Resveratrol and calcium signaling: Molecular mechanisms and clinical relevance

Molecules

Volumn 19, Issue 6, 2014, Pages 7327-7340

  McCalley, Audrey E ^a   Kaja, Simon ^a   Payne, Andrew J ^a   Koulen, Peter ^a,b  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; And amyotrophic lateral sclerosis; Autoimmune; Calcium; Cancer; Cardiovascular disease; Diabetes mellitus; Huntington's disease; Inflammation; Pain; Parkinson's disease; Resveratrol; Signaling

Indexed keywords

RESVERATROL; STILBENE DERIVATIVE;

ANIMAL; AUTOIMMUNE DISEASES; CALCIUM SIGNALING; DRUG EFFECTS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; AUTOIMMUNE DISEASES; CALCIUM SIGNALING; HUMANS; SIGNAL TRANSDUCTION; STILBENES;

EID: 84903287177     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules19067327     Document Type: Review

References (79)

1. Jeandet P.; Delaunois B.; Conreux A.; Donnez D.; Nuzzo V.; Cordelier S.; Clé ment C.; Courot E. Biosynthesis metabolism molecular engineering and biological functions of stilbene phytoalexins in plants. BioFactors 2010 36 331-341.
2. Jeandet P.; Clé ment C.; Courot E.; Cordelier S. Modulation of phytoalexin biosynthesis in engineered plants for disease resistance. Int. J. Mol. Sci. 2013 14 14136-14170.
3. Neves A.R.; Lucio M.; Lima J.L.; Reis S. Resveratrol in medicinal chemistry: A critical review of its pharmacokinetics drug-delivery and membrane interactions. Curr. Med. Chem. 2012 19 1663-1681.
4. Richard J.L. Coronary risk factors. The French paradox. Arch. Mal. Coeur Vaiss. 1987 80 17-21.
5. St Leger A.S.; Cochrane A.L.; Moore F. Factors associated with cardiac mortality in developed countries with particular reference to the con sumption of wine. Lancet 1979 1 1017-1020.
6. Criqui M.H.; Ringel B.L. Does diet or alcohol explain the French paradox? Lancet 1994 344 1719-1723.
7. Kroon P .A.; Iyer A.; Chunduri P.; Chan V.; Brown L. The cardiovascular nutrapharmacology of resveratrol: Pharmacokinetics molecular mechanisms and therapeutic potential. Curr. Med. Chem. 2010 17 2442-2455.
8. Bagatini P.B.; Saur L.; Rodrigues M.F.; Bernardino G.C.; Paim M.F.; Coelho G.P.; Silva D.V.; de Oliveira R.M.; Schirmer H.; Souto A.A.; et al. The role of calcium channel blockers and res veratrol in the prevention of paraquat-induced parkinsonism in Drosophila melanogaster: A locomotor analysis. Invertebr. Neurosci. 2011 11 43-51.
9. Granados-Soto V.; Arguelles C.F.; Ortiz M.I. The peripheral antinociceptive effect of resveratrol is associated with activation of potassium channels. Neuropharmacology 2002 43 917-923.
10. Park S.J.; Ahmad F.; Philp A.; Baar K.; Williams T.; Luo H.; Ke H.; Rehmann H.; Taussig R.; Brown A.L.; et al. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 2012 148 421-433.
11. Athar M.; Back J.H.; Tang X.; Kim K.H.; Kopelovich L.; Bickers D.R.; Kim A.L. Resveratrol: A review of preclinical studies for human cancer prevention. Toxicol. Appl. Pharm. 2007 224 274-28 3.
12. Yuan M.; Li J.; Lv J.; Mo X.; Yang C.; Chen X.; Liu Z.; Liu J. Polydatin (PD) inhibits IgE-mediated passive cutaneous anaphylaxis in mice by stabilizing mast cells through modulating Ca (2)(+) mobilization. Toxicol. Appl. Pharm. 2012 264 462-469.
13. Venkatesan B.; Valente A.J.; Reddy V.S.; Siwik D.A.; Chandrasekar B. Resveratrol blocks interleukin-18-EMMPRIN cross-regula tion and smooth muscle cell migration. Am. J. Physiol. Heart Circ. Physiol. 2009 297 H874-H886.
14. Naylor J.; Al-Shawaf E.; McKeown L.; Manna P.T.; Porter K.E.; O'Regan D.; Muraki K.; Beech D.J. TRPC5 channel sensitivities to antioxidants and hydroxylated stilbenes. J. Biol. Chem. 2011 286 5078-5086.
15. Wang Q.; Xu J.; Rottinghaus G.E.; Simony i A.; Lubahn D.; Sun G.Y.; Sun A.Y. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 2002 958 439-447.
16. Zhang H.; Schools G.P.; Lei T.; Wang W.; Kimelberg H.K.; Zhou M. Resveratrol attenuates early pyramidal neuron excitability impairment and death in acute rat hippocampal slices caused by oxygen-glucose deprivation. Exp. Neurol. 2008 212 44-52.
17. Chen W.P. Su M.J. Hung L.M Vitro electrophysiological mechanisms for antiarrhythmic efficacy of resveratrol a red wine antioxidant. Eur. J. Pharmacol. 2007 554 196-204
18. Ch en Y.R.; Yi F.F.; Li X.Y.; Wang C.Y.; Chen L.; Yang X.C.; Su P.X.; Cai J. Resveratrol attenuates ventricular arrhythmias and improves the long-term survival in rats with myocardial infarction. Cardiovasc. Drug. The r. 2008 22 479-485.
19. Calderone V.; Martelli A.; Testai L.; Martinotti E.; Breschi M.C. Functional contribution of the endothelial component to the vasorelaxing effect of resveratrol and N S 1619 activators of the large-conductance calcium-activated potassium channels. Naunyn-Schmiedeberg's Arch. Pharm. 2007 375 73-80.
20. Gojkovic-Bukarica L.; Novakovic A.; Kanjuh V.; Bumbasirevic M. ; Lesic A.; Heinle H. A role of ion channels in the endothelium-independent relaxation of rat mesenteric artery induced by resveratrol. J. Pharmacol. Sci. 2008 108 124-130.
21. Gao X.; Xu Y.X.; Janakiraman N.; Chapman R.A.; Gautam S.C. Immunomodulatory activity of resveratrol: Suppression of lymphocyte proliferation development of cell-mediated cytotoxicity and cytokine production. Biochem. Pharmacol. 2001 62 1299-1308.
22. Sharma S.; Anjaneyulu M.; Kulkarni S.K.; Chopra K. Resveratrol a polyphenolic phytoalexin attenuates diabetic nephropathy in rats. Pharmacology 2006 76 69-75.
23. Sheu S.J.; Wu T.T. Resveratrol protects against ultraviolet A-mediated inhibition of the phagocytic function of human retinal pigment epithelial cells via large-conductance calciumactivated potassium channels. Kaohsiung J. Med. Sci. 2009 25 381-388.
24. Sheu S.J.; Bee Y.S.; Chen C.H. Resveratrol and large-conductance calcium-activated potassium channels in the protection of human retinal pigment epithelial cells. J. Ocul. P harmacol. 2008 24 551-555.
25. Pirola L.; Frojdo S. Resveratrol: One molecule many targets. IUBMB Life 2008 60 323-332.
26. Sulaiman M.; Matta M.J.; Sunderesan N.R.; Gupta M.P.; Periasamy M.; Gupta M. Resveratrol an activator of SIRT1 upregulates sarcoplasmic calcium ATPase and improves cardiac function in diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 2010 298 H833-H843.
27. Sareen D.; Darjatmoko S.R.; Albert D.M.; Polans A.S. Mitochondria calcium and calpain are key mediators of resveratrol-induced apoptosis in breast cancer. Mol. Pharmacol. 2007 72 1466-1475.
28. Duncan R.S.; Goad D.L.; Grillo M.A.; Kaja S.; Payne A.J.; Koulen P. Control of intracellular calcium signaling as a neuroprotective strategy. Molecules 2010 15 1168-1195.
29. Jakab M.; Lach S.; Bacova Z.; Langeluddecke C.; Strbak V.; Schmidt S.; Iglseder E.; Paulmichl M.; Geibel J.; Ritter M. Resveratrol inhibits electrical activity and insulin release from ins ulinoma cells by block of voltage-gated Ca+ channels and swelling-dependent Cl-currents. Cell Physiol. Biochem. 2008 22 567-578.
30. Zhang L.P.; Yin J.X.; Liu Z.; Zhang Y.; Wang Q.S.; Zhao J. Effect of resveratrol on L-type calcium current in rat ventricular myocytes. Acta Pharmacol. Sin. 2006 27 179-183.
31. Dobrydneva Y.; Williams R.L.; Blackmore P.F. trans-Resveratrol inhibits calcium influx in thrombin-stimulated human platelets. Br. J. Pharmacol. 1999 128 149-157.
32. Tian X.M.; Zhang Z.X. [Resveratrol promote permeability transition pore opening mediated by Ca2+]. Yao Xue Xue Bao 2003 38 81-84.
33. Dobrydneva Y.; Williams R.L.; Blackmore P.F. Diethylstilbestrol and other nonsteroidal estrogens: Novel class of store-operated calcium channel modulators. J. Cardiovasc. Ph armacol. 2010 55 522-530.
34. Dobrydneva Y.; Williams R.L.; Katzenellenbogen J.A.; Ratz P.H.; Blackmore P.F. Diethylstilbestrol and tetrahydrochrysenes are calcium channel blockers in huma n platelets: Relationship to the stilbene pharmacophore. Thromb. Res. 2003 110 23-31.
35. Wang L.; Ma Q.; Chen X.; Sha H.; Ma Z. Effects of resveratrol on calcium regulation in rats with severe acute pancreatitis. Eur. J. Pharmacol. 2008 580 271-276.
36. Buluc M.; Demirel-Yilmaz E. Resveratrol decreases calcium sensitivity of vascular smooth muscle and enhances cytosolic calcium increase in endothelium. Vascul. Pharmacol. 2006 44 231-237.
37. Campos-Toimil M.; Elies J.; Alvarez E.; Verde I.; Orallo F. Effects of trans-and cis-resveratrol on Ca2+ handling in A7r5 vascular myoc ytes. Eur. J. Pharmacol. 2007 577 91-99.
38. Sangeetha M.K. Eazhisai Vallabi D. Sali V.K. Thanka J. Vasanthi H.RSub-acute toxicity profile of a modified resveratrol supplement. Food C hem. Toxicol. 2013 59 492-500.
39. Cottart C.H.; Nivet-Antoine V.; Beaudeux J.L. Review of recent data on the metabolism biological effects and toxicity of resveratrol in humans. Mol. Nutr. Food R es. 2013 58 7-21.
40. Zhang L.P.; Ma H.J.; Zhao J.; Wang Q.S. Effects of resveratrol on delayed afterdepolarization and triggered activity induced by ouabain in guinea pig papillary muscles. Sheng Li Xue Bao 2005 57 361-366.
41. Liu Z.; Zhang L.P.; Ma H.J.; Wang C.; Li M.; Wang Q.S. Resveratrol reduces intracellular free calcium concentration in rat ventricular myocytes . Sheng Li Xue Bao 2005 57 599-604.
42. Campos-Toimil M.; Elies J.; Orallo F. Trans-and cis-resveratrol increase cytoplasmic calcium levels in A7r5 vascular smooth muscle cells. Mol. Nutr. Food Res. 2005 49 396-404.
43. Li H.; Xia N.; Forstermann U. Cardiovascular effects and molecular targets of resveratrol. Nitric Oxide 2012 26 102-110.
44. Baur J.A.; Sinclair D.A. Therapeutic potential of resveratrol: The in vivo evidence. Nat. Rev. Drug Discovery 2006 5 493-506.
45. Elí es J.; Cuínas A.; García-Morales V.; Orallo F.; Campos-Toimil M. Trans-resveratrol simultaneously increases cytoplasmic Ca2+ levels and nitric oxide release in human endothelial cells. Mol. Nutr. Food Res. 2011 55 1237-1248.
46. Protic D.; Beleslin-Cokic B.; Novakovic R.; Kanjuh V.; Heinle H.; Scepanovic R.; Gojkovic-Bukarica L. Effect of Wine Polyphenol Resveratrol on the Contractions Elicited Electrically or by Norepinephrine in the Rat Portal Vein. Phytother. Res. 2013 27 1685-1693.
47. Novakovic A.; Bukarica L.G.; Kanjuh V.; He inle H. Potassium channels-mediated vasorelaxation of rat aorta induced by resveratrol. Basic Clin. Pharmacol. Toxicol. 2006 99 360-364.
48. Su H.C.; Hung L.M.; Chen J.K. Resveratrol a red win e antioxidant possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am. J. Physiol. Endocrinol. Metab. 2006 290 1339-1346.
49. Raval A.P.; Dave K.R.; Perez-Pinzon M.A. Resveratrol mimics ischemic preconditioning in the brain. J. Cereb. Blood Flow Metab. 2006 26 1141-1147.
50. Raval A.P.; Lin H.W.; Dave K.R.; Defazio R.A.; Della Morte D.; Kim E.J.; Perez-Pinzon M.A. Resveratrol and ischemic preconditioning in the brain. Curr. Med. Chem. 2008 15 1545-1551.
51. Li M.; Wang Q.S.; Chen Y.; Wang Z.M.; Liu Z.; Guo S.M. Resveratrol inhibits ne uronal discharges in rat hippocampal CA1 area. Sheng Li Xue Bao 2005 57 355-360.
52. Kundu J.K.; Surh Y.J. Cancer chemopreventive and therapeutic potential of resveratrol: Mechanistic perspectives. Cancer Lett. 2008 269 243-261.
53. Le Ferrec E.; Lagadic-Gossmann D.; Rauch C.; Bardiau C.; Maheo K.; Massiere F.; le Vee M.; Guillouzo A.; Morel F. Transcriptional induction of CYP1A1 by oltipraz in human Caco-2 cells is aryl hydrocarbon receptor-and calcium-dependent. J. Biol. Chem. 2002 277 24780-24787.
54. Chen Y.F.; Chen Y.T.; Chiu W.T.; Shen M.R. Remodeling of calcium signaling in tumor progression. J. Biomed. Sci. 2013 20 doi:10.1186/1423-0127- 20-23.
55. Ma X.; Tian X.; Huang X.; Yan F.; Qiao D. Resveratrol-induced mitochondrial dysfu nction and apoptosis are associated with Ca2+ and mCICR-mediated MPT activation in HepG2 cells. Mol. Cell. Biochem. 2007 302 99-109.
56. Yang Y.; Paik J.H.; Cho D.; Cho J.A.; Kim C.W. Resveratrol induces the suppression of tumor-derived CD4+CD25+ regulatory T cells. Int. Immunopharmacol. 2008 8 542-547.
57. Bishayee A. Cancer prevention and treatment with resveratrol: From rodent studies to clinical trials. Cancer Prev. Res. 2009 2 409-418.
58. Feng Y.H.; Zhou W.L.; Wu Q.L.; Li X.Y.; Zhao W.M.; Zou J.P. Low dose of resveratrol enhanced immune response of mice. Acta Pharmacol. Sin. 2002 23 893-897.
59. Falchetti R.; Fuggetta M.P.; Lanzilli G.; Tricarico M.; Ravagnan G. Effects of resveratrol on human immune cell function. Life Sci. 2001 70 81-96.
60. Shin D.H. Seo E.Y. Pang B. Nam J.H. Kim H.S. Kim W.K. Kim S.J Inhibition of Ca2+-release-activated Ca2+ channel (CRAC) and K+ channels by curcumin in Jurkat-T cells. J. Pharmacol. Sci. 201 1 115 144-154.
61. Singh N.P.; Hegde V.L.; Hofseth L.J.; Nagarkatti M.; Nagarkatti P. Resveratrol (trans-3,5,4'-trihydroxystilbene) ameliorates experimental allergic encephalomyelitis pri marily via induction of apoptosis in T cells involving activation of aryl hydrocarbon receptor and estrogen receptor. Mol. Pharmacol. 2007 72 1508-1521.
62. Nour V.; Trandafir I.; Muntean C. Ultravio let irradiation of trans-resveratrol and HPLC determination of trans-resveratrol and cis-resveratrol in Romanian red wines. J. Chromatogr. Sci. 2012 50 920-927.
63. Bertram K.M.; Baglole C.J.; Phipps R.P .; Libby R.T. Molecular regulation of cigarette smoke induced-oxidative stress in human retinal pigment epithelial cells: Implications for age-related macular degeneration. Am. J. Physiol. Cell Physiol. 2009 297 C1200-C1210.
64. King R.E.; Kent K.D.; Bomser J.A. Resveratrol reduces oxidation and proliferation of human retinal pigment epithelial cells via extracellular signal-regulated kinase inhibition. Chem. Biol. Interact. 2005 1 51 143-149.
65. Nagaoka T.; Hein T.W.; Yoshida A.; Kuo L. Resveratrol a component of red wine elicits dilation of isolated porcine retinal arterioles: Role of nitric oxide and potassium channels. Invest . Ophthalmol. Vis. Sci. 2007 48 4232-4239.
66. Berridge M.J. Neuronal calcium signaling. Neuron 1998 21 13-26.
67. Wehrens X.H.; Lehnart S.E.; Marks A.R. Intracellular calcium release and cardiac disease. Annu. Rev. Physiol. 2005 67 69-98.
68. Feske S. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 2007 7 690-702.
69. Dorrie J.; Gerauer H.; Wachter Y.; Zunino S.J. Resveratrol induces extensive apoptosis by depolarizing mitochondrial membranes and activating caspase-9 in acute lymphoblastic leukemia cells. Cance r Res. 2001 61 4731-4739.
70. Wallace C.H.; Baczko I.; Jones L.; Fercho M.; Light P.E. Inhibition of cardiac voltage-gated sodium channels by grape polyphenols. Br. J. Pharmacol. 2006 149 657-665.
71. Anekonda T.S.; Quinn J.F.; Harris C.; Frahler K.; Wadsworth T.L.; Woltjer R.L. L-type voltage-gated calcium channel blockade with isradipine as a therapeutic strategy for Alzheimer's disease. Neurobiol. Dis. 2011 41 62-70.
72. Cain S.M.; Snutch T.P. Voltage-gated calcium channels and disease. Biofactors 2011 37 197-205.
73. Vergara C.; Latorre R.; Marrion N.V.; Adelman J.P. Calcium-activated potassium channels. Curr. Opin. Neurobiol. 1998 8 321-329.
74. Chang Y.; Wang S.J. Inhibitory effect of glutamate release from rat cerebrocortical nerve terminals by resveratrol. Neurochem. Int. 2009 54 135-141.
75. Chen W.-P.; Chi T.-C.; Chuang L.-M.; Su M.-J. Resveratrol enhances insulin secretion by blocking KATP and KV channels of beta cells. Eur. J. Pharmacol. 2007 568 269-277.
76. Kalra N.; Roy P.; Prasad S.; Shukla Y. Resveratrol induces apoptosis involving mitochondrial pathways in mouse skin tumorigenesis. Life Sci. 2008 82 348-358.
77. Sun W.; Wang W.; Kim J.; Keng P.; Yang S.; Zhang H.; Liu C.; Okunieff P.; Zhang L. Anti-cancer effect of resveratrol is associated with induction of apoptosis via a mitochondr ial pathway alignment. Adv. Exp. Med. Biol. 2008 614 179-186.
78. Schmidt A.; Oberle N.; Wei E.M.; Vobis D.; Frischbutter S.; Baumgrass R.; Falk C.S.; Haag M.; Brügger B.; Lin H.; et al. Human regulatory T cells rapidly suppress T cell receptor-induced Ca2+ NF-kappaB and NFAT signaling in conventional T cells. Sci. Signal. 2011 4 doi:10.1126/scisignal.2002179.
79. Qureshi A.A.; Guan X.Q.; Reis J.C.; Papasian C.J.; Jabre S.; Morrison D.C.; Qureshi N. Inhibition of nitric oxide and inflammatory cytokines in LPS-stimulated murine macrophages by resveratrol a potent proteasome inh ibitor. Lipids Health Dis. 2012 11 76.