Red blood cell pH, the Bohr effect, and other oxygenation-linked phenomena in blood O2 and CO2 transport

Acta Physiologica Scandinavica

Volumn 182, Issue 3, 2004, Pages 215-227

  Jensen, F B ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Blood gas transport; Bohr Haldane effect; Erythrocyte; Haemoglobin; Membrane interaction; Oxygen sensitive ion transport

Indexed keywords

BICARBONATE; CARBONATE DEHYDRATASE; HEMOGLOBIN; NITROGEN OXIDE; VASODILATOR AGENT;

ALLOSTERISM; BLOOD FLOW; BLOOD OXYGEN TENSION; BLOOD PH; BOHR EFFECT; CARBON DIOXIDE TRANSPORT; CELL PH; DEOXYGENATION; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; GAS EXCHANGE; GAS TRANSPORT; GLYCOLYSIS; HUMAN; HYPERVENTILATION; HYPOXIA; NONHUMAN; OXYGEN AFFINITY; OXYGEN SATURATION; OXYGENATION; PRIORITY JOURNAL; RESPIRATORY ALKALOSIS; RESPIRATORY FUNCTION; REVIEW;

ANIMALS; ANOXIA; BIOLOGICAL TRANSPORT; CARBON DIOXIDE; ERYTHROCYTES; FISHES; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; OXYGEN; RECEPTORS, ADRENERGIC, BETA; VERTEBRATES;

EID: 7944237674     PISSN: 00016772     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-201X.2004.01361.x     Document Type: Review

References (108)

1. Aggergaard, S. & Jensen, F.B. 2001. Cardiovascular changes and physiological response during nitrite exposure in rainbow trout. J Fish Biol 59, 13-27.
2. Albers, C., Goetz, K.H. & Hughes, G.M. 1983. Effect of acclimation temperature on intraerythrocytic acid-base balance and nucleoside triphosphates in the carp, Cyprinus carpio. Respir Physiol 54, 145-159.
3. Astrup, P. & Severinghaus, J.W. 1985. Blodgassernes, syrernes og basernes historie. Munksgaard, Copenhagen.
4. Bauer, C., Rollema, H.S., Till, H.W., & Braunitzer, G. 1980. Phosphate binding by llama and camel hemoglobin. J Comp Physiol 136, 67-70.
5. 2 affinity, cooperativity and pH dependence of transport. J Physiol 526, 69-80.
6. 2 across the human erythrocyte membrane. J Physiol 550, 419-429.
7. Bogdanova, A. & Nikinmaa, M. 2001. Reactive oxygen species regulate oxygen-sensitive potassium flux in rainbow trout erythrocytes. J Gen Physiol 117, 181-190.
8. Bohr, C., Hasselbalch, K. & Krogh, A. 1904. Ueber einen in biologischer beziehung wichtigen einfluss, den die kohlensäurespannung des blutes auf dessen sauerstoffbindung übt. Skand Arch Physiol 16, 402-412.
9. Borgese, F., Motais, R. & Garcia-Romeu, F. 1991. Regulation of Cl-dependent K transport by oxy-deoxyhemoglobin transitions in trout red cells. Biochim Biophys Acta 1066, 252-256.
10. Bouverot, P. 1985. Adaptation to Altitude-Hypoxia in Vertebrates. Springer, Berlin.
11. Brauner, C.J. & Randall, D.J. 1998. The linkage between oxygen and carbon dioxide transport. In: S.F. Perry & B. Tufts (eds) Fish Physiology, Vol. 17. Fish Respiration, pp. 283-319. Academic Press, San Diego, CA.
12. 2 excretion in the rainbow trout. Respir Physiol 106, 65-70.
13. Brittain, T. 1987. The Root effect. Comp Biochem Physiol 86B, 473-481.
14. Bruce, L.J., Beckmann, R., Ribeiro, M.L. et al. 2003. A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood 101, 4180-4188.
15. Bunn, H.F., Gu, J., Huang, L.E., Park, J.-W. & Zhu, H. 1998. Erythropoietin: a model system for studying oxygen-dependent gene regulation. J Exp Biol 201, 1197-1201.
16. Christiansen, J., Douglas, C.G. & Haldane, J.S. 1914. The absorption and dissociation of carbon dioxide by human blood. J Physiol 48, 244-271.
17. Cooper, G.J., Zhou, Y., Bouyer, P., Grichtchenko, I.I. & Boron, W.F. 2002. Transport of volatile solutes through AQP1. J Physiol 542, 17-29.
18. Cosby, K., Partovi, K.S., Crawford, J.H. et al. 2003. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nature Med 9, 1498-1505.
19. Cossins, A.R. & Gibson, J.S. 1997. Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J Exp Biol 200, 343-352.
20. Duhm, J. 1972. The effect of 2,3-DPG and other organic phosphates on the Donnan equilibrium and the oxygen affinity of human blood. In: M. Rörth & P. Astrup (eds) Oxygen Affinity of Hemoglobin and Red Cell Acid Base Status, pp. 583-594. Munksgaard, Copenhagen.
21. Duhm, J. 1976. Dual effect of 2,3-diphosphoglycerate on the Bohr effect of human blood. Pflügers Arch 363, 55-60.
22. Edsall, J.T. 1986. Understanding blood and hemoglobin: an example of international relations in science. Persp Biol Med 29, S107-S123.
23. Ellory, J.C., Wolowyk, M.W. & Young, J.D. 1987. Hagfish (Eptatretus stouti) erythrocytes show minimal chloride transport activity. J Exp Biol 129, 377-383.
24. Ellsworth, M.L. 2000. The red blood cell as an oxygen sensor: what is the evidence? Acta Physiol Scand 168, 551-559.
25. Ellsworth, M.L., Forrester, T., Ellis, C.G. & Dietrich, H.H. 1995. The erythrocyte as a regulator of vascular tone. Am J Physiol 269, H2155-H2161.
26. Fago, A. & Weber, R.E. 1995. The haemoglobin system of the hagfish Myxine glutinosa: aggregation state and functional properties. Biochim Biophys Acta 1249, 109-115.
27. Fago, A., Malte, H. & Dohn, N. 1999. Bicarbonate binding to hemoglobin links oxygen and carbon dioxide transport in hagfish. Respir Physiol 115, 309-315.
28. Fago, A., Crumbliss, A.L., Peterson, J. Pearce, L.L. & Bonaventura, C. 2003. The case of the missing NO-hemoglobin: spectral changes suggestive of heme redox reactions reflect changes in NO-heme geometry. Proc Natl Acad Sci USA 100, 12087-12092.
29. Faraci, F.M. 1991. Adaptations to hypoxia in birds: how to fly high. Annu Rev Physiol 53, 59-70.
30. 2 permeability of the red blood cell membrane. Proc Natl Acad Sci U S A 95, 15815-15820.
31. Funder, J. & Wieth, J.O. 1966. Chloride and hydrogen ion distribution between human red cells and plasma. Acta Physiol Scand 68, 234-245.
32. Geers, C. & Gros, G. 2000. Carbon dioxide transport and carbonic anhydrase in blood and muscle. Physiol Rev 80, 681-715.
33. Gibson, J.S., Cossins, A.R. & Ellory, J.C. 2000. Oxygen-sensitive membrane transporters in vertebrate red cells. J Exp Biol 203, 1395-1407.
34. 2 excretion. Physiol Biochem Zool 74, 477-492.
35. Gladwin, M.T., Shelhamer, J.H., Schechter, A.N. et al. 2000. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc Natl Acad Sci 97, 11482-11487.
36. Gladwin, M.T., Lancaster, J.R. Jr, Freeman, B.A. & Schechter, A.N. 2003. Nitric oxide's reactions with haemoglobin: a view through the SNO-storm. Nat Med 9, 496-500.
37. González-Alonso, J, Olsen, D.B. & Saltin, B. 2002. Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery. Role of circulating ATP. Circ Res 91, 1046-1055.
38. +. Respir Physiol 65, 223-234.
39. Henry, R.P. & Heming, T.A. 1998. Carbonic anhydrase and respiratory gas exchange. In: S.F. Perry & B. Tufts (eds) Fish Physiology, Vol. 17. Fish Respiration, pp. 75-111. Academic Press, San Diego, CA.
40. Herold, S. 2003. Interaction of nitrogen monoxide with haemoglobin and the artefactual production of S-nitroso-hemoglobin. C R Biologies 326, 533-541.
41. Hladky, S.B. & Rink, T.J. 1977. pH equilibrium across the red cell membrane. In: J.C. Ellory & V.L. Low (eds) Membrane Transport in Red Cells, pp. 115-135. Academic Press, London.
42. Holk, K. & Lykkeboe, G. 1995. Catecholamine-induced changes in oxygen affinity of carp and trout blood. Respir Physiol 100, 55-62.
43. Hübner, S., Michel, F., Rudloff, V. & Appelhans, H. 1992. Amino acid sequence of band-3 protein from rainbow trout erythrocytes derived from cDNA. Biochem J 285, 17-23.
44. 2 delivery mediated by haemoglobin oxygenation. Am J Physiol 280, H2833-H2839.
45. Jelkmann, W. 2003. Erythropoietin. J Endocrinol Invest 26, 832-837.
46. 2 saturation on red cell pH in tench blood in vivo and in vitro. J Exp Zool 238, 119-124.
47. Jensen, F.B. 1989. Hydrogen ion equilibria in fish haemoglobins. J Exp Biol 143, 225-234.
48. Jensen, F.B. 1990. Nitrite and red cell function in carp: control factors for nitrite entry, membrane potassium ion permeation, oxygen affinity and methaemoglobin formation. J Exp Biol 152, 149-166.
49. + transport across the carp red blood cell membrane. J Exp Biol 171, 349-371.
50. Jensen, F.B. 2003. Nitrite disrupts multiple physiological functions in aquatic animals. Comp Biochem Physiol 135A, 9-24.
51. Jensen, F.B. & Weber, R.E. 1982. Respiratory properties of tench blood and hemoglobin. Adaptation to hypoxic-hypercapnic water. Mol Physiol 2, 235-250.
52. Jensen, F.B., Nikinmaa, M. & Weber, R.E. 1993. Environmental perturbations of oxygen transport in teleost fishes: causes, consequences and compensations. In: J.C. Rankin & F.B. Jensen (eds) Fish Ecophysiology, pp. 161-179. Chapman and Hall, London.
53. Jensen, F.B., Fago, A. & Weber, R.E. 1998a. Haemoglobin structure and function. In: S.F. Perry & B. Tufts (eds) Fish Physiology, Vol. 17. Fish Respiration, pp. 1-40. Academic Press, San Diego, CA.
54. Jensen, F.B., Jacobsen, M.H. & Weber, R.E. 1998b. Interaction between haemoglobin and synthetic peptides of the N-terminal cytoplasmic fragment of trout band 3 (AE1) protein. J Exp Biol 201, 2685-2690.
55. Jensen, F.B., Wang, T., Jones, D.R. & Brahm, J. 1998c. Carbon dioxide transport in alligator blood and its erythrocyte permeability to anions and water. Am J Physiol 274, R661-R671.
56. Jensen, F.B., Wang, T. & Brahm, J. 2001. Acute and chronic influence of temperature on red blood cell anion exchange. J Exp Biol 204, 39-45.
57. Jensen, F.B., Brahm, J., Koldkjær, P., Wang, T., McKenzie, DJ. & Taylor, E.W. 2003. Anion exchange in the giant erythrocytes of African lungfish. J Fish Biol 62, 1044-1052.
58. Jia, L., Bonaventura, C., Bonaventura, J. & Stamler, J.S. 1996. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380, 221-226.
59. Kilmartin, J.V. & Rossi-Bernardi, L. 1973. Interaction of haemoglobin with hydrogen ions, carbon dioxide, and organic phosphates. Physiol Rev 53, 836-890.
60. 2 exchange in blood. Annu Rev Physiol 50, 625-637.
61. Koldkjær, P., Pottinger, T.G., Perry, S.F. & Cossins, A.R. 2004. Seasonality of the red blood cell stress response in rainbow trout(Oncorhynchus mykiss). J Exp Biol 207, 357-367.
62. Krogh, A. & Leitch, I. 1919. The respiratory function of the blood in fishes. J Physiol 52, 288-300.
63. Lecklin, T., Tuominen, A. & Nikinmaa, M. 2000. The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes. J Exp Biol 203, 3025-3031.
64. Lenfant, C., Torrance, J., English, E. et al. 1968. Effects of altitude on oxygen binding by hemoglobin and on organic phosphate levels. J Clin Invest 47, 2652-2656.
65. Low, P.S. 1986. Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane-peripheral protein interactions. Biochim Biophys Acta 864, 145-167.
66. Lowe, T.E., Brill, R.W. & Cousins, K.L. 1998. Responses of the red blood cells from two high-energy-demand teleosts, yellowfin tuna (Thunnus albacares) and skipjack tuna (Katsuivonus pelamis), to catecholamines. J Comp Physiol B 168, 405-418.
67. Lukin, J. A. & Ho, C. 2004. The structure-function relationship of hemoglobin in solution at atomic resolution. Chem Rev 104, 1219-1230.
68. Maginniss, L.A., Bernstein, M.H., Deitch, M.A. & Pinshow, B. 1997. Effects of chronic hypobaric hypoxia on blood oxygen binding in pigeons. J Exp Zool 277, 293-300.
69. Maren, T.H. & Swenson, E.R. 1980. A comparative study of the kinetics of the Bohr effect in vertebrates. J Physiol 303, 535-547.
70. 2-linked transition of hemoglobin. FEBS Lett 390, 25-28.
71. + exchange by molecular oxygen in trout erythrocytes. A possible role of haemoglobin as a transducer. J Gen Physiol 90, 197-207.
72. 3 dehydration. Am J Physiol 256, C728-C735.
73. Nielsen, O.B., Lykkeboe, G. & Cossins, A.R. 1992. Oxygenation-activated K fluxes in trout red blood cells. Am J Physiol 263, C1057-C1064.
74. Nikinmaa, M. 1983. Adrenergic regulation of haemoglobin oxygen affinity in rainbow trout red cells. J Comp Physiol 152, 67-72.
75. Nikinmaa, M. 1986. Red cell pH of lamprey (Lampetra fluviatilis) is actively regulated. J Comp Physiol B 156, 747-750.
76. Nikinmaa, M. 1990. Vertebrate Red Blood Cells. Springer, Berlin.
77. Nikinmaa, M. 1992. Membrane transport and control of hemoglobin-oxygen affinity in nucleated erythrocytes. Physiol Rev 72, 301-321.
78. Nikinmaa, M. 1997. Oxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transport. J Exp Biol 200, 369-380.
79. Nikinmaa, M. & Railo, E. 1987. Anion movements across lamprey (Lampetra fluviatilis) red cell membrane. Biochim Biophys Acta 899, 134-136.
80. Nikinmaa, M., Airaksinen, S. & Virkki, L.V. 1995. Haemoglobin function in intact lamprey erythrocytes: interactions with membrane function in the regulation of gas transport and acid-base balance. J Exp Biol 198, 2423-2430.
81. Nikinmaa, M., Bogdanova, A. & Lecklin, T. 2003. Oxygen dependency of the adrenergic Na/H exchange in rainbow trout erythrocytes is diminished by a hydroxyl radical scavenger. Acta Physiol Scand 178, 149-154.
82. Ohnishi, S.T. & Asai, H. 1985. Lamprey erythrocytes lack glycoproteins and anion transport. Comp Biochem Physiol 81B, 405-407.
83. Pawloski, J.R., Hess, D.T. & Stamler, J.S. 2001. Export by red blood cells of nitric oxide bioactivity. Nature 409, 622-626.
84. Pelstet, B. 2001. The generation of hyperbaric oxygen tensions in fish. News Physiol Sci 16, 287-291.
85. Perutz, M.F. 1983. Species adaptation in a protein molecule. Mol Biol Evol 1, 1-28.
86. Primmett, D.R.N., Randall, D.J., Mazeaud, M. & 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.
87. Reithmeier, R.A.F. 2001. A membrane metabolon linking carbonic anhydrase with chloride/bicarbonate anion exchangers. Blood Cell Mol Dis 27, 85-89.
88. Riggs, A.F. 1988. The Bohr effect. Annu Rev Physiol 50, 181-204.
89. 2 and pH. J Exp Biol 136, 405-416.
90. Schmidt-Nielsen, B. 1984. August and Marie Krogh and respiratory physiology. J Appl Physiol 57, 293-303.
91. Stamler, J.S., Jia, L., Eu, J.P. et al. 1997. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276, 2034-2037.
92. Stringer, W., Wasserman, K., Casaburi, R., Pórszász, J., Maehara, K. & French, W. 1994. Lactic acidosis as a facilitator of oxyhemoglobin dissociation during exercise. J Appl Physiol 76, 1462-1467.
93. Tetens, V. & Christiansen, N.J. 1987. Beta-adrenergic control of blood oxygen affinity in acutely hypoxia exposed rainbow trout. J Comp Physiol B 157, 667-675.
94. + exchange on blood oxygen and carbon dioxide transport in fish. J Exp Zool 263, 160-175.
95. 2 transport and ion distributions between plasma and erythrocytes in the blood of Petromyzon marinus. J Exp Biol 144, 565-576.
96. Tufts, B. & Perry, S.F. 1998. Carbon dioxide transport and excretion. In: S.F. Perry & B. Tufts (eds) Fish Physiology, Vol. 17. Fish Respiration, pp. 229-281. Academic Press, San Diego, CA.
97. Turek, Z., Kreuzer, F. & Hoofd, L.J.C. 1973. Advantage or disadvantage of a decrease of blood oxygen affinity for tissue oxygen supply at hypoxia. A theoretical study comparing man and rat. Pflügers Arch 342, 185-197.
98. Val, A.L. 2000. Organic phosphates in the red blood cells of fish. Comp Biochem Physiol 125A, 417-435.
99. Verkman, A.S. 2002. Does aquaporin-1 pass gas? An opposing view. J Physiol 542, 31.
100. Walder, J.A., Chatterjee, R., Steck, T.L. et al. 1984. The interaction of hemoglobin with the cytoplasmic domain of band 3 in the human erythrocyte membrane. J Biol Chem 259, 10238-10246.
101. Weber, R.E. 2000. Adaptations for oxygen transport: lessons from fish hemoglobins. In: G. di Frisco, B. Giardina & R.E. Weber (eds) Hemoglobin Function in Vertebrates. Molecular Adaptation in Extreme and Temperate Environments, pp. 23-37. Springer, Milano.
102. Weber, R.E. & Jensen, F.B. 1988. Functional adaptations in hemoglobins from ectothermic vertebrates. Annu Rev Physiol 50, 161-179.
103. 2 on haemoglobin-oxygen affinity. J Comp Physiol 128, 127-137.
104. Wells, R.M.G. & Weber, R.E. 1985. Fixed acid and carbon dioxide Bohr effects as functions of haemoglobin-oxygen saturation and erythrocyte pH in the blood of the frog, Rana temporaria. Pflügers Arch 403, 7-12.
105. Wieth, J.O., Andersen, O.S., Brahm, J., Bjerrum, P.J. & Borders, C.L. 1982. Chloride-bicarbonate exchange in red blood cells: physiology of transport and chemical modification of binding sites. Phil Trans R Soc Lond B 299, 383-399.
106. 2 affinity. Neth J Sea Res 7, 328-338.
107. Wyman, J. 1964. Linked functions and reciprocal effects in haemoglobin: a second look. Adv Prot Chem 19, 223-286.
108. Zhang, D., Kiyatkin, A., Bolin, J.T. & Low, P.S. 2000. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 96, 2925-2933.