Metabolic adaptations supporting anoxia tolerance in reptiles: Recent advances

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 113, Issue 1, 1996, Pages 23-35

  Storey, Kenneth B ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

antioxidant enzymes; enzyme phosphorylation; gene expression; ischemia reperfusion injury; metabolic rate depression; multicatalytic proteinase complex; protein kinase C; turtle anoxia

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C;

ADAPTATION; ANOXIA; CONFERENCE PAPER; ENERGY METABOLISM; GENE EXPRESSION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RNA SYNTHESIS; SNAKE; TURTLE;

EID: 0029917973     PISSN: 03050491     EISSN: None     Source Type: Journal    
DOI: 10.1016/0305-0491(95)02043-8     Document Type: Conference Paper

References (92)

1. +-ATPase inhibits the activity of the enzyme. Proc. Natl. Acad. Sci. USA 88:11359-11362;1991.
2. Bickler, P. E. Cerebral anoxia tolerance in turtles: regulation of intracellular calcium and pH. Am. J. Physiol. 263:R1298-R1302;1992.
3. Bickler, P. E.; Gallego, S. M. Inhibition of brain calcium channels by plasma proteins from anoxic turtles. Am. J. Physiol. 265:R277-R281;1993.
4. Brooks, S. P. J.; Storey, K. B. Anoxic brain function: molecular mechanisms of metabolic depression. FEBS Lett. 232:214-216; 1988a.
5. Brooks, S. P. J.; Storey, K. B. Reevaluation of the "glycolytic complex" in muscle: a multitechnique approach using trout white muscle. Arch. Biochem. Biophys. 267:13-22;1988b.
6. Brooks, S. P. J.; Storey, K. B. Subcellular enzyme binding in glycolytic control: in vivo studies with fish muscle. Am. J. Physiol. 255:R289-R294;1988c.
7. Brooks, S. P. J.; Storey, K. B. Phosphofructokinase from a vertebrate facultative anaerobe: effects of temperature and anoxia on the kinetic parameters of the purified enzyme from turtle white muscle. Biochim. Biophys. Acta 1037:161-164;1989a.
8. Brooks, S. P. J.; Storey, K. B. Regulation of glycolytic enzymes during anoxia in the turtle Pseudemys scripta Am. J. Physiol. 257:R278-R283;1989b.
9. Brooks, S. P. J.; Storey, K. B. De novo protein synthesis and protein phosphorylation during anoxia and recovery in the red-eared turtle. Am. J. Physiol. 265:R1380-R1386;1993a.
10. Brooks, S. P. J.; Storey, K. B. Protein kinase C in turtle brain: changes in enzyme activity during anoxia. J. Comp. Physiol. B 163:84-88;1993b.
11. Brooks, S. P. J.; Storey, K. B. Control of metabolic rate by multienzyme complexes: is glycolysis in hypoxia and anoxia regulated by complex formation? In Surviving Hypoxia: Mechanisms of Control and Adaptation (Edited by Hochachka, P. W.; Lutz, P. L.; Sick, T. J.; Rosenthal, M.; van den Thillart, G.), 1993c: pp. 281-293. CRC Press, Boca Raton.
12. Buzadzic, B.; Spasic, M. B.; Saicic, Z. S.; Radojtcic, R.; Petrovic, V. M.; Halliwell, B. Antioxidant defenses in the ground squirrel Citellus citellus. 2. The effect of hibernation. Free Rad. Biol. Med. 9:407-413;1990a.
13. Buzadzic, B.; Spasic, M. B.; Saicic, Z. S.; Radojicic, R.; Halliwell, B.; Petrovic, V. M. Antioxidant defenses in the ground squirrel Citellus citellus. 1. A comparison with the rat. Free Rad. Biol. Med. 9:401-406;1990b.
14. Caraceni, P.; Rosenblum, E. R.; van Theil, D. H.; Borle, A. B. Reoxygenation injury in isolated rat hepatocytes: relation to oxygen free radicals and lipid peroxidation. Am. J. Physiol. 266: G799-G806;1994.
15. Catterall, W. A. The molecular basis of neuronal excitability. Science 223:653-661;1984.
16. Chih, C. P.; Rosenthal, M.; Sick, T. J. Ion leakage is reduced during anoxia in turtle brain: a potential survival strategy. Am. J. Physiol. 257:R1562-R1564;1989.
17. Clarke, F. M.; Shaw, F. D.; Morton, D. J. Effect of electrical stimulation post-mortem of bovine muscle on the binding of glycolytic enzymes. Biochem. J. 186:105-109;1980.
18. Clarke, F. M.; Stephan, P.; Huxham, G.; Hamilton, D.; Morton, D. J. Metabolic dependence of glycolytic enzyme binding in rat and sheep heart. Eur. J. Biochem. 138:643-649;1984.
19. Dawson, T. L.; Gores, G. J.; Nieminen, A-L.; Herman, B.; Lemasters, J. J. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am. J. Physiol. 264: C961-C967;1993.
20. Domanska-Janik, K.; Zalewska, T. Effect of brain ischemia on protein kinase C. J. Neurochem. 58:1432-1439;1992.
21. Douglas, D. N.; Giband, M.; Altosaar, I.; Storey, K. B. Anoxia induces changes in translatable mRNA populations in turtle organs: a possible adaptive strategy for anaerobiosis. J. Comp. Physiol. B. 164:405-414;1994.
22. Duncan, J. A. Glycolytic enzyme binding and metabolic control. M.Sc. thesis, Carleton University, 1988.
23. Duncan, J. A.; Storey, K. B. Role of enzyme binding in muscle metabolism of the goldfish. Can. J. Zool. 69:1571-1576;1991.
24. Duncan, J. A.; Storey, K. B. Subcellular enzyme binding and the regulation of glycolysis in anoxic turtle brain. Am. J. Physiol. 262:R517-R523;1992.
25. Edwards, R. A.; Lutz, P. L.; Baden, D. G. Relationship between energy expenditure and ion channel density in turtle and rat brain. Am. J. Physiol. 257:R1354-R1358;1989.
26. Frank, L.; Sosenko, I. R. S. Prenatal development of lung antioxidant enzymes in four species. J. Pediatr. 110:106-110;1987.
27. Gething, M. J.; Sambrook, J. Protein folding in the cell. Nature 355:33-45;1992.
28. Gutteridge, J. M. C.; Halliwell, B. Reoxygenation injury and antioxidant protection: a tale of two paradoxes. Arch. Biochem. Biophys. 283:223-226;1990.
29. Halliwell, B.; Gutteridge, J. M. C. Free Radicals in Biology and Medicine. Clarendon Press, Oxford, 1985.
30. Herbert, C. V.; Jackson, D. C. Temperature effects on the response to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes, and cardiovascular function in aerated and anoxic water. Physiol. Zool. 58:670-681;1985.
31. Hermes-Lima, M.; Storey, K. B. Anti-oxidant defenses in the tolerance of freezing and anoxia by garter snakes. Am. J. Physiol. 265:R646-R652;1993.
32. Hochachka, P. W.; Somero, G. N. Biochemical Adaptation. Princeton University Press, Princeton, New Jersey, 1984.
33. Hochachka, P. W.; Lutz, P. L.; Sick, T.; Rosenthal, M.; van den Thillart, G. Surviving Hypoxia.: Mechanisms of Control and Adaptation. CRC Press, Boca Raton, 1993.
34. 2+-activated and phospholipid-dependent protein kinase. Proc. Natl. Acad. Sci. USA 83:8535-8539;1986.
35. Jeffrey, P. L.; Brown, D. H.; Brown, B. I. Studies of lysosomal α-glucosidase. I. Purification and properties of the rat liver enzyme. Biochemistry 9:1403-1415;1970.
36. Kaczmarek, L. K. The role of protein kinase C in the regulation of ion channels and neurotransmitter release. Trends Neurosci. 10:30-34;1987.
37. Keiver, K. M.; Weinberg, J.; Hochachka, P. W. The effect of anoxic submergence and recovery on circulating levels of catecholamines and corticosterone in the turtle, Chrysemys picta. Gen. Comp. Endocrinol. 85:308-315;1992.
38. Keiver, K. M.; Hochachka, P. W. Catecholamine stimulation of hepatic glycogenolysis during anoxia in the turtle, Chrysemys picta. Am. J. Physiol. 261:R1341-R1345;1991.
39. Keleti, T.; Ovadi, J. Control of metabolism by dynamic macromolecular interactions. Curr. Top. Cell. Regul. 29:1-33;1988.
40. Kelly, D. A.; Storey, K. B. Organ-specific control of glycolysis in the anoxic turtle. Am. J. Physiol. 255:R774-R779;1988.
41. Kikkawa, U.; Kishimoto, A.; Nishizuka, Y. The protein kinase C family: heterogeneity and its implications. Annu. Rev. Biochem. 58:31-44;1989.
42. Land, S. C.; Buck, L. T.; Hochachka, P. W. Response of protein synthesis to anoxia and recovery in anoxia-tolerant hepatocytes. Am. J. Physiol. 265:R41-R48;1993.
43. Land, S. C.; Hochachka, P. W. Protein turnover during metabolic arrest in turtle hepatocytes: role and energy dependence of proteolysis. Am. J. Physiol. 266:C1028-C1036;1994.
44. Lopez-Torres, M.; Perez-Campo, R.; Cadenas, S.; Rojas, C.; Barja, G. A comparative study of free radicals in vertebrates. II. Non-enzymatic antioxidants and oxidative stress. Comp. Biochem. Physiol. B 105:757-763;1993.
45. Lowery, M. S.; Roberts, S. J.; Somero, G. N. Effects of starvation on the activities and localization of glycolytic enzymes in the white muscle of the barred sand bass Paralabrax nebulifer. Physiol. Zool. 60:538-549;1987.
46. Lutz, P. L.; McMahon, P.; Rosenthal, M.; Sick, T. J. Relationships between aerobic and anaerobic energy production in turtle brain in situ. Am. J. Physiol. 247:R240-R247;1984.
47. Lutz, P. L.; Storey, K. B. Adaptations to variations in oxygen tension by vertebrates and invertebrates. In Handbook of Comparative Physiology, CRC Press, Boca Raton, in press; 1995.
48. + pump. Biochem. J. 248:807-813;1987.
49. Marais, R. M.; Parker, P. J. Purification and characterization of bovine protein kinase C isotypes α, β and γ. Eur. J. Biochem. 182:129-137;1989.
50. Masters, C. J. Interactions between soluble enzymes and subcellular structure. CRC Crit. Rev. Biochem. 11:105-143;1981.
51. Matthews, W.; Tanaka, K.; Driscoll, J.; Ichihara, A.; Goldberg, A. L. Involvement of the proteasome in various degradative processes in mammalian cells. Proc. Natl. Acad. Sci. USA 86:2597-2601;1989.
52. McGuire, M. J.; DeMartino, G. N. The latent form of macropain (high molecular weight multicatalytic protease) restores ATP-dependent proteolysis in soluble extracts of BHK fibroblasts pretreated with anti-macropain antibodies. Biochem. Biophys. Res. Commun. 160:911-916;1989.
53. Mehrani, H.; Storey, K. B. Characterization of α-glucosidases from rainbow trout liver. Arch. Biochem. Biophys. 306;188-194;1993.
54. Mehrani, H.; Storey, K. B. Anoxia survival and the control of glycogenolysis in organs of the freshwater turtle Trachemys scripta. Int. J. Biochem. Cell Biol. 27:821-830;1995a.
55. Mehrani, H.; Storey, K. B. cAMP-Dependent protein kinase and anoxia survival in turtles: purification and properties of liver PKA. Mol. Cell. Biochem. 145:81-88;1995b.
56. Mehrani, H.; Storey, K. B. Effects of anoxia on protein phosphatase in turtle organs: purification and properties of protein phosphatase type-1 from turtle liver. Arch. Biochem. Biophys. 316:836-843; 1995c.
57. Murat, J. C. Studies on glycogenolysis in carp liver: Evidence for an amylase pathway for glycogen breakdown. Comp. Biochem. Physiol. B 55:461-466;1976.
58. Nishizuka, Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661-665;1989.
59. Numann, R.; Catterall, W. A.; Scheuer, T. Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science 254:115-118;1991.
60. Okuno, S.; Fujisawa, H. Stabilization, purification and crystallization of catalytic subunit of cAMP-dependent protein kinase from bovine heart. Biochem. Biophys. Acta 1038:204-208;1990.
61. Orlowski, M. The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry 29:10289-10297;1990.
62. Pacifici, R. E.; Davies, K. J. A. A 700-kDa red cell proteinase which selectively oxidatively denatured hemoglobin. FASEB J. 2: A1007;1988.
63. Pereira, M. E.; Wilk, S. Phosphorylation of the multicatalytic proteinase complex from bovine pituitaries by a copurifying cAMP-dependent protein kinase. Arch. Biochem. Biophys. 283:68-74;1990.
64. Picukans, I.; Umminger, B. L. Comparative activities of glycogen phosphorylase and α-amylase in livers of carp (Cyprinus carpio) and goldfish (Carassius auratus). Comp. Biochem. Physiol. B 62: 455-457;1979.
65. Plaxton, W. C.; Storey, K. B. Glycolytic enzyme binding and metabolic control in anaerobiosis. J. Comp. Physiol. B 156:635-640;1986.
66. Rahman, M. S.; Storey, K. B. Role of covalent modification in the control of glycolytic enzymes in response to environmental anoxia in goldfish. J. Comp. Physiol. B 157:813-820;1988.
67. Reischl, E. High sulfhydryl content in turtle erythrocytes: is there a relation with resistance to hypoxia? Comp. Biochem. Physiol. B 85:723-726;1986.
68. Reuter, H. Modulation of ion channels by phosphorylation and second messengers. News Physiol. Sci. 2:168-171;1987.
69. Rivett, A. J. Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase. J. Biol. Chem. 260: 12600-12606;1985.
70. Rivett, A. J. The multicatalytic proteinase. Multiple proteolytic activities. J. Biol. Chem. 264:12215-12219;1989.
71. Rivett, A. J. Proteasomes: multicatalytic proteinase complexes. Biochem. J. 291:1-10;1993.
72. Rundell, K. W.; Tullson, P. C.; Terjung, R. L. AMP-deaminase binding in rat skeletal muscle after high-intensity running. J. Appl. Physiol. 74:2004-2006;1993.
73. Schlesinger, M. J.; Ashburner, M.; Tissieres, A. Heat Shock from Bacteria to Man. Cold Spring Harbor Laboratory Press, New York, 1982.
74. Sies, H. Strategies of antioxidant defense. Eur. J. Biochem. 215: 213-219;1993.
75. Srere, P. A. Complexes of sequential metabolic enzymes. Annu. Rev. Biochem. 56:89-124;1987.
76. Storey, K. B. Tissue specific controls on carbohydrate catabolism during anoxia in goldfish. Physiol. Zool. 60:601-607;1987.
77. Storey, K. B. Molecular mechanisms of metabolic arrest in mollusks. In Surviving Hypoxia: Mechanisms of Control and Adaptation (Edited by Hochachka, P. W.; Lutz, P. L.; Sick, T. J.; Rosenthal, M.; van den Thillart, G.), 1993: pp. 253-269. CRC Press, Boca Raton.
78. Storey, K. B.; Storey, J. M. Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation, and estivation. Quart. Rev. Biol. 65;145-174;1990.
79. Storey, K. B.; Storey, J. M. Cellular adaptations for freezing survival by amphibians and reptiles. In Advances in Low Temperature Biology (Edited by P. L. Steponkus), Vol. 2, 1993: pp. 101-129. JAI Press, London.
80. Subjeck, J. R.; Shyy, T. T. Stress protein systems of mammalian cells. Am. J. Physiol. 250:C1-C17;1986.
81. Tanaka, K.; Yoshimura, T.; Kumatori, A.; Ichihara, A.; Ikai, A.; Nishigai, M.; Kamenyama, K.; Takagi, T. Proteosomes (multiprotease complexes) as 20 S ring-shaped particles in a variety of eukaryotic cells. J. Biol. Chem. 263:16209-16217;1988.
82. Traystman, R. J.; Kirsch, J. R.; Koehler, R. C. Oxygen radical mechanisms of brain injury following ischemia and reperfusion. J. Appl. Physiol. 71:1185-1195;1991.
83. Velazquez, J. M.; Lindquist, S. Hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36:655-662;1984.
84. Vig, E.; Nemcsok, J. The effects of hypoxia and paraquat on the superoxide dismutase activity in different organs of carp, Cyprinus carpio L. J. Fish Biol. 35:23-25;1989.
85. Wasser, J. S.; Jackson, D. C. Effects of anoxia and graded acidosis on the levels of circulating catecholamines in turtles. Resp. Physiol. 84;363-377;1991.
86. + channel by protein kinases A and C. Proc. Natl. Acad. Sci. USA 88:9722-9725;1991.
87. Welch, W. J. Mammalian stress response: cell physiology and biochemistry of stress proteins. In The Role of the Stress Response in Biology and Disease (Edited by Morimoto, R.; Tissieres, A.), 1990: pp. 223-278. Cold Spring Harbor Laboratory Press, New York.
88. Wilk, S.; Orlowski, M. Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex. J. Neurochem. 40:842-849;1983.
89. Willmore, W. G.; Storey, K. B. Multicatalytic proteinase activity in turtle liver: responses to physiological anoxia stress and recovery. Biochem. Mol. Biol. Intl. (in press);1966a.
90. Willmore, W. G.; Storey, K. B. Antioxidant systems and anoxia tolerance in the freshwater turtle Trachemys scripta elegans. J. Comp. Physiol. B. submitted; 1996b.
91. Willmore, W. G.; Storey, K. B. Glutathione function and anoxia tolerance in the freshwater turtle Trachemys scripta elegans. J. Comp. Physiol. B. submitted. 1996c.
92. Zetterqvist, O.; Ragnarsson, U.; Engstrom, L. Substrate specificity of cyclic AMP-dependent protein kinase. In Peptide and Protein Phosphorylation (Edited by Kemp, B. E.), 1990: pp. 171-187. CRC Press, Boca Raton.