Ovarian cancer: Ion channel and aquaporin expression as novel targets of clinical potential

European Journal of Cancer

Volumn 49, Issue 10, 2013, Pages 2331-2344

  Frede, Julia ^a,b   Fraser, Scott P ^a   Oskay Özcelik, Gülten ^c   Hong, Yeosun ^a   Ioana Braicu, E ^c,d   Sehouli, Jalid ^c   Gabra, Hani ^e   Djamgoz, Mustafa B A ^a,f  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

^d IULIU HATIEGANU UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

^f CYPRUS INTERNATIONAL UNIVERSITY   (Turkey)

Author keywords

Aquaporin; Chloride; Growth factor; Invasion; Ion channel; Multidrug resistance; Ovarian cancer; Potassium; Sodium; Transient receptor potential

Indexed keywords

AQUAPORIN; CA 125 ANTIGEN; CHLORIDE CHANNEL; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; ION CHANNEL; MIBEFRADIL; MULTIDRUG RESISTANCE PROTEIN 1; NERVE GROWTH FACTOR; NNC 550396; POTASSIUM CHANNEL; TETRODOTOXIN; TIPIFARNIB; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; UNCLASSIFIED DRUG; VERAPAMIL; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ASCITES; CALCIUM CELL LEVEL; CANCER CELL; CANCER DIAGNOSIS; CANCER TISSUE; CARCINOGENESIS; CELL ADHESION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CHANNEL GATING; DISEASE ASSOCIATION; EARLY DIAGNOSIS; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MICROVASCULATURE; MULTIDRUG RESISTANCE; MULTIPLE MYELOMA; NONHUMAN; OVARY CANCER; OVERALL SURVIVAL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; RNA INTERFERENCE; WATER PERMEABILITY;

EID: 84878393994     PISSN: 09598049     EISSN: 18790852     Source Type: Journal    
DOI: 10.1016/j.ejca.2013.03.016     Document Type: Article

References (211)

1. M. Sant, C. Allemani, M. Santaquilani, A. Knijn, F. Marchesi, and R. Capocaccia EUROCARE-4. Survival of cancer patients diagnosed in 1995-1999. Results and commentary Eur J Cancer 45 2009 931 991
2. A.P. Heintz, F. Odicino, and P. Maisonneuve Carcinoma of the ovary. FIGO 6th annual report on the results of treatment in gynecological cancer Int J Gynaecol Obstet 95 Suppl. 1 2006 S161 S192
3. K.R. Cho, and I.-M. Shih Ovarian cancer Annu Rev Pathol 4 2009 287 313
4. J. Sehouli, F. Senyuva, and C. Fotopoulou Intra-abdominal tumor dissemination pattern and surgical outcome in 214 patients with primary ovarian cancer J Surg Oncol 99 2009 424 427
5. D. Vergara, B. Merlot, and J.P. Lucot Epithelial-mesenchymal transition in ovarian cancer Cancer Lett 291 2010 59 66
6. T. Fan, Q. Zhao, J.J. Chen, W.T. Chen, and M.L. Pearl Clinical significance of circulating tumor cells detected by an invasion assay in peripheral blood of patients with ovarian cancer Gynecol Oncol 112 2009 185 191
7. A. Feki, P. Berardi, and G. Bellingan Dissemination of intraperitoneal ovarian cancer: discussion of mechanisms and demonstration of lymphatic spreading in ovarian cancer model Crit Rev Oncol Hematol 72 2009 1 9
8. B. Cheng, W. Lu, W. Xiaoyun, C. YaXia, and X. Xie Extra-abdominal metastases from epithelial ovarian carcinoma: an analysis of 20 cases Int J Gynecol Cancer 19 2009 611 614
9. K. Pietzner, G. Oskay-Oezcelik, K. El Khalfaoui, D. Boehmer, W. Lichtenegger, and J. Sehouli Brain metastases from epithelial ovarian cancer: overview and optimal management Anticancer Res 29 2009 2793 2798
10. R.C. Bast Jr, B. Hennessy, and G.B. Mills The biology of ovarian cancer: new opportunities for translation Nat Rev Cancer 9 2009 415 428
11. A.J. Dembo, M. Davy, A.E. Stenwig, E.J. Berle, R.S. Bush, and K. Kjorstad Prognostic factors in patients with stage I epithelial ovarian cancer Obstet Gynecol 75 1990 263 273
12. R.E. Bristow, R.S. Tomacruz, D.K. Armstrong, E.L. Trimble, and F.J. Montz Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis J Clin Oncol 20 2002 1248 1259
13. R.C. Bast Jr., D. Badgwell, and Z. Lu New tumor markers: CA125 and beyond Int J Gynecol Cancer 15 Suppl. 3 2005 274 281
14. I.J. Jacobs, and U. Menon Progress and challenges in screening for early detection of ovarian cancer Mol Cell Proteomics 3 2004 355 366
15. U. Menon, A. Gentry-Maharaj, and R. Hallett Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS) Lancet Oncol 10 2009 327 340
16. J. Sehouli, Z. Akdogan, and T. Heinze Preoperative determination of CASA (Cancer Associated Serum Antigen) and CA-125 for the discrimination between benign and malignant pelvic tumor mass: a prospective study Anticancer Res 23 2003 1115 1118
17. G.L. Anderson, M. McIntosh, and L. Wu Assessing lead time of selected ovarian cancer biomarkers: a nested case-control study J Natl Cancer Inst 102 2010 26 38
18. R.G. Moore, S. MacLaughlan, and R.C. Bast Jr. Current state of biomarker development for clinical application in epithelial ovarian cancer Gynecol Oncol 116 2010 240 245
19. C. Kuk, C.G. Gunawardana, and A. Soosaipillai Nidogen-2: a new serum biomarker for ovarian cancer Clin Biochem 43 2010 355 361
20. X. Hu, D.M. Macdonald, and P.C. Huettner A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer Gynecol Oncol 114 2009 457 464
21. H. Lee, C.S. Park, G. Deftereos, J. Morihara, J.E. Stern, and S.E. Hawes MicroRNA expression in ovarian carcinoma and its correlation with clinicopathological features World J Surg Oncol 10 2012 174
22. V. Kulasingam, M.P. Pavlou, and E.P. Diamandis Integrating high-throughput technologies in the quest for effective biomarkers for ovarian cancer Nature Rev Cancer 10 2010 371 378
23. S.A. Bapat, A. Krishnan, A.D. Ghanate, A.P. Khsumbe, and R.S. Kalra Gene expression: protein interaction systems network modeling identifies transformation-associated molecules and pathways in ovarian cancer Cancer Res 70 2010 4809 4819
24. C.S. Zhu, P.F. Pinsky, and D.W. Cramer A framework for evaluating biomarkers for early detection: validation of biomarker panels for ovarian cancer Cancer Prev Res 4 2011 375 383
25. S. Blagden, and H. Gabra Promising molecular targets in ovarian cancer Curr Opin Oncol 21 2009 412 419
26. S. Vaughan, J.I. Coward, and R.C. Bast Jr Rethinking ovarian cancer: recommendations for improving outcomes Nat Rev Cancer 11 2011 719 725
27. R. Onkal, and M.B.A. Djamgoz Molecular pharmacology of voltage-gated sodium channel expression in metastatic disease: clinical potential of neonatal Nav1.5 in breast cancer Eur J Pharmacol 625 2009 206 219
28. M.B.A. Djamgoz, and R. Onkal Persistent current blockers of voltage-gated sodium channels: a clinical opportunity for controlling metastatic disease Recent Pat Anticancer Drug Discov 8 2013 66 84
29. N. Prevarskaya, R. Skryma, and Y. Shuba Ion channels and the hallmarks of cancer Trends Mol Med 16 2010 107 121
30. S.P. Fraser, and L.A. Pardo Ion channels: functional expression and therapeutic potential in cancer. Colloquium on Ion Channels and Cancer EMBO Rep 9 2008 512 515
31. S.F. Pedersen, and C. Stock Ion channels and transporters in cancer: pathophysiology, regulation and clinical potential Cancer Res 73 2013 1658 1661
32. S.P. Fraser, J.K. Diss, and A.M. Chioni Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis Clin Cancer Res 11 2005 5381 5389
33. + channels in human prostate cancer cell lines and their contribution to invasion in vitro Am J Pathol 150 1997 1213 1221
34. + channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion Cancer Res 70 2010 6957 6967
35. K.H. Tung, M.T. Goodman, and A.H. Wu Aggregation of ovarian cancer with breast, ovarian, colorectal, and prostate cancer in first-degree relatives Am J Epidemiol 159 2004 750 758
36. +-transport Arch Geschwulstforsch 51 1981 96 102
37. S. Walliser, and K. Redmann Effects of cytostatic drugs on the transmembrane potential and surface charge of cultured cells Arch Geschwulstforsch 51 1981 125 132
38. C.K. Bose Role of nerve growth factor and FSH receptor in epithelial ovarian cancer Reprod Biomed Online 11 2005 194 197
39. R. Zeineldin, C.Y. Muller, M.S. Stack, and L.G. Hudson Targeting the EGF receptor for ovarian cancer therapy J Oncol 2010 2010 414676
40. + channel subunit in rat prostate cancer cell lines: electrophysiological, pharmacological and molecular characterisation Pflugers Arch 446 2003 559 571
41. M. Brevet, D. Fucks, and D. Chatelain Deregulation of 2 potassium channels in pancreas adenocarcinomas: implication of Kv1.3 gene promoter methylation Pancreas 38 2009 649 654
42. B. Hemmerlein, R.M. Weseloh, and F. Mello de Queiroz Overexpression of Eag1 potassium channels in clinical tumours Mol Cancer 5 2006 41
43. A. Arcangeli Expression and role of hERG channels in cancer cells Novartis Found Symp 266 2005 225 232
44. + channel modulators on human prostate cancer cell proliferation Eur J Pharmacol 471 2003 157 164
45. + channels in breast cancer cells: association with cell cycle progression Am J Physiol Cell Physiol 287 2004 C125 C134
46. + channel mediates B lymphoma cell cycle progression induced by serum Pflugers Arch 4546 2007 945 956
47. + channels inhibits progression of human endometrial cancer Oncogene 26 2007 5107 5114
48. + channels (IKCa1) regulate human prostate cancer cell proliferation through a close control of calcium entry Oncogene 28 2009 1792 1806
49. H.K. Plummer 3rd, Q. Yu, Y. Cakir, and H.M. Schuller Expression of inwardly rectifying potassium channels (GIRKs) and beta-adrenergic regulation of breast cancer cell lines BMC Cancer 4 2004 93
50. B.K. Stringer, A.G. Cooper, and S.B. Shepard Overexpression of the G-protein inwardly rectifying potassium channel 1 (GIRK1) in primary breast carcinomas correlates with axillary lymph node metastasis Cancer Res 61 2001 582 588
51. G. Tan, S.Q. Sun, and D.L. Yuan Expression of Kir4.1 in human astrocytic tumors: correlation with pathologic grade Biochem Biophys Res Commun 367 2008 743 747
52. D. Mu, L. Chen, and X. Zhang Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene Cancer Cell 3 2003 297 302
53. + channels in breast cancer cells Biochem Biophys Res Commun 316 2004 244 251
54. + channel block-induced mammalian neuroblastoma cell swelling: a possible mechanism to influence proliferation J Physiol 510 1998 93 102
55. 2+ influx in carcinoma cells of colon cancer Life Sci 65 1999 55 62
56. W.F. Wonderlin, and J.S. Strobl Potassium channels, proliferation and G1 progression J Membr Biol 154 1996 91 107
57. M. Gomez-Angelats, C.D. Bortner, and J.A. Cidlowski Cell volume regulation in immune cell apoptosis Cell Tissue Res 301 2000 33 42
58. F. Lang, G.L. Busch, and M. Ritter Functional significance of cell volume regulatory mechanisms Physiol Rev 78 1998 247 306
59. C.D. Bortner, and J.A. Cidlowski Cell shrinkage and monovalent cation fluxes: role in apoptosis Arch Biochem Biophys 462 2007 176 188
60. C.D. Bortner, M.I. Sifre, and J.A. Cidlowski Cationic gradient reversal and cytoskeleton-independent volume regulatory pathways define an early stage of apoptosis J Biol Chem 283 2008 7219 7229
61. + channels are associated with cell proliferation and cell cycle of ovarian cancer cell Gynecol Oncol 104 2007 455 460
62. X. Han, L. Xi, and H. Wang The potassium ion channel opener NS1619 inhibits proliferation and induces apoptosis in A2780 ovarian cancer cells Biochem Biophys Res Commun 375 2008 205 209
63. W. ZhanPing, W. Chun, and T. Hong Expression and activity of Kv1.3 potassium ion channels in human ovarian cancer cells Prog Modern Biomed 11 2011 2053 2057
64. V. Asher, A. Warren, and R. Shaw The role of Eag and HERG channels in cell proliferation and apoptotic cell death in SK-OV-3 ovarian cancer cell line Cancer Cell Int 11 2011 6
65. T. Yasukagawa, Y. Niwa, and S. Simizu Suppression of cellular invasion by glibenclamide through inhibited secretion of platelet-derived growth factor in ovarian clear cell carcinoma ES-2 cells FEBS Lett 586 2012 1504 1509
66. J.A. Rodríguez-Rasgado, I. Acuña-Macías, and J. Camacho Eag1 channels as potential cancer biomarkers Sensors 12 2012 5986 5995
67. V. Asher, R. Khan, G. Schalkwyk, A. Bali, and H. Sowter The Eag potassium channel as a new prognostic marker in ovarian cancer Diagn Pathol 5 2010 78
68. M. Oeggerli, Y. Tian, and C. Ruiz Role of KCNMA1 in Breast Cancer PLoS One 7 2012 e41664
69. + channels and the intracellular calcium signal in human melanoma cell proliferation J Membr Biol 151 1996 149 157
70. T.J. Jentsch, V. Stein, F. Weinreich, and A.A. Zdebik Molecular structure and physiological function of chloride channels Physiol Rev 82 2002 503 568
71. M.L. Olsen, S. Schade, S.A. Lyons, M.D. Amaral, and H. Sontheimer Expression of voltage-gated chloride channels in human glioma cells J Neurosci 23 2003 5572 5582
72. C.W. Habela, M.L. Olsen, and H. Sontheimer ClC3 is a critical regulator of the cell cycle in normal and malignant glial cells J Neurosci 28 2008 9205 9217
73. J. Mao, L. Wang, and A. Fan Blockage of volume-activated chloride channels inhibits migration of nasopharyngeal carcinoma cells Cell Physiol Biochem 19 2007 249 258
74. J. Mao, L. Chen, and B. Xu Suppression of ClC-3 channel expression reduces migration of nasopharyngeal carcinoma cells Biochem Pharmacol 75 2008 1706 1716
75. J. Mao, L. Chen, and B. Xu Volume-activated chloride channels contribute to cell-cycle-dependent regulation of HeLa cell migration Biochem Pharmacol 77 2009 159 168
76. - current associated with neuroendocrine differentiation of prostate cancer epithelial cells Endocr Relat Cancer 12 2005 335 349
77. R.C. Elble, and B.U. Pauli Tumor suppression by a proapoptotic calcium-activated chloride channel in mammary epithelium J Biol Chem 276 2001 40510 40517
78. M. Spitzner, J.R. Martins, and R.B. Soria Eag1 and Bestrophin 1 are up-regulated in fast-growing colonic cancer cells J Biol Chem 283 2008 7421 7428
79. U. Duvvuri, D.J. Shiwarski, and D. Xiao TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression Cancer Res 72 2012 3270 3281
80. M. Li, B. Wang, and W. Lin Cl-channel blockers inhibit cell proliferation and arrest the cell cycle of human ovarian cancer cells Eur J Gynaecol Oncol 29 2008 267 271
81. M. Li, Q. Wang, W. Lin, and B. Wang Regulation of ovarian cancer cell adhesion and invasion by chloride channels Int J Gynecol Cancer 19 2009 526 530
82. G. Edwards, and A.H. Weston Pharmacology of the potassium channel openers Cardiovasc Drugs Ther 9 Suppl. 2 1995 185 193
83. Z. Yu, Z.-X. Zhang, and S. Li Effect of a chloride channel inhibitor, 5-nitro-2-(3-phenylpropylamino)-benzoate, on ovarian cancer cell migration Clin Lab 57 2011 543 550
84. H.-Y. Tang, L.A. Beer, and T. Chang-Wong A xenograft mouse model coupled with in-depth plasma proteome analysis facilitates identification of novel serum biomarkers for human ovarian cancer J Proteome Res 11 2012 678 691
85. M.A. Dozynkiewicz, N.B. Jamieson, and I. MacPherson Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression Dev Cell 22 2012 131 145
86. K.S. Suh, J.M. Crutchley, and A. Koochek Reciprocal modifications of CLIC4 in tumor epithelium and stroma mark malignant progression of multiple human cancers Clin Cancer Res 13 2007 121 131
87. G. Lorusso, and C. Ruegg The tumor microenvironment and its contribution to tumor evolution toward metastasis Histochem Cell Biol 130 2008 1091 1103
88. D. Gkika, and N. Prevarskaya Molecular mechanisms of TRP regulation in tumor growth and metastasis Biochim Biophys Acta 1793 2009 953 958
89. L. Zhuang, J.B. Peng, and L. Tou Calcium-selective ion channel, CaT1, is apically localized in gastrointestinal tract epithelia and is aberrantly expressed in human malignancies Lab Invest 82 2002 1755 1764
90. V. Lehen'kyi, M. Raphael, and N. Prevarskaya The role of the TRPV6 channel in cancer J Physiol 590 2012 1369 1376
91. 2+-selective cation channel TRPV6 in human prostate cancer: a novel prognostic marker for tumor progression Oncogene 22 2003 7858 7861
92. 2+ channel expression Biochem Biophys Res Commun 322 2004 1359 1363
93. S.L. Yang, Q. Cao, K.C. Zhou, Y.J. Feng, and Y.Z. Wang Transient receptor potential channel C3 contributes to the progression of human ovarian cancer Oncogene 28 2009 1320 1328
94. D.V. Hansen, J.J. Tung, and P.K. Jackson CaMKII and polo-like kinase 1 sequentially phosphorylate the cytostatic factor Emi2/XErp1 to trigger its destruction and meiotic exit Proc Natl Acad Sci USA 103 2006 608 613
95. J. Liu, and J.L. Maller Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor Curr Biol 15 2005 1458 1468
96. T. Lorca, F.H. Cruzalegui, and D. Fesquet Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs Nature 366 1993 270 273
97. N.R. Rauh, A. Schmidt, J. Bormann, E.A. Nigg, and T.U. Mayer Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation Nature 437 2005 1048 1052
98. 2+/calmodulin-dependent protein kinase II. Mutation of threonine 286 to alanine and aspartate J Biol Chem 264 1989 16759 16763
99. + channel alpha-subunit genes in rat and human prostate cancer cell lines Prostate 48 2001 165 178
100. + channel expression in vitro J Membr Biol 204 2005 67 75
101. S. Roger, J. Rollin, and A. Barascu Voltage-gated sodium channels potentiate the invasive capacities of human non-small-cell lung cancer cell lines Int J Biochem Cell Biol 39 2007 774 786
102. G. Fulgenzi, L. Graciotti, and M. Faronato Human neoplastic mesothelial cells express voltage-gated sodium channels involved in cell motility Int J Biochem Cell Biol 38 2006 1146 1159
103. D. Diaz, D.M. Delgadillo, and E. Hernández-Gallegos Functional expression of voltage-gated sodium channels in primary cultures of human cervical cancer J Cell Physiol 210 2007 469 478
104. S. Sharma, T.K. Kelly, and P.A. Jones Epigenetics in cancer Carcinogenesis 31 2010 27 36
105. M. Monk, and C. Holding Human embryonic genes re-expressed in cancer cells Oncogene 20 2001 8085 8091
106. R. Gao, Y. Shen, J. Cai, M. Lei, and Z. Wang Expression of voltage-gated sodium channel α subunit in human ovarian cancer Oncol Rep 23 2010 1293 1299
107. J.A. Rosado, P.C. Redondo, J.A. Pariente, and G.M. Salido Calcium signalling and tumorigenesis Cancer Ther 2 2004 263 270
108. G. Shapovalov, R. Skryma, and N. Prevarskaya Calcium channels and prostate cancer Recent Pat Anticancer Drug Discov 8 2013 18 26
109. 2+ channels suppresses human breast cancer cell proliferation Cancer Lett 267 2008 116 124
110. I. Latour, D.F. Louw, A.M. Beedle, J. Hamid, G.R. Sutherland, and G.W. Zamponi Expression of T-type calcium channel splice variants in human glioma Glia 48 2004 112 119
111. M. Toyota, C. Ho, M. Ohe-Toyota, S.B. Baylin, and J.P. Issa Inactivation of CACNA1G, a T-type calcium channel gene, by aberrant methylation of its 5′CpG island in human tumors Cancer Res 59 1999 4535 4541
112. 2+ entry Cancer Res 60 2000 1002 1008
113. G.E. Bertolesi, C. Shi, and L. Elbaum The Ca(2+) channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxic mechanisms Mol Pharmacol 62 2002 210 219
114. F. Gackiere, G. Bidaux, and P. Delcourt CaV3.2 T-type calcium channels are involved in calcium-dependent secretion of neuroendocrine prostate cancer cells J Biol Chem 283 2008 10162 10173
115. K. Kunzelmann Ion channels and cancer J Membr Biol 205 2005 159 173
116. 2+ transport Nat Rev Cancer 7 2007 519 530
117. 2+ channels inhibits human ovarian cancer cell proliferation Cancer Invest 29 2011 339 346
118. I. Mertens-Walker, C. Bolitho, R.C. Baxter, and D.J. Marsh Gonadotropin-induced ovarian cancer cell migration and proliferation require extracellular signal-regulated kinase 1/2 activation regulated by calcium and protein kinase C delta Endocrine-Related Cancer 17 2010 335 349
119. A.S. Verkman Aquaporins: translating bench research to human disease Ann Rev Med 63 2012 303 316
120. M. Hara-Chikuma, and A.S. Verkman Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule J Am Soc Nephrol 17 2006 39 45
121. M. Hara-Chikuma, and A.S. Verkman Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing J Mol Med 86 2008 221 231
122. K.I. Auguste, S. Jin, and K. Uchida Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury FASEB J 21 2007 108 116
123. S. Saadoun, M.C. Papadopoulos, H. Watanabe, D. Yan, G.T. Manley, and A.S. Verkman Involvement of aquaporin-4 in astroglial cell migration and glial scar formation J Cell Sci 118 2005 5691 5698
124. S. Ishimoto, K. Wada, and Y. Usami Differential expression of aquaporin 5 and aquaporin 3 in squamous cell carcinoma and adenoid cystic carcinoma Int J Oncol 41 2012 67 75
125. C. Yan, J. Yang, L. Shen, and X. Chen Inhibitory effect of epigallocatechin gallate on ovarian cancer cell proliferation associated with aquaporin 5 expression Arch Gynecol Obstet 285 2012 459 467
126. J. Yang, C. Yan, W. Zheng, and X. Chen Proliferation inhibition of cisplatin and aquaporin 5 expression in human ovarian cancer cell CAOV3 Arch Gynecol Obstet 285 2012 239 245
127. C. Ji, C. Cao, and S. Lu Curcumin attenuates EGF-induced AQP3 up-regulation and cell migration in human ovarian cancer cells Cancer Chemother Pharmacol 62 2008 857 865
128. J.H. Yang, Y.Q. Yu, and C.X. Yan Localisation and expression of aquaporin subtypes in epithelial ovarian tumours Histol Histopathol 26 2011 1197 1205
129. J.H. Yang, Y.F. Shi, X.D. Chen, and W.J. Qi The influence of aquaporin-1 and microvessel density on ovarian carcinogenesis and ascites formation Int J Gynecol Cancer 16 Suppl. 1 2006 400 405
130. J.H. Yang, Y.F. Shi, Q. Cheng, and L. Deng Expression and localization of aquaporin-5 in the epithelial ovarian tumors Gynecol Oncol 100 2006 294 299
131. A. Mobasheri, R. Airley, S.M. Hewitt, and D. Marples Heterogeneous expression of the aquaporin 1 (AQP1) water channel in tumors of the prostate, breast, ovary, colon and lung: a study using high density multiple human tumor tissue microarrays Int J Oncol 26 2005 1149 1158
132. + channels: multiplicity of expression, plasticity, functional implications and pathophysiological aspects Eur Biophys J 33 2004 180 193
133. + channel gene expression in differentiated cells J Neurobiol 37 1998 60 68
134. D. Shao, K. Okuse, and M.B.A. Djamgoz Protein-protein interactions involving voltage-gated sodium channels: post-translational regulation, intracellular trafficking and functional expression Int J Biochem Cell Biol 41 2009 1471 1481
135. L. Albanito, R. Lappano, and A. Madeo G-protein-coupled receptor 30 and estrogen receptor-alpha are involved in the proliferative effects induced by atrazine in ovarian cancer cells Environ Health Perspect 116 2008 1648 1655
136. L.A. Sheach, E.M. Adeney, and A. Kucukmetin Androgen-related expression of G-proteins in ovarian cancer Br J Cancer 101 2009 498 503
137. E.J. Filardo, J.A. Quinn, K.I. Bland, and A.R. Frackelton Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF Mol Endocrinol 14 2000 1649 1660
138. E.J. Filardo, J.A. Quinn, A.R. Frackelton Jr., and K.I. Bland Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis Mol Endocrinol 16 2002 70 84
139. M. Maggiolini, A. Vivacqua, and G. Fasanella The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells J Biol Chem 279 2004 27008 27016
140. C.M. Revankar, D.F. Cimino, L.A. Sklar, J.B. Arterburn, and E.R. Prossnitz A transmembrane intracellular estrogen receptor mediates rapid cell signaling Science 307 2005 1625 1630
141. + channel activity in MDA-MB-231 human breast cancer cells: role in adhesion J Cell Physiol 224 2010 527 539
142. X. Campos, Y. Munoz, and A. Selman Nerve growth factor and its high-affinity receptor trkA participate in the control of vascular endothelial growth factor expression in epithelial ovarian cancer Gynecol Oncol 104 2007 168 175
143. A. Obermair, P. Speiser, and K. Reisenberger Influence of intratumoral basic fibroblast growth factor concentration on survival in ovarian cancer patients Cancer Lett 130 1998 69 76
144. B. Davidson, I. Goldberg, and W.H. Gotlieb The prognostic value of metalloproteinases and angiogenic factors in ovarian carcinoma Mol Cell Endocrinol 187 2002 39 45
145. N.M. Moss, Y. Liu, and J.J. Johnson Epidermal growth factor receptor-mediated membrane type 1 matrix metalloproteinase endocytosis regulates the transition between invasive versus expansive growth of ovarian carcinoma cells in three-dimensional collagen Mol Cancer Res 7 2009 809 820
146. + channel activity and Transwell migration in Mat-LyLu rat prostate cancer cell line J Cell Physiol 210 2007 602 608
147. T.L. Pena, S.H. Chen, S.F. Konieczny, and S.G. Rane Ras/MEK/ERK Up-regulation of the fibroblast KCa channel FIK is a common mechanism for basic fibroblast growth factor and transforming growth factor-beta suppression of myogenesis J Biol Chem 275 2000 13677 13682
148. C. Jeulin, V. Seltzer, D. Bailbe, K. Andreau, and F. Marano EGF mediates calcium-activated chloride channel activation in the human bronchial epithelial cell line 16HBE14o-: involvement of tyrosine kinase p60c-src Am J Physiol Lung Cell Mol Physiol 295 2008 L489 L496
149. R.A. Falin, and C.U. Cotton Acute downregulation of ENaC by EGF involves the PY motif and putative ERK phosphorylation site J Gen Physiol 130 2007 313 328
150. C.T. Chang, C.C. Hung, and Y.C. Chen Transforming growth factor-beta1 decreases epithelial sodium channel functionality in renal collecting duct cells via a Smad4-dependent pathway Nephrol Dial Transplant 23 2008 1126 1134
151. Y. Hayabuchi, G.B. Willars, N.B. Standen, and N.W. Davies Insulin-like growth factor-I inhibits rat arterial K(ATP) channels through PI3-kinase Biochem Biophys Res Commun 374 2008 742 746
152. G.E. Konecny, R. Glas, and J. Dering Activity of the multikinase inhibitor dasatinib against ovarian cancer cells Br J Cancer 101 2009 1699 1708
153. + channel activity J Cell Physiol 215 2008 77 81
154. P. Uysal-Onganer, and M.B.A. Djamgoz Epidermal growth factor potentiates in vitro metastatic behaviour of human prostate cancer PC-3M cells: involvement of voltage-gated sodium channel Mol Cancer 6 2007 76
155. B. Isbilen, S.P. Fraser, and M.B.A. Djamgoz Docosahexaenoic acid (omega-3) blocks voltage-gated sodium channel activity and migration of MDA-MB-231 human breast cancer cells Int J Biochem Cell Biol 38 2006 2173 2182
156. M.H. Lee, B.Y. Choi, J.K. Kundu, Y.K. Shin, H.K. Na, and Y.J. Surh Resveratrol suppresses growth of human ovarian cancer cells in culture and in a murine xenograft model: eukaryotic elongation factor 1A2 as a potential target Cancer Res 69 2009 7449 7458
157. K.S. Stakleff, T. Sloan, D. Blanco, S. Marcanthony, T.D. Booth, and A. Bishayee Resveratrol exerts differential effects in vitro and in vivo against ovarian cancer cells Asian Pac J Cancer Prev 13 2012 1333 1340
158. C.H. Wallace, I. Baczko, L. Jones, M. Fercho, and P.E. Light Inhibition of cardiac voltage-gated sodium channels by grape polyphenols Br J Pharmacol 149 2006 657 665
159. P.J. DiSaia, and J.D. Bloss Treatment of ovarian cancer: new strategies Gynecol Oncol 90 2003 S24 S32
160. C. Balch, T.H. Huang, R. Brown, and K.P. Nephew The epigenetics of ovarian cancer drug resistance and resensitization Am J Obstet Gynecol 191 2004 1552 1572
161. R.T. Greenlee, M.B. Hill-Harmon, T. Murray, and M. Thun Cancer statistics, 2001 CA Cancer J Clin 51 2001 15 36
162. R. Agarwal, and S.B. Kaye Ovarian cancer: strategies for overcoming resistance to chemotherapy Nat Rev Cancer 3 2003 502 516
163. P. Borst, R. Evers, M. Kool, and J. Wijnholds A family of drug transporters: the multidrug resistance-associated proteins J Natl Cancer Inst 92 2000 1295 1302
164. G. Jedlitschky, U. Hoffmann, and H.K. Kroemer Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition Expert Opin Drug Metab Toxicol 2 2006 351 366
165. L. Duncan, H. Shelmerdine, M.P. Hughes, H.M. Coley, Y. Hubner, and F.H. Labeed Dielectrophoretic analysis of changes in cytoplasmic ion levels due to ion channel blocker action reveals underlying differences between drug-sensitive and multidrug-resistant leukaemic cells Phys Med Biol 53 2008 N1 N7
166. S.C. Lee, C. Deutsch, and W.T. Beck Comparison of ion channels in multidrug-resistant and -sensitive human leukemic cells Proc Natl Acad Sci USA 85 1988 2019 2023
167. Y. Huang, and W. Sadee Membrane transporters and channels in chemo-resistance and -sensitivity of tumor cells Cancer Lett 239 2006 168 182
168. - channels in multi-drug resistant MCF7 cells Biochem Biophys Res Commun 334 2005 1266 1278
169. M.A. Valverde, M. Diaz, F.V. Sepulveda, D.R. Gill, S.C. Hyde, and C.F. Higgins Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein Nature 355 1992 830 833
170. D.R. Gill, S.C. Hyde, C.F. Higgins, M.A. Valverde, G.M. Mintenig, and F.V. Sepulveda Separation of drug transport and chloride channel functions of the human multidrug resistance P-glycoprotein Cell 71 1992 23 32
171. + channels and volume-regulated anion channels in multidrug-resistant small cell lung cancer cells Cancer Res 53 1993 4156 4160
172. C.F. Higgins Volume-activated chloride currents associated with the multidrug resistance P-glycoprotein J Physiol 482 1995 31S 36S
173. Y. Dong, G. Chen, and G.E. Duran Volume-activated chloride current is not related to P-glycoprotein overexpression Cancer Res 54 1994 5029 5032
174. G.R. Ehring, Y.V. Osipchuk, and M.D. Cahalan Swelling-activated chloride channels in multidrug-sensitive and -resistant cells J Gen Physiol 104 1994 1129 1161
175. K. Kunzelmann, I.N. Slotki, and P. Klein Effects of P-glycoprotein expression on cyclic AMP and volume-activated ion fluxes and conductances in HT-29 colon adenocarcinoma cells J Cell Physiol 161 1994 393 406
176. A. Rasola, L.J. Galietta, D.C. Gruenert, and G. Romeo Volume-sensitive chloride currents in four epithelial cell lines are not directly correlated to the expression of the MDR-1 gene J Biol Chem 269 1994 1432 1436
177. C. De Greef, J. Sehrer, and F. Viana Volume-activated chloride currents are not correlated with P-glycoprotein expression Biochem J 307 1995 713 718
178. K.A. Poulsen, E.C. Andersen, and C.F. Hansen Deregulation of apoptotic volume decrease and ionic movements in multidrug-resistant tumor cells: role of chloride channels Am J Physiol Cell Physiol 298 2010 C14 C25
179. M.K. Kang, and S.K. Kang Pharmacologic blockade of chloride channel synergistically enhances apoptosis of chemotherapeutic drug-resistant cancer stem cells Biochem Biophys Res Commun 373 2008 539 544
180. L.Y. Chiu, J.L. Ko, Y.J. Lee, T.Y. Yang, Y.T. Tee, and G.T. Sheu L-type calcium channel blockers reverse docetaxel and vincristine-induced multidrug resistance independent of ABCB1 expression in human lung cancer cell lines Toxicol Lett 192 2010 408 418
181. 2+ channels J Pharmacol Exp Ther 337 2011 636 643
182. D.J. Triggle L-type calcium channels Curr Pharm Des 12 2006 443 457
183. 2+-homeostasis of cisplatin-treated and low level resistant non-small-cell and small-cell lung cancer cells Cell Oncol 31 2009 301 315
184. S. Huet, and J. Robert The reversal of doxorubicin resistance by verapamil is not due to an effect on calcium channels Int J Cancer 41 1988 283 286
185. + current in small-cell lung cancer cells J Pharmacol Exp Ther 257 1991 184 191
186. A. Teisseyre, N. Duarte, M.J. Ferreira, and K. Michalak Influence of the multidrug transporter inhibitors on the activity of Kv1.3 voltage-gated potassium channels J Physiol Pharmacol 60 2009 69 76
187. E. Zitron, E. Scholz, and R. Owen QTc prolongation by grapefruit juice and its potential pharmacological basis: HERG channel blockade by flavonoids Circulation 111 2005 835 838
188. A.A. Harper, L. Catacuzzeno, C. Trequattrini, A. Petris, and F. Franciolini Verapamil block of large-conductance Ca-activated K channels in rat aortic myocytes J Membr Biol 179 2001 103 111
189. Y. Han, Y. Shi, Z. Han, L. Sun, and D. Fan Detection of potassium currents and regulation of multidrug resistance by potassium channels in human gastric cancer cells Cell Biol Int 31 2007 741 747
190. V. Gérard, B. Rouzaire-Dubois, P. Dilda, and J.M. Dubois Alterations of ionic membrane permeabilities in multidrug-resistant neuroblastoma × glioma hybrid cells J Exp Biol 201 1998 21 31
191. + channel current associated with multidrug resistance in human leukemia cells Cancer Res 47 1987 3736 3741
192. + channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers Neuroscientist 14 2008 571 583
193. Z.F. Miao, E.E. Chang, and F.Y. Tsai Increased aquaglyceroporin 9 expression disrupts arsenic resistance in human lung cancer cells Toxicol In Vitro 23 2009 209 216
194. H. Bhattacharjee, J. Carbrey, B.P. Rosen, and R. Mukhopadhyay Drug uptake and pharmacological modulation of drug sensitivity in leukemia by AQP9 Biochem Biophys Res Commun 322 2004 836 841
195. J.M. Carbrey, D.A. Gorelick-Feldman, D. Kozono, J. Praetorius, S. Nielsen, and P. Agre Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver Proc Natl Acad Sci USA 100 2003 2945 2950
196. P.D. Roepe The role of the MDR protein in altered drug translocation across tumor cell membranes Biochim Biophys Acta 1241 1995 385 405
197. P.D. Roepe, L.Y. Wei, M.M. Hoffman, and F. Fritz Altered drug translocation mediated by the MDR protein: direct, indirect, or both? J Bioenerg Biomembr 28 1996 541 555
198. H.G. Keizer, and H. Joenje Increased cytosolic pH in multidrug-resistant human lung tumor cells: effect of verapamil J Natl Cancer Inst 81 1989 706 709
199. M.M. Hoffman, L.Y. Wei, and P.D. Roepe Are altered pHi and membrane potential in hu MDR 1 transfectants sufficient to cause MDR protein-mediated multidrug resistance? J Gen Physiol 108 1996 295 313
200. P.P. Szotek, R. Pieretti-Vanmarcke, and P.T. Masiakos Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian inhibiting substance responsiveness Proc Natl Acad Sci USA 103 2006 11154 11159
201. C. Aguilar-Gallardo, E. Cecilia Rutledge, A.M. Martinez-Arroyo, J.J. Hidalgo, S. Domingo, and C. Simon Overcoming challenges of ovarian cancer stem cells: novel therapeutic approaches Stem Cell Rev Reports 8 2012 994 1010
202. + channels and SDF-1 in acute leukemic cell migration Exp Cell Res 315 2009 2256 2264
203. + channel in the CD133(+) subpopulation of SH-SY5Y neuroblastoma cells Biochem Biophys Res Commun 396 2010 637 642
204. K.S. Suh, and S.H. Yuspa Intracellular chloride channels: critical mediators of cell viability and potential targets for cancer therapy Curr Pharm Des 11 2005 2753 2764
205. J.L. Fiske, V.P. Fomin, M.L. Brown, R.L. Duncan, and R.A. Sikes Voltage-sensitive ion channels and cancer Cancer Metastasis Rev 25 2006 493 500
206. S. Roger, M. Potier, C. Vandier, P. Besson, and J.Y. Le Guennec Voltage-gated sodium channels: new targets in cancer therapy? Curr Pharm Des 12 2006 3681 3695
207. J.Y. Le Guennec, H. Ouadid-Ahidouch, O. Soriani, P. Besson, A. Ahidouch, and C. Vandier Voltage-gated ion channels, new targets in anti-cancer research Recent Pat Anticancer Drug Discov 2 2007 189 202
208. H. Wulff, N.A. Castle, and L.A. Pardo Voltage-gated potassium channels as therapeutic targets Nat Rev Drug Discov 8 2009 982 1001
209. L.A. Pardo, D. del Camino, and A. Sanchez Oncogenic potential of EAG K(+) channels EMBO J 18 1999 5540 5547
210. K. Shield, M.L. Ackland, N. Ahmed, and G.E. Rice Multicellular spheroids in ovarian cancer metastases: biology and pathology Gynecol Oncol 113 2009 143 148
211. I.M. Shih, and R.J. Kurman Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis Am J Pathol 164 2004 1511 1518