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012298 Respiratory Function of Hemoglobin

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012298 Respiratory Function of Hemoglobin MECHANISMS OF DISEASE Review Article Mechanisms of Disease resulting standard P50 (normally, 26.3 mm Hg in adults at sea level) is useful in detecting abnormali- ties in the affinity of hemoglobin for oxygen result- F RANKLIN H. EPSTEIN, M.D., Editor ing from hemoglobin variants or from disease. However, the important physiologic effects are de- termined by the in vivo P50, which changes rapidly RESPIRATORY FUNCTION in response to changes in body temperature, carbon dioxide tension, and pH. In vivo P can be estimat- OF HEMOGLOBIN 50 ed from standard P50 by applying appropriate correc- tions to the Hill equation5,6 or by using a computer CONNIE C.W. HSIA, M.D. subroutine.7 Structure–Function Relations EMOGLOBIN is essential for oxygen trans- Normal adult hemoglobin (molecular weight, port, and the study of its structure and 64,500) consists of two a and two b polypeptide function has led to numerous discoveries chains, each bound to a heme group. Each heme H 1 that have shaped modern biologic science. This re- group contains a porphyrin ring and a ferrous atom view will examine how hemoglobin actively regulates capable of reversibly binding one oxygen molecule.4 oxygen transport and will illustrate the clinical and The globin units of deoxyhemoglobin are tightly physiologic importance of this regulation. held by electrostatic bonds in a tense (T) conforma- tion with a relatively low affinity for oxygen. Binding OXYHEMOGLOBIN DISSOCIATION CURVE of oxygen imposes chemical and mechanical stresses The oxyhemoglobin dissociation curve describes that break these electrostatic bonds, leading to a the relation between the oxygen saturation or con- relaxed (R) conformation in which the remaining tent of hemoglobin and the oxygen tension at equi- binding sites become more exposed and have an af- librium. Bohr2,3 first showed that the dissociation finity for oxygen that is 500 times as high as when curve was sigmoid-shaped, leading Hill4 to postulate the molecule is in the T conformation.8 Conforma- that there were multiple oxygen-binding sites on he- tional changes lead to cooperativity among binding moglobin and to derive an empirical approximation sites, so that binding of one oxygen molecule to of the relation: deoxyhemoglobin increases the oxygen affinity of n the remaining binding sites on the same hemoglo- oxygen tension ϭ oxygen saturation ------------------------------------- ---------------------------------------------------------- bin molecule. Thus, the binding curve assumes a sig- P50 100– oxygen saturation moid shape, reflecting the transition from low to where P50 is the oxygen tension (in millimeters of high affinity as more binding sites become occu- mercury) when the binding sites are 50 percent sat- pied.4 This cooperativity during oxygen transport urated. Within the range of saturation between 15 provided the first clear insight into how an allosteric and 95 percent, the sigmoid shape of the curve can 9 ϭ enzyme regulates a metabolic pathway. The proper- be described by the Hill coefficient (n 2.7; range, ties of an allosteric protein include multiple interact- 2.4 to 2.9), and its position along the oxygen-ten- ing binding sites, reversible noncovalent binding to sion axis can be described by the P50, which is in- a primary ligand, quaternary conformational chang- versely related to the binding affinity of hemoglobin es induced by ligand binding (homotropic effects), for oxygen. The P50 can be estimated by measuring and modulation of ligand binding by secondary ef- the oxygen saturation of blood equilibrated to dif- fectors (heterotropic effects).10 The major hetero- ferent levels of oxygen tension, correcting to stand- tropic effectors of hemoglobin are hydrogen ion, car- ard conditions (37°C, pH 7.40, and carbon dioxide bon dioxide, and red-cell 2,3-bisphosphoglycerate. tension of 40 mm Hg), and fitting the results to a straight line in logarithmic form to solve for P50. The Hydrogen Ion and Oxygen–Carbon Dioxide Coupling Adding hydrogen ion or carbon dioxide to blood reduces the oxygen-binding affinity of hemoglobin; this is known as the Bohr effect (Fig. 1A).3 Con- From the Department of Medicine, University of Texas Southwestern versely, oxygenation of hemoglobin reduces its affin- Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9034, where reprint requests should be addressed to Dr. Hsia. ity for carbon dioxide; this is known as the Haldane ©1998, Massachusetts Medical Society. effect (Fig. 1B).11 These effects arise from interac- Volume 338 Number 4 ؒ 239 Downloaded from www.nejm.org on November 8, 2006 . Copyright © 1998 Massachusetts Medical Society. All rights reserved. The New England Journal of Medicine can also directly stabilize the T conformation (the pH carbon dioxide Bohr effect). Deoxyhemoglobin, in Lung turn, increases the uptake of carbon dioxide by fa- voring the formation of bicarbonate and carbamino- pH hemoglobin (the Haldane effect).13-15 About 80 per- Tissue cent of the output of carbon dioxide from tissue is transported as bicarbonate, 10 percent as carbami- nohemoglobin, and 10 percent in physical solu- tion.16,17 As blood passes through the tissue capillaries, the or Content (ml/dl) uptake of carbon dioxide by red cells raises the oxy- Oxygen Saturation (%) gen tension of oxyhemoglobin at a given oxygen sat- uration by means of the Bohr effect, thereby facil- itating the unloading of oxygen (Fig. 1A, tissue A Oxygen Tension (mm Hg) arrow). The unloading of oxygen lowers the carbon dioxide tension inside the red cells at a given carbon dioxide content by means of the Haldane effect, thereby facilitating the uptake of carbon dioxide (Fig. Tissue 1B, tissue arrow). The reverse occurs in pulmonary Deoxyhemoglobin capillaries, as illustrated by the opposite directions of the corresponding lung arrows in Figure 1. These rapid interactions between the Bohr and Haldane ef- Oxyhemoglobin fects promote the optimal transport of both oxygen and carbon dioxide by red cells, particularly during exercise. The net effects are to maximize the differ- ence in oxygen content between arterial and venous blood and to minimize both the difference in car- Lung bon dioxide tension between arterial and venous blood and tissue acidosis. Up to 40 percent of the Carbon Dioxide Content (ml/dl) exchange of carbon dioxide in the tissues and 20 percent of the exchange of oxygen in the tissues can B Carbon Dioxide Tension (mm Hg) be attributed to these coupled oxygen–carbon diox- 13 Figure 1. Reciprocal Interactions between Oxygen and Carbon ide transport mechanisms. Dioxide Binding to Hemoglobin. Red-Cell 2,3-Bisphosphoglycerate Panel A shows the Bohr effect: binding of carbon dioxide to hemoglobin reduces the pH and the binding affinity of hemo- Red-cell metabolism depends solely on glycolysis, globin for oxygen, leading to a higher P50. Panel B shows the and 2,3-bisphosphoglycerate is a normal metabol- Haldane effect: binding of oxygen to hemoglobin reduces its ic intermediate (Fig. 3). Usually, 1,3-bisphospho- binding affinity for carbon dioxide, leading to a rightward shift of the carbon dioxide dissociation curve. These interactions glycerate is converted to 3-phosphoglycerate, pro- work in opposite directions in the lungs and peripheral tissues ducing one ATP molecule. 1,3-Bisphosphoglycerate to maximize the difference in arteriovenous oxygen content can also be converted to 2,3-bisphosphoglycerate by (Panel A) and minimize the difference in arteriovenous carbon bisphosphoglycerate synthase through a minor path- dioxide tension (Panel B). way without producing ATP. In most cells, the con- centration of 2,3-bisphosphoglycerate is very low, because of potent feedback inhibition of bisphos- phoglycerate synthase. However, in red cells, 2,3-bis- phosphoglycerate becomes sequestered by binding tions among oxygen, hydrogen ion, and carbon di- to deoxyhemoglobin; without the normal inhibi- oxide bound to different sites on hemoglobin. In tion, 2,3-bisphosphoglycerate accumulates in high the tissue capillaries, carbon dioxide can diffuse as a concentrations.18 dissolved gas, bind to the a-amino terminus of the The binding of 2,3-bisphosphoglycerate in an globin chain as carbaminohemoglobin, or be hy- electrically charged pocket between the b chains of drated by the action of carbonic anhydrase to form hemoglobin stabilizes the T conformation and re- bicarbonate (Fig. 2). The hydrogen ions released by duces its affinity for oxygen.4,18 The binding of 2,3- the latter two reactions bind to specific amino acid bisphosphoglycerate also lowers the intracellular pH residues on the globin chain to stabilize the T con- and further enhances the Bohr effect. The P50 in- formation and facilitate the release of oxygen (the creases directly with the 2,3-bisphosphoglycerate con- acid Bohr effect).4,12 Carbaminohemoglobin itself centration,19 which increases whenever the availabil- January 22, 1998 ؒ 240 Downloaded from www.nejm.org on November 8, 2006 . Copyright © 1998 Massachusetts Medical Society. All rights reserved. MECHANISMS OF DISEASE Red Cell Tissue CO2 ϩ CO2 H2O Carbonic anhydrase O2 CO2 Carbamino- Hb–O ϩ ϩ H2CO3 2 Hb H Ϫ ϩ ϩ HCO3 H CIϪ ϩ H O2 ϩ Hb–O2 Hb–H Figure 2. Coupled Oxygen and Carbon Dioxide Transport within the Red Cell. In the peripheral tissues, the uptake of carbon dioxide by red cells and chemical reactions with hemo- globin facilitate the release of oxygen from hemoglobin. Hb denotes hemoglobin. ity of oxygen is diminished (as in hypoxia or anemia) 37°C), the true in vivo oxygen tension is approxi- or the flux through glycolysis is stimulated (as in al- mately 20 percent higher (72 mm Hg). The same kalosis). The 2,3-bisphosphoglycerate concentration measurement in a patient with hypothermia (tem- is reduced in aging red cells and under conditions of perature, 33°C) corresponds to an in vivo oxygen hyperoxia or inhibition of glycolysis (by acidosis or tension of approximately 48 mm Hg. The carbon di- hypophosphatemia).
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