Big Potassium (BK) ion channels in biology, disease and possible targets for cancer immunotherapy

International Immunopharmacology

Volumn 22, Issue 2, 2014, Pages 427-443

  Ge, Lisheng ^a   Hoa, Neil T ^a   Wilson, Zechariah ^a   Arismendi Morillo, Gabriel ^b   Kong, Xiao Tang ^c   Tajhya, Rajeev B ^d   Beeton, Christine ^d   Jadus, Martin R ^a,e  

^a VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^b UNIVERSIDAD DEL ZULIA   (Venezuela)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BK ion channels; Cancer; Glioma; Microarray; Migration; Proliferation

Indexed keywords

BK CHANNEL GAMMA SUBUNIT; CANCER VACCINE; GBK PROTEIN; HBR5 PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; ION CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; STRESS AXIS REGULATED EXON PROTEIN; UNCLASSIFIED DRUG; ISOPROTEIN; PROTEIN SUBUNIT;

CANCER CELL; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CELL DEATH; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; DRUG TARGETING; GENE SWITCHING; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEOMICS; REGULATORY MECHANISM; REVIEW; SPLICING DEFECT; ANIMAL; CHEMISTRY; IMMUNOTHERAPY; METABOLISM; NEOPLASMS; PROTEIN SUBUNIT;

ANIMALS; CANCER VACCINES; HUMANS; IMMUNOTHERAPY; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; NEOPLASMS; PROTEIN ISOFORMS; PROTEIN SUBUNITS;

EID: 84928741390     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2014.06.040     Document Type: Review

References (221)

1. E.C. Cooper, and L.Y. Jan Ion channel genes and human neurological disease: recent progress, prospects, and challenges Proc Natl Acad Sci U S A 96 9 1999 4759 4766
2. S.M. Huber Oncochannels Cell Calcium 53 4 Apr 2013 241 255
3. B. Hille Ion channels of excitable membranes 3rd ed. 2001 Sinauer Assoc. Sunderland, MA
4. F.M. Ashcroft Molecule to malady Nature 440 7083 2006 440 447
5. J.P. Overington, B. Al-Lazikani, and A.L. Hopkins How many drug targets are there? Nat Rev Drug Discov 5 12 2006 993 996
6. L.A. Pardo, and W. Stühmer The roles of K(+) channels in cancer Nat Rev Cancer 14 1 2014 39 48
7. A. Arcangeli, O. Crociani, E. Lastraioli, A. Masi, S. Pillozzi, and A. Becchetti Targeting ion channels in cancer: a novel frontier in antineoplastic therapy Curr Med Chem 16 1 2009 66 93
8. S.F. Pedersen, and C. Stock Ion channels and transporters in cancer: pathophysiology, regulation, and clinical potential Cancer Res 73 2013 1658 1661
9. N. Prevarskaya, R. Skryma, and Y. Shuba Ion channels and the hallmarks of cancer Trends Mol Med 16 2010 107 121
10. M. Li, and Z.G. Xiong Ion channels as targets for cancer therapy Int J Physiol Pathophysiol Pharmacol 3 2011 249 256
11. V.A. Cuddapah, and H. Sontheimer Ion channels and transporters in cancer. 2. Ion channels and the control of cancer cell migration Am J Physiol Cell Physiol 301 2011 156 166
12. R. Schönherr Clinical relevance of ion channels for diagnosis and therapy of cancer J Membr Biol 205 3 2005 175 184
13. X. Ding, H. He, Y. Lu, and Y. Wang Ionic channels in the therapy of malignant glioma, novel therapeutic concepts in targeting glioma 2012 Multidisciplinary Open Access Publisher: Intech 32
14. K. Kunzelmann Ion channels and cancer J Membr Biol 205 3 Jun 2005 159 173
15. A. Felipe, R. Vicente, N. Villalonga, M. Roura-Ferrer, R. Martínez-Mármol, and L. Solé et al. Potassium channels: new targets in cancer therapy Cancer Detect Prev 30 2006 375 385
16. R.J. Molenaar Ion channels in glioblastoma 2011 ISRN Neurology
17. L. Toro, M. Li, Z. Zhang, H. Singh, Y. Wu, and E. Stefani MaxiK channel and cell signalling Pflugers Arch 466 5 2014 875 886
18. R. Lu, A. Alioua, Y. Kumar, M. Eghbali, E. Stefani, and L. Toro Maxi-K channel partners: physiological impact J Physiol 570 2006 65 72
19. R. Latorre, A. Oberhauser, P. Labarca, and O. Alvarez Varieties of calcium-activated potassium channels Annu Rev Physiol 51 1989 385 399
20. V.K. Gribkoff, J.E. Starrett Jr.; and S.I. Dworetzky The pharmacology and molecular biology of large-conductance calcium-activated (BK) potassium channels Adv Pharmacol 37 1997 319 348
21. V.K. Gribkoff, J.E. Starret Jr.; and S.I. Dworetzky Maxi-K potassium channels: form, function, and modulation of a class of endogenous regulators of intracellular calcium Neuroscientist 7 2001 166 177
22. M.J. Ackerman, and D.E. Clapham Ion channels - basic science and clinical disease N Engl J Med 336 1997 1575 1586
23. U.S. Lee, and J. Cui BK channel activation: structural and functional insights Trends Neurosci 33 9 2010 415 423
24. F. Vetri, M.S.R. Choudhury, D.A. Pelligrino, and P. Sundivakkam BKCa channels as physiological regulators: a focused review J Receptor Ligand Channel Res 7 2014 3 13
25. Y.N. Jan, L.Y. Jan, and M.J. Dennis Two mutations of synaptic transmission in Drosophila Proc R Soc Lond B Biol Sci 198 1130 1977 87 108
26. D.M. Papazian, T.L. Schwarz, B.L. Tempel, Y.N. Jan, and L.Y. Jan Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila Science 237 4816 1987 749 753
27. L. Pallanck, and B. Ganetzky Cloning and characterization of human and mouse homologs of the Drosophila calcium-activated potassium channel gene, slowpoke Hum Mol Genet 3 8 Aug 1994 1239 1243
28. R.W. Meech Calcium-dependent potassium activation in nervous tissues Annu Rev Biophys Bioeng 7 1978 1 18
29. J. Tseng-Crank, C.D. Foster, J.D. Krause, R. Mertz, N. Godinot, and T.J. DiChiara et al. Cloning, expression, and distribution of functionally distinct Ca(2 +)-activated K + channel isoforms from human brain Neuron 13 6 1994 1315 1330
30. P.R. Adams, A. Constanti, D.A. Brown, and R.B. Clark Intracellular Ca2 + activates a fast voltage-sensitive K + current in vertebrate sympathetic neurones Nature 296 5859 1982 746 749
31. X. Hu, T. Laragione, L. Sun, S. Koshy, K.R. Jones, and I.I. Ismailov et al. KCa1.1 potassium channels regulate key proinflammatory and invasive properties of fibroblast-like synoviocytes in rheumatoid arthritis J Biol Chem 287 6 2012 4014 4022
32. K. Nehrke, C.C. Quinn, and T. Begenisich Molecular identification of Ca2 +-activated K + channels in parotid acinar cells Am J Physiol Cell Physiol 284 2 Feb 2003 C535 C546
33. M.E. Werner, P. Zvara, A.L. Meredith, R.W. Aldrich, and M.T. Nelson Erectile dysfunction in mice lacking the large-conductance calcium-activated potassium (BK) channel J Physiol 567 Pt 2 2005 545 556
34. + channel J Biol Chem 279 2004 36746 36752
35. 2 +-activated potassium (BK) alpha-subunit but not the BKbeta1-subunit leads to progressive hearing loss Proc Natl Acad Sci U S A 101 2004 12922 12927
36. + channel deficiency Proc Natl Acad Sci U S A 101 2004 9474 9478
37. 2 + sensing Neuron 66 2010 871 883
38. W. Du, J.F. Bautista, H. Yang, A. Diez-Sampedro, S.A. You, and L. Wang et al. Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder Nat Genet 37 2005 733 738
39. M, E. Vázquez, J.M. Fernández-Fernández, I. Subirana, C. Plata, and M. Heras et al. Genetic variation in the KCNMA1 potassium channel alpha subunit as risk factor for severe essential hypertension and myocardial infarction J Hypertens 26 2008 2147 2153
40. + channel of the BK-type in the inner mitochondrial membrane of a human glioma cell line Biochem Biophys Res Commun 257 1999 549 554
41. + channel openers NS1619 and NS004 as inhibitors of mitochondrial function in glioma cells Biochem Pharmacol 65 2003 1827 1834
42. H. Singh, R. Lu, J.C. Bopassa, A.L. Meredith, E. Stefani, and L. Toro MitoBK(Ca) is encoded by the Kcnma1 gene, and a splicing sequence defines its mitochondrial location Proc Natl Acad Sci U S A 110 2013 10836 10841
43. M.J. Shipston Alternative splicing of potassium channels: a dynamics switch of cellular excitability Trends Cell Biol 11 2001 353 358
44. H.A. Widmer, I.C.M. Rowe, and M.J. Shipston Conditional protein phosphorylation regulates BK channel activity in rat cerebellar Pukinje neurons J Physiol 552 2003 379 391
45. + channel transcripts in inner ear hair cells Gene 386 2007 11 23
46. + channel splice variants among hair cells along the tonotopic axis of the chick cochlea Neuron 19 1997 1077 1085
47. J. Liu, M. Asuncion-Chin, P. Liu, and A.M. Dopico CaM kinase II phosphorylation of slo Thr107 regulates activity and ethanol responses of BK channels Nat Neurosci 9 2005 41 49
48. O. Jeffries, N. Geiger, I.C.M. Rowe, L. Tian, H. McClafferty, and L. Chen et al. Palmitoylation of the S0-S1 linker regulates cell surface expression of voltage- and calcium-activated potassium (BK) channels J Biol Chem 285 2010 33307 33314
49. L.J. Tian, H. McClafferty, O. Jeffries, and M.J. Shipston Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels J Biol Chem 285 2010 23954 23962
50. X. Zhou, I. Wulfsen, M. Korth, H. McClafferty, R. Lukowski, and M.J. Shipston et al. Palmitoylation and membrane association of STREX controls BK channel regulation by protein kinase C J Biol Chem 287 2012 32161 32171
51. M.J. Shipston Ion channel regulation by protein S-acylation J Gen Physiol 2014 10.1085/jgp.201411176
52. + channel (Slo1) via serine/threonine residues regulates channel surface expression Proc Natl Acad Sci U S A 108 2011 10744 10749
53. D.A. Doyle, J. Morais Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, and S.L. Cohen et al. The structure of the potassium channel: molecular basis of K + conduction and selectivity Science 280 5360 Apr 3 1998 69 77
54. 2 +-activation apparatus at 3.0 Å resolution Science 329 2010 182 186
55. L. Wang, and F.J. Sigworth Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy Nature 461 2009 292 295
56. X.M. Xia, X. Zeng, and C.J. Lingle Multiple regulatory sites in large-conductance calcium-activated potassium channels Nature 418 2002 880 884
57. X. Liu, Y. Chang, P.H. Reinhart, H. Sontheimer, and Y. Chang Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in glioma cells J Neurosci 22 2002 1840 1849
58. L. Ge, A.N. Cornforth, N. Hoa, D.A. Bota, A. Mai, and D.I. Kim et al. Glioma BK channel expression in human cancers and possible T cell epitopes for their immunotherapy J Immunol 189 2012 2625 2634
59. J.A. Steitz Snurps Sci Am 258 1988 56 63
60. B. Chabot, and J.A. Steitz Multiple interactions between the splicing substrate and small nuclear ribonucleoproteins in spliceosomes Mol Cell Biol 7 1987 281 293
61. D. Dixit, V. Sharma, S. Ghosh, V.S. Mehta, and E. Sen Inhibition of casein kinase-2 induces p53-dependent cell cycle arrest and sensitizes glioblastoma cells to tumor necrosis factor (TNFα)-induced apoptosis through SIRT1 inhibition Cell Death Dis 3 2012 e271
62. J. Kroonen, M. Artesi, V. Capraro, M.T. Nguyen-Khac, M. Willems, and A. Chakravarti et al. Casein kinase 2 inhibition modulates the DNA damage response but fails to radiosensitize malignant glioma cells Int J Oncol 41 2012 776 782
63. M. Agarwal, R.T. Nitta, and G. Li Casein kinase 2: a novel player in glioblastoma therapy and cancer stem cells J Mol Genet Med 7 2014 94 10.4172/1747-0862.1000094
64. B.F. Yang, C. Xiao, W.H. Roa, P.H. Krammer, and C. Hao Calcium/calmodulin-dependent protein kinase II regulation of c-FLIP expression and phosphorylation in modulation of fas-mediated signaling in malignant glioma cells J Biol Chem 278 2003 7043 7050
65. E.H.C. Cheng, F.S. Gorelick, A.J. Czernik, D.M. Bagaglio, and W.N. Hait Calmodulin-dependent protein kinases in rat glioblastoma Cell Growth Differ 6 1995 615 621
66. A. Misra-Press, A.P. Fields, D. Samols, and D.A. Goldthwait Protein kinase C isoforms in human glioblastoma cells Glia 6 1992 188 197
67. H. Xiao, D.A. Goldthwait, and T. Mapstone The identification of four protein kinase C isoforms in human glioblastoma cell lines: PKC alpha, gamma, epsilon, and zeta J Neurosurg 81 1994 734 740
68. G.J. Lai, and D.P. McCobb Opposing actions of adrenal androgens and glucocorticoids on alternative splicing of Slo potassium channels in bovine chromaffin cells Proc Natl Acad Sci U S A 99 2002 7722 7727
69. N. Zhu, M. Eghbali, G. Helguera, M. Song, E. Stefani, and L. Toro Alternative splicing of Slo channel gene programmed by estrogen, progesterone and pregnancy FEBS Lett 579 2005 4856 4860
70. J. Xie, and D.P. McCobb Control of alternative splicing of potassium channels by stress hormones Science 280 1998 443 446
71. G. Liu, A. Razanau, Y. Hai, J. Yu, M. Sohail, and V.G. Lobo et al. A conserved serine of heterogeneous nuclear ribonucleoprotein L (hnRNPL) mediates depolarization-regulated alternative splicing of potassium channels J Biol Chem 287 2012 22709 22716
72. N. Yajima, R. Yamanaka, T. Mine, N. Tsuchiya, J. Homma, and M. Sano et al. Immunologic evaluation of personalized peptide vaccination for patients with advanced malignant glioma Clin Cancer Res 11 2005 5900 5911
73. J.G. Zhang, C.A. Kruse, L. Driggers, N. Hoa, J. Wisoff, and J.C. Allen et al. Tumor antigenic profiles of adult and pediatric brain tumors J Neurooncol 88 2008 65 76
74. N.T. Hoa, L. Ge, C. Beeton, R.B. Tajhya, A. Abolhoda, and A.N. Cornforth et al. Small cell lung cancer cells express a late stage tumor antigen, gBK; its implications for preventing the terminal disease Am J Trans Med 6 2014 188 205
75. P. Orio, P. Rojas, G. Ferreira, and R. Latorre New disguises for an old channel: MaxiK channel beta-subunits News Physiol Sci 17 2002 156 161
76. R. Brenner, T.J. Jegla, A. Wickenden, Y. Liu, and R.W. Aldrich Cloning and functional characterization of novel large conductance calcium-activated potassium channel β subunits, hKCNMB3 and hKCNMB4 J Biol Chem 275 2000 6453 6461
77. Z. Jiang, M. Wallner, P. Meera, and L. Toro Human and rodent maxiK channel β-subunit genes: cloning and characterization Genomics 55 1999 57 67
78. M.A. Valverde, P. Rojas, J. Amigo, D. Cosmelli, P. Orio, and M.I. Bahamonde et al. Acute activation of maxi-K channels (hSlo) by estradiol binding to the β-subunit Science 285 1999 1929 1931
79. J.T. King, P.V. Lovell, M. Rishniw, M.I. Kotlikoff, M.L. Zeeman, and D.P. McCobb β2 and β4 subunits of BK channels confer differential sensitivity to acute modulation by steroid hormones J Neurophysiol 95 2006 2878 2888
80. I.A. Greenwood, L.J. Miller, S. Ohya, and B. Horowitz The large conductance potassium channel-subunit can interact with and modulate the functional properties of a calcium-activated chloride channel, CLCA1 J Biol Chem 277 2002 22119 22122
81. Z.L. Bergeron, and J.P. Bingham Scorpion toxins specific for potassium (K +) channels: a historical overview of peptide bioengineering Toxins 4 2012 1082 1119
82. M.J. Schneider, R.S. Rogowski, B.K. Krueger, and M.P. Blaustein Charybdotoxin blocks both Ca-activated K channels and Ca-independent voltage-gated K channels in rat brain synaptosomes FEBS Lett 250 1989 433 446
83. + channel resistant to charybdotoxin and iberiotoxin Proc Natl Acad Sci U S A 97 2000 5562 5567
84. Y.D. Gao, and M.L. Garcia Interaction of agitoxin2, charybdotoxin, and iberiotoxin with potassium channels: selectivity between voltage-gated and Maxi-K channels Proteins 52 2003 146 154
85. J. Garcia-Valdes, F.Z. Zamudio, L. Toro, and L.D. Possan Slotoxin, αKTx1.11, a new scorpion peptide blocker of MaxiK channels that differentiates between α and α + β (β1 or β4) complexes FEBS Lett 505 2001 369 373
86. J. Shi, H.Q. He, R. Zhao, Y.H. Duan, J. Chen, and Y. Chen et al. Inhibition of martentoxin of neuronal BK channel subtype (α + β4): implications for a novel interaction model Biophys J 94 2008 3706 3713
87. J. Tao, J. Shi, L. Yan, Y. Chen, Y.H. Duan, and P. Ye et al. Enhancement effects of martentoxin on glioma BK channel and BK channel (α + β1) subtypes PLoS One 6 2012 e15896 10.1371/journal.pone.0015896
88. W.X. Wang, and Y.H. Ji Scorpion venom induces glioma cell apoptosis in vitro and inhibits glioma tumor growth in vivo J Neuro-Oncol 73 2005 1 7
89. M. Li, S. Chang, L. Yang, J. Shi, K. McFarland, and X. Yang et al. Conopeptide Vt3.1 preferentially inhibits BK potassium channels containing β4 subunits via electrostatic interactions J Biol Chem 289 2014 4735 4742
90. S. Shruti, J. Urban-Ciecko, J.A. Fitzpatrick, R. Brenner, M.P. Bruchez, and A.L. Barth The brain-specific beta4 subunit down-regulates BK channel cell surface expression PLoS One 7 2012 e33429 10.1371/journal.pone.0033429
91. E.Y. Kim, S. Zou, L.D. Ridgway, and S.E. Dryer β1-Subunits increase surface expression of a large-conductance Ca2 +-activated K + channel isoform J Neurophysiol 97 2007 3508 3516
92. 2 +)-activated K + channel 2007
93. X. Zeng, X.M. Xia, and C.J. Lingle Species-specific differences among KCNMB3 BKβ3 auxiliar;y subunits: some β3 N-terminal variants may be primate-specific subunits J Gen Physiol 132 2008 115 129
94. S. Hu, M.Z. Labuda, M. Pandolfo, G.G. Goss, H.E. McDermid, and D.W. Ali Variants of the KCNMB3 regulatory subunit of maxi BK channels affect channel inactivation Physiol Genomics 15 2003 191 198
95. S. Lorenz, A. Heils, J.M. Kasper, and T. Sander Allelic association of a truncation mutation of the KCNMB3 gene with idiopathic generalized epilepsy Am J Med Genet B Neuropsychiatr Genet 144B 2007 10 13
96. J. Yan, and R.W. Aldrich BK potassium channel modulation by leucine-rich repeat-containing proteins Proc Natl Acad Sci U S A 109 2012 7917 7922
97. J. Almassy, and T. Begenisich The LRRC26 protein selectivity alters the efficacy of BK channel activators Mol Pharmacol 8 2012 21 30
98. F. Lang, M. Föller, K.S. Lang, P.A. Lang, M. Ritter, and E. Gulbins et al. Ion channels in cell proliferation and apoptotic cell death J Membr Biol 205 2005 147 157
99. S.N. MacFarlane, and H. Sontheimer Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes Glia 30 2000 39 48
100. D. Urrego, A.P. Tomczak, F. Zahed, W. Stühmer, and L.A. Pardo Potassium channels in cell cycle and cell proliferation Phil Trans R Soc B 369 2014 20130094 10.1098/rstb.2013.0094
101. A.K. Weaver, X. Liu, and H. Sontheimer Role for calcium-activated potassium channels (BK) in growth control of human malignant glioma cells J Neurosci Res 78 2004 224 234
102. + conductance and cell proliferation in small-cell lung cancer Anticancer Res 13 1993 1231 1234
103. D. Khaitan, U.T. Sankpal, B. Weksler, E.A. Meister, I.A. Romero, and P.O. Couraud et al. Role of KCNMA1 gene in breast cancer invasion and metastasis to brain BMC Cancer 9 2009 258 10.1186/1471-2407-9-258
104. M. Bloch, J. Ousingsawat, R. Simon, P. Schraml, T.C. Gasser, and M.J. Mihatsch et al. KCNMA1 gene amplification promotes tumor cell proliferation in human prostate cancer Oncogene 26 2007 2525 2534
105. M. Oeggerli, Y. Tian, C. Ruiz, B. Wijker, G. Sauter, and E. Obermann et al. Role of KCNMA1 in breast cancer PLoS One 7 2012 e41664 10.1371/journal.pone. 0041664
106. G. Coiret, A.S. Borowiec, P. Mariot, H. Ouadid-Ahidouch, and F. Matifat The anti-estrogen tamoxifen activates BK channels and stimulates proliferation of MCF-7 breast cancer cells Mol Pharmacol 71 2007 843 851
107. M. Bury, A. Girault, V. Mégalizzi, S. Spiegl-Kreinecker, V. Mathieu, and W. Berger et al. Ophiobolin A induces paraptosis-like cell death in human glioblastoma cells by decreasing BKCa channel activity Cell Death Dis. 4 2013 e561
108. X. Han, L. Xi, H. Wang, X. Huang, X. Ma, and Z. Han et al. The potassium ion channel opener NS1619 inhibits proliferation and induces apoptosis in A2780 ovarian cancer cells Biochem Biophys Res Commun 375 2008 205 209
109. + channels support proliferation of colonic carcinoma cells FASEB J 21 2007 35 44
110. D. Basrai, R. Kraft, C. Bollensdorff, L. Liebmann, K. Benndorf, and C.A.S. Patt BK channel blockers inhibit potassium-induced proliferation of human astrocytoma cells Neuroreport 13 2002 403 407
111. I.F. Abdullaev, A. Rudkouskaya, A.A. Mongin, and Y.H. Kuo Calcium-activated potassium channels BK and IK1 are functionally expressed in human gliomas but do not regulate cell proliferation PLoS One 5 2010 e12304 10.1371/journal.pone.0012304
112. B. Cambien, R. Rezzonico, S. Vitale, B. Rouzaire-Dubois, J.M. Dubois, and R. Barthel et al. Silencing of hSlo potassium channels in human osteosarcoma cells promotes tumorigenesis Int J Cancer 123 2008 365 371
113. N. Hoa, J.G. Zhang, C. Delgado, M.P. Myers, L.L. Callahan, and G. Vandeusen et al. BK channel activation results in paraptosis: A possible mechanism to explain monocyte-mediated killing of tumor cells expressing membrane macrophage colony stimulating factor Lab Invest 87 2007 115 129
114. W.E. Dandy Removal of right cerebral hemisphere for certain tumors with hemiplegia: a preliminary report JAMA 90 1928 823 825
115. A. Bordey, H. Sontheimer, and J. Trouslard Muscarinic activation of BK channels induces membrane oscillations in glioma cells and leads to inhibition of cell migration J Membr Biol 176 2000 31 40
116. R. Kraft, P. Krause, S. Jung, D. Basrai, L. Liebmann, and J. Bolz et al. BK channel openers inhibit migration of human glioma cells Pflugers Arch 446 2003 248 255
117. L. Soroceanu, T.J. Manning Jr.; and H. Sontheimer Modulation of glioma cell migration and invasion using Cl - and K + ion channel blockers J Neurosci 19 1999 5942 5954
118. 2 +, BK channel activity and cell migration J Biomed Sci 16 2009 90 10.1186/1423-0127-16-90
119. A. Schwab Ion channels and transporters on the move Physiology 16 2001 29 33
120. H. Sontheimer An unexpected role for ion channels in brain tumor metastasis Exp Biol Med 233 2008 779 791
121. S. Watkins, and H. Sontheimer Hydrodynamic cellular volume changes enable glioma cell invasion J Neurosci 31 2011 17250 17259
122. + channels Radiother Oncol 101 2011 122 126
123. H. Zhao, and M. Sokabe Tuning the mechanosensitivity of a BK channel by changing the linker length Cell Res 18 2008 871 878
124. R. Rezzonico, C. Cayatte, I. Bourget-Ponzio, G. Romey, N. Belhacene, and A. Loubat et al. Focal adhesion kinase pp125FAK interacts with the large conductance calcium-activated hSlo potassium channel in human osteoblasts: potential role in mechanotransduction J Bone Miner Res 18 2003 1863 1871
125. L. Tian, H. McClafferty, L. Chen, and M.J. Shipston Reversible tyrosine protein phosphorylation regulates large conductance voltage- and calcium-activated potassium channels via cortactin J Biol Chem 283 2008 3067 3076
126. D. O'Malley, A.J. Irving, and J. Harvey Leptin-induced dynamic changes in the actin cytoskeleton mediated the activation and synaptic clustering of BK channels FASEB J 19 2005 1917 1919
127. C. Albiges-Rizo, O. Destaing, B. Fourcade, E. Planus, and M.R. Block Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions J Cell Sci 122 2009 3037 3049
128. N. Hoa, L. Ge, Y. Kuznetsov, A. McPherson, A.N. Conforth, and J.T.H. Pham et al. Glioma cells display complex cell surface topographies that resist the actions of cytolytic effector lymphocytes J Immunol 185 2010 4793 4803
129. G.J. Arismendi-Morillo, and A.V. Castellano-Ramirez Ultrastructural mitochondrial pathology in human astrocytic tumors: potential implications pro-therapeutics strategies J Electron Microsc 57 2008 33 39
130. G. Arismendi-Morillo, N.T. Hoa, L. Ge, and M. Jadus Mitochondrial network in glioma's invadopodia displays an activated state both in situ and in vitro: potential functional implications Ultrastruct Pathol 36 2012 409 414
131. A.Q. Dang, N.T. Hoa, L. Ge, G. Arismendi-Morillo, B. Paleo, and E.J. Gomez et al. Using REMBRANDT to paint in the details of glioma biology: applications for future immunotherapy Chapter 6 Terry Lichtor, Evolution of the molecular biology of brain tumors and the therapeutic implications 2013 978-953-51-0989-1 167 200
132. H.J. Scherer Structural development in gliomas Am J Cancer 34 1938 333 351
133. H.J. Scherer The forms of growth in gliomas and their practical significance Brain 63 1940 1 35
134. S.I. Poonnoose, and R.T. Daniel Radiological evidence of glioma invasion in the central nervous system along tracts Surg Neurol 54 2000 194 196
135. T. Donnem, J. Hu, M. Ferguson, O. Adighibe, C. Snell, and A.L. Harris et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med 2 2013 427 436
136. G. Arismendi-Morillo, and A. Castellano Tumoral micro-blood vessels and vascular microenvironment in human astrocytic tumors. A transmission electron microscopy study J Neurooncol 73 2005 211 217
137. R.G. Parton, and K. Simons The multiple faces of caveolae Nat Rev Mol Cell Biol 8 2007 185 194
138. M.O. Parat, and G.J. Riggens Caveolin-1 caveolae and glioblastoma Neuro Oncol 14 2012 679 688
139. E. Burgermeister, M. Liscovitcch, C. Röcken, R.M. Schmid, and M.P.A. Ebert Caveats of caveolin-1 in cancer progression Cancer Lett 268 2008 187 201
140. J.R. Martens, K. O'Connell, and M. Tamkun Targeting of ion channels to membrane microdomains: localization of KV channels to lipid rafts Trends Pharmacol Sci 25 2004 16 21
141. E.E. Daniel, A. El-Yazbi, and W.J. Cho Caveolae and calcium handling, a review and a hypothesis J Cell Mol Med 10 2006 529 544
142. A.F.G. Quest, J.L. Gutierrez-Pajares, and V.A. Torres Caveolin-1: an ambiguous partner in cell signaling and cancer J Cell Mol Med 12 2008 1130 1150
143. L.G. Pike Growth factor receptors, lipid rafts and caveolae: an evolving story Biochem Biophys Acta 1746 2005 260 273
144. A. Abulrob, S. Giuseppin, M.F. Andrade, A. McDermid, M. Moreno, and D. Stanimirovic Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae Oncogene 23 2004 6967 6979
145. + channels in vascular endothelial cells J Biol Chem 280 2005 11656 11664
146. M. Yamamoto, Y. Toya, R.A. Jensen, and Y. Ishikawa Caveolin is an inhibitor of platelet-derived growth factor receptor signaling Exp Cell Res 247 1999 380 388
147. A. Alioua, R. Lu, Y. Kumar, M. Eghbali, P. Kundu, and L. Toro et al. Slo1 caveolin-binding motif, a mechanism of caveolin-1-Slo1 interaction regulating Slo1 surface expression J Biol Chem 283 2008 4808 4817
148. A.M. Brainard, V.P. Korovkina, and S.K. England Disruption of the maxi-K-caveolin-1 interaction alters current expression in human myometrical cells Reprod Biol Endocrinol 7 2009 131 10.1186/1477-7827-7-131
149. E.P. Reeves, H. Lu, H.L. Jacobs, C.G.M. Messina, S. Bolsover, and G. Gabella et al. Killing activity of neutrophils is mediated through activation of proteases by K + flux Nature 416 2002 291 297
150. + channel is essential for innate immunity Nature 427 2004 853 858
151. J.K. Femling, V.V. Cherny, D. Morgan, B. Rada, A.P. Davis, and G. Czirják et al. The antibacterial activity of human neutrophils and eosinophils requires proton channels but not BK channels J Gen Physiol 127 2006 659 672
152. K. Essin, M. Gollasch, S. Rolle, P. Weissgerber, M. Sausbier, and E. Bohn et al. BK channels in innate immune functions of neutrophils and macrophages Blood 113 2009 1326 1331
153. T.E. DeCoursey, S.Y. Kim, M.R. Silver, and F.N. Quandt Ion channels expression in PMA-differentiated human THP-1 macrophages J Membr Biol 152 1996 141 157
154. O. Scheel, M. Papavlassopoulos, R. Blunck, A. Gebert, T. Hartung, and U. Zähringer et al. Cell activation by ligands of the toll-like receptor and interleukin-1 receptor family depends on the function of the large-conductance potassium channel MaxiK in human macrophages Infect Immun 74 2006 4354 4356
155. M. Papavlassopoulos, C. Stamme, L. Thon, D. Adam, D. Hillemann, and U. Seydel et al. MaxiK blockade selectively inhibits the lipopolysaccharide-induced I kappa B-alpha/NF-kappa B signaling pathway in macrophages J Immunol 177 2006 4086 4093
156. G. Panyi, C. Beeton, and A. Felipe Ion channels and anti-cancer immunity Phil Trans R Soc B 369 1638 2014 20130106
157. V. Chi, M.W. Pennington, R.S. Norton, E. Tarcha, L. Londono, and B. Sims-Fahey et al. Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases Toxicon 59 2012 529 546
158. C. Beeton, M.W. Pennington, and R.S. Norton Analogs of the sea anemone potassium channel blocker ShK for the treatment of autoimmune diseases Inflamm Allergy Drug Targets 10 2011 313 321
159. D.E. Bredeson, R.V. Rao, and P. Mehlen Cell death in the nervous system Nature 443 2006 796 802
160. A. Linkerman, and D.R. Green Necroptosis N Engl J Med 370 2014 455 465
161. I.S. Park, and J.E. Kim Potassium efflux during apoptosis J Biochem Mol Biol 35 2002 41 46
162. E. Maeno, Y. Ishizaki, T. Kanaseki, A. Hazama, and Y. Okada Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis Proc Natl Acad Sci U S A 97 2000 9487 9492
163. H. Yang, H. Wang, C.J. Czura, and K.J. Tracey The cytokine activity of HGMB1 J Leukoc Biol 78 2005 1 8
164. Y. Sha, J. Zmijewski, Z. Xu, and E. Abraham HMGB1 develops enhanced proinflammatory activity by binding to cytokines J Immunol 180 2008 2531 2537
165. S.P. Yu, and D.W. Choi Ions, cell volume, and apoptosis Proc Natl Acad Sci U S A 97 2000 9487 9492
166. + channels: an essential pathway in programmed cell death Am J Physiol Lung Cell Mol Physiol 286 2004 L49 L67
167. L. Wang, T. Li, and L. Lu UV-induced corneal epithelial cell death by activation of potassium channels Invest Ophthalmol Vis Sci 44 12 2003 5095 5101
168. +-exchanger leads to caspase-independent death of cerebellar granule neurons resembling paraptosis Cell Death Differ 11 2004 760 770
169. + efflux in the activation of apoptosis J Biol Chem 272 1997 32436 32442
170. + suppresses the activation of apoptosis in lymphocytes J Biol Chem 272 1997 30567 30576
171. J. Vakkila, and M.T. Lotze Inflammation and necrosis promote tumour growth Nat Rev Immunol 4 2004 641 648
172. M.P. Myers, J.G. Zhang, C. Delgado, L. Driggers, and L.L. Callahan et al. Molecular mechanisms of paraptosis induction: implications for a non-genetic modified tumor vaccine PLoS One 4 2009 e4631 10.1371/journal.pone0004631 [147-157]
173. S.E. Williams, S.P. Brazier, N. Baban, V. Telezhkin, C.T. Müller, and D. Riccardi et al. A structural motif in the C-terminal tail of Slo1 confers carbon monoxide sensitivity to human BKCa channels Pflugers Arch 456 2008 561 572
174. V. Telezhkin, S.P. Brazier, R. Mears, C.T. Müller, D. Riccardi, and P.J. Kemp Cysteine residue 911 in C-terminal tail of human BKCaα channel subunit is crucial for its activation by carbon monoxide Pflugers Arch 461 2011 665 675
175. S.E. Williams, P. Wootton, H.S. Mason, J. Bould, D.E. Iles, and D. Riccardi et al. Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel Science 306 2004 2093 2097
176. T.G. Douglass, L. Driggers, J.G. Zhang, N. Hoa, C. Delgado, and C.C. Williams et al. Macrophage colony stimulating factor: Not just for macrophages anymore! A gateway into complex biologies Int Immunopharmacol 8 2008 1354 1376
177. + antiport in cultured rat cells J Biol Chem 261 1986 5460 5466
178. +-exchanger leads to caspase-independent death of cerebellar granule neurons resembling paraptosis Cell Death Differ 11 2004 760 770
179. C. Delgado, N. Hoa, L.L. Callahan, P.M. Schiltz, R.A. Jahroudi, and J.G. Zhang et al. Generation of human immune responses towards a living U251MG glioma vaccine within SCID/beige mice Cytokine 38 2007 165 176
180. S. Basu, R.J. Binder, R. Suto, K.M. Anderson, and P.K. Srivastava Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate NF-κB pathway Int Immunol 12 2000 1539 1546
181. S. Basu, R.J. Binder, T. Ramalingam, and P.K. Srivastava CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70 and calreticulin Immunity 14 2001 303 313
182. M.C. Kuppner, R. Gastpar, S. Gelwar, E. Nossner, O. Ochmann, and A. Scharner et al. The role of heat shock protein (HSP70) in dendritic cell maturation: Hsp70 induces the maturation of immature dendritic cells but reduce DC differentiation from monocyte precursors Eur J Immunol 31 2001 1602 1609
183. A. Asea, S.K. Kraeft, E.A. Kurt-Jones, M.A. Stevenson, L.B. Chen, and R.W. Finberg et al. HSP70 stimulates cytokine production through a CD14-dependent pathway, demonstrating its dual role as a chaperone and cytokine Nat Med 6 2000 435 442
184. K. Chen, J. Huang, W. Gong, P. Iribarren, N.M. Dunlop, and J.M. Wang Toll-like receptors in inflammation, infection and cancer Int Immunopharmacol 7 2007 1271 1285
185. E. Pamer, and P. Cresswell Mechanisms of MHC class I-restricted antigen processing Annu Rev Immunol 16 1998 323 358
186. A.O. Gure, E. Stockert, M.J. Scanlan, R.S. Keresztes, D. Jager, and N.K. Altorki et al. Serological identification of embryonic neural proteins as highly immunogenic tumor antigens in small cell lung cancer Proc Natl Acad Sci U S A 97 2000 4198 4203
187. N.L. Müller, and R.R. Miller Neuroendocrine carcinomas of the lung Semin Roentgenol 25 1990 96 104
188. G. Bepler, G. Jaques, K. Neumann, G. Aumüller, C. Gropp, and K. Havemann Establishment, growth properties, and morphological characteristics of permanent human small cell lung cancer cell lines J Clin Oncol 113 1987 31 40
189. D.N. Carney, A.F. Gazdar, G. Bepler, J.G. Guccion, P.G. Marangos, and T.W. Moody et al. Establishment and identification of small cell lung cancer cell lines having classic and variant features Cancer Res 45 1985 2913 2923
190. H. Denz, M. Lechleitner, C. Marth, G. Daxenbichler, G. Gastl, and H. Braunsteiner Effect of human recombinant alpha-2-and gamma-interferon on the growth of human cell lines from solid tumors and hematologic malignancies J Interferon Res 5 1985 147 157
191. Y. Ücer, H. Bartsch, P. Scheurich, and K. Pfizenmaier Biological effects of γ-interferon on human tumor cells: quantity and affinity of cell membrane receptors for γ-IFN in relation to growth inhibition and induction of HLA-DR expression Int J Cancer 36 1985 103 108
192. H. Braumuller, T. Wieder, E. Brenner, S. Amann, M. Hahn, and M. Alkhaled et al. T-helper-1 cell cytokines drive cancer into senescence Nature 494 2013 361 365
193. M.M. Knüpfer, H. Knüpfer, V. Jendrossek, S. Van Gool, J.E. Wolff, and E. Keller Interferon-γ inhibits growth and migration of A172 human glioblastoma cells Anticancer Res 21 2001 3989 3994
194. Y.M. Ma, T. Sun, Y.X. Liu, N. Zhao, Q. Gu, and D.F. Zhang et al. A pilot study on acute inflammation and cancer: a new balance between IFN-γ and TGF-β in melanoma J Exp Clin Cancer Res 28 2009 23 10.1186/1756-9966-28-23
195. I. Yip, X.P. Pang, L. Berg, and J.M. Hershman Antitumor actions of interferon-γ and interleukin-1β on human papillary thyroid carcinoma cell lines J Clin Endocrinol Metab 80 1995 1664 1669
196. 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
197. G.E. Bertolesi, R. Walia Da Silva, C.A.B. Jollimore, C. Shi, S. Barnes, and M.E.M. Kelly Cav3.1 splice variant expression during neuronal differentiation of Y-79 retinoblastoma cells Neuroscience 141 2006 259 268
198. K. Nosho, S. Kure, N. Irahara, K. Shima, Y. Baba, and D. Spiegelman et al. A prospective cohort study shows unique epigenetic, genetic, and prognostic features of synchronous colorectal cancers Gastroenterology 137 2009 1609 1620
199. 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
200. S. Kure, K. Nosho, Y. Baba, N. Irahara, K. Shima, and K. Ng et al. Vitamin D receptor expression is associated with PIK3CA and KRAS mutations in colorectal cancer Cancer Epidemiol Biomarkers Prev 18 2009 2765 2772
201. S. Ogino, K. Nosho, N. Irahara, J.A. Meyerhardt, Y. Baba, and K. Shima et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype Clin Cancer Res 15 2009 6412 6420
202. F. Pagès, A. Berger, M. Camus, F. Sanchez-Cabo, A. Costes, and R. Molidor et al. Effector memory T cells, early metastasis, and survival in colorectal cancer N Engl J Med 353 2005 2654 2666
203. H. Colman, L. Zhang, E.P. Sulman, J.M. McDonald, N.L. Shooshtari, and A. Rivera et al. A multigene predictor of outcome in glioblastoma Neuro Oncol 12 2010 49 57
204. R. Bonavia, Inda MdM, W.K. Cavenee, and F.B. Furnari Heterogeneity maintenance in glioblastoma: a social network Cancer Res 71 2011 4055 4060
205. A. Sottoriva, I. Spiteri, S.G.M. Piccirillo, A. Touloumis, V.P. Collins, and J.C. Marioni et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics Proc Natl Acad Sci U S A 110 2013 4009 4014
206. H.S. Phillips, S. Kharbanda, R. Chen, W.F. Forrest, R.H. Soriano, and T.D. Wu et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis Cancer Cell 9 2006 157 173
207. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, and J. Squire et al. Identification of a cancer stem cell in human brain tumors Cancer Res 63 2003 5821 5828
208. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, and T. Hide et al. Identification of human brain tumour initiating cells Nature 432 2004 396 401
209. D. Beier, P. Hau, M. Proescholdt, A. Lohmeier, J. Wischhusen, and P.J. Oefner et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles Cancer Res 67 2007 4010 4015
210. S.K. Rao, J. Edwards, A.D. Joshi, I.M. Siu, and G.J. Riggins A survey of glioblastoma genomic amplifications and deletions J Neurooncol 96 2010 169 179
211. M.A. Pershouse, E. Stubblefield, A. Hadi, A.M. Killary, W.K.A. Yung, and P.A. Steck Analysis of the functional role of chromosome 10 loss in human glioblastomas Cancer Res 53 1993 5043 5050
212. Y. Hu, N. Ru, H. Xiao, A. Chaturbedi, N.T. Hoa, and X.J. Tian et al. Tumor-specific chromosome mis-segregation controls cancer plasticity by maintaining tumor heterogeneity PLoS One 8 11 2013 e80898 10.1371/journal.pone. 0080898
213. B. Sokolowski, S. Orchard, M. Harvey, S. Sridhar, and Y. Sakai Conserved BK channel-protein interactions reveal signals relevant to cell death and survival PLoS One 6 12 2010 e28532 10.1371/journal.pone.0028532
214. + channel in the mouse cochlea Mol Cell Proteomics 8 8 2009 1972 1987
215. P. Kundu, A. Alioua, Y. Kumar, R. Lu, J.W. Ou, and E. Sanchez-Pastor et al. Chapter 12: BK-channels: regulation of expression and physiological impact V.K. Gribkoff, L.K. Kaczmaerk, Function and modulation of neuronal voltage-gated ion channels 2009 Wiley
216. Ashraf A. Khalil Biomarker discovery: a proteomic approach for brain cancer profiling Cancer Sci 98 2007 201 213
217. Y. Iwadate, T. Sakaida, T. Hiwasa, Y. Nagai, H. Ishikura, and M. Takiguchi et al. Molecular classification and survival prediction in human gliomas based on proteome analysis Cancer Res 64 2004 2496 2501
218. B. Collet, N. Guitton, S. Saïkali, T. Avril, C. Pineau, and A. Hamlat et al. Differential analysis of glioblastoma multiforme proteome by a 2D-DIGE approach Proteome Sci 9 2011 16
219. R. Jiang, C. Mircean, I. Shmulevich, D. Cogdel, Y. Jia, and I. Tabus et al. Pathway alterations during glioma progression revealed by reverse phase protein lysate arrays Proteomics 6 2006 2964 2971
220. R. Zhang, T.L. Tremblay, A. McDermid, P. Thibault, and D. Stanimorovic Identification of differentially expressed proteins in human glioblastoma cell lines and tumors Glia 42 2003 194 208
221. Deighton R.F.; Mcgregor R.; Kemp J.; Mcculloch J.; Whittle I.R.; Glioma pathophysiology: insights emerging from proteomics.; Brain Pathol.; 2010.; 20.; 691-703