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  • 1 Ege University, Turkey
  • 2 Izmir University of Economics, Turkey
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The purpose of our study was to investigate whether endothelium-derived relaxations induced by store depletion are altered in aging rat thoracic aorta. Vascular responses were measured in aortic segments isolated from young (2–4 month) and old (20–24 month) male Sprague-Dawley rats. In phenylephrine-contracted intact tissues, receptor-mediated and receptor-independent endothelium-derived relaxations were induced by acetylcholine (ACh) and sarcoplasmic/endoplasmic reticulum Ca2+ ATPase (SERCA) blocker cyclopiazonic acid (CPA), respectively. In addition, CPA-induced changes in intracellular calcium levels were monitored in fura-2-loaded endothelium-denuded tissues. Real-time quantitative reverse transcription polymerase chain reaction and western blot analysis were performed to determine the transient receptor potential canonical (TRPC) 4 mRNA and protein levels. Endothelial TRPC4 mRNA levels were apparently decreased in aging rats. Immunoblot analysis showed that TRPC4 protein levels significantly decreased in intact aorta from 20- to 24-month-old rats compared to that from 2- to 4-month-old rats. ACh- and CPA-induced endothelium-dependent relaxations decreased in old rat aorta without any change in direct vasodilation induced by sodium nitroprusside. Store-operated Ca2+ entry (SOCE) induced by CPA was significantly decreased, whereas sarcoplasmic reticulum Ca2+ release was unaffected in endothelium-denuded aging rat aorta. In conclusion, TRPC4 downregulation could be associated with decreased endothelium-dependent vasorelaxations. As endothelial nitric oxide synthase is activated by SOCE-induced caveolar internalization, tracking the expression levels of SERCA, ion channels, and/or associated proteins involved in SOCE would lead to the development of novel therapeutics for age-related vasospastic disorders with dysfunctional endothelium.

  • 1.

    Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M: Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ. Res. 103, 12891299 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Albert AP, Saleh SN, Large WA: Identification of canonical transient receptor potential (TRPC) channel proteins in native vascular smooth muscle cells. Curr. Med. Chem. 16, 11581165 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Ambudkar IS: Ca2+ signaling microdomains: platforms for the assembly and regulation of TRPC channels. Trends Pharmacol. Sci. 27, 2532 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Atkinson J: Age-related medial elastocalcinosis in arteries: mechanisms, animal models, and physiological consequences. J. Appl. Physiol. 105, 16431651 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Barton M, Cosentino F, Brandes RP, Moreau P, Shaw S, Luscher TF: Anatomic heterogeneity of vascular aging: role of nitric oxide and endothelin. Hypertension 30, 817824 (1997)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Bergdahl A, Gomez MF, Wihlborg AK, Erlinge D, Eyjolfson A, Xu SZ, Beech DJ, Dreja K, Hellstrand P: Plasticity of TRPC expression in arterial smooth muscle: correlation with store-operated Ca2+ entry. Am. J. Physiol. Cell Physiol. 288, C872C880 (2005)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Berra-Romani R, Mazzocco-Spezzia A, Pulina MV, Golovina VA: Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am. J. Physiol. Cell Physiol. 295, C779C790 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Brandes RP, Fleming I, Busse R: Endothelial aging. Cardiovasc. Res. 66, 286294 (2005)

  • 9.

    Brotto M: Aging, sarcopenia and store-operated calcium entry: a common link? Cell Cycle 10, 42014202 (2011)

  • 10.

    Cheng KT, Ong HL, Liu X, Ambudkar IS: Contribution and regulation of TRPC channels in store-operated Ca2+ entry. Curr. Top. Membr. 71, 149179 (2013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Chou TC, Yen MH, Li CY, Ding YA: Alterations of nitric oxide synthase expression with aging and hypertension in rats. Hypertension 31, 643648 (1998)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Cogolludo AL, Perez-Vizcaino F, Zaragoza-Arnaez F, Ibarra M, Lopez-Lopez G, Lopez-Miranda V, Tamargo J: Mechanisms involved in SNP-induced relaxation and [Ca2+]i reduction in piglet pulmonary and systemic arteries. Br. J. Pharmacol. 132, 959967 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Corbi G, Conti V, Russomanno G, Rengo G, Vitulli P, Ciccarelli AL, Filippelli A, Ferrara N: Is physical activity able to modify oxidative damage in cardiovascular aging? Oxid. Med. Cell Longev. 2012, 728547 (2012)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Csiszar A, Ungvari Z, Edwards JG, Kaminski P, Wolin MS, Koller A, Kaley G: Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ. Res. 90, 11591166 (2002)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Davis MJ, Hill MA: Signaling mechanisms underlying the vascular myogenic response. Physiol. Rev. 79, 387423 (1999)

  • 16.

    del Corsso C, Ostrovskaya O, McAllister CE, Murray K, Hatton WJ, Gurney AM, Spencer NJ, Wilson SM: Effects of aging on Ca2+ signaling in murine mesenteric arterial smooth muscle cells. Mech. Ageing Dev. 127, 315323 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Dietrich A, Chubanov V, Kalwa H, Rost BR, Gudermann T: Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol. Ther. 112, 744760 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Edwards JN, Blackmore DG, Gilbert DF, Murphy RM, Launikonis BS: Store-operated calcium entry remains fully functional in aged mouse skeletal muscle despite a decline in STIM1 protein expression. Aging Cell 10, 675685 (2011)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Erac Y, Selli C, Kosova B, Akcali KC, Tosun M: Expression levels of TRPC1 and TRPC6 ion channels are reciprocally altered in aging rat aorta: implications for age-related vasospastic disorders. Age (Dordr) 32, 223230 (2010)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Freichel M, Suh SH, Pfeifer A, Schweig U, Trost C, Weissgerber P, Biel M, Philipp S, Freise D, Droogmans G, Hofmann F, Flockerzi V, Nilius B: Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat. Cell Biol. 3, 121127 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC: Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J. Biol. Chem. 272, 2543725440 (1997)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Goettsch W, Lattmann T, Amann K, Szibor M, Morawietz H, Munter K, Muller SP, Shaw S, Barton M: Increased expression of endothelin-1 and inducible nitric oxide synthase isoform II in aging arteries in vivo: implications for atherosclerosis. Biochem. Biophys. Res. Commun. 280, 908913 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Gryglewski RJ, Palmer RM, Moncada S: Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320, 454456 (1986)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Hamilton CA, Brosnan MJ, McIntyre M, Graham D, Dominiczak AF: Superoxide excess in hypertension and aging: a common cause of endothelial dysfunction. Hypertension 37, 529534 (2001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Heymes C, Habib A, Yang D, Mathieu E, Marotte F, Samuel J, Boulanger CM: Cyclo-oxygenase-1 and -2 contribution to endothelial dysfunction in ageing. Br. J. Pharmacol. 131, 804810 (2000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Inoue R, Jian Z, Kawarabayashi Y: Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol. Ther. 123, 371385 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Jacobson A, Yan C, Gao Q, Rincon-Skinner T, Rivera A, Edwards J, Huang A, Kaley G, Sun D: Aging enhances pressure-induced arterial superoxide formation. Am. J. Physiol. Heart Circ. Physiol. 293, H1344H1350 (2007)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Jeong SM, Lee JH, Kim S, Rhim H, Lee BH, Kim JH, Oh JW, Lee SM, Nah SY: Ginseng saponins induce store-operated calcium entry in Xenopus oocytes. Br. J. Pharmacol. 142, 585593 (2004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Ju H, Zou R, Venema VJ, Venema RC: Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J. Biol. Chem. 272, 1852218525 (1997)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Kan H, Ruan Y, Malik KU: Signal transduction mechanism(s) involved in prostacyclin production elicited by acetylcholine in coronary endothelial cells of rabbit heart. J. Pharmacol. Exp. Ther. 282, 113122 (1997)

    • Search Google Scholar
    • Export Citation
  • 31.

    Karavidas A, Lazaros G, Tsiachris D, Pyrgakis V: Aging and the cardiovascular system. Hellenic J. Cardiol. 51, 421427 (2010)

  • 32.

    Kovacic JC, Moreno P, Nabel EG, Hachinski V, Fuster V: Cellular senescence, vascular disease, and aging: part 2 of a 2-part review: clinical vascular disease in the elderly. Circulation 123, 19001910 (2011)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Kuriyama H, Kitamura K, Itoh T, Inoue R: Physiological features of visceral smooth muscle cells, with special reference to receptors and ion channels. Physiol. Rev. 78, 811920 (1998)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Kwan HY, Huang Y, Yao X: TRP channels in endothelial function and dysfunction. Biochim. Biophys. Acta 1772, 907914 (2007)

  • 35.

    Kwiatek AM, Minshall RD, Cool DR, Skidgel RA, Malik AB, Tiruppathi C: Caveolin-1 regulates store-operated Ca2+ influx by binding of its scaffolding domain to transient receptor potential channel-1 in endothelial cells. Mol. Pharmacol. 70, 11741183 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Leung FP, Yung LM, Yao X, Laher I, Huang Y: Store-operated calcium entry in vascular smooth muscle. Br. J. Pharmacol. 153, 846857 (2008)

  • 37.

    Matz RL, de Sotomayor MA, Schott C, Stoclet JC, Andriantsitohaina R: Vascular bed heterogeneity in age-related endothelial dysfunction with respect to NO and eicosanoids. Br. J. Pharmacol. 131, 303311 (2000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Matz RL, Schott C, Stoclet JC, Andriantsitohaina R: Age-related endothelial dysfunction with respect to nitric oxide, endothelium-derived hyperpolarizing factor and cyclooxygenase products. Physiol. Res. 49, 1118 (2000)

    • Search Google Scholar
    • Export Citation
  • 39.

    Norwood N, Moore TM, Dean DA, Bhattacharjee R, Li M, Stevens T: Store-operated calcium entry and increased endothelial cell permeability. Am. J. Physiol. Lung Cell Mol. Physiol. 279, L815L824 (2000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Parekh AB, Putney JW Jr: Store-operated calcium channels. Physiol. Rev. 85, 757810 (2005)

  • 41.

    Philipp S, Trost C, Warnat J, Rautmann J, Himmerkus N, Schroth G, Kretz O, Nastainczyk W, Cavalie A, Hoth M, Flockerzi V: TRP4 (CCE1) protein is part of native calcium release-activated Ca2+-like channels in adrenal cells. J. Biol. Chem. 275, 2396523972 (2000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Potier M, Gonzalez JC, Motiani RK, Abdullaev IF, Bisaillon JM, Singer HA, Trebak M: Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 23, 24252437 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Putney JW Jr: TRP, inositol 1, 4, 5-trisphosphate receptors, and capacitative calcium entry. Proc. Natl. Acad. Sci. U S A 96, 1466914671 (1999)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Selli C, Erac Y, Tosun M: Cyclopiazonic acid alters serotonin-induced responses in rat thoracic aorta. Vasc. Pharmacol. 61, 4348 (2014)

  • 45.

    Simon AM, McWhorter AR: Decreased intercellular dye-transfer and downregulation of non-ablated connexins in aortic endothelium deficient in connexin37 or connexin40. J. Cell Sci. 116, 22232236 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Sowa G: Caveolae, caveolins, cavins, and endothelial cell function: new insights. Front. Physiol. 2, 120 (2012)

  • 47.

    Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P: STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat. Cell Biol. 10, 688697 (2008)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48.

    Sun D, Huang A, Yan EH, Wu Z, Yan C, Kaminski PM, Oury TD, Wolin MS, Kaley G: Reduced release of nitric oxide to shear stress in mesenteric arteries of aged rats. Am. J. Physiol. Heart Circ. Physiol. 286, H2249H2256 (2004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Sundivakkam PC, Freichel M, Singh V, Yuan JP, Vogel SM, Flockerzi V, Malik AB, Tiruppathi C: The Ca(2+) sensor stromal interaction molecule 1 (STIM1) is necessary and sufficient for the store-operated Ca(2+) entry function of transient receptor potential canonical (TRPC) 1 and 4 channels in endothelial cells. Mol. Pharmacol. 81, 510526 (2012)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50.

    Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, Tiruppathi C: Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am. J. Physiol. Cell Physiol. 296, C403C413 (2009)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51.

    Sweeney M, Yu Y, Platoshyn O, Zhang S, McDaniel SS, Yuan JX: Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am. J. Physiol. Lung Cell Mol. Physiol. 283, L144L155 (2002)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 52.

    Tanabe T, Maeda S, Miyauchi T, Iemitsu M, Takanashi M, Irukayama-Tomobe Y, Yokota T, Ohmori H, Matsuda M: Exercise training improves ageing-induced decrease in eNOS expression of the aorta. Acta Physiol. Scand. 178, 310 (2003)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 53.

    Targos B, Barańska J, Pomorski P: Store-operated calcium entry in physiology and pathology of mammalian cells. Acta Biochim. Pol. 52, 379409 (2005)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54.

    Thornton AM, Zhao X, Weisleder N, Brotto LS, Bougoin S, Nosek TM, Reid M, Hardin B, Pan Z, Ma J, Parness J, Brotto M: Store-operated Ca(2+) entry (SOCE) contributes to normal skeletal muscle contractility in young but not in aged skeletal muscle. Aging (Albany NY) 3, 621634 (2011)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55.

    Tiruppathi C, Freichel M, Vogel SM, Paria BC, Mehta D, Flockerzi V, Malik AB: Impairment of store-operated Ca2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ. Res. 91, 7076 (2002)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56.

    Tosun M, Erac Y, Selli C, Karakaya N: Sarcoplasmic-endoplasmic reticulum Ca2+-ATPase inhibition prevents endothelin A receptor antagonism in rat aorta. Am. J. Physiol. Heart Circ. Physiol. 292, H19611966 (2006)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 57.

    Tosun M, Paul RJ, Rapoport RM: Coupling of store-operated Ca++ entry to contraction in rat aorta. J. Pharmacol. Exp. Ther. 285, 759766 (1998)

    • Search Google Scholar
    • Export Citation
  • 58.

    Tschudi MR, Barton M, Bersinger NA, Moreau P, Cosentino F, Noll G, Malinski T, Luscher TF: Effect of age on kinetics of nitric oxide release in rat aorta and pulmonary artery. J. Clin. Invest. 98, 899905 (1996)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 59.

    Ungvari Z, Kaley G, de Cabo R, Sonntag WE, Csiszar A: Mechanisms of vascular aging: new perspectives. J. Gerontol. A Biol. Sci. Med. Sci. 65, 10281041 (2010)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60.

    van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V, Luscher TF: Enhanced peroxynitrite formation is associated with vascular aging. J. Exp. Med. 192, 17311744 (2000)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 61.

    Watanabe H, Murakami M, Ohba T, Takahashi Y, Ito H: TRP channel and cardiovascular disease. Pharmacol. Ther. 118, 337351 (2008)

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