Differential Redox Regulation of Ca2+ Signaling and Viability in Normal and Malignant Prostate Cells

Biophysical Journal

Volumn 109, Issue 7, 2015, Pages 1410-1419

  Holzmann, Christian ^a   Kilch, Tatiana ^a   Kappel, Sven ^a   Dörr, Kathrin ^a   Jung, Volker ^a   Stöckle, Michael ^a   Bogeski, Ivan ^a   Peinelt, Christine ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; ORAI1 PROTEIN, HUMAN; ORAI3 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE; STIM1 PROTEIN, HUMAN; STROMAL INTERACTION MOLECULE 1; TUMOR PROTEIN;

CALCIUM SIGNALING; CELL SURVIVAL; EPITHELIUM CELL; GENE SILENCING; GENETICS; HUMAN; INTRACELLULAR SPACE; MALE; METABOLISM; OXIDATION REDUCTION REACTION; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROSTATE; PROSTATE TUMOR; RNA INTERFERENCE; TUMOR CELL LINE;

CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL LINE, TUMOR; CELL SURVIVAL; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR SPACE; MALE; MEMBRANE PROTEINS; NEOPLASM PROTEINS; ORAI1 PROTEIN; OXIDATION-REDUCTION; PATCH-CLAMP TECHNIQUES; PROSTATE; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; STROMAL INTERACTION MOLECULE 1;

EID: 84943555544     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.08.006     Document Type: Article

References (62)

1. D.C. Malins, and P.M. Johnson M.A. Vinson Age-related radical-induced DNA damage is linked to prostate cancer Cancer Res. 61 2001 6025 6028
2. H. Miyake, and I. Hara H. Eto Oxidative DNA damage in patients with prostate cancer and its response to treatment J. Urol. 171 2004 1533 1536
3. D.G. Bostwick, and E.E. Alexander T.D. Oberley Antioxidant enzyme expression and reactive oxygen species damage in prostatic intraepithelial neoplasia and cancer Cancer 89 2000 123 134
4. L. Khandrika, and B. Kumar H.K. Koul Oxidative stress in prostate cancer Cancer Lett. 282 2009 125 136
5. S.D. Lim, and C. Sun R.S. Arnold Increased Nox1 and hydrogen peroxide in prostate cancer Prostate 62 2005 200 207
6. I.P. Harrison, and S. Selemidis Understanding the biology of reactive oxygen species and their link to cancer: NADPH oxidases as novel pharmacological targets Clin. Exp. Pharmacol. Physiol. 41 2014 533 542
7. Y. Yang, and S. Karakhanova A.V. Bazhin Reactive oxygen species in cancer biology and anticancer therapy Curr. Med. Chem. 20 2013 3677 3692
8. A. Paschos, and R. Pandya J.H. Pinthus Oxidative stress in prostate cancer: changing research concepts towards a novel paradigm for prevention and therapeutics Prostate Cancer Prostatic Dis. 16 2013 217 225
9. J.A. Rosado, and P.C. Redondo J.A. Pariente Calcium signalling and reactive oxygen species in non-excitable cells Mini Rev. Med. Chem. 6 2006 409 415
10. Y. Yan, and C.L. Wei J. Liu Cross-talk between calcium and reactive oxygen species signaling Acta Pharmacol. Sin. 27 2006 821 826
11. A.V. Gordeeva, R.A. Zvyagilskaya, and Y.A. Labas Cross-talk between reactive oxygen species and calcium in living cells Biochemistry (Mosc.) 68 2003 1077 1080
12. K.Y. Kim, and H.J. Cho S.C. Ahn Interplay of reactive oxygen species, intracellular Ca2+ and mitochondrial homeostasis in the apoptosis of prostate cancer cells by deoxypodophyllotoxin J. Cell. Biochem. 114 2013 1124 1134
13. J.A. Savino 3rd, and J.F. Evans T.H. Carter Multiple, disparate roles for calcium signaling in apoptosis of human prostate and cervical cancer cells exposed to diindolylmethane Mol. Cancer Ther. 5 2006 556 563
14. I. Bogeski, and R. Kappl B.A. Niemeyer Redox regulation of calcium ion channels: chemical and physiological aspects Cell Calcium 50 2011 407 423
15. M. Grupe, and G. Myers A. Fleig Activation of store-operated I(CRAC) by hydrogen peroxide Cell Calcium 48 2010 1 9
16. S. Shimizu, N. Takahashi, and Y. Mori TRPs as chemosensors (ROS, RNS, RCS, gasotransmitters) Handbook Exp. Pharmacol. 223 2014 767 794
17. A.B. Parekh, and R. Penner Activation of store-operated calcium influx at resting InsP3 levels by sensitization of the InsP3 receptor in rat basophilic leukaemia cells J. Physiol. 489 1995 377 382
18. I. Bogeski, T. Kilch, and B.A. Niemeyer ROS and SOCE: recent advances and controversies in the regulation of STIM and Orai J. Physiol. 590 2012 4193 4200
19. R.S. Lewis Store-operated calcium channels: new perspectives on mechanism and function Cold Spring Harb. Perspect. Biol. 3 2011 a003970
20. W. Ji, and P. Xu L. Chen Functional stoichiometry of the unitary calcium-release-activated calcium channel Proc. Natl. Acad. Sci. USA 105 2008 13668 13673
21. A. Penna, and A. Demuro M.D. Cahalan The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers Nature 456 2008 116 120
22. A. Demuro, and A. Penna I. Parker Subunit stoichiometry of human Orai1 and Orai3 channels in closed and open states Proc. Natl. Acad. Sci. USA 108 2011 17832 17837
23. J. Madl, and J. Weghuber G.J. Schütz Resting state Orai1 diffuses as homotetramer in the plasma membrane of live mammalian cells J. Biol. Chem. 285 2010 41135 41142
24. Y. Maruyama, and T. Ogura C. Sato Tetrameric Orai1 is a teardrop-shaped molecule with a long, tapered cytoplasmic domain J. Biol. Chem. 284 2009 13676 13685
25. J.L. Thompson, and T.J. Shuttleworth How many Orai's does it take to make a CRAC channel? Sci. Rep. 3 2013 1961
26. X. Hou, and L. Pedi S.B. Long Crystal structure of the calcium release-activated calcium channel Orai Science 338 2012 1308 1313
27. M.M. Wu, E.D. Covington, and R.S. Lewis Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at endoplasmic reticulum-plasma membrane junctions Mol. Biol. Cell 25 2014 3672 3685
28. D. Balasuriya, and S. Srivats J.M. Edwardson Atomic force microscopy (AFM) imaging suggests that stromal interaction molecule 1 (STIM1) binds to Orai1 with sixfold symmetry FEBS Lett. 588 2014 2874 2880
29. A. Amcheslavsky, and M.L. Wood M.D. Cahalan Molecular biophysics of Orai store-operated Ca2+ channels Biophys. J. 108 2015 237 246
30. S.L. Zhang, and J.A. Kozak M.D. Cahalan Store-dependent and -independent modes regulating Ca2+ release-activated Ca2+ channel activity of human Orai1 and Orai3 J. Biol. Chem. 283 2008 17662 17671
31. A. Lis, and C. Peinelt R. Penner CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties Curr. Biol. 17 2007 794 800
32. Y. Gwack, and S. Srikanth A. Rao Biochemical and functional characterization of Orai proteins J. Biol. Chem. 282 2007 16232 16243
33. R. Schindl, and I. Frischauf C. Romanin Plasticity in Ca2+ selectivity of Orai1/Orai3 heteromeric channel Proc. Natl. Acad. Sci. USA 106 2009 19623 19628
34. C. Holzmann, and T. Kilch C. Peinelt ICRAC controls the rapid androgen response in human primary prostate epithelial cells and is altered in prostate cancer Oncotarget 4 2013 2096 2107
35. I. Bogeski, and C. Kummerow B.A. Niemeyer Differential redox regulation of ORAI ion channels: a mechanism to tune cellular calcium signaling Sci. Signal. 3 2010 ra24
36. O. Mignen, J.L. Thompson, and T.J. Shuttleworth The molecular architecture of the arachidonate-regulated Ca2+-selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits J. Physiol. 587 2009 4181 4197
37. D. Alansary, I. Bogeski, and B.A. Niemeyer Facilitation of Orai3 targeting and store-operated function by Orai1 Biochim. Biophys. Acta 1853 2015 1541 1550
38. R. Gulaboski, and I. Bogeski R. Kappl Hydroxylated derivatives of dimethoxy-1,4-benzoquinone as redox switchable earth-alkaline metal ligands and radical scavengers Sci. Rep. 3 2013 1865
39. B. Bufe, and T. Schumann F. Zufall Recognition of bacterial signal peptides by mammalian formyl peptide receptors: a new mechanism for sensing pathogens J. Biol. Chem. 290 2015 7369 7387
40. S.M. Davidson, and M.R. Duchen Calcium microdomains and oxidative stress Cell Calcium 40 2006 561 574
41. P.A. Singleton, and S. Pendyala V. Natarajan Dynamin 2 and c-Abl are novel regulators of hyperoxia-mediated NADPH oxidase activation and reactive oxygen species production in caveolin-enriched microdomains of the endothelium J. Biol. Chem. 284 2009 34964 34975
42. N. Kaludercic, S. Deshwal, and F. Di Lisa Reactive oxygen species and redox compartmentalization Front. Physiol. 5 2014 285
43. G.A. Gmyrek, and M. Walburg B.S. Knudsen Normal and malignant prostate epithelial cells differ in their response to hepatocyte growth factor/scatter factor Am. J. Pathol. 159 2001 579 590
44. A. Mantei, and S. Rutz A. Scheffold siRNA stabilization prolongs gene knockdown in primary T lymphocytes Eur. J. Immunol. 38 2008 2616 2625
45. G. Grynkiewicz, M. Poenie, and R.Y. Tsien A new generation of Ca2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
46. D. Alansary, and T. Kilch A. Lis The minimal requirements to use calcium imaging to analyze ICRAC Cold Spring Harb. Protoc. 2014 2014 638 642
47. CRAC and ORAI channel activity Cold Spring Harb. Protoc. 2014 2014 602 607
48. D. Alansary, and T. Kilch A. Lis Measuring endogenous ICRAC and ORAI currents with the patch-clamp technique Cold Spring Harb. Protoc. 2014 2014 630 637
49. H. Maeda, and S. Hori A. Kakizuka Effective treatment of advanced solid tumors by the combination of arsenic trioxide and L-buthionine-sulfoximine Cell Death Differ. 11 2004 737 746
50. M. Kobayashi, and M. Yamamoto Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation Antioxid. Redox Signal. 7 2005 385 394
51. J.M. Lee, and A.Y. Shih J.A. Johnson NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons J. Biol. Chem. 278 2003 37948 37956
52. H.L. Roderick, and S.J. Cook Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival Nat. Rev. Cancer 8 2008 361 375
53. M. Faouzi, and P. Kischel H. Ouadid-Ahidouch ORAI3 silencing alters cell proliferation and cell cycle progression via c-myc pathway in breast cancer cells Biochim. Biophys. Acta 1833 2013 752 760
54. R.K. Motiani, I.F. Abdullaev, and M. Trebak A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells J. Biol. Chem. 285 2010 19173 19183
55. + channel that promotes tumorigenesis FASEB J. 27 2013 63 75
56. M. Faouzi, and F. Hague H. Ouadid-Ahidouch Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells J. Cell. Physiol. 226 2011 542 551
57. C. Dubois, and F. Vanden Abeele N. Prevarskaya Remodeling of channel-forming ORAI proteins determines an oncogenic switch in prostate cancer Cancer Cell 26 2014 19 32
58. M. Flourakis, and V. Lehen'kyi N. Prevarskaya Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells Cell Death Dis. 1 2010 e75
59. K.A. Ahmad, and K.B. Iskandar S. Pervaiz Hydrogen peroxide-mediated cytosolic acidification is a signal for mitochondrial translocation of Bax during drug-induced apoptosis of tumor cells Cancer Res. 64 2004 7867 7878
60. 2+ currents by pH Cell Calcium 56 2014 235 243
61. S. Mancarella, and Y. Wang D.L. Gill Hypoxia-induced acidosis uncouples the STIM-Orai calcium signaling complex J. Biol. Chem. 286 2011 44788 44798
62. C.J. Schwiening, and D. Willoughby Depolarization-induced pH microdomains and their relationship to calcium transients in isolated snail neurones J. Physiol. 538 2002 371 382