Acquired cisplatin resistance in human ovarian A2780 cancer cells correlates with shift in taurine homeostasis and ability to volume regulate

American Journal of Physiology - Cell Physiology

Volumn 307, Issue 12, 2014, Pages C1071-C1080

  Sørensen, Belinda Halling ^a   Thorsteinsdottir, Unnur Arna ^a   Lambert, Ian Henry ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell volume regulation; Drug resistance; LRRC8A; Platinum drugs; TauT

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; ARACHIDONATE 5 LIPOXYGENASE ACTIVATING PROTEIN INHIBITOR; BROMENOL LACTONE; CASPASE 9; CISPLATIN; ETH 615-139; ION TRANSPORT AFFECTING AGENT; LEUCINE RICH REPEAT CONTAINING PROTEIN 8A; PEPTIDES AND PROTEINS; PHOSPHOLIPASE A2 INHIBITOR; TAURINE; UNCLASSIFIED DRUG; ZAFIRLUKAST; ANTINEOPLASTIC AGENT; CARRIER PROTEIN; LEUKOTRIENE RECEPTOR BLOCKING AGENT; LIPOXYGENASE INHIBITOR; LRRC8A PROTEIN, HUMAN; MEMBRANE PROTEIN; TAURINE TRANSPORTER; TUMOR MARKER;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL SURVIVAL; CELL SWELLING; CELL VIABILITY; CELL VOLUME; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; OVARIAN CANCER CELL LINE; OVARY CANCER; PROTEIN EXPRESSION; CELL SIZE; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; OSMOTIC PRESSURE; OVARY TUMOR; PATHOLOGY; TIME; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SIZE; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HOMEOSTASIS; HUMANS; LEUKOTRIENE ANTAGONISTS; LIPOXYGENASE INHIBITORS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; OSMOTIC PRESSURE; OVARIAN NEOPLASMS; PHOSPHOLIPASE A2 INHIBITORS; TAURINE; TIME FACTORS; TUMOR MARKERS, BIOLOGICAL;

EID: 84918798472     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00274.2014     Document Type: Article

References (69)

1. Abascal F, Zardoya R. LRRC8 proteins share a common ancestor with pannexins, and may form hexameric channels involved in cell-cell communication. Bioessays 34: 551–560, 2012.
2. Bradley A, Zheng H, Ziebarth A, Sakati W, Branham-O’Connor M, Blumer JB, Liu Y, Kistner-Griffin E, Rodriguez-Aguayo C, Lopez- Berestein G, Sood AK, Landen CN, Jr., Eblen ST. EDD enhances cell survival and cisplatin resistance and is a therapeutic target for epithelial ovarian cancer. Carcinogenesis 35: 1100–1109, 2014.
3. Chen K, Zhang Q, Wang J, Liu F, Mi M, Xu H, Chen F, Zeng K. Taurine protects transformed rat retinal ganglion cells from hypoxiainduced apoptosis by preventing mitochondrial dysfunction. Brain Res 1279: 131–138, 2009.
4. Das J, Ghosh J, Manna P, Sil PC. Taurine protects rat testes against doxorubicin-induced oxidative stress as well as p53, Fas and caspase 12-mediated apoptosis. Amino Acids 42: 1839–1855, 2012.
5. Franke RM, Gardner ER, Sparreboom A. Pharmacogenetics of drug transporters. Curr Pharm Des 16: 220–230, 2010.
6. Friis MB, Friborg C, Schneider L, Nielsen MB, Lambert IH, Christensen ST, Hoffmann EK. Cell shrinkage as a signal to apoptosis in NIH3T3 fibroblasts. J Physiol 567: 427–443, 2005.
7. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene 31: 1869–1883, 2012.
8. Giacomini KM, Huang SM, Tweedie DJ, Benet LZ, Brouwer KL, Chu X, Dahlin A, Evers R, Fischer V, Hillgren KM, Hoffmaster KA, Ishikawa T, Keppler D, Kim RB, Lee CA, Niemi M, Polli JW, Sugiyama Y, Swaan PW, Ware JA, Wright SH, Yee SW, Zamek- Gliszczynski MJ, Zhang L. Membrane transporters in drug development. Nat Rev Drug Discov 9: 215–236, 2010.
9. Han X, Patters AB, Jones DP, Zelikovic I, Chesney RW. The taurine transporter: mechanisms of regulation. Acta Physiol (Oxf) 187: 61–73, 2006.
10. Han X, Yue J, Chesney RW. Functional TauT protects against acute kidney injury. J Am Soc Nephrol 20: 1323–1332, 2009.
11. Hanigan MH, Deng M, Zhang L, Taylor PT, Jr., Lapus MG. Stress response inhibits the nephrotoxicity of cisplatin. Am J Physiol Renal Physiol 288: F125–F132, 2005.
12. Hansen DB, Friis MB, Hoffmann EK, Lambert IH. Down-regulation of the taurine transporter TauT during hypoosmotic stress in NIH3T3 mouse fibroblasts. J Membr Biol 245: 77–87, 2012.
13. Hansen DB, Guerra B, Jacobsen JH, Lambert IH. Regulation of taurine homeostasis by protein kinase CK2 in mouse fibroblasts. Amino Acids 40: 1091–1106, 2011.
14. Heimlich G, Cidlowski JA. Selective role of intracellular chloride in the regulation of the intrinsic but not extrinsic pathway of apoptosis in Jurkat T-cells. J Biol Chem 281: 2232–2241, 2006.
15. Hoffmann EK, Lambert IH. Amino acid transport and cell volume regulation in Ehrlich ascites tumour cells. J Physiol 338: 613–625, 1983.
16. Hoffmann EK, Lambert IH. Ion channels and transporters in the development of drug resistance in cancer cells. Philos Trans R Soc Lond B Biol Sci 369: 20130109, 2014.
17. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193–277, 2009.
18. Hoffmann EK, Lambert IH, Simonsen LO. Separate, Ca2+-activated K+ and Cl– transport pathways in Ehrlich ascites tumor cells. J Membr Biol 91: 227–244, 1986.
19. Holm JB, Grygorczyk R, Lambert IH. Volume-sensitive release of organic osmolytes in the human lung epithelial cell line A. Am J Physiol Cell Physiol 305: C48–C60, 2013.
20. Huxtable RJ. Physiological actions of taurine. Physiol Rev 72: 101–163, 1992.
21. Inohara N, Koseki T, del PL, Hu Y, Yee C, Chen S, Carrio R, Merino J, Liu D, Ni J, Nunez G. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kappaB. J Biol Chem 274: 14560–14567, 1999.
22. Jacobsen JH, Clement CA, Friis MB, Lambert IH. Casein kinase 2 regulates the active uptake of the organic osmolyte taurine in NIH3T3 mouse fibroblasts. Pflügers Arch 457: 327–337, 2008.
23. Jong CJ, Azuma J, Schaffer S. Mechanism underlying the antioxidant activity of taurine: prevention of mitochondrial oxidant production. Amino Acids 42: 2223–2232, 2012.
24. Klausen TK, Hougaard C, Hoffmann EK, Pedersen SF. Cholesterol modulates the volume-regulated anion current in Ehrlich-Lettre ascites cells via effects on Rho and F-actin. Am J Physiol Cell Physiol 291: C757–C771, 2006.
25. Koberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: preclinical findings and clinical implications. Biochim Biophys Acta 1806: 172–182, 2010.
26. Lambert IH. Regulation of the volume-sensitive taurine efflux pathway in NIH3T3 mouse fibroblasts. In: Taurine in the 21st Century, edited by Lombardini JB, Schaffer SW, Azuma J. New York: Springer, 2003, p. 115–122.
27. Lambert IH. Regulation of the cellular content of the organic osmolyte taurine in mammalian cells. Neurochem Res 29: 27–63, 2004.
28. Lambert IH, Hansen DB. Regulation of taurine transport systems by protein kinase CK2 in mammalian cells. Cell Physiol Biochem 28: 1099–1110, 2011.
29. Lambert IH, Hoffmann EK, Pedersen SF. Cell volume regulation: physiology and pathophysiology. Acta Physiol Scand 194: 255–282, 2008.
30. Lambert IH, Jensen JV, Pedersen PA. mTOR ensures increased release and reduced uptake of the organic osmolyte taurine under hypoosmotic conditions in mouse fibroblasts. Am J Physiol Cell Physiol 306: C1028–C1040, 2014.
31. Lambert IH, Kristensen DM, Holm JB, Mortensen OH. Physiological role of taurine–from organism to organelle. Acta Physiol (Oxf) 2014 Aug 20 [Epub ahead of print].
32. Lang F, Hoffmann EK. Role of ion transport in control of apoptotic cell death. Compr Physiol 2: 2037–2061, 2012.
33. Lang PA, Warskulat U, Heller-Stilb B, Huang DY, Grenz A, Myssina S, Duszenko M, Lang F, Haussingr D, Vallon V, Wieder T. Blunted apoptosis of erythrocytes from taurine transporter deficient mice. Cell Physiol Biochem 13: 337–346, 2003.
34. Lee EL, Shimizu T, Ise T, Numata T, Kohno K, Okada Y. Impaired activity of volume-sensitive Cl- channel is involved in cisplatin resistance of cancer cells. J Cell Physiol 211: 513–521, 2007.
35. Lehen’kyi V, Shapovalov G, Skryma R, Prevarskaya N. Ion channels and transporters in cancer. 5. Ion channels in control of cancer and cell apoptosis. Am J Physiol Cell Physiol 301: C1281–C1289, 2011.
36. Liang F, Schulte BA, Qu C, Hu W, Shen Z. Inhibition of the calciumand voltage-dependent big conductance potassium channel ameliorates cisplatin-induced apoptosis in spiral ligament fibrocytes of the cochlea. Neuroscience 135: 263–271, 2005.
37. Lin S, Yang J, Wu G, Liu M, Lv Q, Yang Q, Hu J. Inhibitory effects of taurine on STZ-induced apoptosis of pancreatic islet cells. Adv Exp Med Biol 775: 287–297, 2013.
38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275, 1951.
39. Min XJ, Li H, Hou SC, He W, Liu J, Hu B, Wang J. Dysfunction of volume-sensitive chloride channels contributes to cisplatin resistance in human lung adenocarcinoma cells. Exp Biol Med (Maywood) 236: 483–491, 2011.
40. Mollerup J, Lambert IH. Phosphorylation is involved in the regulation of the taurine influx via the beta-system in Ehrlich ascites tumor cells. J Membr Biol 150: 73–82, 1996.
41. Mollerup J, Lambert IH. Calyculin A modulates the kinetic constants for the Na–-coupled taurine transport in Ehrlich ascites tumour cells. Biochim Biophys Acta 1371: 335–344, 1998.
42. Moran J, Miranda D, Pena-Segura C, Pasantes-Morales H. Volume regulation in NIH/3T3 cells not expressing P-glycoprotein. II. Chloride and amino acid fluxes. Am J Physiol Cell Physiol 272: C1804–C1809, 1997.
43. Motohashi H, Inui K. Organic cation transporter OCTs (SLC22) and MATEs (SLC47) in the human kidney. AAPS J 15: 581–588, 2013.
44. Okada Y, Maeno E. Apoptosis, cell volume regulation and volumeregulatory chloride channels. Comp Biochem Physiol A Mol Integr Physiol 130: 377–383, 2001.
45. Ørtenblad N, Young JF, Oksbjerg N, Nielsen JH, Lambert IH. Reactive oxygen species are important mediators of taurine release from skeletal muscle cells. Am J Physiol Cell Physiol 284: C1362–C1373, 2003.
46. Poulsen KA, Andersen EC, Hansen CF, Klausen TK, Hougaard C, Lambert IH, Hoffmann EK. Deregulation of apoptotic volume decrease and ionic movements in multidrug-resistant tumor cells: role of chloride channels. Am J Physiol Cell Physiol 298: C14–C25, 2010.
47. Poulsen KA, Litman T, Eriksen J, Mollerup J, Lambert IH. Downregulation of taurine uptake in multidrug resistant Ehrlich ascites tumor cells. Amino Acids 22: 333–350, 2002.
48. Poulsen KA, Pedersen SF, Kolko M, Lambert IH. Induction of group VIA phospholipase A2 activity during in vitro ischemia in C2C12 myotubes is associated with changes in the level of its splice variants. Am J Physiol Cell Physiol 293: C1605–C1615, 2007.
49. Qiu Z, Dubin AE, Mathur J, Tu B, Reddy K, Miraglia LJ, Reinhardt J, Orth AP, Patapoutian A. SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell 157: 447–458, 2014.
50. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186: 6553–6561, 2011.
51. Reinehr R, Schliess F, Haussinger D. Hyperosmolarity and CD95L trigger CD95/EGF receptor association and tyrosine phosphorylation of CD95 as prerequisites for CD95 membrane trafficking and DISC formation. FASEB J 17: 731–733, 2003.
52. Roos WP, Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett 332: 237–248, 2013.
53. Sawada A, Takihara Y, Kim JY, Matsuda-Hashii Y, Tokimasa S, Fujisaki H, Kubota K, Endo H, Onodera T, Ohta H, Ozono K, Hara J. A congenital mutation of the novel gene LRRC8 causes agammaglobulinemia in humans. J Clin Invest 112: 1707–1713, 2003.
54. Suzuki T, Nagao A, Suzuki T. Human mitochondrial diseases caused by lack of taurine modification in mitochondrial tRNAs. Wiley Interdiscip Rev RNA 2: 376–386, 2011.
55. Takahashi K, Azuma M, Yamada T, Ohyabu Y, Takahashi K, Schaffer SW, Azuma J. Taurine transporter in primary cultured neonatal rat heart cells: a comparison between cardiac myocytes and nonmyocytes. Biochem Pharmacol 65: 1181–1187, 2003.
56. Takahashi K, Ohyabu Y, Schaffer SW, Azuma J. Taurine prevents ischemia damage in cultured neonatal rat cardiomyocytes. In: Taurine 4, Taurine and Excitable Tissues, edited by Corte LD, Huxtable RJ, Sgaragli G, Tipton KF. New York: Klüwer Academic/Plenum, 2000, vol. 483, p. 109–116.
57. Takatani T, Takahashi K, Uozumi Y, Shikata E, Yamamoto Y, Ito T, Matsuda T, Schaffer SW, Fujio Y, Azuma J. Taurine inhibits apoptosis by preventing formation of the Apaf-1/caspase-9 apoptosome. Am J Physiol Cell Physiol 287: C949–C953, 2004.
58. Taranukhin AG, Taranukhina EY, Saransaari P, Djatchkova IM, Pelto-Huikko M, Oja SS. Taurine reduces caspase-8 and caspase-9 expression induced by ischemia in the mouse hypothalamic nuclei. Amino Acids 34: 169–174, 2008.
59. Tastesen HS, Holm JB, Møller J, Poulsen KA, Møller C, Stürup S, Hoffmann EK, Lambert IH. Pinpointing differences in cisplatin-induced apoptosis in adherent and non-adherent cancer cells. Cell Physiol Biochem 26: 809–820, 2010.
60. Todd RC, Lippard SJ. Inhibition of transcription by platinum antitumor compounds. Metallomics 1: 280–291, 2009.
61. Villumsen KR, Duelund L, Lambert IH. Acute cholesterol depletion leads to net loss of the organic osmolyte taurine in Ehrlich Lettré tumor cells. Amino Acids 39: 1521–1536, 2010.
62. Voss FK, Ullrich F, Munch J, Lazarow K, Lutter D, Mah N, Andrade- Navarro MA, von Kries JP, Stauber T, Jentsch TJ. Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344: 634–638, 2014.
63. Voss JW, Pedersen SF, Christensen ST, Lambert IH. Regulation of the expression and subcellular localisation of the taurine transporter TauT in mouse NIH3T3 fibroblasts. Eur J Biochem 271: 4646–4658, 2004.
64. Wu H, Wang K, Liu W, Hao Q. PTEN overexpression improves cisplatin-resistance of human ovarian cancer cells through upregulating KRT10 expression. Biochem Biophys Res Commun 444: 141–146, 2014.
65. Wu QD, Wang JH, Fennessy F, Redmond HP, Bouchier-Hayes D. Taurine prevents high-glucose-induced human vascular endothelial cell apoptosis. Am J Physiol Cell Physiol 277: C1229–C1238, 1999.
66. Yasunaga M, Matsumura Y. Role of SLC6A6 in promoting the survival and multidrug resistance of colorectal cancer. Sci Rep 4: 4852, 2014.
67. Yu SP. Regulation and critical role of potassium homeostasis in apoptosis. Prog Neurobiol 70: 363–386, 2003.
68. Zhang HY, Zhang PN, Sun H. Aberration of the PI3K/AKT/mTOR signaling in epithelial ovarian cancer and its implication in cisplatin-based chemotherapy. Eur J Obstet Gynecol Reprod Biol 146: 81–86, 2009.
69. Zhang Z, Xu X, Xiang Z, Yu Z, Feng J, He C. LINGO-1 receptor promotes neuronal apoptosis by inhibiting WNK3 activity. J Biol Chem 288: 12152–12160, 2013.