Paradoxical effects of sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) activator gingerol on NG115-401L neuronal cells: Failure to augment ER Ca2+ uptake and protect against ER stress-induced cell death

European Journal of Pharmacology

Volumn 762, Issue 1, 2015, Pages 165-173

  Zhang, Changfeng ^a   Bose, Diptiman D ^b   Thomas, David W ^a  

^a UNIVERSITY OF THE PACIFIC   (United States)

^b WESTERN NEW ENGLAND UNIVERSITY   (United States)

Author keywords

Calcium; ER stress; Gingerol; Neuroprotection; SERCA

Indexed keywords

CALCIUM ION; CASPASE; GINGEROL; REACTIVE OXYGEN METABOLITE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN; CALCIUM; CATECHOL DERIVATIVE; CYCLOPIAZONIC ACID; ENZYME ACTIVATOR; ENZYME INHIBITOR; FATTY ALCOHOL; INDOLE DERIVATIVE;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELL ISOLATION; CELL PROTECTION; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; ENDOPLASMIC RETICULUM STRESS; MICROSOME; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; ENDOPLASMIC RETICULUM; HOMEOSTASIS; METABOLISM; RABBIT; SARCOPLASMIC RETICULUM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CATECHOLS; CELL DEATH; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATORS; ENZYME INHIBITORS; FATTY ALCOHOLS; HOMEOSTASIS; INDOLES; MICROSOMES; NEURONS; RABBITS; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; THAPSIGARGIN;

EID: 84937424024     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.05.055     Document Type: Article

References (47)

1. M.T. Alonso, I.M. Manjarres, and J. Garcia-Sancho Privileged coupling between Ca(2+) entry through plasma membrane store-operated Ca(2+) channels and the endoplasmic reticulum Ca(2+) pump Mol. Cell. Endocrinol. 353 2012 37 44
2. D.D. Bose, R. Rahimian, and D.W. Thomas Activation of ryanodine receptors induces calcium influx in a neuroblastoma cell line lacking calcium influx factor activity Biochem. J. 386 2005 291 296
3. D.D. Bose, and D.W. Thomas 2-Aminoethoxydiphenyl borate (2-APB) stimulates a conformationally coupled calcium release pathway in the NG115-401L neuronal cell line Neuropharmacology 50 2006 532 539
4. D.D. Bose, and D.W. Thomas The actin cytoskeleton differentially regulates NG115-401L cell ryanodine receptor and inositol 1,4,5-trisphosphate receptor induced calcium signaling pathways Biochem. Biophys. Res. Commun. 379 2009 594 599
5. A. Chu, M.C. Dixon, A. Saito, S. Seiler, and S. Fleischer Isolation of sarcoplasmic reticulum fractions referable to longitudinal tubules and junctional terminal cisternae from rabbit skeletal muscle Methods Enzymol. 157 1988 36 46
6. J.D. Clausen, I. Vandecaetsbeek, F. Wuytack, P. Vangheluwe, and J.P. Andersen Distinct roles of the C-terminal 11th transmembrane helix and luminal extension in the partial reactions determining the high Ca2+ affinity of sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2b (SERCA2b) J. Biol. Chem. 287 2012 39460 39469
7. B. Costello, C. Chadwick, and S. Fleischer Isolation of the junctional face membrane of sarcoplasmic reticulum Methods Enzymol. 157 1988 46 50
8. P. Csutora, K. Peter, H. Kilic, K.M. Park, V. Zarayskiy, T. Gwozdz, and V.M. Bolotina Novel role for STIM1 as a trigger for calcium influx factor production J. Biol. Chem. 283 2008 14524 14531
9. G.W. Glazner, and P. Fernyhough Neuronal survival in the balance: are endoplasmic reticulum membrane proteins the fulcrum? Cell Calcium 32 2002 421 433
10. N. Henke, P. Albrecht, A. Pfeiffer, D. Toutzaris, K. Zanger, and A. Methner Stromal interaction molecule 1 (STIM1) is involved in the regulation of mitochondrial shape and bioenergetics and plays a role in oxidative stress J. Biol. Chem. 287 2012 42042 42052
11. A.M. Hofer, and T.E. Machen Technique for in situ measurement of calcium in intracellular inositol 1,4,5-trisphosphate-sensitive stores using the fluorescent indicator mag-fura-2 Proc. Natl. Acad. Sci. USA 90 1993 2598 2602
12. A.M. Hofer, and T.E. Machen Direct measurement of free Ca in organelles of gastric epithelial cells Am. J. Physiol. 267 1994 G442 G451
13. G. Inesi, T. Cantilina, X. Yu, D. Nikic, Y. Sagara, and M.E. Kirtley Long-range intramolecular linked functions in activation and inhibition of SERCA ATPases Ann. N. Y. Acad. Sci. 671 1992 32 47 (discussion 48)
14. G. Inesi, M. Kurzmack, and D. Lewis Kinetic and equilibrium characterization of an energy-transducing enzyme and its partial reactions Methods Enzymol. 157 1988 154 190
15. G. Inesi, C. Sumbilla, and M.E. Kirtley Relationships of molecular structure and function in Ca2(+)-transport ATPase Physiol. Rev. 70 1990 749 760
16. T.R. Jackson, S.I. Patterson, O. Thastrup, and M.R. Hanley A novel tumour promoter, thapsigargin, transiently increases cytoplasmic free Ca2+ without generation of inositol phosphates in NG115-401L neuronal cells Biochem. J. 253 1988 81 86
17. H. Jousset, M. Frieden, and N. Demaurex STIM1 knockdown reveals that store-operated Ca2+ channels located close to sarco/endoplasmic Ca2+ ATPases (SERCA) pumps silently refill the endoplasmic reticulum J. Biol. Chem. 282 2007 11456 11464
18. C. Kho, A. Lee, and R.J. Hajjar Altered sarcoplasmic reticulum calcium cycling - targets for heart failure therapy Nat. Rev. Cardiol. 9 2012 717 733
19. M. Kobayashi, Y. Ishida, N. Shoji, and Y. Ohizumi Cardiotonic action of [8]-gingerol, an activator of the Ca++-pumping adenosine triphosphatase of sarcoplasmic reticulum, in guinea pig atrial muscle J. Pharmacol. Exp. Ther. 246 1988 667 673
20. M. Kobayashi, N. Shoji, and Y. Ohizumi Gingerol, a novel cardiotonic agent, activates the Ca2+-pumping ATPase in skeletal and cardiac sarcoplasmic reticulum Biochim. Biophys. Acta 903 1987 96 102
21. E.G. Kranias, and R.J. Hajjar Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome Circ. Res. 110 2012 1646 1660
22. G. Krapivinsky, L. Krapivinsky, S.C. Stotz, Y. Manasian, and D.E. Clapham POST, partner of stromal interaction molecule 1 (STIM1), targets STIM1 to multiple transporters Proc. Natl. Acad. Sci. USA 108 2011 19234 19239
23. A.M. Lompre, R.J. Hajjar, S.E. Harding, E.G. Kranias, M.J. Lohse, and A.R. Marks Ca2+ cycling and new therapeutic approaches for heart failure Circulation 121 2010 822 830
24. J. Lytton, M. Westlin, S.E. Burk, G.E. Shull, and D.H. MacLennan Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps J. Biol. Chem. 267 1992 14483 14489
25. I.M. Manjarres, A. Rodriguez-Garcia, M.T. Alonso, and J. Garcia-Sancho The sarco/endoplasmic reticulum Ca(2+) ATPase (SERCA) is the third element in capacitative calcium entry Cell Calcium 47 2010 412 418
26. M.P. Mattson Calcium and neurodegeneration Aging Cell 6 2007 337 350
27. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Gorgun, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
28. S.W. Park, Y. Zhou, J. Lee, and U. Ozcan Sarco(endo)plasmic reticulum Ca2+-ATPase 2b is a major regulator of endoplasmic reticulum stress and glucose homeostasis in obesity Proc. Natl. Acad. Sci. USA 107 2010 19320 19325
29. J.A. Rosado, J.A. Pariente, G.M. Salido, and P.C. Redondo SERCA2b activity is regulated by cyclophilins in human platelets Arterioscler. Thromb. Vasc. Biol. 30 2010 419 425
30. Y. Sagara, and G. Inesi Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations J. Biol. Chem. 266 1991 13503 13506
31. A. Sampieri, A. Zepeda, A. Asanov, and L. Vaca Visualizing the store-operated channel complex assembly in real time: identification of SERCA2 as a new member Cell Calcium 45 2009 439 446
32. D. Scheuner, and R.J. Kaufman The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes Endocr. Rev. 29 2008 317 333
33. J.P. Schmitt, M. Kamisago, M. Asahi, G.H. Li, F. Ahmad, U. Mende, E.G. Kranias, D.H. MacLennan, J.G. Seidman, and C.E. Seidman Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban Science 299 2003 1410 1413
34. N.W. Seidler, I. Jona, M. Vegh, and A. Martonosi Cyclopiazonic acid is a specific inhibitor of the Ca2+-ATPase of sarcoplasmic reticulum J. Biol. Chem. 264 1989 17816 17823
35. N. Shoji, A. Iwasa, T. Takemoto, Y. Ishida, and Y. Ohizumi Cardiotonic principles of ginger (Zingiber officinale Roscoe) J. Pharm. Sci. 71 1982 1174 1175
36. G.E. Stutzmann, and M.P. Mattson Endoplasmic reticulum Ca(2+) handling in excitable cells in health and disease Pharmacol. Rev. 63 2011 700 727
37. D. Thomas, and M.R. Hanley Evaluation of calcium influx factors from stimulated Jurkat T-lymphocytes by microinjection into Xenopus oocytes J. Biol. Chem. 270 1995 6429 6432
38. D. Thomas, H.Y. Kim, and M.R. Hanley Regulation of inositol trisphosphate-induced membrane currents in Xenopus oocytes by a Jurkat cell calcium influx factor Biochem. J. 318 1996 649 656
39. D. Thomas, H.Y. Kim, and M.R. Hanley Capacitative calcium influx Vitam. Horm. 54 1998 97 119
40. X. Tong, A. Evangelista, and R.A. Cohen Targeting the redox regulation of SERCA in vascular physiology and disease Curr. Opin. Pharmacol. 10 2010 133 138
41. L. Vaca SOCIC: the store-operated calcium influx complex Cell Calcium 47 2010 199 209
42. A. Verkhratsky Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons Physiol. Rev. 85 2005 201 279
43. A. Verkhratsky, and O.H. Petersen The endoplasmic reticulum as an integrating signalling organelle: from neuronal signalling to neuronal death Eur. J. Pharmacol. 447 2002 141 154
44. F. Wuytack, L. Raeymaekers, H. De Smedt, J.A. Eggermont, L. Missiaen, L. Van Den Bosch, S. De Jaegere, H. Verboomen, L. Plessers, and R. Casteels Ca(2+)-transport ATPases and their regulation in muscle and brain Ann. N. Y. Acad. Sci. 671 1992 82 91
45. F. Wuytack, L. Raeymaekers, and L. Missiaen Molecular physiology of the SERCA and SPCA pumps Cell Calcium 32 2002 279 305
46. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
47. B. Zhivotovsky, and S. Orrenius Calcium and cell death mechanisms: a perspective from the cell death community Cell Calcium 50 2011 211 221