17β-Oestradiol inhibits doxorubicin-induced apoptosis via block of the volume-sensitive Cl - current in rabbit articular chondrocytes

British Journal of Pharmacology

Volumn 166, Issue 2, 2012, Pages 702-720

  Kumagai, Kousuke ^a   Imai, Shinji ^a   Toyoda, Futoshi ^a   Okumura, Noriaki ^a   Isoya, Eiji ^a   Matsuura, Hiroshi ^a   Matsusue, Yoshitaka ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

17 oestradiol; apoptosis; caspase; chondrocyte; doxorubicin; osteoarthritis; volume sensitive Cl current

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; CASPASE 7; DOXORUBICIN; ESTRADIOL; FULVESTRANT; MEMBRANE RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; TESTOSTERONE; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL SWELLING; CHLORIDE CURRENT; CONTROLLED STUDY; MEMBRANE CURRENT; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RABBIT;

ANIMALS; APOPTOSIS; CARTILAGE, ARTICULAR; CASPASE 3; CASPASE 7; CELLS, CULTURED; CHLORIDES; CHONDROCYTES; DOXORUBICIN; ESTRADIOL; ESTROGENS; MALE; NADPH OXIDASE; PATCH-CLAMP TECHNIQUES; PHOSPHATIDYLINOSITOL 3-KINASES; RABBITS; REACTIVE OXYGEN SPECIES;

EID: 84859909950     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01802.x     Document Type: Article

References (72)

1. Adams CS, Shapiro IM, (2002). The fate of the terminally differentiated chondrocyte: evidence for microenvironmental regulation of chondrocyte apoptosis. Crit Rev Oral Biol Med 13: 465-473. (Pubitemid 36570020)
2. Alexander SPH, Mathie A, Peters JA, (2011). Guide to Receptors and Channels (GRAC), 5th Edition. Br J Pharmacol 164 (Suppl. 1): S1-S324.
3. Almeida M, Martin-Millan M, Ambrogini E, Bradsher R 3rd, Han L, Chen X-D, et al,. (2010). Estrogens attenuate oxidative stress and the differentiation and apoptosis of osteoblasts by DNA-binding-independent actions of the ERα. J Bone Miner Res 25: 769-781.
4. Cl,vol) mediate doxorubicin-induced apoptosis through apoptotic volume decrease in cardiomyocytes. Fundam Clin Pharmacol 18: 531-538. (Pubitemid 39468961)
5. Bénitah JP, Gomez AM, Bailly P, Da Ponte JP, Berson G, Delgado C, et al,. (1993). Heterogeneity of the early outward current in ventricular cells isolated from normal and hypertrophied rat hearts. J Physiol 469: 111-138. (Pubitemid 23281572)
6. Bernard GR, Lucht WD, Niedermeyer ME, Snapper JR, Olgetree ML, Brigham KL, (1984). Effects of N-acetylcysteine on pulmonary response to endotoxin in the awake sheep and upon in vitro granulocyte function. J Clin Invest 73: 1772-1784. (Pubitemid 14084495)
7. Björnström L, Sjöberg M, (2005). Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19: 833-842. (Pubitemid 40397050)
8. Blanco FJ, Ochs RL, Schwarz H, Lotz M, (1995). Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 146: 75-85.
9. Blanco FJ, Guitian R, Vázquez-Martul E, de Toro FJ, Galdo F, (1998). Osteoarthritis chondrocytes die by apoptosis. A possible pathway for osteoarthritis pathology. Arthritis Rheum 41: 284-289. (Pubitemid 28087696)
10. Bortner CD, Cidlowski JA, (1998). A necessary role for cell shrinkage in apoptosis. Biochem Pharmacol 56: 1549-1559. (Pubitemid 28561474)
11. Bortner CD, Cidlowski JA, (2007). Cell shrinkage and monovalent cation fluxes: role in apoptosis. Arch Biochem Biophys 462: 176-188. (Pubitemid 46863418)
12. - current elicited by β1 integrin stretch in rabbit ventricular myocytes. J Gen Physiol 124: 273-287. (Pubitemid 39244526)
13. Browe DM, Baumgarten CM, (2006). EGFR kinase regulates volume-sensitive chloride current elicited by integrin stretch via PI-3K and NADPH oxidase in ventricular myocytes. J Gen Physiol 127: 237-251.
14. Bush PG, Hall AC, (2001). Regulatory volume decrease (RVD) by isolated and in situ bovine articular chondrocytes. J Cell Physiol 187: 304-314. (Pubitemid 32378355)
15. Cannon CL, Basavappa S, Strange K, (1998). Intracellular ionic strength regulates the volume sensitivity of a swelling-activated anion channel. Am J Physiol 275: C416-C422.
16. 1-Integrin-collagen interaction reduces chondrocyte apoptosis. Matrix Biol 18: 343-355. (Pubitemid 29397446)
17. Castoria G, Migliaccio A, Bilancio A, Di Domenico M, de Falco A, Lombardi M, et al,. (2001). PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. EMBO J 20: 6050-6059. (Pubitemid 33049280)
18. Chen W, Gabel S, Steenbergen C, Murphy E, (1995). A redox-based mechanism for cardioprotection induced by ischemic preconditioning in perfused rat heart. Circ Res 77: 424-429.
19. Cl,swell and prevents swelling-induced shortening of guinea-pig atrial action potential duration. Br J Pharmacol 134: 1467-1479. (Pubitemid 33131898)
20. - current via NADPH oxidase and mitochondrial reactive oxygen species. Cardiovasc Res 88: 93-100.
21. Fabiato A, Fabiato F, (1979). Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75: 463-505. (Pubitemid 10241310)
22. Falkenstein E, Tillmann HC, Christ M, Feuring M, Wehling M, (2000). Multiple actions of steroid hormones-a focus on rapid, nongenomic effects. Pharmacol Rev 52: 513-555.
23. Feranchak AP, Roman RM, Schwiebert EM, Fitz JG, (1998). Phosphatidylinositol 3-kinase contributes to cell volume regulation through effects on ATP release. J Biol Chem 273: 14906-14911. (Pubitemid 28272780)
24. Garcia-Calvo M, Peterson EP, Rasper DM, Vaillancourt JP, Zamboni R, Nicholson DW, et al,. (1999). Purification and catalytic properties of human caspase family members. Cell Death Differ 6: 362-369. (Pubitemid 29186880)
25. Gatson JW, Kaur P, Singh M, (2006). Dihydrotestosterone differentially modulates the mitogen-activated protein kinase and the phosphoinositide 3-kinase/Akt pathways through the nuclear and novel membrane androgen receptor in C6 cells. Endocrinology 147: 2028-2034.
26. Goggs R, Carter SD, Schulze-Tanzil G, Shakibaei M, Mobasheri A, (2003). Apoptosis and the loss of chondrocyte survival signals contribute to articular cartilage degradation in osteoarthritis. Vet J 166: 140-158. (Pubitemid 37554969)
27. Gokhale JA, Frenkel SR, Dicesare PE, (2004). Estrogen and osteoarthritis. Am J Orthop 33: 71-80.
28. Hall AC, (1995). Volume-sensitive taurine transport in bovine articular chondrocytes. J Physiol 484: 755-766.
29. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ, (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391: 85-100. (Pubitemid 11012976)
30. Hampton MB, Winterbourn CC, (1995). Modification of neutrophil oxidant production with diphenyleneiodonium and its effect on bacterial killing. Free Radic Biol Med 18: 633-639.
31. - channels. J Physiol 587: 2127-2139.
32. Hashimoto S, Ochs RL, Komiya S, Lotz M, (1998). Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Arthritis Rheum 41: 1632-1638. (Pubitemid 28459922)
33. Hoffmann EK, (2000). Intracellular signalling involved in volume regulatory decrease. Cell Physiol Biochem 10: 273-288. (Pubitemid 32012400)
34. Honda K, Shimohama S, Sawada H, Kihara T, Nakamizo T, Shibasaki H, et al,. (2001). Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. J Neurosci Res 64: 466-475. (Pubitemid 32521766)
35. Hume JR, Duan D, Collier ML, Yamazaki J, Horowitz B, (2000). Anion transport in heart. Physiol Rev 80: 31-81. (Pubitemid 30060561)
36. - current in isolated rabbit articular chondrocytes: inhibition by arachidonic acid. J Pharmacol Sci 109: 293-304.
37. Kalyanaraman B, Joseph J, Kalivendi S, Wang S, Konorev E, Kotamraju S, (2002). Doxorubicin-induced apoptosis: implications in cardiotoxicity. Mol Cell Biochem 234-235: 119-124. (Pubitemid 34777848)
38. Kim JK, Pedram A, Razandi M, Levin ER, (2006). Estrogen prevents cardiomyocyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J Biol Chem 281: 6760-6767. (Pubitemid 43847612)
39. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, et al,. (2001). Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104: 19-30.
40. Kr channels and drug-induced prolongation of cardiac repolarization. J Physiol 586: 2961-2973. (Pubitemid 351837288)
41. Lewis RS, Ross PE, Cahalan MD, (1993). Chloride channels activated by osmotic stress in T lymphocytes. J Gen Physiol 101: 801-826. (Pubitemid 23175827)
42. Lo MY, Kim HT, (2004). Chondrocyte apoptosis induced by hydrogen peroxide requires caspase activation but not mitochondrial pore transition. J Orthop Res 22: 1120-1125. (Pubitemid 39145132)
43. Lotz M, Hashimoto S, Kuhn K, (1999). Mechanisms of chondrocyte apoptosis. Osteoarthritis Cartilage 7: 389-391. (Pubitemid 29331557)
44. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y, (2000). Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97: 9487-9492. (Pubitemid 30650802)
45. Martina M, Mozrzymas JW, Vittur F, (1997). Membrane stretch activates a potassium channel in pig articular chondrocytes. Biochim Biophys Acta 1329: 205-210. (Pubitemid 27466809)
46. Mizutani H, Tada-Oikawa S, Hiraku Y, Kojima M, Kawanishi S, (2005). Mechanism of apoptosis induced by doxorubicin through the generation of hydrogen peroxide. Life Sci 76: 1439-1453. (Pubitemid 40164773)
47. Mobasheri A, (2002). Role of chondrocyte death and hypocellularity in ageing human articular cartilage and the pathogenesis of osteoarthritis. Med Hypotheses 58: 193-197. (Pubitemid 34664889)
48. Mukhopadhyay P, Rajesh M, Bátkai S, Kashiwaya Y, Haskõ G, Liaudet L, et al,. (2009). Role of superoxide, nitric oxide, and peroxynitrite in doxorubicin-induced cell death in vivo and in vitro. Am J Physiol 296: H1466-H1483.
49. Nicholson DW, Thornberry NA, (1997). Caspases: killer proteases. Trends Biochem Sci 22: 299-306. (Pubitemid 27327087)
50. Okada Y, Shimizu T, Maeno E, Tanabe S, Wang X, Takahashi N, (2006). Volume-sensitive chloride channels involved in apoptotic volume decrease and cell death. J Membr Biol 209: 21-29. (Pubitemid 43725454)
51. Okada Y, Sato K, Numata T, (2009). Pathophysiology and puzzles of the volume-sensitive outwardly rectifying anion channel. J Physiol 587: 2141-2149.
52. Okumura N, Imai S, Toyoda F, Isoya E, Kumagai K, Matsuura H, et al,. (2009). Regulatory role of tyrosine phosphorylation in the swelling-activated chloride current in isolated rabbit articular chondrocytes. J Physiol 587: 3761-3776.
53. Olsen H, ter Veld F, Herbrand U, Ahmadian MR, Kinne RK, Wehner F, (2007). Differential regulation of cell volume and shape in confluent rat hepatocytes under hypertonic stress. Cell Physiol Biochem 19: 259-268. (Pubitemid 46701501)
54. Roman-Blas JA, Castaneda S, Largo R, Herrero-Beaumont G, (2009). Osteoarthritis associated with estrogen deficiency. Arthritis Res Ther 11: 241.
55. - current in guinea-pig atrial myocytes: inhibition by glibenclamide. J Physiol 505: 41-52. (Pubitemid 27504280)
56. Saraste A, Pulkki K, (2000). Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45: 528-537. (Pubitemid 30047119)
57. Schliess F, von Dahl S, Haussinger D, (2001). Insulin resistance induced by loop diuretics and hyperosmolarity in perfused rat liver. Biol Chem 382: 1063-1069. (Pubitemid 32750603)
58. - channel. Proc Natl Acad Sci USA 101: 6770-6773. (Pubitemid 38586049)
59. Sniekers YH, Weinans H, Bierma-Zeinstra SM, van Leeuwen JP, van Osch GJ, (2008). Animal models for osteoarthritis: the effect of ovariectomy and estrogen treatment-a systematic approach. Osteoarthritis Cartilage 16: 533-541.
60. Souktani R, Berdeaux A, Ghaleh B, Giudicelli JF, Guize L, Le Heuzey JY, et al,. (2000). Induction of apoptosis using sphingolipids activates a chloride current in Xenopus laevis oocytes. Am J Physiol 279: C158-C165. (Pubitemid 30616630)
61. Sugimoto T, Yoshino M, Nagao M, Ishii S, Yabu H, (1996). Voltage-gated ionic channels in cultured rabbit articular chondrocytes. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 115: 223-232. (Pubitemid 27013436)
62. Takano H, Aizawa T, Irie T, Kokubun S, Itoi E, (2007). Estrogen deficiency leads to decrease in chondrocyte numbers in the rabbit growth plate. J Orthop Sci 12: 366-374. (Pubitemid 47174857)
63. Tokudome T, Horio T, Yoshihara F, Suga S, Kawano Y, Kohno M, et al,. (2002). Adrenomedullin inhibits doxorubicin-induced cultured rat cardiac myocyte apoptosis via a cAMP-dependent mechanism. Endocrinology 143: 3515-3521. (Pubitemid 34925726)
64. Tsang WP, Chau SP, Kong SK, Fung KP, Kwok TT, (2003). Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci 73: 2047-2058. (Pubitemid 36930039)
65. Tsien RY, Rink TJ, (1980). Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim Biophys Acta 599: 623-638.
66. 2 signals chloride channel activation in cell volume regulation and cell proliferation. J Biol Chem 279: 13301-13304. (Pubitemid 38468851)
67. Vittur F, Grandolfo M, Fragonas E, Godeas C, Paoletti S, Pollesello P, et al,. (1994). Energy metabolism, replicative ability, intracellular calcium concentration, and ionic channels of horse articular chondrocytes. Exp Cell Res 210: 130-136. (Pubitemid 24168505)
68. Voets T, Manolopoulos V, Eggermont J, Elory C, Droogmans G, Nilius B, (1998). Regulation of a swelling-activated chloride current in bovine endothelium by protein tyrosine phosphorylation and G proteins. J Physiol 506: 341-352. (Pubitemid 28048364)
69. Wagner BA, Evig CB, Reszka KJ, Buettner GR, Burns CP, (2005). Doxorubicin increases intracellular hydrogen peroxide in PC3 prostate cancer cells. Arch Biochem Biophys 440: 181-190. (Pubitemid 41140383)
70. Wang X, Takahashi N, Uramoto H, Okada Y, (2005). Chloride channel inhibition prevents ROS-dependent apoptosis induced by ischemia-reperfusion in mouse cardiomyocytes. Cell Physiol Biochem 16: 147-154. (Pubitemid 41643015)
71. + current contributes to membrane potential of acutely isolated canine articular chondrocytes. J Physiol 557: 93-104. (Pubitemid 38771639)
72. Yang PC, Kurokawa J, Furukawa T, Clancy CE, (2010). Acute effects of sex steroid hormones on susceptibility to cardiac arrhythmias: a simulation study. PLoS Comput Biol 29: e1000658.