Erythrocyte Metabolism and Enzyme Defects
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1 CE UPDATE HEMATOLOGY I Karen A. B r o w n, M S, MT(ASCP) Erythrocyte Metabolism and Enzyme Defects Red blood cells circulate for approximately 120 days without nuclei or cytoplasmic organelles. Components needed for function and survival already are present when erythrocytes reach maturity. Red blood cells therefore are capable of limited metabolic activity. Fortunately, these erythrocytic processes do not require the consumption of much energy. The major role of red cells in binding, transporting, and releasing oxygen and carbon dioxide is a passive activity that uses, not consumes, these gases. The erythrocyte's limited metabolic processes, which include the Embden-Meyerhof pathway and the hexose monophosphate shunt, provide energy to accomplish several of the cell's functions. When these processes do not function properly, several clinical and hematologic changes occur. Although problems may appear in any of a number of metabolic reactions in the red blood cell, enzyme defects are the most significant. The concentrations and activities of the enzymes that catalyze the necessary reactions are essential for overall survival of the erythrocyte. Red blood cells cannot compensate for enzyme imperfections and cannot synthesize new enzymes to replace those that become exhausted during the cell's lifetime. The complement of enzymes present in each red blood cell forms in nucleated precursors and, to a limited degree, in reticulocytes.1 Glucose is the major energy source for the red blood cell. Mature erythrocytes, however, lack the oxidative enzymes present in mitochondria of most other cells. Red blood cells cannot depend on aerobic glycolysis, as in the Kreb's cycle, to extract energy from glucose. They therefore use the Embden-Meyerhof pathway (Figure) to anaerobically process glucose into usable energy, or adenosine triphosphate (). ABSTRACT Erythrocytes rely on metabolic processes to maintain cellular shape andflexibilityand to keep essential constituents in reduced, active form. When these processes do not function properly, problems may occur in a number of reactions in a metabolic pathway. Enzyme defects have been associated with each of the major erythrocyte metabolic processes, although not all enzymopathies are associated with hematologic problems inpatients. Common enzyme defects include pyruvate kinase and glucose-6-phosphate dehydrogenase deficiencies. Other defects impair the red blood cell's ability to reduce oxidants and preserve heme iron in afunctional state. Enzymes involved in catalyzing reactions of nucleotide metabolism also have been associated with defects. This is the first in a two-part continuing education series on hematology. By the end of the series, the reader will be able to identify the major metabolic pathways of erythrocytes and identify disorders of anaerobic glycolysis, including pyruvate kinase deficiency, glucose-6-phosphate dehydrogenase deficiency, and disorders of nucleotide metabolism. 0 0 o In addition to production, the EmbdenMeyerhof pathway maintains pyridine nucleotides in a reduced state. Nicotinamide adenine dinucleotide (NAD) is reduced two times in the pathway. The first reduction occurs as NAD is a coenzyme with glyceraldehyde-3-phosphate dehydrogenase in forming 1,3-diphosphoglycerate (1,3-DPG). Then, reduced NAD (NADH), along with lactate dehydrogenase, catalyzes the conversion of pyruvate to lactate. An offshoot of the Embden-Meyerhof pathway is the Luebering-Rapaport bypass. This pathway provides 2,3-diphosphoglycerate (2,3-DPG), an important regulator of the oxygen-carrying capacity of red blood cells. The 2,3-DPG alternate route does not yield, but does modulate levels of 2,3-DPG. Erythrocyte 2,3-DPG concentration is especially sensitive to ph because the enzymes catalyzing its production are inhibited or stimulated by hydrogen ions.1 From Medical Laboratory Sciences Program, Department of Pathology, University of Utah, Salt Lake City. Reprint requests to Ms Brown, Medical Laboratory Sciences Program, Department of Pathology, University of Utah, 50 N Medical Center Dr, Salt Lake City, Utah LABORATORY MEDICINE 329 6
2 The EmbdenMeyerhof pathway. indicates adenosine triphosphate;, adenosine diphosphate; NAD, nicotinamide adenine dinucleotide; NADH, reduced nicotinamide adenine dinucleotide. Defects in the Luebering-Rapaport bypass can affect the levels of 2,3-DPG available to erythrocytes. Red blood cell 2,3-DPG regulates oxygen release depending on the needs of tissues. Whenever the peripheral tissues have an increased amount of deoxygenated blood (deoxyhemoglobin), glycolysis is stimulated and 2,3DPG levels rise. Again, ph changes within the cell probably contribute to this process. The result is that 2,3-DPG attaches to deoxyhemoglobin and causes hemoglobin to resist binding to oxygen. This decrease in oxygen affinity by hemoglobin increases oxygen release to tissues. Red blood cells are capable of limited aerobic glycolysis through the hexose monophosphate shunt, also called the phosphogluconate pathway or the pentose phosphate shunt. The major role of the hexose monophosphate shunt, however, is not the oxidative metabolism of glucose, but rather the generation of reduced nicotinamide adenine dinucleotide phosphate (NH). Erythrocyte NH converts oxidized glutathione to reduced glutathione, the major red blood cell antioxidant. Red blood cell enzymes, and especially hemoglobin, are protected from oxidant damage through the action of glutathione, which maintains hemoglobin in a reduced, active form. Although oxidants are damaging to cells, cells commonly produce them. Macrophages, for example, produce them in response to infection. Erythrocytes even produce r Hexokinase Glucose Hexose Monophosphate Shunt - ^ Glucose-6-phosphate them when certain drugs are present. If the level of reduced glutathione is not sufficient to neutralize intracellular red blood cell oxidants, globin will denature and precipitate as Heinz bodies, ultimately producing membrane damage. The levels of nicotinamide adenine dinucleotide phosphate (N)/NH regulate the amount of glucose metabolized by the hexose monophosphate shunt. As NH generates reduced glutathione, N is produced, which stimulates glucose metabolism in the hexose monophosphate shunt. This mechanism arms the red blood cell with more reducing capability during an oxidative challenge. Finally, an important auxiliary process of erythrocyte metabolism is the methemoglobin reductase pathway. This pathway maintains heme iron in the reduced, or active state (ferrous). The methemoglobin reductase pathway requires reduced pyridine nucleotides generated from the Embden-Meyerhof pathway. Unlike the hexose monophosphate shunt, which provides a mechanism for preventing the denaturation of the globin component of hemoglobin, the methemoglobin reductase pathway ensures that the iron (heme) in the hemoglobin molecule does not become oxidized. Methemoglobin with iron in the ferric state is useless as an oxygen carrier. This pathway uses the enzyme methemoglobin reductase and NAD to maintain hemoglobin in a reduced state. Further detail regarding Glucophosphate isomerase - Phosphofructokinase Fructose-6-phosphate 7V Fructose 1,6-diphosphate Aldolase Phosphoglycerate kinase 3-phosphoglycerate - < y^ Enolase 1,3-diphosphoglycerate -< Glvceraldehyde-3-phosphate dehydrogenase! - ^ NADH _A y Pyruvate kinase TT 7^ Lactate Pyruvate / Methemoglobin Reductase Pathway Luebering-Rapaport Bypass Phosphoenolpyruvate NAD dehydrogenase 7^ "TV NADH NAD LABORATORY MEDICINE May Lactate Glyceraldehyde-3-phosphate
3 biochemical pathways and metabolic processes can be found in the suggested readings listed at the end of this article. Enzyme Defects Defects in red blood cell enzymes can be classified as a general group of disorders called the inherited hemolytic anemias. An inherited hemolytic anemia occurs when an intrinsic cellular defect increases the occurrence of erythrocyte destruction. This category includes not only hereditary enzyme defects, but also inherited erythrocyte membrane disorders and qualitative and quantitative hereditary hemoglobin abnormalities. Some inherited conditions result in hematologic manifestations other than a hemolytic process. One example is a deficiency in the enzyme ribose-phosphate pyrophosphokinase, which causes a megaloblastic anemia.2 Enzyme defects have been associated with each of the erythrocyte's major metabolic pathways, although not all enzyme deficiencies are associated with hematologic problems in patients or with decreased red blood cell survival. Several inherent flaws are significant, however, such as defects in the Embden-Meyerhof pathway that compromise the erythrocyte's ability to circulate in a structurally stable form. The erythrocyte's shape and flexibility depend on a reliable energy source. The mature, resting erythrocyte often is described as a biconcave disc, somewhat like a rubber ball indented simultaneously on the top and the bottom. This shape facilitates the transportation of oxygen and carbon dioxide because it allows the small red blood cell to maximize its entire surface area. The biconcavity and structural integrity of the erythrocyte results from the lipids and proteins that comprise the cellular membrane. The proteins form a framework and contractile network for the erythrocyte, maintaining the classic shape of the cell as well as allowing the cell to squeeze and deform as it negotiates small passages within the circulation. Essential to erythrocyte's survival is this ability to easily undergo shape changes and squeeze through the microcirculation. Flexibility depends on the membrane's composition and structure as well as on the fluidity of hemoglobin within the cell. The red cell is supple; its pliability might be compared with that of a water balloon. The erythrocyte is able to adjust to vessel size while still maintaining a stable surface-to-volume ratio. Major changes in this ratio result in a less-flexible cell that cannot survive sheer forces and small spaces as it circulates. Red blood cells that have lost their deformability may assume many appearances on a stained peripheral blood smear, including spherocytes, schistocytes, and various other poikilocytes. Cells that do not survive contribute to a hemolytic event. The red blood cell also must be able to preserve high potassium, low calcium, and low sodium levels, intracellularly, against an external concentration gradient of low potassium, high calcium, and high sodium levels. Pumping these molecules requires energy. Cells that cannot energize the metabolic pumps have uncontrolled cation flux and will not survive normally. For example, increased intracellular sodium without a corresponding decrease in potassium results in cellular swelling and eventual lysis as the cell literally drinks water; decreased potassium with no associated sodium increase may cause cells to shrink. In addition, calcium is important in regulating and stabilizing membrane phospholipids.3 High levels of intracellular calcium also cause inflexibility of the erythrocyte. General clinical findings in patients with an inherited enzyme abnormality include symptoms of a hemolytic process, such as jaundice and hemoglobinuria. The medical laboratory plays an important role in the investigation of enzyme defects associated with the various metabolic activities of erythrocytes, especially through hematologic evaluation of the hemolytic presentation. Pyruvate Kinase Deficiency Pyruvate kinase (PK) is the most common deficiency discovered for the EmbdenMeyerhof pathway. The term hereditary nonspherocytic hemolytic anemia has been used to describe this and similar disorders in which no erythrocyte abnormalities, and specifically no spherocytosis, can be detected on the stained peripheral blood smear. Pyruvate kinase plays a critical role in the formation of pyruvate from phosphoenolpyruvate (PEP) with the simultaneous generation of from (adenosine diphosphate). Red blood cells deficient in pyruvate kinase cannot produce enough energy to maintain normal membrane function. Potassium and water leak from the cell, while calcium concentrations increase. The cell becomes rigid, loses flexibility, and is susceptible to early splenic sequestration and eventual hemolysis. Fortunately, PK defects are rare. Deficiencies are inherited as autosomal recessive traits, so Test Your Knowledge Look for the CE Update exam on Hematology (603) in the June issue of Laboratory Medicine. Participants will earn 2 CMLE credit hours. LABORATORY MEDICINE
4 both sexes are affected equally. Individuals heterozygous for the enzyme defect are clinically normal because they are able to produce some ; homozygotes will display signs and symptoms of a hemolytic process. Pyruvate kinase defects have been documented worldwide, although the majority of cases have been identified in people of Northern European ancestry.4 Although the first cases of PK deficiencies were described in 1961, molecular studies have defined structural mutations of the PK-L gene as the cause of this enyzmopathy. The majority of these mutations result in amino acid substitutions.5 The age of onset and clinical features of PK deficiency vary widely. The disorder may be detected in infancy or early childhood, although mild deficiencies may not be discovered until adulthood. Some infants may have such severe hemolytic episodes that exchange transfusion is required, while others experience no symptoms. The clinical features manifested in any patient depend on the severity of the hemolytic process and on the extent of the resulting anemia. Clinical findings usually include jaundice, splenomegaly, intermittent passage of dark urine, gallstones, and the signs of a mild to moderate anemia. The laboratory diagnosis of a PK deficiency depends on specialized procedures and a quantitative enzyme assay because routine hematologic methods yield only nonspecific results. Hematocrit values range from 18% to 36%. 6 Erythrocytes are normocytic, normochromic, but may be slightly macrocytic when reticulocytosis is prominent. An elevated reticulocyte count is a classic finding in any hemolytic anemia. Although no prominent morphologic abnormalities are present, polychromasia, poikilocytosis and nucleated red cells may be observed. Again, no spherocytes will be noted. Leukocyte and platelet counts usually are normal. A negative direct antiglobulin test is important in distinguishing this disorder from an immune hemolytic anemia. Chemistry tests usually will demonstrate a moderately elevated unconjugated serum bilirubin, decreased haptoglobin, lactate, and pyruvate levels, and increased 2,3-DPG and PEP concentrations. The lack of PK causes a block in the Embden-Meyerhof pathway, and 2,3-DPG and LABORATORY MEDICINE VOLUME 26, NUMBER 5 PEP will accumulate. The increase in 2,3-DPG becomes significant because it allows erythrocytes to release oxygen more easily to tissues as a compensatory mechanism for the developing hemolytic anemia. One screening procedure is the fluorescent spot test.3 Recall that PK catalyzes the formation of pyruvate from PEP. The reduction of NADH to NAD and production of from also occurs. In the fluorescent spot test, erythrocytes are incubated in PEP, NADH, and lactate dehydrogenase (LD). As pyruvate is produced, it is exposed to NADH and LD and eventually is converted to lactate. NADH is fluorescent under ultraviolet light. Red blood cells deficient in PK will not be able to generate pyruvate, so NADH will not be reduced. Persistence of the fluorescent NADH indicates a PK defect. White blood cells also contain PK that can catalyze this reaction, so all leukocytes must be completely removed before the test is begun. Also, patients who have recently received transfusions have normal donor cells that may mask PK-deficient erythrocytes. Any positive screening procedure should be confirmed using a specific PK quantitative assay. The principle of the PK assay also is based on the fluorescent properties of NADH. The same constituents are mixed as in the spot test. The endpoint, however, is not a visual observation of fluorescence, but rather is the spectrophotometrically measured change in absorbance of the reaction mixture, which can be used to quantitate PK activity. Because PK deficiency is an inherited disorder, no cure exists. Splenectomy has been useful in patients who depend on transfusion. Reticulocytes become more pronounced in individuals who have undergone splenectomy. Pyruvate kinase activity generally is greater in reticulocytes than in mature red blood cells; this may explain the appearance of hemolytic anemia in patients with normal enzyme levels.7 Recent studies have explored the possibility of curing PK deficiency with gene therapy. 8 Although several problems still need to be addressed, researchers are studying molecular intervention in treatment protocols for this and many of the inherited enzymopathies. The development of molecular studies furthermore provides an opportunity for prenatal diagnosis in families affected by a PK deficiency. Elevated enzyme levels have been identified as a source of polycythemia. Increases in the amount of cellular PK result in decreases in 2,3-DPG concentrations. This triggers tissue hypoxia because
5 hemoglobin is reluctant to release oxygen. Red blood cell and hemoglobin production increase as a compensatory mechanism. Two processes have been proposed for this unusual defect. One possibility resides in an abnormality in the coding region of the gene. The other proposed mechanism is that the cell retains a type of PK, normally not present in mature erythrocytes, causing elevated enzyme levels.9 In rare cases, high levels of PK have been associated with hemolytic anemia. Hematologic manifestations resulted from the inheritance of a functionally abnormal enzyme.9 Other Disorders of Anaerobic Glycolysis Researchers have identified many other erythrocyte enzyme abnormalities in the EmbdenMeyerhof pathway, although these abnormalities are much less common than PK deficiency. These include disorders involving hexokinase, glucose phosphate isomerase, phosphoglycerate kinase, phosphofructose kinase, aldolase, and triosephosphate isomerase, to mention a few.10 Various studies using recombinant DNA technology have greatly expanded the molecular information now available for many of these enzymes and have defined enzyme defects at the nucleotide level.11 The inheritance pattern is autosomal recessive for all of these abnormalities with the exception of phosphoglycerate kinase deficiency, which is sexlinked. Again, the erythrocyte morphology as seen on stained peripheral blood smears is unremarkable in these uncommon enzyme defects. It is interesting to note that although these disorders most often are associated with a nonspherocytic hemolytic anemia, at times nonhematologic features may be the only indicator of an enzyme deficiency. For instance, patients with a phosphofructose abnormality may have an associated muscle glycogen storage disease without any symptoms of a hemolytic episode. Serious neuromuscular disease almost always is present in individuals with triosephosphate isomerase deficiency. Complications such as this can be very severe; most patients deficient in triosephosphate isomerase die in their first decade of life.12 Conclusion Defects in erythrocytic enzymes result in hemolysis in some cases, although even more severe deficiencies of the same enzyme cause no clinical features. Such variety of clinical manifestations may depend on how different genetic mutants are expressed in various tissues. 9 Multiple isoenzymes, encoded by separate genes, may contribute to the severity of an enzyme deficiency and indicate whether that deficiency will result in hematologic or nonhematologic symptoms. The major consequence of a PK deficiency, for instance, is hemolytic anemia; PK has isoenzymes present in varying proportions in erythrocytes and other cells. On the other hand, triosephosphate isomerase has no isoenzymes, but a deficiency usually results in a fatal neurological disease.13 Future molecular research may define the connection between clinical or laboratory manifestations of an enzymopathy and the genetic basis of the abnormality References 1. Beutler E. Energy metabolism and maintenance of erythrocytes. In: Williams WJ, Beutler E, Erslev A, Lichtman M, eds. Hematology. 4th ed. New York, NY: McGraw-Hill; 1990: Valentine WN, Paglia DE. Erythrocyte enzymopathies, hemolytic anemia, and multisystem disease: an annotated review. Blood. 1984; 64: Lotspeich-Steininger CA, Stiene-Martin EA, Koepke J, eds. Clinical Hematology Principles, Procedures, Correlations. Philadelphia, Pa: JB Lippincott; 1992: Department of Medicine, Hammersmith Hospital, London. Pyruvate kinase deficiency. Association with G6PD deficiency. BMJ. 1992;305: Lenzner C, Nurnberg P, Thiele BJ, et al. Mutations in the pyruvate kinase L gene in patients with hereditary hemolytic anemia. Blood. 1994;83: Brown BA. Hematology Principles and Procedures. 6th ed. Philadelphia, Pa: Lea & Febiger; 1993: Beutler E, Forman L, Rios-Larrain E. Elevated pyruvate kinase activity in patients with hemolytic anemia due to red cell pyruvate kinase "deficiency." Am]Med. 1987;83: Tani K, Yoshikubo T, Ikebuchi K, et al. Retrovirus-mediated gene transfer of human pyruvate kinase (PK) cdna into murine hematopoietic cells: implications for gene therapy of human PK deficiency. Blood. 1994;83: Beutler E. Red cell enzyme defects. Hematol Pathol. 1990; 4: Valentine WN, Tanaka KR, Paglia DE. Hemolytic anemias and erythrocyte enzymopathies. Ann Intern Med. 1985; 103: Fujii H, Miwa S. Recent progress in the molecular genetic analysis of erythroenzymopathy. Am J Hematol. 1990;34: Williams WJ, Beutler E, Erslev A, Lichtman M, eds. Hematology. 4th ed. New York, NY: McGraw-Hill; 1990: Luzzatto L. Hemolytic anemias due to enzyme deficiencies. SchweizMed Wochenschr Suppl. 1991;43: Suggested Readings Montgomery R. Biochemistry: A Case-Oriented Approach. 5th ed. St Louis, Mo: CV Mosby; Murray R, Granner D, Mayes P, Rodwell V. Harpers's Biochemistry. 22nd ed. Conn.: Appleton and Lange; Saleem A. Hereditary hemolytic anemias associated with erythrocytic enzymopathies. In Bick RL, Bennett JM, Brynes RK eds. Hematology Clinical and Laboratory Practice, vol 1, St Louis, Mo: CV. Mosby, Stryer L. Biochemistry. 3rd ed. New York, NY: WH Freeman; LABORAT
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