Myoglobin function reassessed

Journal of Experimental Biology

Volumn 206, Issue 12, 2003, Pages 2011-2020

  Wittenberg, Jonathan B ^a   Wittenberg, Beatrice A ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cytochrome oxidase; Dimensionality in diffusion; Facilitated diffusion; Heart; Krogh cylinder; Mitochondria; Myoglobin; Nitric oxide; Oxygen; Red skeletal muscle

Indexed keywords

CYTOCHROME C OXIDASE; MYOGLOBIN; OXYGEN;

ANIMAL; DIFFUSION; HEART; METABOLISM; PHYSIOLOGY; REVIEW; SARCOLEMMA; SKELETAL MUSCLE;

ANIMALS; DIFFUSION; ELECTRON TRANSPORT COMPLEX IV; HEART; MUSCLE, SKELETAL; MYOGLOBIN; OXYGEN; SARCOLEMMA;

ANIMALIA;

EID: 0037933181     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00243     Document Type: Review

References (97)

1. Acierno, R., Agnisola, C., Tota, B. and Sidell, B. D. (1997). Myoglobin enhances cardiac performance in Antarctic fish species that express the protein. Am. J. Physiol. 273, R100-R106.
2. Adam, G. and Delbruck, M. (1968). Reduction of dimensionality in biological diffusion processes. In Structural Chemistry and Molecular Biology (ed. A. Rich and N. Davidson), pp. 198-215. San Francisco, London: W. H. Freeman & Co.
3. Appleby, C. A. (1969). Properties of leghemoglobin in vivo, and its isolation as ferrous oxyhemoglobin. Biochim. Biophys. Acta 188, 222-229.
4. Appleby, C. A. (1984). Leghemoglobin and rhizobium respiration. Annu. Rev. Plant Physiol. 35, 443-478.
5. Baylor, S. M. and Pape, P. C. (1988). Measurement of myoglobin diffusivity in the myoplasm of frog skeletal muscle fibers. J. Physiol. Soc. 406, 247-275.
6. Berg, H. C. (1983). Random Walks in Biology. Princeton, Guildford: Princeton University Press.
7. Bergersen, F. J., Turner, G. L. and Appleby, C. A. (1973). Studies on the physiological role of leghemoglobin in soybean root nodules. Biochim. Biophys. Acta 292, 271-282.
8. Block, B. A. and Franzini-Armstrong, C. (1988). The structure of the membrane systems in a novel muscle cell modified for heat production. J. Cell Biol. 107, 1099-1119.
9. Boushel, R. and Piantadosi, C. A. (2000). Near-infrared spectroscopy for monitoring muscle oxygenation. Acta Physiol. Scand. 168, 615-622.
10. Brunori, M. (2001a). Nitric oxide, cytochrome-c oxidase and myoglobin. Trends Biochem. Sci. 26, 21-23.
11. Brunori, M. (2001b). Nitric oxide moves myoglobin centre stage. Trends Biochem. Sci. 26, 209-210.
12. Cashon, R. E., Vayda, M. E. and Sidell, B. D. (1997). Kinetic characterization of myoglobins from vertebrates with vastly different body temperatures. Comp. Biochem. Physiol. B 117, 613-620.
13. Chance, B. (1965). Reaction of oxygen with the respiratory chain in cells and tissues. J. Gen. Physiol. 49, 163-188.
14. Chance, B., Saronio, C. and Leigh, J. S. (1975). Functional intermediates in the reaction of membrane-bound cytochrome oxidase with oxygen. J. Biol. Chem. 250, 9226-9237.
15. Clark, A., Clark, P. A. A., Connett, R. J., Gayeski, T. E. J. and Honig, C. R. (1987). How large is the drop in PO2 between cytosol and mitochondrion. Am. J. Physiol. 252, C583-C587.
16. Cole, R. P., Sukanek, P. C., Wittenberg, J. B. and Wittenberg, B. A. (1982). Mitochondrial function in the presence of myoglobin. J. Appl. Physiol. 53, 1116-1124.
17. Duhaylongsod, F. G., Griebel, J. A., Bacon, D. S., Wolfe, W. G. and Piantadosi, C. A. (1993). Effects of muscle contraction on cytochrome a, a3 redox state. J. Appl. Physiol. 75, 790-797.
18. 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.
19. Fabel, H. and Lubbers, D. W. (1965). Measurements of reflectance spectra of the beating rabbit heart in situ. Biochem. Z. 341, 351-356.
20. Fawcett, D. W. (1966). An Atlas of Fine Structure. Philadelphia: W. B. Saunders.
21. Fawcett, D. W. and McNutt, N. S. (1969). The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42, 1-45.
22. Flogel, U., Merx, M. W., Godecke, A., Decking, U. K. M. and Schrader, J. (2001). Myoglobin: a scavenger of bioactive NO. Proc. Natl. Acad. Sci. USA 98, 735-740.
23. Garry, D. J., Ordway, G. A., Lorenz, J. N., Radford, N. B., Chin, E. R., Grange, R. W., Bassel-Duby, R. and Williams, R. S. (1998). Mice without myoglobin. Nature 395, 905-908.
24. Gayeski, T. E. J., Connett, R. J. and Honig, C. (1987). Minimum intracellular PO2 for maximum cytochrome turnover in red muscle in situ. Am. J. Physiol. 252, H906-H915.
25. 2 gradients from sarcolemma to cell interior in red muscle at maximal VO2. Am. J. Physiol. 251, H789-H799.
26. Gayeski, T. E. J. and Honig, C. R. (1988). Intracellular oxygen pressure in the long axis of individual fibers in working gracilis muscle. Am. J. Physiol. 254, H1179-H1186.
27. Gayeski, T. E. J. and Honig, C. R. (1991). Intracellular PO2 in individual cardiac myocytes in dogs, cats, rabbits, ferrets and rats. Am. J. Physiol. 260, H522-H531.
28. Giardina, B., Ascenzi, P., Clementi, M. E., De Sanctis, G., Rizzi, M. and Coletta, M. (1996). Functional modulation by lactate of myoglobin. J. Biol. Chem. 271, 16999-17001.
29. Gibson, Q. H., Wittenberg, J. B., Wittenberg, B. A., Bogusz, D. and Appleby, C. A. (1989). The kinetics of ligand binding to plant hemoglobin: structural implications. J. Biol. Chem. 264, 100-107.
30. Godecke, A., Flogel, U., Zhanger, K., Ding, Z., Hirchenhain, J., Decking, U. K. M. and Schrader, J. (1999). Disruption of myoglobin in mice induces multiple compensatory mechanisms. Proc. Natl. Acad. Sci. USA 96, 10495-10500.
31. Grange, R. W., Meeson, A., Chin, E., Lau, K. S., Stull, J. T., Shelton, J. M., Williams, R. S. and Garry, D. J. (2001). Functional and molecular adaptations in skeletal muscle of myoglobin-mutant mice. Am. J. Physiol. Cell Physiol. 281, C1487-C1494.
32. 2 supply to red muscle. Validity of assumptions, sensitivity to errors in data. Biophys. J. 68, 1246-1269.
33. Hassinen, I. E., Hiltunen, J. K. and Takala, T. E. S. (1981). Reflectance spectrophotometric monitoring of the isolated perfused heart as a method of measuring the oxidation-reduction state of cytochromes and oxygenation of myoglobin. Cardiovasc. Res. 15, 86-91.
34. Hill, A. V. (1928). The diffusion of oxygen and lactic acid through tissues. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 104, 39-96.
35. 2 transport and its interaction with metabolism; a systems view of aerobic capacity. Med. Sci. Sports Exerc. 24, 47-53.
36. Honig, C. R., Gayeski, T. E. J., Federspiel, W., Clark, A. and Clark, P. (1984). Muscle oxygen gradients from hemoglobin to cytochrome: new concepts; new complexities. Adv. Exp. Med. Biol. 169, 23-38.
37. Jelicks, L. A. and Wittenberg, B. A. (1995). 1H nuclear magnetic resonance studies of sarcoplasmic oxygenation in the red cell-perfused rat heart. Biophys. J. 68, 2129-2136.
38. Jobsis, F. F. and Stainsby, W. N. (1968). Oxidation of NADH during contractions of circulated mammalian skeletal muscle. Resp. Physiol. 4, 292-300.
39. Jurgens, K. D., Papadopoulos, S., Peters, T. and Gros, G. (2000). Myoglobin: just an oxygen store or also an oxygen transporter? News Physiol. Sci. 15, 269-274.
40. Jurgens, K. D., Peters, T. and Gros, G. (1994). Diffusivity of myoglobin in intact skeletal muscle cells. Proc. Natl. Acad. Sci. USA 91, 3829-3833.
41. Kanai, A. J., Pearce, L. L., Clemens, P. R., Birder, L. A., VanBibber, M. M., Choi, S.-Y., de Groat, W. C. and Peterson, J. (2001). Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc. Natl. Acad. Sci. USA 98, 14126-14131.
42. Katz, I. R., Wittenberg, J. B. and Wittenberg, B. A. (1984). Monoamine oxidase an intracellular probe of oxygen pressure in isolated cardiac myocytes. J. Biol. Chem. 259, 7504-7509.
43. Kayar, S. R., Conley, K. E., Claassen, H. and Hoppeler, H. (1986). Capillarity and mitochondrial distribution in rat myocardium following exercise training. J. Exp. Biol. 120, 189-199.
44. Keener, J. and Sneyd, J. (1998). Mathematical Physiology. New York: Springer.
45. Klucas, R. V., Lee, K. K., Saari, L. and Erickson, B. K. (1985). Factors Effecting Functional Leghemoglobin in Legume Nodules. New York: Elsevier Science.
46. Kreuzer, F. (1970). Facilitated diffusion of oxygen and its possible significance; a review. Resp. Physiol. 10, 686-692.
47. Kreuzer, F. and Hoofd, L. J. C. (1970). Facilitated diffusion of oxygen in the presence of hemoglobin. Resp. Physiol. 10, 542-558.
48. Krogh, A. (1919a). The number and distribution of capillaries in muscle with calculations of the oxygen pressure head necessary for supplying the tissue. J. Physiol. 52, 409-415.
49. Krogh, A. (1919b). The supply of oxygen to the tissues and the regulation of capillary circulation. J. Physiol. 52, 457-474.
50. Landis, E. M. and Pappenheimer, J. R. (1963). Exchange of Substances Through the Capillary Walls. Bethesda, MD: American Physiological Society.
51. Lawrie, R. A. (1953). The activity of the cytochrome system in muscle and its relation to myoglobin. Biochem. J. 55, 298-305.
52. Loke, E. K., McConnell, P. I., Tuzman, J. M., Shesely, E. G., Smith, C. J., Stackpole, C. J., Thompson, C. I., Kaley, G., Wolin, M. S. and Hintze, T. H. (1999). Endogenous endothelial nitric oxide synthase-delivered nitric oxide is a physiological regulator of myocardial oxygen consumption. Circ. Res. 84, 840-845.
53. Marcinek, D. J., Bonaventura, J., Wittenberg, J. B. and Block, B. A. (2001). Oxygen affinity and amino acid sequence of myoglobins from endothermic and ectothermic fish. Am. J. Physiol. Reg. Integ. Comp. Physiol. 280, R1123-R1133.
54. Meeson, A. P. R. N., Shelton, J. M., Mammen, P. P. A., DiMaio, J. M., Hutcheson, K., Kong, Y., Elterman, J., Williams, R. S. and Garry, D. J. (2001). Adaptive mechanisms that preserve cardiac function in mice without myoglobin. Circ. Res. 88, 713-720.
55. Merx, M. W., Flogel, U., Stumpe, T., Godecke, A., Decking, U. K. M. and Schrader, J. (2001). Myoglobin facilitates oxygen diffusion. FASEB. J. 2001, 1077-1079.
56. Meyer, R. A., Sweeney, H. L. and Kushmerick, M. J. (1984). A simple analysis of the phosphocreatine shuttle. Am. J. Physiol. 246, C365-C377.
57. Millikan, G. A. (1937). Experiments on muscle haemoglobin in vivo; the instantaneous measurement of muscle metabolism. Proc. R. Soc. Lond Ser. B 123, 218-241.
58. Millikan, G. A. (1939). Muscle hemoglobin. Physiol. Rev. 19, 503-523.
59. Moncada, S. and Erusalimsky, J. D. (2002). Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell. Biol. 3, 214-220.
60. Murakami, Y., Zhang, Y., Yong, K. C., Mansoor, A. M., Chung, J. K., Chu, C., Francis, G., Ugurbil, K., Bache, R. J., From, A. H. L., Jerosch-Herold, M., Wilke, N. and Zhang, J. (1999). Myocardial oxygenation during high work states in hearts with post infarction remodeling. Circulation 99, 942-948.
61. Murray, J. D. (1971). On the molecular mechanism of facilitated oxygen diffusion by haemoglobin and myoglobin. Proc. R. Soc. Lond. B 178, 95-110.
62. Murray, J. D. (1977). Lectures on Nonlinear-Differential Equation Models in Biology. Oxford: Clarendon.
63. Papadopoulos, S., Endeward, V., Revesz-Walker, B., Jurgens, K. D. and Gros, G. (2001). Radial and longitudinal diffusion of myoglobin in single living heart and skeletal muscle cells. Proc. Natl. Acad. Sci. USA 98, 5904-5909.
64. Papadopoulos, S., Jurgens, K. D. and Gros, G. (2000). Protein diffusion in living skeletal muscle fibers: dependence on protein size, fiber type, and contraction. Biophys. J. 79, 2084-2094.
65. Papadopoulos, S., Jurgens, K. D. and Gros, G. (1995). Diffusion of Myoglobin in skeletal muscle cells: dependence on fibre type, contraction and temperature. Eur. J. Physiol. 430, 519-525.
66. Pearce, L. L., Kanai, A. J., Birder, L. A., Pitt, B. R. and Peterson, J. (2002). The catabolic fate of nitric oxide. The nitric oxide oxidase and peroxynitrite reductase ativities of cytochrome oxidase. J. Biol. Chem. 277, 13556-13562.
67. Pesce, A., Bolognesi, M., Bocedi, A., Ascenzi, P., Dewilde, S., Moens, L., Hankeln, T. and Burmester, T. (2002). Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep. 3, 1146-1151.
68. Richardson, R. S., Newcomer, S. C. and Noyszewski, E. A. (2001). Skeletal muscle intracellular PO2 assessed by myoglobin desaturation: response to graded exercise. J. Appl. Physiol. 91, 2679-2685.
69. Richmond, K. M., Shonat, R. D., Lynch, R. M. and Johnson, P. C. (1999). Critical PO2 of skeletal muscle in vivo. Am. J. Physiol. 277, H1831-H1840.
70. Riveros-Moreno, V. and Wittenberg, J. B. (1972). The self-diffusion coefficients of myoglobin and hemoglobin in concentrated solutions. J. Biol. Chem. 247, 895-901.
71. Rumsey, W. L., Schlosser, C., Nuutinen, E. M., Robiolo, M. and Wilson, D. F. (1990). Cellular energetics and the oxygen dependence of respiration in cardiac myocytes isolated from adult rat. J. Biol. Chem. 265, 15392-15399.
72. Schenkman, K. A., Marble, D. R., Burns, D. H. and Feigl, E. O. (1997). Myoglobin oxygen dissociation by multiwavelength spectroscopy. J. Appl. Physiol. 82, 86-92.
73. Schmidt, M., Geissl, A., Laufs, T., Hankeln, T., Wolfrum, U. and Burmester, T. (2002). How does the eye breathe? Evidence for neuroglobin-mediated oxygen supply to the mammalian retina. J. Biol. Chem. 278, 1932-1935.
74. Sidell, B. D. (1998). Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J. Exp. Biol. 201, 1118-1127.
75. Studer, P., Hennecke, H. and Muller, M. (1992). High pressure freezing of soybean nodules leads to an improved preservation of ultrastructure. Planta 188, 155-163.
76. 2 gradients in cardiomyocytes at low PO2. Am. J. Physiol. 283, H871-H878.
77. Takahashi, E. and Doi, K. (1998). Impact of diffusional transport on oxidative metabolism in the heart. Jap. J. Physiol. 48, 243-252.
78. 2 delivery in a single isolated cardiomyocyte. Biophys. J. 78, 3252-3259.
79. Takahashi, E., Sato, K., Endoh, H., Xu, Z.-L. and Doi, K. (1998). Direct observation of radial intracellular PO2 gradients in a single cardiomyocyte of the rat. Am. J. Physiol. 275, H225-H233.
80. Vanderkooi, J. M., Wright, W. W. and Erecinska, M. (1990). Oxygen gradients in mitochondria examined with delayed luminescence from excited state triplet probes. Biochemistry 29, 5332-5338.
81. Veldkamp, W. B. and Votano, J. R. (1976). Effects of intermolecular interaction on protein diffusion in solution. J. Phys. Chem. 80, 2794-2801.
82. Verkhovsky, M. I., Morgan, J. E., Puustinen, A. and Wikstrom, M. (1996). Kinetic trapping of oxygen in cell respiration. Nature 380, 268-270.
83. Voter, W. A. and Gayeski, T. E. J. (1995). Determination of myoglobin saturation of frozen specimens using a reflecting cryospectrophotometer. Ant. J. Physiol. 269, H1328-H1341.
84. Wang, D., Kreutzer, F., Chung, Y. and Jue, T. (1997). Myoglobin and hemoglobin rotational diffusion in the cell. Biophys. J. 73, 2764-2770.
85. White, R. L. and Wittenberg, B. A. (1993). NADH fluorescence of isolated ventricular myocytes: effects of pacing, myoglobin, and oxygen supply. Biophys. J. 65, 195-204.
86. Williams, R. S. and Neufer, P. D. (1996). Regulation of Gene Expression in Skeletal Muscle by Contractile Activity. Bethesda, MD: American Physiological Society.
87. Wittenberg, B. A. and Wittenberg, J. B. (1985). Oxygen pressure gradients in isolated cardiac myocytes. J. Biol. Chem. 260, 6548-6554.
88. Wittenberg, B. A. and Wittenberg, J. B. (1987). Myoglobin-mediated oxygen delivery to mitochondria of isolated cardiac myocytes. Proc. Natl. Acad. Sci. USA 84, 7503-7507.
89. Wittenberg, B. A. and Wittenberg, J. B. (1989). Transport of oxygen in muscle. Ann. Rev. Physiol. 51, 857-878.
90. Wittenberg, J. B. (1966). The molecular mechanism of hemoglobin-facilitated oxygen diffusion. J. Biol. Chem. 241, 104-114.
91. Wittenberg, J. B. (1970). Myoglobin facilitated oxygen diffusion and the role of myoglobin in oxygen entry into muscle. Physiol. Rev. 50, 559-636.
92. Wittenberg, J. B., Bergersen, F. J., Appleby, C. A. and Turner, G. L. (1974). Facilitated oxygen diffusion. The role of leghemoglobin in nitrogen fixation by bacteroids isolated from soybean root nodules. J. Biol. Chem. 249, 4057-4066.
93. Wittenberg, J. B. and Wittenberg, B. A. (1981). Facilitated oxygen diffusion by oxygen carriers. In Oxygen and Living Processes (ed. D. L. Gilbert), pp. 177-199. New York: Springer-Verlag.
94. Wittenberg, J. B., Wittenberg, B. A., Day, D. A., Udvardi, M. K. and Appleby, C. A. (1996). Siderophore-bound iron in the peribacteroid space of soybean root nodules. Plant Soil 178, 161-169.
95. Wyman, J. (1966). Facilitated diffusion and the possible role of myoglobin as a transport mechanism. J. Biol. Chem. 241, 115-121.
96. Zhang, J., Murakami, Y., Zhang, Y., Cho, Y. K., Ye, Y., Gong, G., Bache, R. J., Ugurbil, K. and From, A. H. L. (1999). Oxygen delivery does not limit cardiac performance during high work states. Am. J. Physiol. 276, H50-H57.
97. Zhang, J. U. K., From, A. H. L. and Bache, R. J. (2001). Myocardial oxygenation and high energy phosphate levels during graded coronary hypoperfusion. Am. J. Physiol. 280, H318-H326.