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Nitric Oxide Drives Mitochondrial Energetics in Heart and Liver Mitochondria of Hypoxia-Stressed Climbing Perch (Anabas testudineus Bloch)


Affiliations
1 Department of Zoology, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
2 Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
     

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Nitric oxide (NO), a gaseous free radical that functions as signal molecule, regulates several physiological functions. But in teleost fishes, the influence of NO on mitochondrial energetics is not yet understood. With a view to understanding the short-term in vivo action of NO on mitochondrial energetics in fish, we examined the effects of sodium nitroprusside, a NO donor (SNP) and N-omega-nitro-L-arginine methyl ester (L-NAME), a competitive inhibitor of nitric oxide synthase (L-NAME), on major electron carriers and oxidative status in heart and liver mitochondria of an obligate air-breathing fish (Anabas testudineus Bloch) kept at either non-stressed or hypoxia-stressed condition. The total nitrate/nitrite (NO3-/NO2-) level that corresponds to NO content showed a rise after SNP (5 μg g-1) and a decline in the heart and liver of non-stressed fish after L-NAME (100 ng g-1) treatments for 30 min. Water immersion for 30 min that induced hypoxia lowered NO3-/NO2- level in heart and liver, but showed a rise in NO3-/NO2- level after SNP treatment of immersion-stressed fish. Reactive Oxygen Species (ROS) production increased after SNP treatment but decreased after L-NAME treatment in heart of hypoxia-stressed fish where as in liver both SNP and L-NAME treatments caused decrease of ROS in stressed fish. SNP treatment increased and L-NAME treatment lowered peroxynitrite (ONOO-) level in heart and liver of non-stressed fish. SNP treatment lowered the activity of cytochrome c oxidase (COX) but L-NAME treatment increased its activity in mitochondria of heart of hypoxia-stressed fish. In liver mitochondria, however, COX activity showed a rise after these treatments. On the contrary, SNP and L-NAME treatments in stressed fish elevated succinate dehydrogenase (SDH) activity in both heart and liver mitochondria. In heart, LDH activity increased after SNP and L-NAME treatments in both non-stressed and stressed conditions, but not in liver of stressed fish. Put together, the data provide evidence that NO exerts an integrative action on mitochondrial energetics in heart and liver mitochondria of air-breathing fish during their exposure to hypoxia-stress.

Keywords

Anabas testudineus, Cytochrome oxidase, Fish Stress, Hypoxia ROS, Mitochondria Energetics, Nitric Oxide.
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  • Manoli I, Alesci S, Blackman MR, Su YA, Rennert OM, Chrousos GP. Mitochondria as key components of the stress response. Trends Endocrinol Metab. 2007; 18:190-198. https://doi.org/10.1016/j.tem.2007.04.004.
  • Picard M, McEwen BS, Epel ES, Sandi C. An energetic view of stress: Focus on mitochondria. Front Neuroendocrinol. 2018; 49:72-85. https://doi.org/10.1016/j.yfrne.2018.01.001.
  • Demonacos C, Djordjevic-Markovic R, Tsawdaroglou N, Sekeris CE. The mitochondrion as a primary site of action of glucocorticoids: The interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements. J Steroid Biochem Mol Biol. 1995; 55:43-55. https://doi.org/10.1016/0960-0760(95)00159-W.
  • Duclos M, Martin C, Gouarne C, Lettelier C. Effects of corticosterone on muscle mitochondria identifying different sensitivity to glucocorticoids in Lewis and Fischer rats. J Endocrinol Metab. 2003; 286:E159-E167. https://doi.org/10.1152/ajpendo.00281.2003.
  • Tome ME, Lee K, Jaramillo MC, Briehl MM. Mitochondria are the primary source of the H(2) O(2) signal for glucocorticoid-induced apoptosis of lymphoma cells. Exp Ther Med. 2012; 4(2):237-42. https://doi.org/10.3892/etm.2012.595
  • Picard M, Wallace DC, Burelle Y. The rise of mitochondria in medicine. Mitochondrion, 2016; 30:105-116. https://doi.org/10.1016/j.mito.2016.07.003.
  • Midzak A, Papadopoulos V. Adrenal mitochondria and steroidogenesis : From individual proteins to functional protein assemblies. Front Endocrinol. (Lausanne) 2016; 7:106 https://doi.org/10.3389/fendo.2016.00106.
  • Wiest R, Groszmann RJ. The paradox of nitric oxide in cirrhosis and portal hypertension: Too much, not enough. Hepatology 2002; 35(2):478-490. https://doi.org/10.1053/jhep.2002.31432.
  • Hu LS, George J, Wang JH. Current concepts on the role of nitric oxide in portal hypertension. World J Gastroenterol. 2013; 19:1707-17. https://doi.org/10.3748/wjg.v19.i11.1707.
  • Bohlen HG. Nitric oxide and the cardiovascular system. Comp Physiol. 2015; 5(2):808-23. https://doi.org/10.1002/cphy.c140052.
  • Brown GC, Borutaite V. Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res. 2007; 75:283-90. https://doi.org/10.1016/j.cardiores.2007.03.022.
  • Iwakiri Y, Kim MY. Nitric oxide in liver diseases. Trends Pharmacol Sci. 2015; 36(8):524-36. https://doi.org/10.1016/j.tips.2015.05.001.
  • Giulivi C, Kato K, Cooper CE. Nitric oxide regulation of mitochondrial oxygen consumption. II: Molecular mechanism and tissue physiology. AJP Cell Physiol. 2006; 292:C1993-C2003. https://doi.org/10.1152/ajpcell.00310.2006.
  • Brown GC. Nitric oxide and mitochondria. Front Biosci. 2007; 1(12):1024-33. https://doi.org/10.2741/2122.
  • Cooper CE. Nitric oxide and iron proteins. Biochim Biophys Acta - Bioenerg. 1999; 1411(2-3):290-309. https://doi.org/10.1016/S0005-2728(99)00021-3.
  • Lancaster JR. A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1997; 1(1):18-30. https://doi.org/10.1006/niox.1996.0112.
  • Kelm M. Nitric oxide metabolism and breakdown. Biochem Biophys Acta. 1999; 1411(2-3):273-89. https://doi.org/10.1016/S0005-2728(99)00020-1.
  • Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM. Biological aspects of reactive nitrogen species. Biochim Biophys Acta - Bioenerg. 1999; 1411(2-3):385-400. https://doi.org/10.1016/S00052728(99)00028-6.
  • Radi R, Cassina A, Hodara R, Quijano C, Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med. 2002; 33:1451-64. https://doi.org/10.1016/S0891-5849(02)01111-5.
  • Gaston B. Nitric oxide and thiol groups. Biochim Biophys Acta - Bioenerg. 1999; 1411(2-3):323-33. https://doi.org/10.1016/S0005-2728(99)00023-7.
  • Cadenas E, Davies KJA. Mitochondrial free radical generation, oxidative stress and aging. Free Radic Biol Med. 2000; 29:201-383. https://doi.org/10.1016/S0891-5849(00)00315-4.
  • Taylor CT, Moncada S. Nitric oxide, cytochrome c oxidase, and the cellular response to hypoxia. Arterioscler Thromb Vasc Biol. 2010; 30:643-47. https://doi.org/10.1161/ATVBAHA.108.181628.
  • Cooper CE, Brown GC. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significance. J Bioenerg Biomembr. 2008; 40:533-39. https://doi.org/10.1007/s10863-008-9166-6.
  • Palacios-Callender M, Hollis V, Mitchison M, Frakich N, Unitt D, Moncada S. Cytochrome c oxidase regulates endogenous nitric oxide availability in respiring cells: A possible explanation for hypoxic vasodilation. Proc Natl Acad Sci. 2007; 104:18508-18513. https://doi.org/10.1073/pnas.0709440104.
  • Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997; 77:591-625. https://doi.org/10.1152/physrev.1997.77.3.591.
  • Barton BA. Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol. 2002; 42:517-25. https://doi.org/10.1093/icb/42.3.517.
  • Peter MCS. Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation. Gen Comp Endocrinol. 2013; 181:59-64. https://doi.org/10.1016/j.ygcen.2012.09.016.
  • Charmandari E, Tsigos C, Chrousos G. Endocrinology of the stress response. Annu Rev Physiol. 2005; 67:259-84. https://doi.org/10.1146/annurev.physiol.67.040403.120816.
  • Alberti KGMM. The biochemical consequences of hypoxia. J Clin Pathol. 1977; 14-20. https://doi.org/10.1136/jcp.s3-11.1.14
  • Peter MCS, Rejitha V, Dilip DG. Handling of ferric iron by branchial and intestinal epithelia of climbing perch (Anabas testudineus Bloch). Indian J Exp Biol. 2007; 45:896-900.
  • Peter VS, Peter MCS. The interruption of thyroid and interrenal and the inter-hormonal interference in fish: Does it promote physiologic adaptation or maladaptation? Gen Comp Endocrinol. 2011; 174:249-258. https://doi.org/10.1016/j.ygcen.2011.09.018.
  • Simi S, Peter VS, Peter MCS. Zymosan-induced immune challenge modifies the stress response of hypoxic airbreathing fish (Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transport. Gen Comp Endocrinol. 2016; 251:94-108. https://doi.org/10.1016/j.ygcen.2016.11.009.
  • Peter MCS, Mini VS, Bindulekha DS, Peter VS. Short-term in-situ effects of prolactin and insulin on ion transport in liver and intestine of freshwater climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2014; 18(1):47-58.
  • Sastry KVH, Moudgal RP, Mohan J, Tyagi JS, Rao GS. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal Biochem. 2002; 306:79-82. https://doi.org/10.1006/abio.2002.5676.
  • Vanuffelen BE, van der Zee J, de Koster BM, Vansteveninck J, Elferink JG. Intracellular but not extracellular conversion of nitroxyl anion into nitric oxide leads to stimulation of human neutrophil migration. Biochem J. 1998; 330:719-22. https://doi.org/10.1042/bj3300719.
  • Socci DJ, Bjugstad KB, Jones HC, Pattisapu J V, Arendash GW. Evidence that oxidative stress is associated with the pathophysiology of inherited hydrocephalus in the H-Tx rat model. Exp Neurol. 1999; 155:109-117. https://doi.org/10.1006/exnr.1998.6969.
  • Chrzanowska-Lightowlers ZMA, Turnbull DM, Lightqwlers RN. A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Anal Biochem. 1993; 214:45-49. https://doi.org/10.1006/abio.1993.1454.
  • Hollywood KA, Shadi IT, Goodacre R. Monitoring the succinate dehydrogenase activity isolated from mitochondria by surface enhanced Raman scattering. J Phys Chem. 2010; C 114:7308-13. https://doi.org/10.1021/jp908950x.
  • Sensabaugh GFJ, Kaplan NO. Dehydrogenase specific to the liver of Gadoid. J Biol Chem. 1972; 217:585-93.
  • Drapier JC, Hirling H, Wietzerbin J, Kaldy P, Kuhn LC. Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 1993; 12:3643-49. https://doi.org/10.1002/j.1460-2075.1993.tb06038.x.
  • Erusalimsky JD, Moncada S. Nitric oxide and mitochondrial signaling from physiology to pathophysiology. Arterioscler Thromb Vasc Biol. 2007; 27:2524-31. https://doi.org/10.1161/ATVBAHA.107.151167.
  • Pulatova MK, Sharygin VL, Rikhireva GT, Mitrokhin YI, Todorov IN. The mechanisms of nitric oxide production from exogenous and endogenous NO-donating compounds in cells of higher animals and the influence of nitric oxide on deoxyribonucleotide and DNA synthesis. Biol Bull. 2006; 33:441-56. https://doi.org/10.1134/S1062359006050049.
  • Zhang J, Wang X, Vikash V, Ye Q,Wu D, Liu Y, Dong W. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev. 2016; 1-18. https://doi.org/10.1155/2016/4350965.
  • Duranteau J, Chandel NS, Kulisz A, Shao Z, Schumacker PT. Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J Biol Chem. 1998; 273: 11619-24. https://doi.org/10.1074/jbc.273.19.11619.
  • Chandel NS, Schumacker PT. Cellular oxygen sensing by mitochondria: old questions, new insight. J Appl Physiol. 2000; 88:1880-89. https://doi.org/10.1152/jappl.2000.88.5.1880.
  • Guzy RD, Schumacker PT. Oxygen sensing by mitochondria at complex III: The paradox of increased reactive oxygen species during hypoxia. Exp Physiol. 2006; 91:80719. https://doi.org/10.1113/expphysiol.2006.033506.
  • Hill BG, Dranka BP, Bailey SM, Lancaster JR, DarleyUsmar VM. What part of NO don’t you understand? Some answers to the cardinal questions in nitric oxide biology. J Biol Chem. 2010; 285:19699-704. https://doi.org/10.1074/jbc.R110.101618.
  • Arnelle DR, Stamler JS. NO+, NO.and NO- donation by S-nitrosothiols: Implications for regulation of physiological functions by S-nitrosylation and acceleration of disulphide formation. Arch Biochem Biophys. 1995; 318(2):279-85. https://doi.org/10.1006/abbi.1995.1231.
  • Mannick JB, Schonhoff CM. Measurement of protein S-nitrosylation during cell signaling. Methods Enzymol. 2008; 440:231-42. https://doi.org/10.1016/S0076-6879(07)00814-2.
  • Piantadosi CA. Regulation of mitochondrial processes by protein S-nitrosylation. Biochem Biophys Acta. 2012; 1820(6):712-21. https://doi.org/10.1016/j.bbagen.2011.03.008.
  • Poderoso JJ, Peralta JG, Lisdero CL, Carreras MC, Radisic M, Schopfer F, Cadenas E, Boveris A. Nitric oxide regulates oxygen uptake and hydrogen peroxide release by the isolated beating rat heart. Am J Physiol. 1998; 274:C112-C119. https://doi.org/10.1152/ajpcell.1998.274.1.C112.
  • Clementi E, Brown GC, Foxwell N, Moncada S. On the mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc Natl Acad Sci. 1999; 96:1559-62. https://doi.org/10.1073/pnas.96.4.1559.
  • Borutaite V, Budriunaite A, Brown GC. Reversal of nitric oxide- , peroxynitrite- and S -nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. 2000; 1459:405-12. https://doi.org/10.1016/S0005-2728(00)00178-X.
  • Brown GC. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta. 2001; 1504:46-57. https://doi.org/10.1016/ S0005-2728(00)00238-3.
  • Collins-nakai RL, Noseworthy D, Lopaschuk GD. Epinephrine increases ATP production in hearts by preferentially increasing glucose metabolism. Am J Physiol. 1994; 267:H1862-H1871. https://doi.org/10.1152/ajpheart.1994.267.5.H1862.
  • Radi R, Rodriguez M, Castro L, Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys. 1994; 308:89-95. https://doi.org/10.1006/abbi.1994.1013.
  • Sarti P, Arese M, Bacchi A, Barone MC, Forte E, Mastronicola D, Brunori M, Giuffrè A. Nitric oxide and mitochondrial complex IV. IUBMB Life. 2003; 55:605-11. https://doi.org/10.1080/15216540310001628726.
  • Schild L, Reinheckel T, Wiswedel I, Augustin W. Shortterm impairment of energy production in isolated rat liver mitochondria by hypoxia/reoxygenation: Involvement of oxidative protein modification. Biochem J. 1997; 328:205-10. https://doi.org/10.1042/bj3280205.
  • Reinheckel T, Körn S, Möhring S, Augustin W, Halangk W, Schild L. Adaptation of protein carbonyl detection to the requirements of proteome analysis demonstrated for hypoxia/reoxygenation in isolated rat liver mitochondria. Arch Biochem Biophys. 2000; 376:59-65. https://doi.org/10.1006/abbi.1999.1680.
  • Pabla R, Curtis MJ. Effect of endogenous nitric oxide on cardiac systolic and diastolic function during ischemia and reperfusion in the rat isolated perfused heart. J Mol Cell Cardiol. 1996; 28:2111-2121. https://doi.org/10.1006/jmcc.1996.0203.
  • Masini E, Salvemini D, Ndisang JF, Gai P, Berni L, Moncini M, Bianchi S, Mannaioni PF. Cardioprotective activity of endogenous and exogenous nitric oxide on ischaemia reperfusion injury in isolated guinea pig hearts. Inflamm Res. 1999; 48:561-68. https://doi.org/10.1007/s000110050504.

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  • Nitric Oxide Drives Mitochondrial Energetics in Heart and Liver Mitochondria of Hypoxia-Stressed Climbing Perch (Anabas testudineus Bloch)

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Authors

R. Gayathry
Department of Zoology, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
Valsa S. Peter
Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India
M. C. Subhash Peter
Inter-University Centre for Evolutionary and Integrative Biology iCEIB, School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala, India

Abstract


Nitric oxide (NO), a gaseous free radical that functions as signal molecule, regulates several physiological functions. But in teleost fishes, the influence of NO on mitochondrial energetics is not yet understood. With a view to understanding the short-term in vivo action of NO on mitochondrial energetics in fish, we examined the effects of sodium nitroprusside, a NO donor (SNP) and N-omega-nitro-L-arginine methyl ester (L-NAME), a competitive inhibitor of nitric oxide synthase (L-NAME), on major electron carriers and oxidative status in heart and liver mitochondria of an obligate air-breathing fish (Anabas testudineus Bloch) kept at either non-stressed or hypoxia-stressed condition. The total nitrate/nitrite (NO3-/NO2-) level that corresponds to NO content showed a rise after SNP (5 μg g-1) and a decline in the heart and liver of non-stressed fish after L-NAME (100 ng g-1) treatments for 30 min. Water immersion for 30 min that induced hypoxia lowered NO3-/NO2- level in heart and liver, but showed a rise in NO3-/NO2- level after SNP treatment of immersion-stressed fish. Reactive Oxygen Species (ROS) production increased after SNP treatment but decreased after L-NAME treatment in heart of hypoxia-stressed fish where as in liver both SNP and L-NAME treatments caused decrease of ROS in stressed fish. SNP treatment increased and L-NAME treatment lowered peroxynitrite (ONOO-) level in heart and liver of non-stressed fish. SNP treatment lowered the activity of cytochrome c oxidase (COX) but L-NAME treatment increased its activity in mitochondria of heart of hypoxia-stressed fish. In liver mitochondria, however, COX activity showed a rise after these treatments. On the contrary, SNP and L-NAME treatments in stressed fish elevated succinate dehydrogenase (SDH) activity in both heart and liver mitochondria. In heart, LDH activity increased after SNP and L-NAME treatments in both non-stressed and stressed conditions, but not in liver of stressed fish. Put together, the data provide evidence that NO exerts an integrative action on mitochondrial energetics in heart and liver mitochondria of air-breathing fish during their exposure to hypoxia-stress.

Keywords


Anabas testudineus, Cytochrome oxidase, Fish Stress, Hypoxia ROS, Mitochondria Energetics, Nitric Oxide.

References





DOI: https://doi.org/10.18311/jer%2F2018%2F24149