When bad things happen to good fish: The loss of hemoglobin and myoglobin expression in Antarctic icefishes

Journal of Experimental Biology

Volumn 209, Issue 10, 2006, Pages 1791-1802

  Sidell, Bruce D ^a   O'Brien, Kristin M ^b  

^a UNIVERSITY OF MAINE   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Antarctic icefish; Circulation; Heart; Hemoglobin; Myoglobin; Nitric oxide

Indexed keywords

HEMOGLOBIN; MYOGLOBIN; NITRIC OXIDE;

ADAPTATION; ANIMAL; ANTARCTICA; CLASSIFICATION; FISH; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTARCTIC REGIONS; FISHES; GENE EXPRESSION REGULATION; HEMOGLOBINS; MYOGLOBIN; NITRIC OXIDE;

ANIMALIA; CHANNICHTHYIDAE; SALANGINI;

EID: 33745651826     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.02091     Document Type: Review

References (91)

1. Acierno, R., Agnisola, C., Tota, B. and Sidell, B. D. (1997). Myoglobin enhances cardiac performance in Antarctic species that express the pigment. Am. J. Physiol. 273, R100-R106.
2. Anderson, J. E. (2000). A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol. Biol. Cell 11, 1859-1874.
3. Antunes, F., Boveris, A. and Cadenas, E. (2004). On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide. Proc. Natl. Acad. Sci. USA 101, 16774-16779.
4. Axelsson, M., Davison, W., Forster, M. E. and Farrell, A. P. (1992). Cardiovascular responses of the red-blooded Antarctic fishes, Pagothenia bernacchii and Pagothenia borchgrevinki. J. Exp. Biol. 167, 179-201.
5. Axelsson, M., Agnisola, C., Nilsson, S. and Tota, B. (1998). Fish cardiocirculatory function in the cold. In Cold Ocean Physiology (ed. H. O. Pörtner and R. Playle), pp. 327-364. Cambridge: Cambridge University Press.
6. Bargelloni, L., Ritchie, P. A., Patarnello, T., Battaglia, B., Lambert, D. M. and Meyer, A. (1994). Molecular evolution at subzero temperatures: mitochondrial and nuclear phylogenies of fishes from Antarctica (Suborder Notothenioidei) and the evolution of antifreeze glycoproteins. Mol. Biol. Evol. 11, 854-863.
7. Bargelloini, L., Marcatao, S., Lorenzo, Z. and Patarnello, T. (2000). Mitochondrial phylogeny of Notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst. Biol. 49, 114-129.
8. Baum, D. A. and Larson, A. (1991). Adaptation reviewed: a phlyogenetic methodology for studying character macroevolution. Syst. Zool. 40, 1-18.
9. 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. 117B, 613-620.
10. Cocca, E., Ratnayake-Lecamwasam, M., Parker, S. K., Camardella, L., Ciaramella, M., diPrisco, G. and Detrich, H. W., III (1995). Genomic remnants of α-globin genes in the hemoglobinless Antarctic icefishes. Proc. Natl. Acad. Sci. USA 92, 1817-1821.
11. Cocca, E., Ratnayake-Lecamwasam, M., Parker, S. K., Camardella, L., Ciaramella, M., diPrisco, G. and Detrich, H. W., III (1997). Do the hemoglobinless icefishes have globin genes? Comp. Biochem. Physiol. 118A, 1027-1030.
12. Conway, E. J., Collen, D. and Carmeliet, P. (2001). Molecular mechanisms of blood vessel growth. Cardiovasc. Res. 49, 507-521.
13. DeWitt, H. H. (1971). Folio 15. In Antarctic Map Folio Series (ed. V. C. Bushnell), pp. 1-10. New York: American Geographical Society.
14. di Prisco, G., D'Avino, R., Caruso, C., Tamburini, M., Camardella, L., Rutigliano, B., Carratore, V. and Romano, M. (1991). The biochemistry of oxygen transport in red-blooded Antarctic fish. In Biology of Antarctic Fish (ed. G. di Prisco, B. Maresca and B. Tota), pp. 263-281. Berlin: Springer-Verlag.
15. Eastman, J. T. (1993). Antarctic Fish Biology: Evolution in a Unique Environment. New York: Academic Press.
16. Eastman, J. T. (2005). The nature of the diversity of Antarctic fishes. Polar Biol. 28, 93-107.
17. Eastman, J. T. and Lannoo, M. J. (2004). Brain and sense organ anatomy and histology in hemoglobinless Antarctic icefishes (Perciformes: Notothenioidei: Channichthyidae). J. Morphol. 260, 117-140.
18. Egginton, S. (1996). Blood rheology of Antarctic fishes: viscosity adaptations at very low temperatures. J. Fish Biol. 48, 513-521.
19. 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.
20. 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.
21. Egginton, S., Skilbeck, C., Hoofd, L., Calvo, J. and Johnston, I. A. (2002). Peripheral oxygen transport in skeletal muscle of Antarctic and sub-Antarctic notothenioid fish. J. Exp. Biol. 205, 769-779.
22. Ekau, W. (1990). Demersal fish fauna of the Weddell sea, Antarctica. Antarct. Sci. 2, 129-137.
23. Farrell, A. P. and Jones, D. R. (1992). The heart. In Physiology of Fishes, Vol. XIIA (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 1-88. Academic Press. New York.
24. Fitch, N. A., Johnston, I. A. and Wood, R. E. (1984). Skeletal muscle capillary supply in a fish that lacks respiratory pigments. Respir. Physiol. 57, 201-211.
25. Flögel, U., Merx, M. W., Gödecke, A., Kecking, U. K. J. and Schrader, J. (2001). Myoglobin: a scavenger of bioactive NO. Proc. Natl. Acad. Sci. USA 98, 735-740.
26. Fritsche, R., Schwerte, T. and Pelster, B. (2000). Nitric oxide and vascular reactivity in developing zebrafish, Danio rerio. Am. J. Physiol. 279, R2200-R2207.
27. Gardner, P. R. (2005). Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 99, 247-266.
28. Gardner, P. R., Gardner, A. M., Martin, L. A. and Salzman, A. L. (1998). Nitric oxide dioxygenase: an enzymatic function for flavohemoglobin. Proc. Natl. Acad. Sci. USA 95, 10378-10383.
29. 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.
30. Gödecke, A., Molojavyi, A., Heger, J., Flögel, U., Ding, Z., Jacoby, C. and Schrader, J. (2003). Myoglobin protects the heart from inducible nitric-oxide synthase (iNOS)-mediated nitrosative stress. J. Biol. Chem. 278, 21761-21766.
31. Gödecke, A., Flögel, U., Zanger, 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.
32. 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.
33. Grove, T. J., Hendrickson, J. W. and Sidell, B. D. (2004). Two species of Antarctic icefishes (Genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression. Polar Biol. 27, 579-585.
34. Hemmingsen, E. A. (1991). Respiratory and cardiovascular adaptation in hemoglobin-free fish: resolved and unresolved problems. In Biology of Antarctic Fish (ed. G. di Prisco, B. Maresca and B. Tota), pp. 191-203. New York: Springer-Verlag.
35. Hemmingsen, E. A. and Douglas, E. L. (1977). Respiratory and circulatory adaptations to the absence of hemoglobin in chaenichthyid fishes. In Adaptations within Antarctic Ecosystems (ed. G. A. Llano), pp. 479-487. Washington: Smithsonian Institution.
36. Hemmingsen, E. A., Douglas, E. L., Johansen, K. and Millard, R. W. (1972). Aortic blood flow and cardiac output in the hemoglobin-free fish Chaenocephalus aceratus. Comp. Biochem. Physiol. 43A, 1045-1051.
37. Herold, S., Fago, A., Weber, R. E., Dewilde, S. and Moens, L. (2004). Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress. J. Biol. Chem. 279, 22841-22847.
38. Holmqvist, B., Goksøyer, A. and Øyan, A. (1998). Distributional expression of brain neuronal nitric oxide synthase mRNA during developmental life stages of Atlantic salmon. Soc. Neurosci. Abstr. 24, 215.14.
39. Holmqvist, B., Ellinsen, B., Forsell, J., Zhadanova, I. and Alm, P. (2004). The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish. J. Exp. Biol. 207, 923-935.
40. Holeton, G. F. (1970). Oxygen uptake and circulation by a hemoglobinless Antarctic fish (Chaenocephalus aceratus, Lonnberg) compared with three red-blooded Antarctic fish. Comp. Biochem. Physiol. 34, 457-471.
41. 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.
42. Kennett, J. P. (1977). Cenozoic evolution of Antarctic glaciation, the circum-Antarctic Ocean and their impact on global paleooceanography. J. Geophys. Res. 82, 3843-3860.
43. Kerwin, J. F., Jr, Lancaster, J. R., Jr and Feldman, P. L. (1995). Nitric oxide: a new paradigm for second messengers. J. Med. Chem. 38, 4343-4362.
44. Kimura, H. and Esumi, H. (2003). Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis. Acta Biochim. Pol. 50, 49-59.
45. Kimura, H., Weisz, A., Kurashima, Y., Hashimoto, K., Ogura, T., D'Acquisto, R., Addeo, R., Makuuchi, M. and Esumi, H. (2000). Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-I activity by nitric oxide. Blood 95, 189-197.
46. Kock, K.-H. (2005). Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I. Polar Biol. 28, 862-895.
47. Krogh, A. (1929). The progress of physiology. Am. J. Physiol. 90, 243-251.
48. Littlepage, J. L. (1965). Oceanographic investigation in McMurdo Sound. Antarctica. In Biology of the Antarctic Seas, Vol. II (ed. G. A. Llano), pp. 1-37. Washington, DC: American Geophysical Union.
49. Liu, L., Zeng, M., Hausladen, A., Heitman, J. and Stamler, J. S. (2000). Protection from nitrosative stress by yeast flavohemoglobin. Proc. Natl. Acad. Sci. USA 97, 4672-4676.
50. Milkiewicz, M., Hudlicka, O., Brown, M. D. and Silgram, H. (2005). Nitric oxide, VEGF, and VEGF-2: interactions in activity-induced angiogenesis and rat skeletal muscle. Am. J. Physiol. 289, H336-H343.
51. Minning, D. M., Gow, A. J., Bonaventura, J., Braun, R., Dewhirst, M., Goldberg, D. E. and Stamler, J. S. (1999). Ascaris haemoglobin is a nitric oxide-activated deoxygenase. Nature 401, 497-502.
52. Moncada, S. and Higgs, A. (1993). The L-arginine-nitric oxide pathway. New Engl. J. Med. 329, 2002-2012.
53. Montgomery, J. and Clements, K. (2000). Disaptation and recovery in the evolution of Antarctic fishes. Trends Ecol. Evol. 15, 267-271.
54. Morlá, M., Augusti, A. G. N., Hahman, I., Motterlini, R., Saus, C., Morales-Nin, B., Company, J. B. and Busquets, X. (2003). Nitric oxide synthase type I (nNOS), vascular endothelial growth factor (VEGF) and myoglobin-like expression in skeletal muscle of Antarctic icefishes (Notothenioidei: Channichthyidae). Polar Biol. 26, 458-462.
55. 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.
56. Near, T. J., Pesavento, J. J. and Cheng, C.-H. C. (2003). Mitochondrial DNA, morphology and the phlyogenetic relationships of Antarctic icefishes. (Notothenoidei: Channichthyidae). Mol. Phylogenet. Evol. 28, 87-98.
57. Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S. et al. (2003). Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299, 896-899.
58. Nisoli, E., Falcone, S., Tonello, C., Cozzi, V., Palomba, L., Fiorani, M., Pisconti, A., Brunelli, S., Cardile, A., Francolini, M. et al. (2004). Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl. Acad. Sci. USA 101, 16507-16512.
59. 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.
60. O'Brien, K. M., Xue, H. and Sidell, B. D. (2000). Quantification of diffusion distance within the spongy myocardium of hearts from Antarctic fishes. Respir. Physiol. 122, 71-80.
61. O'Brien, K. M., Skilbeck, C., Sidell, B. D. and Egginton, S. (2003). Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes. J. Exp. Biol. 206, 411-421.
62. Ordway, G. A. and Garry, D. J. (2004). Myoglobin: an essential hemoprotein in striated muscle. J. Exp. Biol. 207, 3441-3446.
63. Palmer, R. M., Ferrige, A. G. and Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxation factor. Nature 327, 524-526.
64. Pellegrino, D., Sprovieri, E., Mazza, R., Randall, D. J. and Tota, B. (2002). Nitric oxide-cGMP-mediated vasoconstriction and effects of acetylcholine in the branchial circulation of the eel. Comp. Biochem. Physiol. 132A, 447-457.
65. Pellegrino, D., Acierno, R. and Tota, B. (2003). Control of cardiovascular function in the icefish Chionodraco hamatus: involvement of serotonin and nitric oxide. Comp. Biochem. Physiol. 134A, 471-480.
66. Pellegrino, D., Palmerini, C. A. and Tota, B. (2004). No hemoglobin but NO: the icefish (Chionodraco hamatus) heart as a paradigm. J. Exp. Biol. 207, 3855-3864.
67. Pesce, A., Bolognesi, M., Bocedi, A., Ascenzi, P., Dewilde, S., Moens, L., Hanklen, T. and Burmester, T. (2002). Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep. 3, 1146-1151.
68. Powers, D. A. (1974). Structure, function and molecular ecology of fish hemoglobins. Ann. NY Acad. Sci. 241, 472-490.
69. Puigserver, P. and Spiegelman, B. M. (2003). Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90.
70. 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.
71. Ruud, J. T. (1954). Vertebrates without erythrocytes and blood pigment. Nature 173, 848-850.
72. Ruud, J. T. (1965). The icefish. Sci. Am. 213, 108-114.
73. Scarpulla, R. C. (1997). Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembr. 29, 109-119.
74. Scholander, P. F. and Van Dam, L. (1957). The concentration of hemoglobin in some cold water arctic fishes. J. Cell. Comp. Physiol. 49, 1-4.
75. Shadel, G. S. and Clayton, D. A. (1993). Mitochondrial transcription initiation. J. Biol. Chem. 268, 16083-16086.
76. Shaul, P. W. (2002). Regulation of endothelial nitric oxide synthase: location, location, location. Annu. Rev. Physiol. 64, 749-774.
77. Sidell, B. D. (1998). Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J. Exp. Biol. 201, 1118-1127.
78. Sidell, B. D., Vayda, M. E., Small, D. J., Moylan, T. J., Londraville, R. L., Yuan, M.-L., Rodnick, K. J., Eppley, Z. A. and Costello, L. (1997). Variation in the expression of myoglobin among species of hemoglobinless Antarctic icefishes. Proc. Natl. Acad. Sci. USA 94, 3420-3424.
79. Small, D. J., Vayda, M. E. and Sidell, B. D. (1998). A novel vertebrate myoglobin gene containing three A+T-rich introns is conserved among Antarctic teleost species, which differ in myoglobin expression. J. Mol. Evol. 47, 156-166.
80. Small, D. J., Moylan, T., Vayda, M. E. and Sidell, B. D. (2003). The myoglobin gene of the Antarctic icefish, Chaenocephalus aceratus, contains a duplicated TATAAAA sequence that interferes with transcription. J. Exp. Biol. 206, 131-139.
81. Smith, L. W., Smith, J. D. and Criswell, D. S. (2002). Involvement of nitric oxide synthase in skeletal muscle adaption to chronic overload. J. Appl. Physiol. 92, 2005-2011.
82. Suri, C., McClain, J., Thurston, G., McDonald, D. J., Zhou, H., Oldmixon, E.-H., Sato, T. N. and Yancopoulos, G. D. (1998). Increased vascularization in mice overexpressing Angiopoietin-1. Science 282, 468-471.
83. Tidball, J. G., Spencer, M. J., Wehling, M. and Lavergne, E. (1999). Nitric-oxide synthase is a mechanical signal transducer that modulates talin and vinculin expression. J. Biol. Chem. 274, 33155-33160.
84. Tota, B. and Gattuso, A. (1996). Heart ventricle pumps in teleosts and elasmobranchs: a morphodynamic approach. J. Exp. Zool. 275, 162-171.
85. Tota, B., Acierno, R. and Agnisola, C. (1991). Mechanical performance of the isolated and perfused heart of the haemoglobinless Antarctic icefish Chionodraco rastrospinosus (Lönnberg): effects of loading conditions and temperature. Philos. Trans. R. Soc. Lond. B Biol. Sci. 332, 191-198.
86. Tota, B., Amelio, D., Pellegrino, D., Ip, Y. K. and Cerra, M. C. (2005). NO modulation of myocardial performance in fish hearts. Comp. Biochem. Physiol. 142A, 164-177.
87. Webb, P.-N. (1990). The Cenozoic history of Antarctica and its global impact. Antarct. Sci. 2, 3-21.
88. Wells, R. M. G. (1990). Hemoglobin physiology in vertebrate animals: a cautionary approach to adaptationist thinking. Adv. Comp. Environ. Physiol. 6, 143-161.
89. Wittenberg, B. A. and Wittenberg, J. B. (2003). Myoglobin function assessed. J. Exp. Biol. 206, 2011-2020.
90. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C. et al. (1999). Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124.
91. Zhao, Y., Ratnayake-Lecamwasam, M., Parker, S. K., Cocca, E., Camardella, L., di Prisco, G. and Detrich, H. W., III (1998). The major adult α-globin gene of Antarctic teleosts and its remnants in the hemoglobinless icefishes. J. Biol. Chem. 273, 14745-14752.