Alternative oxidase in the branched mitochondrial respiratory network: An overview on structure, function, regulation, and role

Brazilian Journal of Medical and Biological Research

Volumn 31, Issue 6, 1998, Pages 733-747

  Sluse, F E ^a   Jarmuszkiewicz, W ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Alternative oxidase; Electron partitioning; Mitochondria; Regulation; Structure

Indexed keywords

PROTISTA;

ALTERNATIVE OXIDASE; CYANIDE; OXIDOREDUCTASE;

CELL RESPIRATION; ELECTRON TRANSPORT; ENZYMOLOGY; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PLANT; REVIEW;

CELL RESPIRATION; CYANIDES; ELECTRON TRANSPORT; MITOCHONDRIA; OXIDOREDUCTASES; PLANTS;

EID: 0032090845     PISSN: 0100879X     EISSN: 1414431X     Source Type: Journal    
DOI: 10.1590/S0100-879X1998000600003     Document Type: Review

References (90)

1. Genevois ML (1929). Sur la fermentation et sur la respiration chez les végétaux chlorophylliens. Revue Génétique Botanique, 41: 252-271.
2. Lance C (1972). La respiration de l'Arum maculatum au cours du développement de l'inflorescence. Annales des Sciences Naturelles Botaniques, 12: 477-495.
3. Meeuse BJD (1975). Thermogenic respiration in Aroids. Annual Review of Plant Physiology, 26: 117-126.
4. Hup S & Palmer JM (1978). Isolation of a cyanide-resistant duroquinol oxidase from Arum maculatum mitochondria. FEBS Letters, 95: 217-220.
5. Rich PR (1978). Quinol oxidation in Arum maculatum mitochondria and its application to the assay, solubilisation and partial purification of the alternative oxidase. FEBS Letters. 96: 252-256.
6. Bonner Jr WD, Clarke SD & Rich PR (1986). Partial purification and characterization of the quinol oxidase activity of Arum maculatum mitochondria. Plant Physiology. 80: 838-842.
7. Elthon TE & Mclntosh L (1986). Characterization and solubilization of the alternative oxidase of Sauromatum guttatum mitochondria. Plant Physiology. 82: 1-6.
8. Elthon TE, Nickels RL & McIntosh L (1989). Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiology, 89: 1311-1317.
9. Day DA, Whelan J, Millar AH, Siedow JN & Wiskich JT (1995). Regulation of the alternative oxidase in plants and fungi. Australian Journal of Plant Physiology, 22: 497-509.
10. Siedow JN & Umbach AL (1995). Plant mitochondrial electron transfer and molecular biology. Plant Cell. 7: 821-831.
11. Lambowitz AM, Sabourin JR, Bertrand H, Nickels R & McIntosh L (1989). Immunological identification of the alternative oxidase of Neurospora crassa mitochondria. Molecular Cell Biology, 9: 1362-1364.
12. Sakajo S, Minagawa N, Komiyama T & Yoshimoto A (1991). Molecular cloning of cDNA for antimycin A-inducible mRNA and its role in cyanide-resistant respiration in Hansenula anomala. Biochimica et Biophysica Acta, 1090: 102-108.
13. Clarkson AB, Bienen EJ, Pollakis G & Grady RJ (1989). Respiration of blood-stream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. Journal of Biological Chemistry, 264: 17770-17776.
14. Jarmuszkiewicz W, Wagner AM, Wagner JM & Hryniewiecka L (1997). Immunological identification of the alternative oxidase of Acanthamoeba castellanii mitochondria. FEBS Letters, 411: 110-114.
15. Rhoads DM & McIntosh L (1991). Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott), Proceedings of the National Academy of Sciences, USA, 88: 2122-2126.
16. Moore AL & Siedow JN (1991).The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochimica et Biophysica Acta. 1059: 121-140.
17. Siedow JN, Whelan J, Kearns A, Wiskich JT & Day DA (1992). Topology of the alternative oxidase in soybean mitochondria. In: Lambers H & van der Plas LHW (Editors), Molecular, Biochemical and Physiological Aspects of Plant Respiration. SPB Academic Publishing, The Netherlands, 19-27.
18. Moore AL, Umbach AL & Siedow JN (1995). Structure-function relationships of the alternative oxidase of plant mitochondria: a model of the active site. Journal of Bioenergetics and Biomembranes. 27: 367-377.
19. McIntosh L (1994). Molecular biology of the alternative oxidase Plant Physiology, 105: 781-786.
20. Day DA & Wiskich J (1995). Regulation of alternative oxidase activity in higher plants. Journal of Bioenergetics and Biomembranes, 27: 379-385.
21. Wagner AM & Krab K (1995). The alternative respiration pathway in plants: role and regulation. Physiologie Plantarum, 94: 318-325.
22. Krab K (1995). Kinetic and regulatory aspects of the function of the alternative oxidase in plant respiration. Journal of Bioenergetics and Biomembranes, 27: 387-396.
23. Vanlerberghe GC & Mclntosh L (1997). Alternative oxidase: from gene to function. Annual Review of Plant Physiology and Molecular Biology, 48: 703-734.
24. Schonbaum GR, Bonner WD, Storey BT & Bahr JT (1971). Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiology, 47: 124-128.
25. Parrish DJ & Leopold AC (1978). Confounding of alternate respiration by lipoxygenase activity. Plant Physiology. 62: 470-472.
26. Siedow JN & Grivin ME (1980). Alternative respiratory pathway. Its role in seed respiration and its inhibition by propyl gallate. Plant Physiology, 65: 669-674.
27. Grover SD & Laties GG (1978). Characterization of the binding properties of disulfiram, an inhibitor of cyanide-resistant respiration. In: Ducet G & Lance C (Editors), Plant Mitochondria. Elsevier/North Holland Biomedical Press, Amsterdam, 259-266.
28. Huq S & Palmer JM (1978). Superoxide and hydrogen peroxide production in the cyanide resistant Arum maculatum mitochondria. Plant Science Letters, 11: 351-358.
29. Siedow JN (1982). The nature of the cyanide-resistant pathway in plant mitochondria. Recent Advancements in Phytochemistry, 16: 47-83.
30. Minagawa N, Sakajo S, Komiyama T & Yoshimoto A (1990). A 36-kDa mitochondrial protein is responsible for cyanide-resistant respiration in Hansenula anomala. FEBS Letters. 264: 149-152.
31. Siedow JN, Umbach AL & Moore AL (1995). The active site of the cyanide-resistant oxidase from plant mitochondria contains a binuclear iron center. FEBS Letters, 362: 10-14.
32. Umbach AL & Siedow JN (1993). Covalent and non-covalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiology, 103: 845-854.
33. Umbach AL & Siedow JN (1996). The reaction of the soybean cotyledon mitochondrial cyanide-resistant oxidase with sulfhydryl reagents suggests that α-keto acid activation involves the formation of a thiohemiacetal. Journal of Biological Chemistry, 271: 25019-25026.
34. Whelan J, Millar AH & Day DA (1996). The alternative oxidase is encoded in a multigene family in soybean. Planta, 198: 197-201.
35. Finnengan PM, Whelan J, Millar AH, Zhang Q, Smith K, Wiskich J & Day DA (1997). Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiology; 114: 455-466.
36. Elthon TE, Nickels RL & Mclntosh L (1989). Mitochondrial events during development of thermogenesis in Sauromatum guttatum (Schott). Planta, 180: 82-89.
37. Laties GG (1982). The cyanide-resistant, alternative pathway in plant mitochondria. Annual Review of Plant Physiology, 33: 519-555.
38. Minagawa N, Koga S, Nakano M, Sakajo S & Yoshimoto A (1992). Generation of superoxide anion detected by chemiluminescence method in the cyanide-insensitive mitochondria and the induction of the cyanide-resistant respiration in the yeast Hansenula anomala. In: Yagi H, Kondo M, Niki E & Yoshikawa T (Editors), Oxygen Radicals. Elsevier, New York, 203-206.
39. Minagawa N, Koga S, Nakano M, Sakajo S & Yoshimoto A (1992). Possible involvement of Superoxide anion in the induction of cyanide-resistant respiration in Hansenula anomala. FEBS Letters, 302: 217-219.
40. Vanlerberghe GC & Mclntosh L (1996). Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiology, 111: 589-595.
41. Rhoads DM & Mclntosh L (1992). Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell, 4: 1131-1139.
42. Rhoads DM & Mclntosh L (1993). Cytochrome and alternative pathway respiration in tobacco: Effects of salicylic acid. Plant Physiology, 103: 877-883.
43. Ribas-Carbo M, Lennon AM, Robinson SA, Giles L, Berry JA & Siedow JN (1997). The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiology. 113: 903-911.
44. Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE & Mclntosh L (1995). Alternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiology, 109: 353-361.
45. Umbach AL & Siedow AL (1997). Changes in the redox state of the alternative oxidase regulatory sulfhydryl/disulfide system during mitochondrial isolation: implications for inferences of activity in vivo. Plant Science, 123: 19-28.
46. Millar AH, Wiskich JT, Whelan J & Day DA (1993). Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Letters, 329: 259-262.
47. Millar AH, Hoefnagel MHN, Day DA & Wiskich JT (1996). Specificity of the organic acid activation of alternative oxidase in plant mitochondria. Plant Physiology, 111: 613-618.
48. Day DA, Millar AH, Wiskich JT & Whelan J (1994). Regulation of alternative oxidase activity by pyruvate in soybean mitochondria. Plant Physiology. 106: 1421-1427.
49. Umbach AL, Wiskich JT & Siedow JN (1994). Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Letters, 348: 181-184.
50. Hryniewiecka L, Jenek J & Michejda J (1978). Cyanide resistance in soil amoeba Acanthamoeba castellanii. In: Ducet G & Lance C (Editors), Plant Mitochondria. Elsevier/North-Holland, Amsterdam, New York, Oxford, 307-314.
51. Hryniewiecka L & Michejda J (1988). In amoeba mitochondria phosphate mononucleotides stimulate specially the alternative respiratory pathway but not the rotenone-sensitive NADH dehydrogenase. 5th European Bioenergetic Conference Reports, Aberystwyth, UK, 20-26 July 1998, 286 (Abstract).
52. Edwards SW & Lloyd D (1978). Properties of mitochondria isolated from cyanide-stimulated and cyanide-sensitive cultures of Acanthamoeba castellanii. Biochemical Journal, 174: 203-211.
53. Sharpless TK & Butow RA (1970). An inducible alternative terminal oxidase in Euglena gracilis mitochondria. Journal of Biological Chemistry, 245: 58-70.
54. Hanssens L & Verachtert H (1976). Adenosine 5′-monophosphate stimulates cyanide-insensitive respiration in mitochondria of Moniliella tomentosa. Journal of Bacteriology, 125: 829-836.
55. Vanderleyden J, Van den Eynde E & Verachtert H (1980). Nature of the effect of adenosine 5′monophosphate on the cyanide-insensitive respiration in mitochondria of Moniliella tomentosa. Biochemical Journal, 186: 309-316.
56. Doussiere J & Vignais PV (1984). AMP-dependence of the cyanide-insensitive pathway in the respiratory chain of Paramecium tetraurelia. Biochemical Journal, 220: 787-794.
57. Vanderleyden J, Peeters C, Verachtert H & Bertrandt H (1980). Stimulation of the alternative oxidase of Neurospora crassa by nudeoside phosphates. Biochemical Journal, 188: 141-144.
58. Sakajo S, Minagawa N & Yoshimoto Y (1997). Effects of nucleotides on cyanideresistant respiratory activity in mitochondria isolated from antimycin A-treated yeast Hansenula anomala. Bioscience of Biotechnology and Biochemistry, 61:397-399.
59. Vanderleyden J, Kurth J & Verachtert H (1979). Characterization of cyanide-insensitive respiration in mitochondria and submitochondrial particles of Moniliella tamentosa. Biochemical Journal, 182: 437-443.
60. Jarmuszkiewicz W, Wagner AM & Hryniewiecka L (1996). Regulation of the activity of the alternative oxidase in amoeba A. castellanii mitochondria. Biochimica et Biophysica Acta, 9th European Bioenergetic Conference Reports, Louvain la Neuve, Belgium, 17-22 August 1996, 36 (Abstract C. V-5).
61. Li Q, Ritzel RG, McLean LLT, McIntosh L, Ko T, Bertrand H & Nargang FE (1996). Cloning and analysis of the alternative oxidase gene of Neurospora crassa. Genetics, 142: 129-140.
62. Ribas-Carbo M, Wiskich JT, Berry JA & Siedow JN (1995). Ubiquinone redox behaviour in plant mitochondria during electron transport. Archives of Biochemistry and Biophysis, 317: 156-160.
63. Bahr JT & Bonner WD (1973). Cyanideinsensitive respiration. I. The steady states of skunk cabbage spadix and bean hypocotyl mitochondria. Journal of Biological Chemistry, 248: 3441-3445.
64. Bahr JT & Bonner WD (1973). Cyanideinsensitive respiration. II. Control of the alternative pathway. Journal of Biological Chemistry, 248: 3446-3450.
65. Lambers H (1980). The physiological significance of cyanide-resistant respiration in higher plants. Plant Cell and Environment, 3: 293-302.
66. Lambers H (1982). Cyanide-resistant respiration: a non-phosphorylating electron transport pathway acting as an energy overflow. Physiologie Plantarum, 55: 478-485.
67. Moore AL, Dry IB & Wiskich JT (1988). Measurement of the redox state of the ubiquinone pool in plant mitochondria. FEBS Letters, 235: 76-80.
68. Dry JB, Moore AL, Day DA & Wiskich JT (1989). Regulation of alternative pathway activity in plant mitochondria: nonlinear relationship between electron flux and the redox poise of the quinone pool. Archives of Biochemistry and Biophysics. 273: 148-157.
69. Van den Bergen CWM, Wagner AM, Krab K & Moore AL (1994). The relationship between electron flux and the redox poise of the quinone pool in plant mitochondria. European Journal of Biochemistry, 226: 1071-1078.
70. Hoefnagel MHN & Wiskich JT (1996). Alternative oxidase activity and the ubiquinone redox level in soybean cotyledon and Arum spadix mitochondria during NADH and succinate oxidation. Plant Physiology, 110: 1329-1335.
71. Ikuma H, Schindler FJ & Bonner WD (1964). Kinetic analysis of oxidases in tightly coupled plant mitochondria. Plant Physiology, 39:S-1x.
72. Bendall DS & Bonner WD (1971). Cyanide-insensitive respiration in plant mitochondria. Plant Physiology, 47: 236-245.
73. Millar AH, Bergersen FJ & Day DA (1994). Oxygen affinity of terminal oxidases in soybean mitochondria. Plant Physiology and Biochemistry, 32: 847-852.
74. Barzu O & Satre M (1970). Determination of oxygen affinity of respiratory systems using oxyhemoglobin as oxygen donor. Analytical Biochemistry, 36: 428-433.
75. Rawsthorne S & LaRue TA (1986). Metabolism under microaerobic conditions of mitochondria from cowpea nodules. Plant Physiology, 81: 1097-1102.
76. Ribas-Carbo M, Berry JA, Azcon-Bieto J & Siedow JN (1994). The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen. Biochimica et Biophysica Acta, 1188: 205-212.
77. Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM & Wiskich JT (1996) The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiology, 110: 1-2.
78. Millar AH, Atkin OK, Lambers H, Wiskich JT & Day DA (1995). A critique of the use of inhibitors to estimate partitioning of electrons between mitochondrial respiratory pathways in plants. Physiologia Plantarum, 95: 523-532.
79. Guy RG, Berry JA, Fogel ML & Hoerinng TC (1989). Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-insensitive respiration in plants. Planta, 177: 483-491.
80. Guy RG, Berry JA, Fogel ML, Turpin DH & Weger HG (1992). Fractionation of the stable isotopes of oxygen during respiration by plants - the basis for a new technique. In: Lambers H & van der Plas LHW (Editors), Molecular, Biochemical and Physiological Aspects of Plant Respiration. SPB Academic Publishing, Hague, 442-453.
81. Robinson SA, Yakir D, Ribas-Carbo M, Giles L, Osmond CB, Siedow JT & Berry JA (1992). Measurements of the engagement of cyanide-resistant respiration in crassulacean acid metabolism plant Kalanchoe daigremontiana with the use of on-line oxygen isotope discrimination. Planta, 164: 415-422.
82. Robinson SA, Ribas-Carbo M, Yakir D, Giles L, Reuveni Y & Berry JA (1995). Beyond SHAM and cyanide: opportunities for studing the alternative oxidase in plant respiration using oxygen isotope discrimination. Australian Journal of Plant Physiology, 22: 487-496.
83. Ribas-Carbo M, Berry JA, Yakir D, Giles L, Robinson SA, Lennon AM & Siedow JN (1995). Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiology, 109: 829-837.
84. Jarmuszkiewicz W, Sluse-Goffart CM, Hryniewiecka L, Michejda J & Sluse FE (1996). Determination of the respective contributions of the cytochrome and alternative oxidase pathways in Acanthamoeba castellanii mitochondria. In: Westerhoff HV, Snoep JL, Wijker J, Sluse FE & Kholodenko BN (Editors), BioThermoKinetics of the Living Cell. BTK Publishing, Amsterdam, The Netherlands, 31-34.
85. Jarmuszkiewicz W, Sluse-Goffart CM, Hryniewiecka L, Michejda J & Sluse FE (1998). Electron partitioning between the two branching quinol-oxidizing pathways in Acanthamoeba castellanii mitochondria during steady-state 3 respiration. Journal of Biological Chemistry (in press).
86. Lambowitz AM, Smith EW & Slayman CW (1972). Oxidative phosphorylation in Neurospora mitochondria. Studies on wild-type, poky and chloramphenicol induced wild type. Journal of Biological Chemistry, 247: 4859-4865.
87. Meese BJD (1975). Thermogenic respiration in aroids. Annual Review of Plant Physiology, 26: 117-126.
88. Purvis AC & Shewfelt RL (1993). Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiologia Plantarum, 88: 712-718.
89. Purvis AC (1997). Role of the alternative oxidase in limiting Superoxide production by plant mitochondria. Physiologia Plantarum, 100: 165-170.
90. Kromer S (1995). Respiration during photosynthesis. Annual Review of Plant Physiology and Molecular Biology, 46: 45-70.