JL, (2005). Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett 579: 4966-4972. (Pubitemid 41242837)
28. Kruidering M, van de Water B, Zhan Y, Baelde JJ, Heer E, Mulder GJ, et al,. (1998). Cisplatin effects on F-actin and matrix proteins precede renal tubular cell detachment and apoptosis in vitro. Cell Death Differ 5: 601-614. (Pubitemid 28356582)
29. Kwak HJ, Park KM, Choi HE, Chung KS, Lim HJ, Park HY, (2008). PDE4 inhibitor, roflumilast protects cardiomyocytes against NO-induced apoptosis via activation of PKA and Epac dual pathways. Cell Signal 20: 803-814.
30. Kwon G, Pappan KL, Marshall CA, Schaffer JE, McDaniel ML, (2004). cAMP Dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem 279: 8938-8945. (Pubitemid 38295955)
31. Lewis JM, Truong TN, Schwartz MA, (2002). Integrins regulate the apoptotic response to DNA damage through modulation of p53. Proc Natl Acad Sci USA 99: 3627-3632. (Pubitemid 34252157)
32. Li Y, Konings IB, Zhao J, Price LS, de Heer E, Deen PM, (2008). Renal expression of exchange protein directly activated by cAMP (Epac) 1 and 2. Am J Physiol Renal Physiol 295: F525-F533.
33. Li M, Balamuthusamy S, Khan AM, Maderdrut JL, Simon EE, Batuman V, (2010). Pituitary adenylate cyclase-activating polypeptide ameliorates cisplatin-induced acute kidney injury. Peptides 31: 592-602.
34. Lieberthal W, Triaca V, Levine J, (1996). Mechanisms of death induced by cisplatin in proximal tubular epithelial cells: apoptosis vs. necrosis. Am J Physiol 270: F700-F708.
35. Livak KJ, Schmittgen TD, (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
36. Lyle KS, Raaijmakers JH, Bruinsma W, Bos JL, de Rooij J, (2008). cAMP-induced Epac-Rap activation inhibits epithelial cell migration by modulating focal adhesion and leading edge dynamics. Cell Signal 20: 1104-1116.
37. Ma SF, Nishikawa M, Hyoudou K, Takahashi R, Ikemura M, Kobayashi Y, et al,. (2007). Combining cisplatin with cationized catalase decreases nephrotoxicity while improving antitumor activity. Kidney Int 72: 1474-1482. (Pubitemid 350197948)
38. McPhee I, Houslay MD, Yarwood SJ, (2000). Use of an activation-specific probe to show that Rap1A and Rap1B display different sensitivities to activation by forskolin in rat1 cells. FEBS Lett 477: 213-218. (Pubitemid 30450169)
39. Mathe C, Bohacs A, Duffek L, Lukacsovits J, Komlosi ZI, Szondy K, et al,. (2011). Cisplatin nephrotoxicity aggravated by cardiovascular disease and diabetes in lung cancer patients. Eur Respir J 37: 888-894.
40. Mays RW, Nelson WJ, Marrs JA, (1995). Generation of epithelial cell polarity: roles for protein trafficking, membrane-cytoskeleton, and E-cadherin-mediated cell adhesion. Cold Spring Harb Symp Quant Biol 60: 763-773.
41. Meredith JE Jr, Schwartz MA, (1997). Integrins, adhesion and apoptosis. Trends Cell Biol 7: 146-150. (Pubitemid 27135573)
42. Mishima K, Baba A, Matsuo M, Itoh Y, Oishi R, (2006). Protective effect of cyclic AMP against cisplatin-induced nephrotoxicity. Free Radic Biol Med 40: 1564-1577.
43. Murtazina R, Kovbasnjuk O, Zachos NC, Li X, Chen Y, Hubbard A, et al,. (2007). Tissue-specific regulation of sodium/proton exchanger isoform 3 activity in Na(+)/H(+) exchanger regulatory factor 1 (NHERF1) null mice. cAMP inhibition is differentially dependent on NHERF1 and exchange protein directly activated by cAMP in ileum versus proximal tubule. J Biol Chem 282: 25141-25151. (Pubitemid 47347544)
44. Nagai N, Kinoshita M, Ogata H, Tsujino D, Wada Y, Someya K, et al,. (1996). Relationship between pharmacokinetics of unchanged cisplatin and nephrotoxicity after intravenous infusions of cisplatin to cancer patients. Cancer Chemother Pharmacol 39: 131-137. (Pubitemid 26400671)
45. Noda K, Zhang J, Fukuhara S, Kunimoto S, Yoshimura M, Mochizuki N, (2010). Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through alpha- and beta-catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells. Mol Biol Cell 21: 584-596.
46. Price LS, Hajdo-Milasinovic A, Zhao J, Zwartkruis FJ, Collard JG, Bos JL, (2004). Rap1 regulates E-cadherin-mediated cell-cell adhesion. J Biol Chem 279: 35127-35132. (Pubitemid 39100508)
47. Rampersad SN, Ovens JD, Huston E, Umana MB, Wilson LS, Netherton SJ, et al,. (2010). Cyclic AMP phosphodiesterase 4D (PDE4D) Tethers EPAC1 in a vascular endothelial cadherin (VE-Cad)-based signaling complex and controls cAMP-mediated vascular permeability. J Biol Chem 285: 33614-33622.
48. Rangarajan S, Enserink JM, Kuiperij HB, de Rooij J, Price LS, Schwede F, et al,. (2003). Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol 160: 487-493. (Pubitemid 36254387)
49. Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, et al,. (2000). The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol 148: 1151-1158.
50. Rehmann H, Das J, Knipscheer P, Wittinghofer A, Bos JL, (2006). Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature 439: 625-628. (Pubitemid 43185390)
51. Rehmann H, Arias-Palomo E, Hadders MA, Schwede F, Llorca O, Bos JL, (2008). Structure of Epac2 in complex with a cyclic AMP analogue and RAP1B. Nature 455: 124-127.
52. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, et al,. (1998). Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396: 474-477. (Pubitemid 28553318)
53. Severson EA, Lee WY, Capaldo CT, Nusrat A, Parkos CA, (2009). Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate beta1 integrin levels, and enhance cell migration. Mol Biol Cell 20: 1916-1925.
54. Somekawa S, Fukuhara S, Nakaoka Y, Fujita H, Saito Y, Mochizuki N, (2005). Enhanced functional gap junction neoformation by protein kinase A-dependent and Epac-dependent signals downstream of cAMP in cardiac myocytes. Circ Res 97: 655-662. (Pubitemid 41416334)
55. Stokman G, Qin Y, Genieser HG, Schwede F, de Heer E, Bos JL, et al,. (2011). Epac-rap signaling reduces cellular stress and ischemia-induced kidney failure. J Am Soc Nephrol 22: 859-872.
56. Suzuki S, Yokoyama U, Abe T, Kiyonari H, Yamashita N, Kato Y, et al,. (2010). Differential roles of Epac in regulating cell death in neuronal and myocardial cells. J Biol Chem 285: 24248-24259.
57. Thadhani R, Pascual M, Bonventre JV, (1996). Acute renal failure. N Engl J Med 334: 1448-1460. (Pubitemid 126590563)
58. Townsend DM, Deng M, Zhang L, Lapus MG, Hanigan MH, (2003). Metabolism of Cisplatin to a nephrotoxin in proximal tubule cells. J Am Soc Nephrol 14: 1-10. (Pubitemid 36026291)
59. Truong T, Sun G, Doorly M, Wang JY, Schwartz MA, (2003). Modulation of DNA damage-induced apoptosis by cell adhesion is independently mediated by p53 and c-Abl. Proc Natl Acad Sci USA 100: 10281-10286. (Pubitemid 37071869)
60. Ulucan C, Wang X, Baljinnyam E, Bai Y, Okumura S, Sato M, et al,. (2007). Developmental changes in gene expression of Epac and its upregulation in myocardial hypertrophy. Am J Physiol Heart Circ Physiol 293: H1662-H1672. (Pubitemid 47367213)
61. Vickers AE, Rose K, Fisher R, Saulnier M, Sahota P, Bentley P, (2004). Kidney slices of human and rat to characterize cisplatin-induced injury on cellular pathways and morphology. Toxicol Pathol 32: 577-590. (Pubitemid 39258463)
62. Vliem MJ, Ponsioen B, Schwede F, Pannekoek WJ, Riedl J, Kooistra MR, et al,. (2008). 8-pCPT-2′-O-Me-cAMP-AM: an improved Epac-selective cAMP analogue. Chembiochem 9: 2052-2054.
63. Winton T, Livingston R, Johnson D, Rigas J, Johnston M, Butts C, et al,. (2005). Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 352: 2589-2597. (Pubitemid 41007845)
64. Wittchen ES, Worthylake RA, Kelly P, Casey PJ, Quilliam LA, Burridge K, (2005). Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J Biol Chem 280: 11675-11682. (Pubitemid 40418482)