Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes

Journal of Experimental Biology

Volumn 206, Issue 2, 2003, Pages 411-421

  O'Brien, K M ^a,b   Skilbeck, C ^c   Sidell, B D ^a   Egginton, S ^c  

^a UNIVERSITY OF MAINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c NONE

Author keywords

Antarctic icefish; Capillary supply; Haemoglobin; Lipid; Metabolic enzyme; Mitochondria; Muscle

Indexed keywords

HEMOGLOBIN; OXYGEN;

AEROBIC METABOLISM; ANIMAL; ANTARCTICA; ARTICLE; CAPILLARY; ELECTRON MICROSCOPY; FISH; HISTOLOGY; METABOLISM; MUSCLE CELL; MUSCLE MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SKELETAL MUSCLE; SWIMMING; ULTRASTRUCTURE; VASCULARIZATION;

AEROBIOSIS; ANIMALS; ANTARCTIC REGIONS; CAPILLARIES; FISHES; HEMOGLOBINS; MICROSCOPY, ELECTRON; MITOCHONDRIA, MUSCLE; MUSCLE FIBERS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN; SWIMMING;

ANIMALIA; CHAENOCEPHALUS ACERATUS; CHANNICHTHYIDAE; CHIONODRACO RASTROSPINOSUS; GOBIONOTOTHEN GIBBERIFRONS; NOTOTHENIA CORIICEPS; NOTOTHENIIDAE; PISCES; SALANGINI;

EID: 0347298748     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00088     Document Type: Article

References (64)

1. Archer, S. D. and Johnston, I. A. (1989). Kinematics of labriform and subcarangiform swimming in the Antarctic fish Notothenia neglecta. J. Exp. Biol. 143, 195-210.
2. Archer, S. D. and Johnston, I. A. (1991). Density of cristae and distribution of mitochondria in the slow muscle fibers of Antarctic fish. Physiol. Zool. 64, 242-258.
3. Bakeeva, L. E., Chentsov, Y. S. and Skulachev, V. P. (1978). Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochim. Biophys. Acta 501, 349-369.
4. Battino, R., Evans, F. D. and Danforth, W. F. (1968). The solubilities of seven gases in olive oil with reference to theories of transport through the cell membrane. J. Am. Oil Chem. Soc. 45, 830-833.
5. Beenakkers, A. T., Dewaide, J. E., Henderson, P. T. and Lutgerhorst, A. (1967). Fatty acid oxidation and some participating enzymes in animal organs. Comp. Biochem. Physiol. 22, 675-682.
6. Blake, R. W. (1979). The mechanics of labriform locomotion. J. Exp. Biol. 82, 255-271.
7. Crabtree, B. and Newsholme, E. A. (1972a). The activities of phosphorylase, hexokinase, phosphofructokinase, lactate dehydrogenase and glycerol 3-phosphate dehydrogenases in muscles from vertebrates and invertebrates. Biochem. J. 126, 49-58.
8. Crabtree, B. and Newsholme, E. A. (1972b). The activities of lipases and carnitine palmitoyltransferase in muscles from vertebrates and invertebrates. Biochem. J. 130, 697-705.
9. Crockett, E. L. and Sidell, B. D. (1990). Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol. Zool. 63, 472-488.
10. Cruz-Orive, L. M. and Weibel, E. R. (1981). Sampling designs for stereology. J. Microsc. 122, 235-257.
11. Desaulniers, N., Moerland, T. S. and Sidell, B. D. (1996). High lipid content enhances therate of oxygen diffusion through fish skeletal muscle. Am. J. Physiol. 271, R42-R47.
12. Dunn, J. F., Archer, S. D. and Johnston, I. A. (1989). Muscle fibre types and metabolism in post-larval and adult stages of notothenioid fish. Polar Biol. 9, 213-223.
13. Eastman, J. T. (1993). Antarctic Fish Biology: Evolution in a Unique Environment. San Diego: Academic Press.
14. Egginton, S. (1990). Morphometric analysis of tissue capillary supply. In Vertebrate Gas Exchange from Environment to Cell. Advances in Comparative and Environmental Physiology, vol. 6 (ed. R. G. Boutilier), pp. 73-141. Berlin: Springer Verlag.
15. Egginton, S. (1994). Stress response in two Antarctic teleosts (Chaenocephalus aceratus Lönnberg and Notothenia coriiceps Richardson) following capture and surgery. J. Comp. Physiol. B 164, 482-491.
16. Egginton, S. and Cordiner, S. (1994). Effect of fixation protocols on muscle preservation and in situ diffusion distances. J. Fish Biol. 47, 59-69.
17. Egginton, S. and Johnston, I. A. (1984). Effects of acclimatization temperature on routine metabolism muscle mitochondrial volume density and capillary supply in the elver (Anguilla anguilla). J. Therm. Biol. 9, 165-170.
18. Egginton, S. and Rankin, J. C. (1998).Vascular adaptations for a low pressure / high flow brood supply to locomotory muscles of icefish. In Antarctic Fishes: A Biological Overview (ed. G. DiPrisco, A. Clarke and E. Pisano), pp. 185-195. Berlin: Springer Verlag.
19. Egginton, S. and Sidell, B. D. (1989). Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. 256, R1-R9.
20. Egginton, S., Cordiner, S. and Skilbeck, C. (2000). Thermal compensation of peripheral oxygen transport in skeletal muscle of seasonally acclimatized trout. Am. J. Physiol. 279, 375-388.
21. Egginton, S., Ross, H. F. and Sidell, B. D. (1988). Morphometric analysis of intracellular diffusion distances. Acta Stereologica 6, 449-454.
22. Ellsworth, M. L. and Pittman, R. N. (1984). Heterogeneity of oxygen diffusion through hamster striated muscles. Am. J. Physiol. 246, H161-H167.
23. Fitch, N. A., Johnston, I. A. and Wood, R. E. (1984). Skeletal muscle capillary supply in a fish that lacks respiratory pigments. Resp. Physiol. 57, 201-211.
24. Hansen, C. A. and Sidell, B. D. (1983). Atlantic hagfish cardiac muscle: metabolic basis of tolerance to anoxia. Am. J. Physiol. 244, R356-R362.
25. Hochachka, P. W. (1986). Defense strategies against hypoxia and hypothermia. Science 231, 234-241.
26. Hochachka, P. W., Buck, L. T., Doll, C. J. and Land, S. C. (1996). Unifying theory of hypoxia tolerance: molecular/ metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. USA 93, 9493-9498.
27. Holeton, G. (1970). Oxygen uptake and circulation by a haemoglobinless Antarctic fish (Chaenocephalus aceratus Lönnberg) compared with three red-blooded Antarctic fish. Comp. Biochem. Physiol. 34, 457-471.
28. Hoofd, L. and Egginton, S. (1997). The possible role of intracellular lipid in oxygen delivery to fish skeletal muscle. Respir. Physiol. 107, 191-202.
29. Hoppeler, H. and Billeter, R. (1991). Conditions for oxygen and substrate transport in muscles in exercising mammals. J. Exp. Biol. 160, 263-283.
30. Hoppeler, H. and Lindstedt, S. L. (1985). Malleability of skeletal muscle in overcoming limitations: structural elements. J. Exp. Biol. 115, 355-364.
31. Hoppeler, H., Mathieu, O., Weibel, E. R. Krauer, R., Lindstedt, S. L. and Taylor, C. R. (1981a). Design of the mammalian respiratory system. VIII. Capillaries in skeletal muscles. Resp. Physiol. 44, 129-150.
32. Hoppeler, H., Mathieu, O., Krauer, R., Claasen, H., Armstrong, R. B. and Weibel, E. R. (1981b). Design of the mammalian respiratory system. IV. Distribution of mitochondria and capillaries in various muscles. Resp. Physiol. 44, 87-111.
33. Jobling, M. (1994). Fish Bioenergetics. London: Chapman and Hall.
34. Johnston, I. A. (1989). Antarctic fish muscles - structure and function and physiology. Ant. Sci. 1, 97-108.
35. Johnston, I. A. and Harrison, P. (1985). Contractile and metabolic characteristics of muscle fibres from Antarctic fish. J. Exp. Biol. 116, 223-236.
36. Johnston, I. A., Calvo, J., Guderley, H., Fernandez, D. and Palmer, L. (1998). Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J. Exp. Biol. 201, 1-12.
37. Kayar, S. R., Hoppeler, H., Mermod, L. and Weibel, E. R. (1988). Mitochondrial size and shape in equine skeletal muscle: a three-dimensional reconstruction study. Anat. Rec. 222, 333-339.
38. Koyama, T., Zhu, M. Y., Araiso, T., Kinjo, M., Kitagawa, H. and Sugimura, M. (1990). Dynamic microstructure of plasma and mitochondrial membranes from bullfrog myocardium- a nanosecond time-resolved fluorometric study. Jap. J. Physiol. 40, 65-78.
39. Lindsey, C. C. (1978). Form, function, and locomotory habits in fish. In Fish Physiology, vol. VII (ed. W. S. Hoar and D. J. Randall), pp. 1-88. New York: Academic Press.
40. Londraville, R. L. and Sidell, B. D. (1990a). Ultrastructure of aerobic muscle in Antarcticfishes may contribute to maintenance of diffusive fluxes. J. Exp. Biol. 150, 205-220.
41. Londraville, R. L. and Sidell, B. D. (1990b). Maximal diffusion-distance within skeletal muscle can be estimated from mitochondrial distributions. Resp. Physiol. 81, 291-302.
42. Longmuir, I. S. (1980). Channels of oxygen transport from blood to mitochondria. Adv. Physiol. Sci. 25, 19-22.
43. Mathieu-Costello, O., Suarez, R. K. and Hochachka, P. W. (1992). Capillary-to-fiber geometry and mitochondria density in hummingbird flight muscle. Resp. Physiol. 89, 113-132.
44. Montgomery, J. C. and Macdonald, J. A. (1984). Performance of motor systems in Antarctic fishes. J. Comp. Physiol. 154, 241-248.
45. Moylan, T. J. and Sidell, B. D. (2000). Concentrations of myoglobin and myoglobin mRNA in heart ventricles from Antarctic fishes. J. Exp. Biol. 203, 1277-1286.
46. O'Brien, K. M. and Sidell, B. D. (2000). The interplay among cardiac ultrastructure, metabolism and the expression of oxygen-binding proteins in Antarctic fishes. J. Exp. Biol. 203, 1287-1297.
47. Opie, L. H. and Newsholme, E. A. (1967). The activities of fructose 1,6-diphosphate, phosphofructokinase and phosphoenol pyruvate carboxykinase in white muscle and red muscle. Biochem. J. 103, 391-399.
48. Read, G., Crabtree, B. and Smith, G. H. (1977). The activities of 2-oxoglutarate dehydrogenase and pyruvate dehydrogenase in hearts and mammary glands from ruminants and non-ruminants. Biochem. J. 164, 349-355.
49. Rodnick, K. J. and Sidell, B. D. (1994). Cold acclimation increases carnitine palmitoyltransferase I activity in oxidative muscle of striped bass. Am. J. Physiol. 166, R405-R412.
50. Rodnick, K. J. and Sidell, B. D. (1997). Structural and biochemical analyses of cardiac ventricular enlargement in cold-acclimated striped bass. Am. J. Physiol. 42, R252-R258.
51. Ruud, J. T. (1954). Vertebrates without erythrocytes and blood pigment. Nature 173, 848-850.
52. Sänger, A. M. (1999). Morphometric analysis of axial muscle in cyprinid fish provides support that intracellular lipid plays a role in slow fibre oxygen supply. J. Fish Biol. 54, 1029-1037.
53. Schwerzmann, K., Hoppeler, H., Kayar, S. R. and Weibel, E. R. (1989). Oxidative capacity of muscle and mitochondria: correlation of physiological, biochemical, and morphometric characteristics. Proc. Natl. Acad. Sci. USA 86, 1583-1587.
54. Sidell, B. D. (1998). Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J. Exp. Biol. 201, 1118-1127.
55. Smith, P. K., Krohn, R. I., Hermanson, G. T., Malia, A. K., Gartner, M. D., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olsen, B. J. and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
56. Srere, P. A., Brazil, A. and Gonen, L. (1963). The citrate condensing enzyme of pigeon breast muscle and moth flight muscle. Acta Chem. Scand. 17, S219-S234.
57. Tyler, S. and Sidell, B. D. (1984). Changes in mitochondrial distribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperatures. J. Exp. Zool. 232, 1-9.
58. Walesby, N. J. and Johnston, I. A. (1980). Fibre types in the locomotory muscles of an Antarctic teleost, Notothenia rossii. Cell Tiss. Res. 208, 143-164.
59. Webb, P. W. (1990). How does benthic living affect body volume, tissue composition, and density of fishes? Can. J. Zool. 68, 1250-1255.
60. Weibel, E. R. (1979). Stereological Methods, vol 1. New York: Academic Press.
61. Weibel, E. R. (1984). The Pathway for Oxygen. Cambridge: Harvard University Press.
62. Wharton, D. C. and Tzagoloff, A. (1967). Cytochrome oxidase from beef heart mitochondria. Meth. Enzym. 10, 245-260.
63. Wittenberg, B. A. and Wittenberg, J. B. (1989). Transport of oxygen in muscle. Ann. Rev. Physiol. 51, 857-878.
64. Zammit, V. A. and Newsholme, E. A. (1976). The maximum activities of hexokinase, phosphorylase, phosphofructokinase, glycerol phosphate dehydrogenases, lactate dehydrogenase, octopine dehydrogenase, phosphoenolpyruvate, carboxykinase, nucleoside diphosphate kinase, glutamate-oxaloacetate transaminase and arginine kinase in relation to carbohydrate utilization in muscles from marine invertebrates. Biochem. J. 160, 447-462.