1932

Abstract

Resistance arteries and arterioles evolved as specialized blood vessels serving two important functions: () regulating peripheral vascular resistance and blood pressure and () matching oxygen and nutrient delivery to metabolic demands of organs. These functions require control of vessel lumen cross-sectional area (vascular tone) via coordinated vascular cell responses governed by precise spatial-temporal communication between intracellular signaling pathways. Herein, we provide a contemporary overview of the significant roles that redox switches play in calcium signaling for orchestrated endothelial, smooth muscle, and red blood cell control of arterial vascular tone. Three interrelated themes are the focus: () smooth muscle to endothelial communication for vasoconstriction, () endothelial to smooth muscle cell cross talk for vasodilation, and () oxygen and red blood cell interregulation of vascular tone and blood flow. We intend for this thematic framework to highlight gaps in our current knowledge and potentially spark interest for cross-disciplinary studies moving forward.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physiol-031522-021457
2023-02-10
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/physiol/85/1/annurev-physiol-031522-021457.html?itemId=/content/journals/10.1146/annurev-physiol-031522-021457&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Nehls V, Drenckhahn D. 1991. Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J. Cell Biol. 113:147–54
    [Google Scholar]
  2. 2.
    Straub AC, Zeigler AC, Isakson BE. 2014. The myoendothelial junction: connections that deliver the message. Physiology 29:242–49
    [Google Scholar]
  3. 3.
    Rhodin JA. 1967. The ultrastructure of mammalian arterioles and precapillary sphincters. J. Ultrastruct. Res. 18:181–223
    [Google Scholar]
  4. 4.
    Meng J, Lv Z, Zhang Y, Wang Y, Qiao X et al. 2021. Precision redox: the key for antioxidant pharmacology. Antioxid. Redox Signal. 34:1069–82
    [Google Scholar]
  5. 5.
    Förstermann U, Sessa WC. 2012. Nitric oxide synthases: regulation and function. Eur. Heart J. 33:829–37
    [Google Scholar]
  6. 6.
    Negri S, Faris P, Moccia F. 2021. Reactive oxygen species and endothelial Ca2+ signaling: Brothers in arms or partners in crime?. Int. J. Mol. Sci. 22:9821
    [Google Scholar]
  7. 7.
    Snezhkina AV, Kudryavtseva AV, Kardymon OL, Savvateeva MV, Melnikova NV et al. 2019. ROS generation and antioxidant defense systems in normal and malignant cells. Oxid. Med. Cell. Longev. 2019.6175804
    [Google Scholar]
  8. 8.
    Mailloux RJ. 2020. An update on mitochondrial reactive oxygen species production. Antioxidants 9:472
    [Google Scholar]
  9. 9.
    Li Y, Pagano PJ. 2017. Microvascular NADPH oxidase in health and disease. Free Radic. Biol. Med. 109:33–47
    [Google Scholar]
  10. 10.
    Schmidt HM, Kelley EE, Straub AC. 2019. The impact of xanthine oxidase (XO) on hemolytic diseases. Redox Biol 21:101072
    [Google Scholar]
  11. 11.
    Cassuto J, Dou H, Czikora I, Szabo A, Patel VS et al. 2014. Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients. Diabetes 63:1381–93
    [Google Scholar]
  12. 12.
    Beckman JS, Koppenol WH. 1996. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. Cell Physiol. 271:C1424–37
    [Google Scholar]
  13. 13.
    Hippeli S, Elstner EF. 1999. Transition metal ion-catalyzed oxygen activation during pathogenic processes. FEBS Lett 443:1–7
    [Google Scholar]
  14. 14.
    Wang Y, Branicky R, Noë A, Hekimi S. 2018. Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J. Cell Biol. 217:1915–28
    [Google Scholar]
  15. 15.
    George P. 1947. Reaction between catalase and hydrogen peroxide. Nature 160:41–43
    [Google Scholar]
  16. 16.
    Meyer AJ, Hell R. 2005. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res. 86:435–57
    [Google Scholar]
  17. 17.
    Dringen R. 2000. Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62:649–71
    [Google Scholar]
  18. 18.
    Lubos E, Loscalzo J, Handy DE. 2011. Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 15:1957–97
    [Google Scholar]
  19. 19.
    Perkins A, Nelson KJ, Parsonage D, Poole LB, Karplus PA. 2015. Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40:435–45
    [Google Scholar]
  20. 20.
    Yan L-J. 2014. Protein redox modification as a cellular defense mechanism against tissue ischemic injury. Oxid. Med. Cell. Longev. 2014 343154
    [Google Scholar]
  21. 21.
    Wani R, Nagata A, Murray BW. 2014. Protein redox chemistry: post-translational cysteine modifications that regulate signal transduction and drug pharmacology. Front. Pharmacol. 5:224
    [Google Scholar]
  22. 22.
    Kalinowski DS, Stefani C, Toyokuni S, Ganz T, Anderson GJ et al. 2016. Redox cycling metals: pedaling their roles in metabolism and their use in the development of novel therapeutics. Biochim. Biophys. Acta Mol. Cell Res. 1863:727–48
    [Google Scholar]
  23. 23.
    Ottolini M, Hong K, Sonkusare SK. 2019. Calcium signals that determine vascular resistance. Wiley Interdiscip. Rev. Syst. Biol. Med. 11:e1448
    [Google Scholar]
  24. 24.
    Bean BP, Sturek M, Puga A, Hermsmeyer K. 1986. Calcium channels in muscle cells isolated from rat mesenteric arteries: modulation by dihydropyridine drugs. Circ. Res. 59:229–35
    [Google Scholar]
  25. 25.
    Abd El-Rahman RR, Harraz OF, Brett SE, Anfinogenova Y, Mufti RE et al. 2013. Identification of L- and T-type Ca2+ channels in rat cerebral arteries: role in myogenic tone development. Am. J. Physiol. Heart Circ. Physiol. 304:H58–71
    [Google Scholar]
  26. 26.
    Bodi I, Mikala G, Koch SE, Akhter SA, Schwartz A. 2005. The L-type calcium channel in the heart: the beat goes on. J. Clin. Investig. 115:3306–17
    [Google Scholar]
  27. 27.
    Moosmang S, Schulla V, Welling A, Feil R, Feil S et al. 2003. Dominant role of smooth muscle L-type calcium channel Cav1.2 for blood pressure regulation. EMBO J 22:6027–34
    [Google Scholar]
  28. 28.
    Peterson BZ, DeMaria CD, Adelman JP, Yue DT. 1999. Calmodulin is the Ca2+ sensor for Ca2+-dependent inactivation of L-type calcium channels. Neuron 22:549–58
    [Google Scholar]
  29. 29.
    Blatter LA, Wier WG. 1994. Nitric oxide decreases [Ca2+]i in vascular smooth muscle by inhibition of the calcium current. Cell Calcium 15:122–31
    [Google Scholar]
  30. 30.
    Jackson WF. 2017. Potassium channels in regulation of vascular smooth muscle contraction and growth. Adv. Pharmacol. 78:89–144
    [Google Scholar]
  31. 31.
    Muralidharan P, Cserne Szappanos H, Ingley E, Hool L 2016. Evidence for redox sensing by a human cardiac calcium channel. Sci. Rep. 6:19067
    [Google Scholar]
  32. 32.
    Catterall WA. 2011. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3:a003947
    [Google Scholar]
  33. 33.
    VanBavel E, Sorop O, Andreasen D, Pfaffendorf M, Jensen BL. 2002. Role of T-type calcium channels in myogenic tone of skeletal muscle resistance arteries. Am. J. Physiol. Heart Circ. Physiol. 283:H2239–43
    [Google Scholar]
  34. 34.
    Rossier MF. 2016. T-type calcium channel: a privileged gate for calcium entry and control of adrenal steroidogenesis. Front. Endocrinol. 7:43
    [Google Scholar]
  35. 35.
    Harraz OF, Brett SE, Welsh DG. 2014. Nitric oxide suppresses vascular voltage-gated T-type Ca2+ channels through cGMP/PKG signaling. Am. J. Physiol. Heart Circ. Physiol. 306:H279–85
    [Google Scholar]
  36. 36.
    Hashad AM, Harraz OF, Brett SE, Romero M, Kassmann M et al. 2018. Caveolae link Cav3.2 channels to BKCa-mediated feedback in vascular smooth muscle. Arterioscler. Thromb. Vasc. Biol. 38:2371–81
    [Google Scholar]
  37. 37.
    Harraz OF, Welsh DG. 2013. Protein kinase A regulation of T-type Ca2+ channels in rat cerebral arterial smooth muscle. J. Cell Sci. 126:2944–54
    [Google Scholar]
  38. 38.
    Ottolini M, Sonkusare SK. 2021. The calcium signaling mechanisms in arterial smooth muscle and endothelial cells. Compr. Physiol. 11:1831–69
    [Google Scholar]
  39. 39.
    Stojilkovic SS, Leiva-Salcedo E, Rokic MB, Coddou C. 2014. Regulation of ATP-gated P2X channels: from redox signaling to interactions with other proteins. Antioxid. Redox Signal. 21:953–70
    [Google Scholar]
  40. 40.
    Billaud M, Chiu YH, Lohman AW, Parpaite T, Butcher JT et al. 2015. A molecular signature in the pannexin1 intracellular loop confers channel activation by the α1 adrenoreceptor in smooth muscle cells. Sci. Signal. 8:ra17
    [Google Scholar]
  41. 41.
    Zhao X, Falck JR, Gopal VR, Inscho EW, Imig JD. 2004. P2X receptor-stimulated calcium responses in preglomerular vascular smooth muscle cells involves 20-hydroxyeicosatetraenoic acid. J. Pharmacol. Exp. Ther. 311:1211–17
    [Google Scholar]
  42. 42.
    Negri S, Faris P, Berra-Romani R, Guerra G, Moccia F. 2019. Endothelial transient receptor potential channels and vascular remodeling: extracellular Ca2+ entry for angiogenesis, arteriogenesis and vasculogenesis. Front. Physiol. 10:1618
    [Google Scholar]
  43. 43.
    Ramsey IS, Delling M, Clapham DE. 2006. An introduction to TRP channels. Annu. Rev. Physiol. 68:619–47
    [Google Scholar]
  44. 44.
    Planells-Cases R, Valente P, Ferrer-Montiel A, Qin F, Szallasi A. 2011. Complex regulation of TRPV1 and related thermo-TRPs: implications for therapeutic intervention. Transient Receptor Potential Channels MS Islam 491–515 Dordrecht, Neth: Springer
    [Google Scholar]
  45. 45.
    Tajada S, Moreno CM, O'Dwyer S, Woods S, Sato D et al. 2017. Distance constraints on activation of TRPV4 channels by AKAP150-bound PKCα in arterial myocytes. J. Gen. Physiol. 149:639–59
    [Google Scholar]
  46. 46.
    Yang XR, Lin AH, Hughes JM, Flavahan NA, Cao YN et al. 2012. Upregulation of osmo-mechanosensitive TRPV4 channel facilitates chronic hypoxia-induced myogenic tone and pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 302:L555–68
    [Google Scholar]
  47. 47.
    Lee EJ, Shin SH, Hyun S, Chun J, Kang SS 2011. Mutation of a putative S-nitrosylation site of TRPV4 protein facilitates the channel activates. Anim. Cells Syst. 15:95–106
    [Google Scholar]
  48. 48.
    Cao S, Anishkin A, Zinkevich NS, Nishijima Y, Korishettar A et al. 2018. Transient receptor potential vanilloid 4 (TRPV4) activation by arachidonic acid requires protein kinase A-mediated phosphorylation. J. Biol. Chem. 293:5307–22
    [Google Scholar]
  49. 49.
    Earley S. 2013. TRPM4 channels in smooth muscle function. Pflügers Arch 465:1223–31
    [Google Scholar]
  50. 50.
    Kovács ZM, Dienes C, Hézső T, Almássy J, Magyar J et al. 2022. Pharmacological modulation and (patho)physiological roles of TRPM4 channel-part 1: modulation of TRPM4. Pharmaceuticals 15:40
    [Google Scholar]
  51. 51.
    Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G. 1999. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397:259–63
    [Google Scholar]
  52. 52.
    Adebiyi A, Thomas-Gatewood CM, Leo MD, Kidd MW, Neeb ZP, Jaggar JH. 2012. An elevation in physical coupling of type 1 IP3 receptors to TRPC3 channels constricts mesenteric arteries in genetic hypertension. Hypertension 60:1213–19
    [Google Scholar]
  53. 53.
    Potier M, Gonzalez JC, Motiani RK, Abdullaev IF, Bisaillon JM et al. 2009. Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J 23:2425–37
    [Google Scholar]
  54. 54.
    Dietrich A, Kalwa H, Storch U, Mederos y Schnitzler M, Salanova B et al. 2007. Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflügers Arch 455:465–77
    [Google Scholar]
  55. 55.
    Bisaillon JM, Motiani RK, Gonzalez-Cobos JC, Potier M, Halligan KE et al. 2010. Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am. J. Physiol. Cell Physiol. 298:C993–1005
    [Google Scholar]
  56. 56.
    Ng LC, McCormack MD, Airey JA, Singer CA, Keller PS et al. 2009. TRPC1 and STIM1 mediate capacitative Ca2+ entry in mouse pulmonary arterial smooth muscle cells. J. Physiol. 587:2429–42
    [Google Scholar]
  57. 57.
    Denniss A, Dulhunty AF, Beard NA. 2018. Ryanodine receptor Ca2+ release channel post-translational modification: central player in cardiac and skeletal muscle disease. Int. J. Biochem. Cell Biol. 101:49–53
    [Google Scholar]
  58. 58.
    Gonzales AL, Yang Y, Sullivan MN, Sanders L, Dabertrand F et al. 2014. A PLCγ1-dependent, force-sensitive signaling network in the myogenic constriction of cerebral arteries. Sci. Signal. 7:ra49
    [Google Scholar]
  59. 59.
    Dora KA, Doyle MP, Duling BR. 1997. Elevation of intracellular calcium in smooth muscle causes endothelial cell generation of NO in arterioles. PNAS 94:6529–34
    [Google Scholar]
  60. 60.
    Sandow SL, Hill CE. 2000. Incidence of myoendothelial gap junctions in the proximal and distal mesenteric arteries of the rat is suggestive of a role in endothelium-derived hyperpolarizing factor-mediated responses. Circ. Res. 86:341–46
    [Google Scholar]
  61. 61.
    Isakson BE, Duling BR. 2005. Heterocellular contact at the myoendothelial junction influences gap junction organization. Circ. Res. 97:44–51
    [Google Scholar]
  62. 62.
    Isakson BE. 2008. Localized expression of an Ins(1,4,5)P3 receptor at the myoendothelial junction selectively regulates heterocellular Ca2+ communication. J. Cell Sci. 121:3664–73
    [Google Scholar]
  63. 63.
    Straub AC, Billaud M, Johnstone SR, Best AK, Yemen S et al. 2011. Compartmentalized connexin 43 S-nitrosylation/denitrosylation regulates heterocellular communication in the vessel wall. Arterioscler. Thromb. Vasc. Biol. 31:399–407
    [Google Scholar]
  64. 64.
    Straub AC, Johnstone SR, Heberlein KR, Rizzo MJ, Best AK et al. 2010. Site-specific connexin phosphorylation is associated with reduced heterocellular communication between smooth muscle and endothelium. J. Vasc. Res. 47:277–86
    [Google Scholar]
  65. 65.
    Chen G, Suzuki H, Weston AH. 1988. Acetylcholine releases endothelium-derived hyperpolarizing factor and EDRF from rat blood vessels. Br. J. Pharmacol. 95:1165–74
    [Google Scholar]
  66. 66.
    Nakajima S, Ohashi J, Sawada A, Noda K, Fukumoto Y, Shimokawa H. 2012. Essential role of bone marrow for microvascular endothelial and metabolic functions in mice. Circ. Res. 111:87–96
    [Google Scholar]
  67. 67.
    Straub AC, Lohman AW, Billaud M, Johnstone SR, Dwyer ST et al. 2012. Endothelial cell expression of haemoglobin α regulates nitric oxide signalling. Nature 491:473–77
    [Google Scholar]
  68. 68.
    Straub AC, Gladwin MT. 2018. Escorting α-globin to eNOS: α-globin-stabilizing protein paves the way. J. Clin. Investig. 128:4755–57
    [Google Scholar]
  69. 69.
    Lechauve C, Butcher JT, Freiwan A, Biwer LA, Keith JM et al. 2018. Endothelial cell α-globin and its molecular chaperone α-hemoglobin-stabilizing protein regulate arteriolar contractility. J. Clin. Investig. 128:5073–82
    [Google Scholar]
  70. 70.
    Rahaman MM, Nguyen AT, Miller MP, Hahn SA, Sparacino-Watkins C et al. 2017. Cytochrome b5 reductase 3 modulates soluble guanylate cyclase redox state and cGMP signaling. Circ. Res. 121:137–48
    [Google Scholar]
  71. 71.
    DeMartino AW, Amdahl MB, Bocian K, Rose JJ, Tejero J, Gladwin MT. 2021. Redox sensor properties of human cytoglobin allosterically regulate heme pocket reactivity. Free Radic Biol. Med. 162:423–34
    [Google Scholar]
  72. 72.
    Tiso M, Tejero J, Basu S, Azarov I, Wang X et al. 2011. Human neuroglobin functions as a redox-regulated nitrite reductase. J. Biol. Chem. 286:18277–89
    [Google Scholar]
  73. 73.
    Reeder BJ, Ukeri J. 2018. Strong modulation of nitrite reductase activity of cytoglobin by disulfide bond oxidation: implications for nitric oxide homeostasis. Nitric Oxide 72:16–23
    [Google Scholar]
  74. 74.
    Burmester T, Hankeln T. 2014. Function and evolution of vertebrate globins. Acta Physiol 211:501–14
    [Google Scholar]
  75. 75.
    Liu X, El-Mahdy MA, Boslett J, Varadharaj S, Hemann C et al. 2017. Cytoglobin regulates blood pressure and vascular tone through nitric oxide metabolism in the vascular wall. Nat. Commun. 8:14807
    [Google Scholar]
  76. 76.
    Li H, Hemann C, Abdelghany TM, El-Mahdy MA, Zweier JL. 2012. Characterization of the mechanism and magnitude of cytoglobin-mediated nitrite reduction and nitric oxide generation under anaerobic conditions. J. Biol. Chem. 287:36623–33
    [Google Scholar]
  77. 77.
    Zweier JL, Hemann C, Kundu T, Ewees MG, Khaleel SA et al. 2021. Cytoglobin has potent superoxide dismutase function. PNAS 118:e2105053118
    [Google Scholar]
  78. 78.
    Tejero J, Kapralov AA, Baumgartner MP, Sparacino-Watkins CE, Anthonymutu TS et al. 2016. Peroxidase activation of cytoglobin by anionic phospholipids: mechanisms and consequences. Biochim. Biophys. Acta Mol. Cell. Biol. Lipids 1861:391–401
    [Google Scholar]
  79. 79.
    Fordel E, Thijs L, Martinet W, Schrijvers D, Moens L, Dewilde S. 2007. Anoxia or oxygen and glucose deprivation in SH-SY5Y cells: a step closer to the unraveling of neuroglobin and cytoglobin functions. Gene 398:114–22
    [Google Scholar]
  80. 80.
    Amdahl MB, DeMartino AW, Tejero J, Gladwin MT. 2017. Cytoglobin at the crossroads of vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 37:1803–5
    [Google Scholar]
  81. 81.
    Amdahl MB, Sparacino-Watkins CE, Corti P, Gladwin MT, Tejero J. 2017. Efficient reduction of vertebrate cytoglobins by the cytochrome b5/cytochrome b5 reductase/NADH system. Biochemistry 56:3993–4004
    [Google Scholar]
  82. 82.
    Budworth J, Meillerais S, Charles I, Powell K 1999. Tissue distribution of the human soluble guanylate cyclases. Biochem. Biophys. Res. Commun. 263:696–701
    [Google Scholar]
  83. 83.
    Friebe A, Mergia E, Dangel O, Lange A, Koesling D. 2007. Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase. PNAS 104:7699–704
    [Google Scholar]
  84. 84.
    Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J et al. 1994. Mutation of His-105 in the β1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. PNAS 91:2592–96
    [Google Scholar]
  85. 85.
    Ghosh A, Stuehr DJ. 2017. Regulation of sGC via hsp90, cellular heme, sGC agonists, and NO: new pathways and clinical perspectives. Antioxid. Redox Signal. 26:182–90
    [Google Scholar]
  86. 86.
    Stasch J-P, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, HS AK et al. 2006. Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels. J. Clin. Investig. 116:2552–61
    [Google Scholar]
  87. 87.
    Wood KC, Durgin BG, Schmidt HM, Hahn SA, Baust JJ et al. 2019. Smooth muscle cytochrome b5 reductase 3 deficiency accelerates pulmonary hypertension development in sickle cell mice. Blood Adv 3:4104–16
    [Google Scholar]
  88. 88.
    Durgin BG, Wood KC, Hahn SA, McMahon B, Baust JJ, Straub AC. 2022. Smooth muscle cell CYB5R3 preserves cardiac and vascular function under chronic hypoxic stress. J. Mol. Cell. Cardiol. 162:72–80
    [Google Scholar]
  89. 89.
    Alapa M, Cui C, Shu P, Li H, Kholodovych V, Beuve A. 2021. Selective cysteines oxidation in soluble guanylyl cyclase catalytic domain is involved in NO activation. Free Radic. Biol. Med. 162:450–60
    [Google Scholar]
  90. 90.
    Craven PA, DeRubertis FR. 1978. Effects of thiol inhibitors on hepatic guanylate cyclase activity. Evidence for the involvement of vicinal dithiols in the expression of basal and agonist-stimulated activity. Biochim. Biophys. Acta Enzymol. 524:231–44
    [Google Scholar]
  91. 91.
    Fernhoff NB, Derbyshire ER, Underbakke ES, Marletta MA. 2012. Heme-assisted S-nitrosation desensitizes ferric soluble guanylate cyclase to nitric oxide. J. Biol. Chem. 287:43053–62
    [Google Scholar]
  92. 92.
    Huang C, Alapa M, Shu P, Nagarajan N, Wu C et al. 2017. Guanylyl cyclase sensitivity to nitric oxide is protected by a thiol oxidation-driven interaction with thioredoxin-1. J. Biol. Chem. 292:14362–70
    [Google Scholar]
  93. 93.
    Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM et al. 1999. Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase Iα. Science 286:1583–87
    [Google Scholar]
  94. 94.
    Francis SH, Busch JL, Corbin JD, Sibley D. 2010. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol. Rev. 62:525–63
    [Google Scholar]
  95. 95.
    Landgraf W, Regulla S, Meyer H, Hofmann F. 1991. Oxidation of cysteines activates cGMP-dependent protein kinase. J. Biol. Chem. 266:16305–11
    [Google Scholar]
  96. 96.
    Prysyazhna O, Rudyk O, Eaton P. 2012. Single atom substitution in mouse protein kinase G eliminates oxidant sensing to cause hypertension. Nat. Med. 18:286–90
    [Google Scholar]
  97. 97.
    Nakamura T, Ranek MJ, Lee DI, Hahn VS, Kim C et al. 2015. Prevention of PKG1α oxidation augments cardioprotection in the stressed heart. J. Clin. Investig. 125:2468–72
    [Google Scholar]
  98. 98.
    Ghimire K, Altmann HM, Straub AC, Isenberg JS. 2017. Nitric oxide: What's new to NO?. Am. J. Physiol. Cell Physiol. 312:C254–62
    [Google Scholar]
  99. 99.
    Heiss EH, Dirsch VM. 2014. Regulation of eNOS enzyme activity by posttranslational modification. Curr. Pharm. Des. 20:3503–13
    [Google Scholar]
  100. 100.
    Chen F, Kumar S, Yu Y, Aggarwal S, Gross C et al. 2014. PKC-dependent phosphorylation of eNOS at T495 regulates eNOS coupling and endothelial barrier function in response to G+-toxins. PLOS ONE 9:e99823
    [Google Scholar]
  101. 101.
    Moccia F, Berra-Romani R, Tanzi F. 2012. Update on vascular endothelial Ca2+ signalling: a tale of ion channels, pumps and transporters. World J. Biol. Chem. 3:127–58
    [Google Scholar]
  102. 102.
    Foskett JK, White C, Cheung K-H, Mak D-OD. 2007. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 87:593–658
    [Google Scholar]
  103. 103.
    Moccia F, Negri S, Shekha M, Faris P, Guerra G. 2019. Endothelial Ca2+ signaling, angiogenesis and vasculogenesis: just what it takes to make a blood vessel. Int. J. Mol. Sci. 20:3962
    [Google Scholar]
  104. 104.
    Joseph SK, Young MP, Alzayady K, Yule DI, Ali M et al. 2018. Redox regulation of type-I inositol trisphosphate receptors in intact mammalian cells. J. Biol. Chem. 293:17464–76
    [Google Scholar]
  105. 105.
    Lock JT, Sinkins WG, Schilling WP. 2012. Protein S-glutathionylation enhances Ca2+-induced Ca2+ release via the IP3 receptor in cultured aortic endothelial cells. J. Physiol. 590:3431–47
    [Google Scholar]
  106. 106.
    Bansaghi S, Golenar T, Madesh M, Csordas G, RamachandraRao S et al. 2014. Isoform- and species-specific control of inositol 1,4,5-trisphosphate (IP3) receptors by reactive oxygen species. J. Biol. Chem. 289:8170–81
    [Google Scholar]
  107. 107.
    Sun L, Yau HY, Lau OC, Huang Y, Yao X. 2011. Effect of hydrogen peroxide and superoxide anions on cytosolic Ca2+: comparison of endothelial cells from large-sized and small-sized arteries. PLOS ONE 6:e25432
    [Google Scholar]
  108. 108.
    Hu Q, Corda S, Zweier JL, Capogrossi MC, Ziegelstein RC. 1998. Hydrogen peroxide induces intracellular calcium oscillations in human aortic endothelial cells. Circulation 97:268–75
    [Google Scholar]
  109. 109.
    Zheng Y, Shen X. 2005. H2O2 directly activates inositol 1,4,5-trisphosphate receptors in endothelial cells. Redox Rep 10:29–36
    [Google Scholar]
  110. 110.
    Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS et al. 2004. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med. 10:1200–7
    [Google Scholar]
  111. 111.
    Tong X, Ying J, Pimentel DR, Trucillo M, Adachi T, Cohen RA. 2008. High glucose oxidizes SERCA cysteine-674 and prevents inhibition by nitric oxide of smooth muscle cell migration. J. Mol. Cell. Cardiol. 44:361–69
    [Google Scholar]
  112. 112.
    Bhardwaj R, Hediger MA, Demaurex N. 2016. Redox modulation of STIM-ORAI signaling. Cell Calcium 60:142–52
    [Google Scholar]
  113. 113.
    Zhu J, Lu X, Feng Q, Stathopulos PB. 2018. A charge-sensing region in the stromal interaction molecule 1 luminal domain confers stabilization-mediated inhibition of SOCE in response to S-nitrosylation. J. Biol. Chem. 293:8900–11
    [Google Scholar]
  114. 114.
    Gui L, Zhu J, Lu X, Sims SM, Lu WY et al. 2018. S-Nitrosylation of STIM1 by neuronal nitric oxide synthase inhibits store-operated Ca2+ entry. J. Mol. Biol. 430:1773–85
    [Google Scholar]
  115. 115.
    Prins D, Groenendyk J, Touret N, Michalak M. 2011. Modulation of STIM1 and capacitative Ca2+ entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Rep 12:1182–88
    [Google Scholar]
  116. 116.
    Gibhardt CS, Cappello S, Bhardwaj R, Schober R, Kirsch SA et al. 2020. Oxidative stress-induced STIM2 cysteine modifications suppress store-operated calcium entry. Cell Rep 33:108292
    [Google Scholar]
  117. 117.
    Lillo MA, Gaete PS, Puebla M, Ardiles NM, Poblete I et al. 2018. Critical contribution of Na+-Ca2+ exchanger to the Ca2+-mediated vasodilation activated in endothelial cells of resistance arteries. FASEB J 32:2137–47
    [Google Scholar]
  118. 118.
    Wagner S, Rokita AG, Anderson ME, Maier LS. 2013. Redox regulation of sodium and calcium handling. Antioxid. Redox Signal. 18:1063–77
    [Google Scholar]
  119. 119.
    Qian X, Francis M, Solodushko V, Earley S, Taylor MS 2013. Recruitment of dynamic endothelial Ca2+ signals by the TRPA1 channel activator AITC in rat cerebral arteries. Microcirculation 20:138–48
    [Google Scholar]
  120. 120.
    Sullivan MN, Gonzales AL, Pires PW, Bruhl A, Leo MD et al. 2015. Localized TRPA1 channel Ca2+ signals stimulated by reactive oxygen species promote cerebral artery dilation. Sci. Signal. 8:ra2
    [Google Scholar]
  121. 121.
    Loot AE, Popp R, Fisslthaler B, Vriens J, Nilius B, Fleming I 2008. Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc. Res. 80:445–52
    [Google Scholar]
  122. 122.
    Daneva Z, Ottolini M, Chen YL, Klimentova E, Kuppusamy M et al. 2021. Endothelial pannexin 1-TRPV4 channel signaling lowers pulmonary arterial pressure in mice. eLife 10:e67777
    [Google Scholar]
  123. 123.
    Naik JS, Osmond JM, Walker BR, Kanagy NL. 2016. Hydrogen sulfide-induced vasodilation mediated by endothelial TRPV4 channels. Am. J. Physiol. Heart Circ. Physiol. 311:H1437–44
    [Google Scholar]
  124. 124.
    Kochukov MY, Balasubramanian A, Abramowitz J, Birnbaumer L, Marrelli SP. 2014. Activation of endothelial transient receptor potential C3 channel is required for small conductance calcium-activated potassium channel activation and sustained endothelial hyperpolarization and vasodilation of cerebral artery. J. Am. Heart Assoc. 3:e000913
    [Google Scholar]
  125. 125.
    Balzer M, Lintschinger B, Groschner K. 1999. Evidence for a role of Trp proteins in the oxidative stress-induced membrane conductances of porcine aortic endothelial cells. Cardiovasc. Res. 42:543–49
    [Google Scholar]
  126. 126.
    Greenberg HZE, Carlton-Carew SRE, Khan DM, Zargaran AK, Jahan KS et al. 2017. Heteromeric TRPV4/TRPC1 channels mediate calcium-sensing receptor-induced nitric oxide production and vasorelaxation in rabbit mesenteric arteries. Vascul. Pharmacol. 96–98:53–62
    [Google Scholar]
  127. 127.
    Poteser M, Graziani A, Rosker C, Eder P, Derler I et al. 2006. TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J. Biol. Chem. 281:13588–95
    [Google Scholar]
  128. 128.
    Ellsworth ML, Ellis CG, Goldman D, Stephenson AH, Dietrich HH, Sprague RS. 2009. Erythrocytes: oxygen sensors and modulators of vascular tone. Physiology 24:107–16
    [Google Scholar]
  129. 129.
    McMahon TJ, Darrow CC, Hoehn BA, Zhu H. 2021. Generation and export of red blood cell ATP in health and disease. Front. Physiol. 12:754638
    [Google Scholar]
  130. 130.
    Al-Samkari H, van Beers EJ. 2021. Mitapivat, a novel pyruvate kinase activator, for the treatment of hereditary hemolytic anemias. Ther. Adv. Hematol. 12: https://doi.org/10.1177/20406207211066070
    [Crossref] [Google Scholar]
  131. 131.
    Schroeder P, Fulzele K, Forsyth S, Ribadeneira MD, Guichard S et al. 2022. Etavopivat, a pyruvate kinase activator in red blood cells, for the treatment of sickle cell disease. J. Pharmacol. Exp. Ther. 380:210–19
    [Google Scholar]
  132. 132.
    McMahon TJ, Stone AE, Bonaventura J, Singel DJ, Stamler JS. 2000. Functional coupling of oxygen binding and vasoactivity in S-nitrosohemoglobin. J. Biol. Chem. 275:16738–45
    [Google Scholar]
  133. 133.
    Gladwin MT, Wang X, Reiter CD, Yang BK, Vivas EX et al. 2002. S-Nitrosohemoglobin is unstable in the reductive erythrocyte environment and lacks O2/NO-linked allosteric function. J. Biol. Chem. 277:27818–28
    [Google Scholar]
  134. 134.
    Patel RP, Hogg N, Spencer NY, Kalyanaraman B, Matalon S, Darley-Usmar VM. 1999. Biochemical characterization of human S-nitrosohemoglobin. Effects on oxygen binding and transnitrosation. J. Biol. Chem. 274:15487–92
    [Google Scholar]
  135. 135.
    Bailey DM, Rasmussen P, Overgaard M, Evans KA, Bohm AM et al. 2017. Nitrite and S-nitrosohemoglobin exchange across the human cerebral and femoral circulation: relationship to basal and exercise blood flow responses to hypoxia. Circulation 135:166–76
    [Google Scholar]
  136. 136.
    Gladwin MT, Ognibene FP, Pannell LK, Nichols JS, Pease-Fye ME et al. 2000. Relative role of heme nitrosylation and β-cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation. PNAS 97:9943–48
    [Google Scholar]
  137. 137.
    DeMartino AW, Kim-Shapiro DB, Patel RP, Gladwin MT. 2019. Nitrite and nitrate chemical biology and signalling. Br. J. Pharmacol. 176:228–45
    [Google Scholar]
  138. 138.
    Isbell TS, Sun CW, Wu LC, Teng X, Vitturi DA et al. 2008. SNO-hemoglobin is not essential for red blood cell-dependent hypoxic vasodilation. Nat. Med. 14:773–77
    [Google Scholar]
  139. 139.
    Zhang R, Hausladen A, Qian Z, Liao X, Premont RT, Stamler JS. 2022. Hypoxic vasodilatory defect and pulmonary hypertension in mice lacking hemoglobin β-cysteine93 S-nitrosylation. JCI Insight 7:e155234
    [Google Scholar]
  140. 140.
    Sun CW, Yang J, Kleschyov AL, Zhuge Z, Carlstrom M et al. 2019. Hemoglobin β93 cysteine is not required for export of nitric oxide bioactivity from the red blood cell. Circulation 139:2654–63
    [Google Scholar]
  141. 141.
    Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD et al. 2003. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat. Med. 9:1498–505
    [Google Scholar]
  142. 142.
    Huang Z, Shiva S, Kim-Shapiro DB, Patel RP, Ringwood LA et al. 2005. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J. Clin. Investig. 115:2099–107
    [Google Scholar]
  143. 143.
    Shiva S. 2013. Nitrite: a physiological store of nitric oxide and modulator of mitochondrial function. Redox Biol 1:40–44
    [Google Scholar]
  144. 144.
    Dent MR, DeMartino AW, Tejero J, Gladwin MT. 2021. Endogenous hemoprotein-dependent signaling pathways of nitric oxide and nitrite. Inorg. Chem. 60:15918–40
    [Google Scholar]
  145. 145.
    Basu S, Grubina R, Huang J, Conradie J, Huang Z et al. 2007. Catalytic generation of N2O3 by the concerted nitrite reductase and anhydrase activity of hemoglobin. Nat. Chem. Biol. 3:785–94
    [Google Scholar]
  146. 146.
    Wood KC, Cortese-Krott MM, Kovacic JC, Noguchi A, Liu VB et al. 2013. Circulating blood endothelial nitric oxide synthase contributes to the regulation of systemic blood pressure and nitrite homeostasis. Arterioscler. Thromb. Vasc. Biol. 33:1861–71
    [Google Scholar]
  147. 147.
    Leo F, Suvorava T, Heuser SK, Li J, LoBue A et al. 2021. Red blood cell and endothelial eNOS independently regulate circulating nitric oxide metabolites and blood pressure. Circulation 144:870–89
    [Google Scholar]
  148. 148.
    Booth DM, Várnai P, Joseph SK, Hajnóczky G. 2022. Fluorescence imaging detection of nanodomain redox signaling events at organellar contacts. STAR Protoc 3:101119
    [Google Scholar]
  149. 149.
    Dosunmu-Ogunbi AM, Wood KC, Novelli EM, Straub AC. 2019. Decoding the role of SOD2 in sickle cell disease. Blood Adv 3:2679–87
    [Google Scholar]
  150. 150.
    Dosunmu-Ogunbi A, Yuan S, Reynolds M, Giordano L, Sanker S et al. 2022. SOD2 V16A amplifies vascular dysfunction in sickle cell patients by curtailing mitochondria complex IV activity. Blood 139:1760–65
    [Google Scholar]
/content/journals/10.1146/annurev-physiol-031522-021457
Loading
/content/journals/10.1146/annurev-physiol-031522-021457
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error