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Molecular expression and calcium signalling roles of native TRP channels in vascular cells

Year 2012, Volume: 4 Issue: 2, 195 - 201, 14.08.2013

Abstract

In the vasculature, multiple members of the TRP-superfamily of non-selective cation channels (NSCCs) are expressed. These channels mediate diverse non-voltage-gated Ca2+-entry pathways and functions, which involve both vascular myocytes and communicating endothelial cells. Here, we provide an overview of recent progress in this area of research and discuss several specific examples of the important roles of vascular TRP channels in calcium signalling and electrophysiological responses. We especially focus on the recently discovered signal transduction mechanisms involving formation of specific complexes between TRP proteins and other better studied proteins that regulate cell calcium homeostasis, such as voltage-gated calcium channels and ryanodine receptors. Finally, we provide an overview of the progress in our understanding of TRPM8, which is known as the principal neuronal cold receptor, expression, localisation and function in the vasculature. We conclude that this channel is likely involved in complex thermal behaviour of blood vessels, better understanding of which is relevant to hypothermic and cardiovascular surgery conditions, therefore further research in this area is needed.

References

  • Albert AP, Large WA. 2006. Signal transduction pathways and gating mechanisms of native TRP-like cation channels in vascular myocytes. J Physiol 570: 45-51.
  • Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D. 2007. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208.
  • Baylie RL, Cheng H, Langton PD, James AF. 2010. Inhibition of the cardiac L-type calcium channel current by the TRPM8 agonist, (-)-menthol. J Physiol Pharmacol 61: 543-550.
  • Beech DJ. 2005. Emerging functions of 10 types of TRP cationic channel in vascular smooth muscle. Clin Exp Pharmacol P 32: 597-603.
  • Beech DJ. 2007. Ion channel switching and activation in smooth-muscle cells of occlusive vascular diseases. Biochem Soc T 35: 890-894.
  • Beech DJ, Muraki K, Flemming R. 2004. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP, J Physiol 559: 685-706.
  • Benham CD, Bolton TB, Byrne NG, Large WA. 1987. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J Physiol 387: 473-488.
  • Benham CD, Tsien RW. 1987. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature 328: 275-278.
  • Bodding M, Wissenbach U, Flockerzi V. 2007. Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium 42: 618-628.
  • Byrne NG, Large WA. 1988a. Mechanism of action of alpha-adrenoceptor activation in single cells freshly dissociated from the rabbit portal vein. Brit J Pharmacol 94: 475-482.
  • Byrne NG, Large WA. 1988b. Membrane ionic mechanisms activated by noradrenaline in cells isolated from the rabbit portal vein. J Physiol 404: 557-573.
  • Clapham DE, Julius D, Montell C, Schultz G. 2005. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57: 427-450.
  • Earley S, Gonzales AL, Crnich R. 2009b. Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca2+-Activated K+ channels. Circ Res 104: 987-994.
  • Earley S, Heppner TJ, Nelson MT, Brayden JE. 2005. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279.
  • Earley S, Pauyo T, Drapp R, Tavares MJ, Liedtke W, Brayden J. 2009a. TRPV4- dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol-Heart C 297: H1096-H1102.
  • Firth AL, Remillard CV, Yuan,JX. 2007. TRP channels in hypertension. Biochim Biophys Acta 1772: 895-906.
  • Garland CJ, Plane F, Kemp BK, Cocks TM. 1995. Endothelium-dependent hyperpolarization: a role in the control of vascular tone. Trends Pharmacol Sci 16: 23-30.
  • Gees M, Colsoul B, Nilius B. 2010. The role of transient receptor potential cation channels in Ca2+ signalling. Cold Spring Harb Perspect biol 2: a003962.
  • Gryglewski RJ, Botting RM, Vane JR. 1988. Mediators produced by the endothelial cell. Hypertension 12: 530-548.
  • Gryglewski R, Moncada S, Palmer R. 1986. Bioassay of prostacyclin and endothelium-derived relaxing factor (EDRF) from porcine aortic endothelial cells. Brit J Pharmacol 87: 685-694.
  • House SJ, Potier M, Bisaillon J, Singer HA, Trebak M. 2008. The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflug Arch Eur J Phy 456: 769-785.
  • Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. 1987. Endotheliumderived relaxing factor produced and released from artery and vein is nitric oxide. P Natl Acad Sci 84: 9265-9269.
  • Inoue R, Jensen LJ, Shi J, Morita H, Nishida M, Honda A, Ito Y. 2006. Transient receptor potential channels in cardiovascular function and disease. Circ Res 99: 119-131.
  • Inoue R, Jian Z, Kawarabayashi Y. 2009. Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol Therapeut 123: 371-85.
  • Inoue R, Okada T, Onoue H, Hara Y, Shimizu S, Naitoh S, Ito Y, Mori Y. 2001. The transient receptor potential protein homologue TRP6 is the essential component of vascular Į1-adrenoceptor-activated Ca2+-permeable cation channel. Circ Res 88: 325-332.
  • Jenkins CM, Han X, Mancuso DJ, Gross RW. 2002. Identification of calciumindependent phospholipase A2 (iPLA2 )ȕ, and not iPLA2 Ȗ, as the mediator of arginine vasopressin-induced arachidonic acid release in A-10 smooth muscle cells. Enantioselective mechanism-based discrimination of mammalian iPLA2s. J Biol Chem 277: 32807-32814.
  • Johnson CD, Melanaphy D, Purse A, Stokesberry SA, Dickson P, Zholos AV. 2009. Transient receptor potential melastatin 8 channel involvement in the regulation of vascular tone. Am J Physiol-Heart C 296: H1868-H1877.
  • Liu B, Peel SE, Fox J, Hall IP. 2010. Reverse mode Na+ /Ca2+ exchange mediated by STIM1 contributes to Ca2+ influx in airway smooth muscle following agonist stimulation. Respir Res 11: 168-179.
  • McKemy DD, Neuhausser WM, Julius D. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58.
  • Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX. 2002. A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9: 229231.
  • Nakashima M, Mombouli JV, Taylor AA, Vanhoutte PM. 1993. Endotheliumdependent hyperpolarization caused by bradykinin in human coronary arteries. J Clin Invest 92: 2867-2871.
  • Nelson M, Cheng H, Rubart M, Santana L, Bonev A, Knot H, Lederer W. 1995. Relaxation of arterial smooth muscle by calcium sparks. Science 270: 633- 637.
  • Nilius B, Owsianik G, Voets T, Peters JA. 2007. Transient receptor potential cation channels in disease. Physiol Rev 87:165-217.
  • Palmer RMJ, Rees DD, Ashton DS, Moncada S. 1988. L-arginine is the physiological precursor for the formation of nitric oxide in endotheliumdependent relaxation. Biochem Bioph Res Co 153: 1251-1256.
  • Palmer R, Ferrige A, Moncada S. 1987. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524-526.
  • Pedersen SF, Owsianik G, Nilius B. 2005. TRP channels: an overview. Cell Calcium 38: 233-252.
  • Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
  • Poburko D, Liao CH, Lemos VS, Lin E, Maruyama Y, Cole WC, van Breemen C. 2007. Transient receptor potential channel 6-mediated, localized cytosolic [Na+ ] transients drive Na+ /Ca2+ exchanger-mediated Ca2+ entry in purinergically stimulated aorta smooth muscle cells. Circ Res 101: 1030- 1038.
  • Sonkusare SK, Bonev AD, Ledoux J, Liedtke W, Kotliko! MI, Heppner TJ, HillEubanks, DC, Nelson NT. 2012. Elementary Ca2+ signals through endothelial TRPV4 channels regulate vascular function. Science 336: 597-601.
  • Takahashi N, Kuwaki T, Kiyonaka S, Numata T, Kozai D, Mizuno Y, Yamamoto S, Naito S, Knevels E, Carmeliet P, Oga T, Kaneko S, Suga S, Nokami T, Yoshida J, Mori Y. 2011. TRPA1 underlies a sensing mechanism for O2. Nat Chem Biol 7:701-711.
  • Thebault S, Lemonnier L, Bidaux G, Flourakis M, Bavenco!e A, Gordienko D, Roudbaraki M, Delcourt P, Panchin Y, Shuba Y. 2005. Novel role of cold/ menthol-sensitive transient receptor potential melastatine family member 8 (TRPM8) in the activation of store-operated channels in LNCaP human prostate cancer epithelial cells. J Biol Chem 280: 39423-39435.
  • Tsavaler L, Shapero MH, Morkowski S, Laus R. 2001. Trp-p8, a novel prostatespecific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61: 3760-3769
  • Tsuzuki K, Xing H, Ling J, Gu JG. 2004. Menthol-induced Ca2+ release from presynaptic Ca2+ stores potentiates sensory synaptic transmission. J Neurosci 24: 762-771.
  • Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C. 1995. TRPC1, a human homolog of a Drosophila store-operated channel. P Natl Acad Sci USA 92: 9652-9656.
  • Xu SZ, Beech DJ. 2001. TrpC1 is a membrane-spanning subunit of store-operated Ca2+ channels in native vascular smooth muscle cells. Circ Res 88: 84-87.
  • Wu LJ, Sweet TB, Clapham DE. 2010. International Union of Basic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62: 381-404.
  • Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. 1988. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332: 411-415
  • Yang XR, Lin MJ, McIntosh LS, Sham JS. 2006. Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle. Am J Physiol-Lung C 290: L1267-L1276.
  • Yao X, Garland CJ. 2005. Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 97: 853-863.
  • Zhang L, Barritt GJ. 2004. Evidence that TRPM8 is an androgen dependent Ca2+ channel required for the survival of prostate cancer cells. Cancer Res 64: 8365-8373.
  • Zhu X, Chu PB, Peyton M, Birnbaumer L. 1995. Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS let 373: 193-198
Year 2012, Volume: 4 Issue: 2, 195 - 201, 14.08.2013

Abstract

References

  • Albert AP, Large WA. 2006. Signal transduction pathways and gating mechanisms of native TRP-like cation channels in vascular myocytes. J Physiol 570: 45-51.
  • Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D. 2007. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208.
  • Baylie RL, Cheng H, Langton PD, James AF. 2010. Inhibition of the cardiac L-type calcium channel current by the TRPM8 agonist, (-)-menthol. J Physiol Pharmacol 61: 543-550.
  • Beech DJ. 2005. Emerging functions of 10 types of TRP cationic channel in vascular smooth muscle. Clin Exp Pharmacol P 32: 597-603.
  • Beech DJ. 2007. Ion channel switching and activation in smooth-muscle cells of occlusive vascular diseases. Biochem Soc T 35: 890-894.
  • Beech DJ, Muraki K, Flemming R. 2004. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP, J Physiol 559: 685-706.
  • Benham CD, Bolton TB, Byrne NG, Large WA. 1987. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J Physiol 387: 473-488.
  • Benham CD, Tsien RW. 1987. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature 328: 275-278.
  • Bodding M, Wissenbach U, Flockerzi V. 2007. Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium 42: 618-628.
  • Byrne NG, Large WA. 1988a. Mechanism of action of alpha-adrenoceptor activation in single cells freshly dissociated from the rabbit portal vein. Brit J Pharmacol 94: 475-482.
  • Byrne NG, Large WA. 1988b. Membrane ionic mechanisms activated by noradrenaline in cells isolated from the rabbit portal vein. J Physiol 404: 557-573.
  • Clapham DE, Julius D, Montell C, Schultz G. 2005. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57: 427-450.
  • Earley S, Gonzales AL, Crnich R. 2009b. Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca2+-Activated K+ channels. Circ Res 104: 987-994.
  • Earley S, Heppner TJ, Nelson MT, Brayden JE. 2005. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279.
  • Earley S, Pauyo T, Drapp R, Tavares MJ, Liedtke W, Brayden J. 2009a. TRPV4- dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol-Heart C 297: H1096-H1102.
  • Firth AL, Remillard CV, Yuan,JX. 2007. TRP channels in hypertension. Biochim Biophys Acta 1772: 895-906.
  • Garland CJ, Plane F, Kemp BK, Cocks TM. 1995. Endothelium-dependent hyperpolarization: a role in the control of vascular tone. Trends Pharmacol Sci 16: 23-30.
  • Gees M, Colsoul B, Nilius B. 2010. The role of transient receptor potential cation channels in Ca2+ signalling. Cold Spring Harb Perspect biol 2: a003962.
  • Gryglewski RJ, Botting RM, Vane JR. 1988. Mediators produced by the endothelial cell. Hypertension 12: 530-548.
  • Gryglewski R, Moncada S, Palmer R. 1986. Bioassay of prostacyclin and endothelium-derived relaxing factor (EDRF) from porcine aortic endothelial cells. Brit J Pharmacol 87: 685-694.
  • House SJ, Potier M, Bisaillon J, Singer HA, Trebak M. 2008. The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflug Arch Eur J Phy 456: 769-785.
  • Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. 1987. Endotheliumderived relaxing factor produced and released from artery and vein is nitric oxide. P Natl Acad Sci 84: 9265-9269.
  • Inoue R, Jensen LJ, Shi J, Morita H, Nishida M, Honda A, Ito Y. 2006. Transient receptor potential channels in cardiovascular function and disease. Circ Res 99: 119-131.
  • Inoue R, Jian Z, Kawarabayashi Y. 2009. Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol Therapeut 123: 371-85.
  • Inoue R, Okada T, Onoue H, Hara Y, Shimizu S, Naitoh S, Ito Y, Mori Y. 2001. The transient receptor potential protein homologue TRP6 is the essential component of vascular Į1-adrenoceptor-activated Ca2+-permeable cation channel. Circ Res 88: 325-332.
  • Jenkins CM, Han X, Mancuso DJ, Gross RW. 2002. Identification of calciumindependent phospholipase A2 (iPLA2 )ȕ, and not iPLA2 Ȗ, as the mediator of arginine vasopressin-induced arachidonic acid release in A-10 smooth muscle cells. Enantioselective mechanism-based discrimination of mammalian iPLA2s. J Biol Chem 277: 32807-32814.
  • Johnson CD, Melanaphy D, Purse A, Stokesberry SA, Dickson P, Zholos AV. 2009. Transient receptor potential melastatin 8 channel involvement in the regulation of vascular tone. Am J Physiol-Heart C 296: H1868-H1877.
  • Liu B, Peel SE, Fox J, Hall IP. 2010. Reverse mode Na+ /Ca2+ exchange mediated by STIM1 contributes to Ca2+ influx in airway smooth muscle following agonist stimulation. Respir Res 11: 168-179.
  • McKemy DD, Neuhausser WM, Julius D. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58.
  • Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX. 2002. A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9: 229231.
  • Nakashima M, Mombouli JV, Taylor AA, Vanhoutte PM. 1993. Endotheliumdependent hyperpolarization caused by bradykinin in human coronary arteries. J Clin Invest 92: 2867-2871.
  • Nelson M, Cheng H, Rubart M, Santana L, Bonev A, Knot H, Lederer W. 1995. Relaxation of arterial smooth muscle by calcium sparks. Science 270: 633- 637.
  • Nilius B, Owsianik G, Voets T, Peters JA. 2007. Transient receptor potential cation channels in disease. Physiol Rev 87:165-217.
  • Palmer RMJ, Rees DD, Ashton DS, Moncada S. 1988. L-arginine is the physiological precursor for the formation of nitric oxide in endotheliumdependent relaxation. Biochem Bioph Res Co 153: 1251-1256.
  • Palmer R, Ferrige A, Moncada S. 1987. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524-526.
  • Pedersen SF, Owsianik G, Nilius B. 2005. TRP channels: an overview. Cell Calcium 38: 233-252.
  • Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
  • Poburko D, Liao CH, Lemos VS, Lin E, Maruyama Y, Cole WC, van Breemen C. 2007. Transient receptor potential channel 6-mediated, localized cytosolic [Na+ ] transients drive Na+ /Ca2+ exchanger-mediated Ca2+ entry in purinergically stimulated aorta smooth muscle cells. Circ Res 101: 1030- 1038.
  • Sonkusare SK, Bonev AD, Ledoux J, Liedtke W, Kotliko! MI, Heppner TJ, HillEubanks, DC, Nelson NT. 2012. Elementary Ca2+ signals through endothelial TRPV4 channels regulate vascular function. Science 336: 597-601.
  • Takahashi N, Kuwaki T, Kiyonaka S, Numata T, Kozai D, Mizuno Y, Yamamoto S, Naito S, Knevels E, Carmeliet P, Oga T, Kaneko S, Suga S, Nokami T, Yoshida J, Mori Y. 2011. TRPA1 underlies a sensing mechanism for O2. Nat Chem Biol 7:701-711.
  • Thebault S, Lemonnier L, Bidaux G, Flourakis M, Bavenco!e A, Gordienko D, Roudbaraki M, Delcourt P, Panchin Y, Shuba Y. 2005. Novel role of cold/ menthol-sensitive transient receptor potential melastatine family member 8 (TRPM8) in the activation of store-operated channels in LNCaP human prostate cancer epithelial cells. J Biol Chem 280: 39423-39435.
  • Tsavaler L, Shapero MH, Morkowski S, Laus R. 2001. Trp-p8, a novel prostatespecific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61: 3760-3769
  • Tsuzuki K, Xing H, Ling J, Gu JG. 2004. Menthol-induced Ca2+ release from presynaptic Ca2+ stores potentiates sensory synaptic transmission. J Neurosci 24: 762-771.
  • Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C. 1995. TRPC1, a human homolog of a Drosophila store-operated channel. P Natl Acad Sci USA 92: 9652-9656.
  • Xu SZ, Beech DJ. 2001. TrpC1 is a membrane-spanning subunit of store-operated Ca2+ channels in native vascular smooth muscle cells. Circ Res 88: 84-87.
  • Wu LJ, Sweet TB, Clapham DE. 2010. International Union of Basic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62: 381-404.
  • Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. 1988. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332: 411-415
  • Yang XR, Lin MJ, McIntosh LS, Sham JS. 2006. Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle. Am J Physiol-Lung C 290: L1267-L1276.
  • Yao X, Garland CJ. 2005. Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 97: 853-863.
  • Zhang L, Barritt GJ. 2004. Evidence that TRPM8 is an androgen dependent Ca2+ channel required for the survival of prostate cancer cells. Cancer Res 64: 8365-8373.
  • Zhu X, Chu PB, Peyton M, Birnbaumer L. 1995. Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS let 373: 193-198
There are 51 citations in total.

Details

Primary Language English
Journal Section Review
Authors

Alexander Zholos This is me

Donal Melanaphy This is me

Lyudmyla Borysova This is me

Maksym Kustov This is me

Conall Watson This is me

Christopher Johnson This is me

Theodor Burdyga This is me

Publication Date August 14, 2013
Published in Issue Year 2012 Volume: 4 Issue: 2

Cite

APA Zholos, A., Melanaphy, D., Borysova, L., Kustov, M., et al. (2013). Molecular expression and calcium signalling roles of native TRP channels in vascular cells. Cell Membranes and Free Radical Research, 4(2), 195-201.
AMA Zholos A, Melanaphy D, Borysova L, Kustov M, Watson C, Johnson C, Burdyga T. Molecular expression and calcium signalling roles of native TRP channels in vascular cells. Cell Membranes and Free Radical Research. August 2013;4(2):195-201.
Chicago Zholos, Alexander, Donal Melanaphy, Lyudmyla Borysova, Maksym Kustov, Conall Watson, Christopher Johnson, and Theodor Burdyga. “Molecular Expression and Calcium Signalling Roles of Native TRP Channels in Vascular Cells”. Cell Membranes and Free Radical Research 4, no. 2 (August 2013): 195-201.
EndNote Zholos A, Melanaphy D, Borysova L, Kustov M, Watson C, Johnson C, Burdyga T (August 1, 2013) Molecular expression and calcium signalling roles of native TRP channels in vascular cells. Cell Membranes and Free Radical Research 4 2 195–201.
IEEE A. Zholos, “Molecular expression and calcium signalling roles of native TRP channels in vascular cells”, Cell Membranes and Free Radical Research, vol. 4, no. 2, pp. 195–201, 2013.
ISNAD Zholos, Alexander et al. “Molecular Expression and Calcium Signalling Roles of Native TRP Channels in Vascular Cells”. Cell Membranes and Free Radical Research 4/2 (August 2013), 195-201.
JAMA Zholos A, Melanaphy D, Borysova L, Kustov M, Watson C, Johnson C, Burdyga T. Molecular expression and calcium signalling roles of native TRP channels in vascular cells. Cell Membranes and Free Radical Research. 2013;4:195–201.
MLA Zholos, Alexander et al. “Molecular Expression and Calcium Signalling Roles of Native TRP Channels in Vascular Cells”. Cell Membranes and Free Radical Research, vol. 4, no. 2, 2013, pp. 195-01.
Vancouver Zholos A, Melanaphy D, Borysova L, Kustov M, Watson C, Johnson C, Burdyga T. Molecular expression and calcium signalling roles of native TRP channels in vascular cells. Cell Membranes and Free Radical Research. 2013;4(2):195-201.