In vivo red blood cell sickling and mechanism of recovery in whiting, Merlangius merlangus

Journal of Experimental Biology

Volumn 210, Issue 19, 2007, Pages 3451-3460

  Koldkjær, Pia ^a   Berenbrink, Michael ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Fish; Haemoglobin; Hb polymerisation; Merlangius merlangus; Na H exchanger; Red blood cell; Sickle cell disease

Indexed keywords

ANIMAL; ARTICLE; BLOOD; CELL SHAPE; ERYTHROCYTE; GADIFORMES; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CELL SHAPE; ERYTHROCYTES; GADIFORMES;

MERLANGIUS MERLANGUS; PISCES; VERTEBRATA;

EID: 35848942360     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.008524     Document Type: Article

References (63)

1. Aluoch, J. R. (1997). Higher resistance to Plasmodium falciparum infection in patients with homozygous sickle cell disease in western Kenya. Trop. Med. Int. Health 2, 568-571.
2. Appy, R. G., Burt, M. D. B. and Morris, T. J. (1976). Viral nature of piscine erythrocytic necrosis (PEN) in the blood of Atlantic cod (Gadus morhua). J. Fish. Res. Board Can. 33, 1380-1385.
3. Ayi, K., Turrini, F., Piga, A. and Arese, P. (2004). Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 104, 3364-3371.
4. Berenbrink, M. (2006). Evolution of vertebrate haemoglobins: histidine side chains, specific buffer value and Bohr effect. Respir. Physiol. Neurobiol. 154, 165-184.
5. 2 secretion in the eye and swimbladder of fishes. J. Exp. Biol. 209, 1641-1652.
6. --dependent acid extrusion in Atlantic cod red blood cells in winter activated by hypercapnia. J. Exp. Biol. 192, 239-252.
7. Berenbrink, M. and Bridges, C. R. (1994b). Catecholamine-activated sodium/proton exchange in the red blood cells of the marine teleost Gadus morhua. J. Exp. Biol. 192, 253-267.
8. Berenbrink, M., Koldkjær, P., Kepp, O. and Cossins, A. R. (2005). Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307, 1752-1757.
9. Bohr, C. (1894). The influence of secretion of the vagus nerve on the disengagement of gases in the air-bladder of fishes. J. Physiol. 15, 494-500.
10. Bookchin, R. M., Balazs, T. and Landau, L. C. (1976). Determinants of red cell sickling. Effects of varying pH and of increasing intracellular hemoglobin concentration by osmotic shrinkage. J. Lab. Clin. Med. 87, 597-616.
11. Borgese, T. A., Harrington, J. P., Ganjian, I. and Duran, C. (1988). Haemoglobin properties and polymerization in the marine teleost Lophius americanus (Goosefish). Comp. Biochem. Physiol. 91B, 663-670.
12. Borgese, T. A., Harrington, J. P., Duffy, L. and Bourke, S. (1992). Functional studies on goosefish (Lophius americanus) hemoglobin. Comp. Biochem. Physiol. 101B, 535-539.
13. Brauner, C. J. and Berenbrink, M. (2007). Gas transport and exchange. In Primitive Fishes, Fish Physiology 26 (ed. D. J. McKenzie, A. P. Farrell and C. J. Brauner), pp. 213-282. Amsterdam: Elsevier.
14. Bunn, H. F. (1997). Pathogenesis and treatment of sickle cell disease. N. Engl. J. Med. 337, 762-769.
15. Butler, P. J., Axelsson, M., Ehrenström, F., Metcalfe, J. D. and Nilsson, S. (1989). Circulating catecholamines and swimming performance in the Atlantic cod, Gadus morhua. J. Exp. Biol. 141, 377-387.
16. Christoph, G. W., Hofrichter, J. and Eaton, W. A. (2005). Understanding the shape of sickled red cells. Biophys. J. 88, 1371-1376.
17. + exchange in trout erythrocytes and its effects upon oxygen-carrying capacity. J. Exp. Biol. 118, 229-246.
18. Davies, A. J. and Johnston, M. R. L. (2000). The biology of some intraerythrocytic parasites of fishes, amphibia and reptiles. Adv. Parasitol. 45, 1-107.
19. Dawson, A. B. (1930). Changes in the erythrocytes of Nedurus associated with the intracellular crystallization of hemoglobin. Anat. Rec. 46, 161-172.
20. Dawson, A. B. (1932). Intracellular crystallization of hemoglobin in the erythrocytes of the Northern pipefish, Syngnathus fuscus. Biol. Bull. 63, 492-495.
21. Döbler, J. and Bertles, J. F. (1968). The physical state of hemoglobin in sickle-cell anemia erythrocytes in vivo. J. Exp. Med. 127, 711-716 and plates 77-80.
22. Eaton, W. A. and Hofrichter, J. (1987). Hemoglobin S gelation and sickle cell disease. Blood 70, 1245-1266.
23. Egginton, S. (2002). Temperature and angiogenesis: the possible role of mechanical factors in capillary growth. Comp. Biochem. Physiol. 132A, 773-787.
24. 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, R375-R388.
25. Fago, A., Romano, M., Tamburrini, M., Coletta, M., Davino, R. and di Prisco, G. (1993). A polymerizing Root-effect fish hemoglobin with high subunit heterogeneity - correlation with primary structure. Eur. J. Biochem. 218, 829-835.
26. Hárosi, F. I., von Herbing, I. H. and van Keuren, J. R. (1998). Sickling of anoxic red blood cells in fish. Biol. Bull. 195, 5-11.
27. Hemmingsen, W. and MacKenzie, K. (2001). The parasite fauna of the Atlantic cod, Gadus morhua L. Adv. Mar. Biol. 40, 1-80.
28. Hofrichter, J., Ross, P. D. and Eaton, W. A. (1974). Kinetics and mechanism of deoxyhemoglobin S gelation: a new approach to understanding sickle cell disease. Proc. Natl. Acad. Sci. USA 71, 4864-4868.
29. Holeton, G. F., Neumann, P. and Heisler, N. (1983). Branchial ion exchange and acid-base regulation after strenuous exercise in rainbow trout (Salmo gairdneri). Respir. Physiol. 51, 303-318.
30. Ingram, V. M. (1957). Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin. Nature 180, 326-328.
31. Jensen, F. B., Nikinmaa, N. and Weber, R. E. (1983). Effects of exercise stress on acid-base balance and respiratory function in blood of the teleost Tinea tinea. Respir. Physiol. 51, 291-301.
32. Jones, T. R. (1997). Quantitative aspects of the relationship between the sickle cell gene and malaria. Parasitol. Today 13, 107-111.
33. + balance, acid-base status and blood respiratory properties in carp. Comp. Biochem. Physiol. 119A, 301-307.
34. 2 secretion in the swimbladder of the eel. Respir. Physiol. 79, 231-242.
35. Krogh, A. (1922). The Anatomy and Physiology of the Capillaries. New Haven: Yale University Press.
36. Lange, R. D., Minnich, V. and Moore, C. V. (1951). Effect of oxygen tension and of pH on the sickling and mechanical fragility of erythrocytes from patients with sickle cell anemia and the sickle cell trait. J. Lab. Clin. Med. 37, 789-802.
37. Larsen, B. K., Pörtner, H.-O. and Jensen, F. B. (1997). Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar. Biol. 128, 337-346.
38. Mattei, X., Marchand, B. and Mattei, C. (1985). Crystallization of reptile hemoglobin during its digestion in a pentastomide. J. Ultrastruct. Res. 92, 63-71.
39. i after exhaustive activity in rainbow trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). J. Exp. Biol. 133, 263-282.
40. Mozzarelli, A., Hofrichter, J. and Eaton, W. A. (1987). Delay time of haemoglobin S polymerization prevents most cells from sickling in vivo. Science 237, 500-506.
41. Nikinmaa, M. (1982). Effects of adrenaline on red cell volume and concentration gradient of protons across me red cell membrane in the rainbow trout, Salmo gairdneri. Mol. Physiol. 2, 287-297.
42. Nikinmaa, M. (1990). Vertebrate Red Blood Cells. Berlin, Heidelberg: Springer-Verlag.
43. Nikinmaa, M. and Jensen, F. B. (1986). Blood oxygen transport and acid-base status of stressed rainbow trout (Salmo gairdnerii): pre- and postbranchial values in winter fish. Comp. Biochem. Physiol. 84A, 391-396.
44. Perry, S. F., Fritsche, R., Kinkead, R. and Nilsson, S. (1991). Control of catecholamine release in vivo and in situ in the Atlantic cod (Gadus morhua) during hypoxia. J. Exp. Biol. 155, 549-566.
45. Perry, S. F., Reid, S. G. and Salama, A. (1996). The effects of repeated physical stress on the β-adrenergic response of the rainbow trout red blood cell. J. Exp. Biol. 199, 549-562.
46. Perutz, M. F. and Mitchison, J. M. (1950). State of haemoglobin in sickle-cell anaemia. Nature 166, 677-679.
47. Primmett, D. R. N., Randall, D. J., Mazeaud, M. and Boutilier, R. G. (1986). The role of catecholamines in erythrocyte pH regulation and oxygen transport in rainbow trout (Salmo gairdneri) during exercise. J. Exp. Biol. 122, 139-148.
48. Prosser, C. L. (1950). Comparative Animal Physiology. Philadelphia: W. B. Saunders Company.
49. Riggs, A. (1976). Factors in the evolution of hemoglobin function. Fed. Proc. 35, 2115-2118.
50. Scholander, P. F. (1954). Secretion of gases against high pressure in the swimbladder of deep sea fishes II. The rete mirabile. Biol. Bull. 107, 260-277.
51. Serjeant, G. R. (2001). The emerging understanding of sickle cell disease. Br. J. Haematol. 112, 3-18.
52. Smail, D. A. (1982). Viral erythrocytic necrosis in fish: a review. Proc. R. Soc. Edinb. Biol. 81, 169-176.
53. Steen, J. B. (1963). The physiology of the swimbladder in the eel Anguilla vulgaris. 3. The mechanism of gas secretion. Acta Physiol. Scand. 59, 221-241.
54. Thomas, N. W. (1971). The form of haemoglobin in the erythrocytes of the cod, Gadus callarias. J. Cell Sci. 8, 407-412.
55. Ueda, Y. and Bookchin, R. M. (1984). Effects of carbon dioxide and pH variations in vitro on blood respiratory functions, red blood cell volume, transmembrane pH gradients, and sickling in sickle cell anemia. J. Lab. Clin. Med. 104, 146-159.
56. Ultsch, G. R. and Jackson, D. C. (1996). pH and temperature in ectomermic vertebrates. Bull. Alabama Mus. Nat. Hist. 18, 1-41.
57. Undritz, E., Betke, K. and Lehmann, H. (1960). Sickling phenomenon in deer. Nature 187, 333-334.
58. Verde, C., Balestrieri, M., de Pascale, D., Pagnozzi, D., Lecointre, G. and di Prisco, G. (2006). The oxygen transport system in three species of the boreal fish family Gadidae: molecular phylogeny of hemoglobin. J. Biol. Chem. 281, 22073-22084.
59. Vink, H. and Duling, B. R. (1996). Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res. 79, 581-589.
60. Wittenberg, J. B. and Wittenberg, B. A. (1962). Active secretion of oxygen into the eye of fish. Nature 194, 106-107.
61. Wittenberg, J. B. and Wittenberg, B. A. (1974). The choroid rete mirabile of the fish eye. I. Oxygen secretion and structure: Comparison with the swimbladder rete mirabile. Biol. Bull. 146, 116-136.
62. + dynamics after strenuous exercise in the starry flounder Platichthys stellatus. Physiol. Zool. 60, 69-81.
63. Yoffey, J. M. (1929). A contribution to the study of the comparative histology and physiology of the spleen, with reference chiefly to its cellular constituents. I. In fishes. J. Anat. 63, 314-344.