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Mitochondrial Diversity in the Vasculature: Implications for Vascular Oxygen Sensing

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Hypoxic Pulmonary Vasoconstriction

Part of the book series: Developments in Cardiovascular Medicine ((DICM,volume 252))

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Conclusion

The concept of mitochondrial diversity in the vasculature is new and requires further study as it is likely relevant to other aspects of vascular function. In addition to its role in vascular O2-sensing the diversity concept may have implications for apoptosis, vascular wall remodeling or ischemia-reperfusion injury. It remains to be shown whether this mitochondrial diversity is due to a genetic difference intrinsic to the mitochondria or a result of the different redox environment that the PA are exposed to, compared to the RA.

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References

  1. Archer SL, Huang J, Henry T, Peterson D, and Weir EK. A redox based oxygen sensor in rat pulmonary vasculature. Circ. Res. 1993; 73: 1100–1112.

    CAS  PubMed  Google Scholar 

  2. Archer SL, Huang JMC, Reeve HL, Hampl V, Tolarová S, Michelakis ED, and Weir EK. Differential distribution of electrophysiologically distinct myocytes in conduit and resistance arteries determines their response to nitric oxide and hypoxia. Circ. Res. 1996; 78: 431–442.

    CAS  PubMed  Google Scholar 

  3. Archer S and Michelakis E. The mechanism(s) of hypoxic pulmonary vasoconstriction: potassium channels, redox O2 sensors, and controversies. News Physiol. Sci. 2002; 17: 131–137.

    CAS  PubMed  Google Scholar 

  4. Archer SL, Nelson DP, and Weir EK. Simultaneous measurement of oxygen radicals and pulmonary vascular reactivity in the isolated rat lung. J. Appl. Physiol. 1989; 67: 1903–1911.

    CAS  PubMed  Google Scholar 

  5. Ashcroft FM. Adenosine 5′-triphosphate-sensitive potassium channels. Annu. Rev. Neurosci. 1988; 11: 97–118.

    Article  CAS  PubMed  Google Scholar 

  6. Barlow RS and White RE. Hydrogen peroxide relaxes porcine coronary arteries by stimulating BK Ca channel activity. Am. J. Physiol. 1998; 275: H1283–H1289.

    CAS  PubMed  Google Scholar 

  7. Barrientos A and Moraes C. Titrating the effects of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 1999; 274: 16188–16197.

    Article  CAS  PubMed  Google Scholar 

  8. Bennett MR. Apoptosis in the cardiovascular system. Heart. 2002; 87: 480–487.

    Article  PubMed  Google Scholar 

  9. Boveris A and Chance B. The mitochondrial generation of hydrogen peroxide. Biochem. J. 1973; 134: 707–716.

    CAS  PubMed  Google Scholar 

  10. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, and Popov KM. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem. J. 1998; 329: 191–196.

    CAS  PubMed  Google Scholar 

  11. Brooks DE and Mann T. Relation between the oxidation state of nicotinamide-adenine dinucleotide and the metabolism of spermatozoa. Biochem. J. 1972; 129: 1023–1034.

    CAS  PubMed  Google Scholar 

  12. Burke T and Wolin M. Hydrogen peroxide elicits pulmonary arterial relaxation and guanylate cyclase activation. Am. J. Physiol. 1987; 252: H721–H732.

    CAS  PubMed  Google Scholar 

  13. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, and Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 2000; 275: 25130–25138.

    Article  CAS  PubMed  Google Scholar 

  14. Collins TJ, Berridge MJ, Lipp P, and Bootman MD. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 2002; 21: 1616–1627.

    Article  CAS  PubMed  Google Scholar 

  15. Cowan KN, Heilbut A, Humpl T, Lam C, Ito S, and Rabinovitch M. Complete reversal of fatal pulmonary hypertension in rats by a serine elastase inhibitor. Nat. Med. 2000; 6: 698–702.

    CAS  PubMed  Google Scholar 

  16. Cross A and Jones O. The effect of the inhibitor diphenylene iodonium on the superoxide generating system of neutrophils. Biochem. J. 1986; 237: 111–116.

    CAS  PubMed  Google Scholar 

  17. Darley-Usmar VM, Rickwood D, and Wolson MT, Mitochondria: A Practical Approach. Oxford: IRL Press, 1987.

    Google Scholar 

  18. Duchen MR. Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J. Physiol. 1999; 516: 1–17.

    Article  CAS  PubMed  Google Scholar 

  19. Fergus DJ, Martens JR, and England SK. Kv channel subunits that contribute to voltage-gated K+ current in renal vascular smooth muscle. Pflügers Arch. 2003; 445: 697–704.

    CAS  PubMed  Google Scholar 

  20. Gebremedhin D, Bonnet P, Greene AS, England SK, Rusch NJ, Lombard JH, and Harder DR. Hypoxia increases the activity of Ca2+-sensitive K+ channels in cat cerebral arterial muscle cell membranes. Pflügers Arch. 1994; 428: 621–630.

    Article  CAS  PubMed  Google Scholar 

  21. Gordienko DV, Clausen C, and Goligorsky MS. Ionic currents and endothelin signaling in smooth muscle cells from rat renal resistance arteries. Am. J. Physiol. 1994; 266: F325–F341.

    CAS  PubMed  Google Scholar 

  22. Green DR and Reed JC. Mitochondria and apoptosis. Science. 1998; 281: 1309–1312.

    CAS  PubMed  Google Scholar 

  23. Green L and Smith T. The use of digitalis in patients with pulmonary disease. Ann. Intern. Med. 1977; 87: 459–465.

    CAS  PubMed  Google Scholar 

  24. Groen AK, van Roermund CW, Vervoorn RC, and Tager JM. Control of gluconeogenesis in rat liver cells. Flux control coefficients of the enzymes in the gluconeogenic pathway in the absence and presence of glucagon. Biochem. J. 1986; 237: 379–389.

    CAS  PubMed  Google Scholar 

  25. Hayabuchi Y, Nakaya Y, Matsuoka S, and Kuroda Y. Hydrogen peroxide-induced vascular relaxation in porcine coronary arteries is mediated by Ca2+-activated K+ channels. Heart Vessels. 1998; 13: 9–17.

    CAS  PubMed  Google Scholar 

  26. Huttemann M, Kadenbach B, and Grossman LI. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene. 2001; 267: 111–123.

    CAS  PubMed  Google Scholar 

  27. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, Uchida K, Arimura K, Egashira K, and Takeshita A. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ. Res. 1999; 85: 357–363.

    CAS  PubMed  Google Scholar 

  28. Jeffery TK and Morrell NW. Molecular and cellular basis of pulmonary vascular remodeling in pulmonary hypertension. Prog. Cardiovasc. Dis. 2002; 45: 173–202.

    CAS  PubMed  Google Scholar 

  29. Kaminski PM and Wolin MS. Hypoxia increases superoxide anion production from bovine coronary microvessels, but not cardiac myocytes, via increased xanthine oxidase. Microcirculation. 1994; 1: 231–236.

    CAS  PubMed  Google Scholar 

  30. Kovacevic Z, McGivan JD, and Chappell JB. Conditions for activity of glutaminase in kidney mitochondria. Biochem. J. 1970; 118: 265–274.

    CAS  PubMed  Google Scholar 

  31. Krick S, Platoshyn O, Sweeney M, Kim H, and Yuan JX-J. Activation of K+ channels induces apoptosis in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 2001; 280: C970–C979.

    CAS  PubMed  Google Scholar 

  32. Krick S, Platoshyn O, Sweeney M, McDaniel SS, Zhang S, Rubin LJ, and Yuan JX-J. Nitric oxide induces apoptosis by activating K+ channels in pulmonary vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 2002; 282: H184–H193.

    CAS  PubMed  Google Scholar 

  33. Kunz WS. Different metabolic properties of mitochondrial oxidative phosphorylation in different cell types-important implications for mitochondrial cytopathies. Exp. Physiol. 2003; 88: 149–154.

    Article  CAS  PubMed  Google Scholar 

  34. Li Y, Zhu H, Kuppusamy P, Roubaud V, Zweier J, and Trush M. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J. Biol. Chem. 1998; 273: 2015–2023.

    CAS  PubMed  Google Scholar 

  35. Madden J, Vadula M, and Kurup V. Effects of hypoxia and other vasoactive agents on pulmonary and cerebral artery smooth muscle cells. Am. J. Physiol. 1992; 263: L384–L393.

    CAS  PubMed  Google Scholar 

  36. Martens JR and Gelband CH. Alterations in rat interlobar artery membrane potential and K+ channels in genetic and nongenetic hypertension. Circ. Res. 1996; 79: 295–301.

    CAS  PubMed  Google Scholar 

  37. Michelakis ED, Hampl V, Nsair A, Wu X, Harry G, Haromy A, Gurtu R, and Archer SL. Diversity in mitochondrial function explains differences in vascular oxygen sensing. Circ. Res. 2002; 90: 1307–1315.

    Article  CAS  PubMed  Google Scholar 

  38. Michelakis ED, McMurtry MS, Wu XC, Dyck JR, Moudgil R, Hopkins TA, Lopaschuk GD, Puttagunta L, Waite R, and Archer SL. Dichloroacetate, a metabolic modulator, prevents and reverses chronic hypoxic pulmonary hypertension in rats: role of increased expression and activity of voltage-gated potassium channels. Circulation. 2002; 105: 244–250.

    CAS  PubMed  Google Scholar 

  39. Milkowski AL and Lardy HA. Factors affecting the redox state of bovine epididymal spermatozoa. Arch. Biochem. Biophys. 1977; 181: 270–277.

    Article  CAS  PubMed  Google Scholar 

  40. Moyes CD and Hood DA. Origins and consequences of mitochondrial variation in vertebrate muscle. Annu. Rev. Physiol. 2003; 65: 177–201.

    Article  CAS  PubMed  Google Scholar 

  41. Nedergaard J and Cannon B. Overview-Preparation and properties of mitochondria from different sources. Meth. Enzymol. 1979; 55: 3–33.

    CAS  PubMed  Google Scholar 

  42. Palmer JW, Tandler B, and Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J. Biol. Chem. 1977; 252: 8731–8739.

    CAS  PubMed  Google Scholar 

  43. Pettus EH, Betarbet R, Cottrell B, Wallace DC, Madyastha V, and Greenamyre JT. Immunocytochemical characterization of the mitochondrially encoded ND1 subunit of complex I (NADH: ubiquinone oxidoreductase) in rat brain. J. Neurochem. 2000; 75: 383–392.

    Article  CAS  PubMed  Google Scholar 

  44. Pitkanen S, Raha S, and Robinson BH. Diagnosis of complex I deficiency in patients with lactic acidemia using skin fibroblast cultures. Biochem. Mol. Med. 1996; 59: 134–137.

    Article  CAS  PubMed  Google Scholar 

  45. Pitkanen S and Robinson BH. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Invest. 1996; 98: 345–351.

    CAS  PubMed  Google Scholar 

  46. Platoshyn O, Zhang S, McDaniel SS, and Yuan JX-J. Cytochrome c activates K+ channels before inducing apoptosis. Am. J. Physiol. Cell Physiol. 2002; 283: C1298–C1305.

    CAS  PubMed  Google Scholar 

  47. Rotig A, de Lonlay P, Chretien D, Foury F, Koenig M, Sidi D, Munnich A, and Rustin P. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 1997; 17: 215–217.

    CAS  PubMed  Google Scholar 

  48. Scarpulla RC. Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembr. 1997; 29: 109–119.

    Article  CAS  PubMed  Google Scholar 

  49. Vanden Hoek TL, Becker LB, Shao Z, Li C, and Schumacker PT. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J. Biol Chem. 1998; 273: 18092–18098.

    Google Scholar 

  50. Wallace DC. Mitochondrial diseases in man and mouse. Science. 1999; 283: 1482–1488.

    Article  CAS  PubMed  Google Scholar 

  51. Wallace DC, Singh G, Lott MT, Hodge JA, Schurr TG, Lezza AM, Elsas LJ 2nd, and Nikoskelainen EK. Mitochondrial DNA mutation associated with Leber’s hereditary optic neuropathy. Science. 1988; 242: 1427–1430.

    CAS  PubMed  Google Scholar 

  52. Wang D, Youngson C, Wong V, Yeger H, Dinauer MC, Vega-Saenz Miera E, Rudy B, and Cutz E. NADPH-oxidase and a hydrogen peroxide-sensitive K+ channel may function as an oxygen sensor complex in airway chemoreceptors and small cell lung carcinoma cell lines. Proc. Natl. Acad. Sci. USA. 1996; 93: 13182–13187.

    CAS  PubMed  Google Scholar 

  53. Weinstein ES, Benson DW, and Fry DE. Subpopulations of human heart mitochondria. J. Surg. Res. 1986; 40: 495–498.

    Article  CAS  PubMed  Google Scholar 

  54. Williamson DH, Lund P, and Krebs HA. The redox state of free nicotinamide-adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 1967; 103: 514–527.

    CAS  PubMed  Google Scholar 

  55. Wolin MS. Interactions of oxidants with vascular signaling systems. Arterioscler. Thromb. Vasc. Biol. 2000; 20: 1430–1442.

    CAS  PubMed  Google Scholar 

  56. Wolin M and Burke T. Hydrogen peroxide elicits activation of bovine pulmoary arterial soluble guanylate cyclase by a mechanism associated with its metabolism by catalase. Biochem. Biophys. Res. Comm. 1987; 143: 20–25.

    CAS  PubMed  Google Scholar 

  57. Yuan X-J, Aldinger A, Orens J, Conte J, and Rubin L. Dysfunctional voltage-gated potassium channels in the pulmonary artery smooth muscle cells of patients with primary pulmonary hypertension. Circulation. 1996; 94: 1–49.

    Google Scholar 

  58. Yuan X-J, Tod ML, Rubin LJ, and Blaustein MP. Deoxyglucose and reduced glutathione mimic effects of hypoxia on K+ and Ca2+ conductances in pulmonary artery cells. Am. J. Physiol. 1994; 267: L52–L63.

    CAS  PubMed  Google Scholar 

  59. Zamzami N and Kroemer G. The mitochondrion in apoptosis: how Pandora’s box opens. Nat. Rev. Mol. Cell Biol. 2001; 2: 67–71.

    Article  CAS  PubMed  Google Scholar 

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McMurtry, S., Michelakis, E.D. (2004). Mitochondrial Diversity in the Vasculature: Implications for Vascular Oxygen Sensing. In: Yuan, J.X.J. (eds) Hypoxic Pulmonary Vasoconstriction. Developments in Cardiovascular Medicine, vol 252. Springer, Boston, MA. https://doi.org/10.1007/1-4020-7858-7_17

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  • DOI: https://doi.org/10.1007/1-4020-7858-7_17

  • Publisher Name: Springer, Boston, MA

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