Red blood cell dysfunction in septic glucose-6-phosphate dehydrogenase-deficient mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 6 55-6, 2004, Pages

  Spolarics, Zoltán ^a   Condon, Michael R ^a   Siddiqi, Muhammad ^a   Machiedo, George W ^a   Deitch, Edwin A ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Band 3; Cecal ligation and puncture; Cell deformability; Elutriation; Glutathione; Inflammation

Indexed keywords

ACETYLCYSTEINE; ERYTHROCYTE BAND 3 PROTEIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; SPECTRIN;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CECUM; CECUM LIGATION; CECUM PUNCTURE; CONTROLLED STUDY; CYTOSKELETON; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE DISORDER; GENETIC POLYMORPHISM; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HEMOLYSIS; IMMUNOMODULATION; IN VIVO STUDY; INFECTION; INJURY; LIGATION; MEAN CORPUSCULAR HEMOGLOBIN; MOUSE; MOUSE MUTANT; MOUSE STRAIN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PUNCTURE; SEPSIS; STRAIN DIFFERENCE;

ANIMALS; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; DISEASE MODELS, ANIMAL; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTES; FEMALE; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUCOSEPHOSPHATE DEHYDROGENASE DEFICIENCY; MALE; MICE; MICE, MUTANT STRAINS; OXIDATIVE STRESS; SEPSIS;

EID: 2542485490     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.01085.2003     Document Type: Article

References (52)

1. Baker CC, Chaudry IH, Gaines HO, and Baue AE. Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94: 331-335, 1983.
2. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, and Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 90: 9285-9289, 1993.
3. Baskurt OK and Meiselman HJ. Activated polymorphonuclear leukocytes affect red blood cell aggregability. J Leukoc Biol 63: 89-93, 1998.
4. Baskurt OK, Temiz A, and Meiselman HJ. Red blood cell aggregation in experimental sepsis. J Lab Clin Med 130: 183-190, 1997.
5. Bateman RM, Jagger JE, Sharpe MD, Ellsworth ML, Mehta S, and Ellis CG. Erythrocyte deformability is a nitric oxide-mediated factor in decreased capillary density during sepsis. Am J Physiol Heart Circ Physiol 280: H2848-H2856, 2001.
6. Battistuzzi G, D'Urso M, Toniolo D, Persico GM, and Luzzatto L. Tissue-specific levels of human glucose-6-phosphate dehydrogenase correlate with methylation of specific sites at the 3′ end of the gene. Proc Natl Acad Sci USA 82: 1465-1469, 1985.
7. Beutler E. G6PD: population genetics and clinical manifestations. Blood Rev 10: 45-52, 1996.
8. Bosch FH, Werre JM, Schipper L, Roerdinkholder-Stoelwinder B, Huls T, Willekens FLA, Wichers G, and Halie MR. Determinants of red blood cell deformability in relation to cell age. Eur J Haematol 52: 35-41, 1994.
9. Bratosin D, Mazurier J, Tissier JP, Estaquier J, Huart JJ, Ameisen JC, Aminoff D, and Montreuil J. Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 80: 173-195, 1998.
10. Cappadoro M, Giribaldi G, O'Brien E, Turrini F, Mannu F, Ulliers D, Simula G, Luzzatto L, and Arese P. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92: 2527-2534, 1998.
11. Carrillo EH, Gordon LE, Richardson JD, and Polk HC. Free hemoglobin enhances tumor necrosis factor-α production in isolated human monocytes. J Trauma 52: 449-452, 2002.
12. Cavinato RA, Bastos KRB, Sardinha LR, Elias RM, Alvarez JM, and Lima MRD. Susceptibility of the different developmental stages of the asexual (schizogonic) erythrocyte cycle of Plasmodium chabaudi chabaudi to hyperimmune serum, immunoglobulin (Ig)G1, lgG2a and F(ab′)2 fragments. Parasite Immunol 23: 587-597, 2001.
13. Chiu DTY and Liu TZ. Free radical and oxidative damage in human blood cells. J Biomed Sci 4: 256-259, 1997.
14. Clark MR, Mohandas N, Shohet SB, Hoesch RM, and Rossi ME. Osmotic gradient ektacytometry-comprehensive characterization of red cell volume and surface maintenance. Blood 61: 899-910, 1983.
15. Commins LM, Loegering DJ, and Gudewicz PW. Effect of phagocytosis of erythrocytes and erythrocyte ghosts on macrophage phagocytic function and hydrogen peroxide production. Inflammation 14: 705-716, 1990.
16. Condon MR, Kim JE, Deitch EA, Machiedo GW, and Spolarics Z. Appearance of an erythrocyte population with decreased deformability and hemoglobin content following sepsis. Am J Physiol Heart Circ Physiol 284: H2177-H2184, 2003.
17. Dobbe JGG, Hardeman MR, Streekstra GJ, Strackee J, Ince C, and Grimbergen CA. Analyzing red blood cell-deformability distributions. Blood Cells Mol Dis 28: 373-384, 2002.
18. Dondorp AM, Angus BJ, Hardeman MR, Chotivanich KT, Silamut K, Ruangveerayuth R, Kager PA, White NJ, and Vreeken J. Prognostic significance of reduced red blood cell deformability in severe falciparum malaria. Am J Trop Med Hyg 57: 507-511, 1997.
19. Ebong S, Call D, Nemzek J, Bolgos G, Newcomb D, and Remick D. Immunopathologic alterations in murine models of sepsis of increasing severity. Infect Immun 67: 6603-6610, 1999.
20. Ebong SJ, Call DR, Bolgos G, Newcomb DE, Granger JI, O'Reilly M, and Remick DG. Immunopathologic responses to non-lethal sepsis. Shock 12: 118-126, 1999.
21. Giger U, Sticher B, Naef R, Burger R, and Lutz HU. Naturally occurring human anti-band 3 autoantibodies accelerate clearance of erythrocytes in guinea pigs. Blood 85: 1920-1928, 1995.
22. Heller AR, Groth G, Heller SC, Breitkreutz R, Nebe T, Quintel M, and Koch T. N-acetylcysteine reduces respiratory burst but augments neutrophil phagocytosis in intensive care unit patients. Crit Care Med 29: 272-276, 2001.
23. Hoffmann-Fezer G, Maschke H, Zeitler HJ, Gais P, Heger W, Ellwart J, and Thierfelder S. Direct in vivo biotinylation of erythrocytes as an assay for red cell survival studies. Ann Hematol 63: 214-217, 1991.
24. Jain M, Brenner DA, Cui L, Lim CC, Wang B, Pimentel DR, Koh S, Sawyer DB, Leopold JA, Handy DE, Loscalzo J, Apstein CS, and Liao R. Glucose-6-phosphate dehydrogenase modulates cytosolic redox status and contractile phenotype in adult cardiomyocytes. Circ Res 93: e9-e16, 2003.
25. Kasper ML, Miller WJ, and Jacob HS. G6PD-deficiency infectious haemolysis: a complement dependent innocent bystander phenomenon. Br J Haematol 63: 85-91, 1986.
26. Kayar E, Mat F, Meiselman HJ, and Baskurt OK. Red blood cell rheological alterations in a rat model of ischemia-reperfusion injury. Biorheology 38: 405-414, 2001.
27. Kletzien RF. Glucose-6-phosphate dehydrogenase: a housekeeping enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J 8: 174-181, 1994.
28. Langenfeld JE, Machiedo GW, Lyons M, Rush BFJ, Dikdan G, and Lysz TW. Correlation between red blood cell deformability and changes in hemodynamic function. Surgery 116: 859-867, 1994.
29. Liese AM, Siddiqi MQ, Siegel JH, Deitch EA, and Spolarics Z. Attenuated monocyte IL-10 production in glucose-6-phosphate dehydrogenase-deficient trauma patients. Shock 18: 18-23, 2002.
30. Liese AM, Siddiqi MQ, Siegel JH, Denny T, and Spolarics Z. Augmented TNF-α and IL-10 production by primed human monocytes following interaction with oxidatively modified autologous erythrocytes. J Leukoc Biol 70: 289-296, 2001.
31. Lineweaver H and Burk DJ. Determination of enzyme dissociation constants. J Am Chem Soc 56, 658-666, 1934.
32. Liu X and Spolarics Z. Methemoglobin is a potent activator of endothelial cells by stimulating IL-6 and IL-8 production and E-selectin membrane expression. Am J Physiol Cell Physiol 285: C1036-C1046, 2003.
33. Loegering DJ, Commins LM, Minnear FL, Gary LA, and Hill LA. Effect of Kupffer cell phagocytosis of erythrocytes and erythrocyte ghosts on susceptibility to endotoxemia and bacteremia. Infect Immun 55: 2074-2080, 1987.
34. Luzzatto L and Mehta A. Glucose 6 phosphate dehydrogenase deficiency. In: The Metabolic and Molecular Bases of Inherited Disease, edited by Scriver CR, Beaudet AL, Sly WS, and Valle D. New York: McGraw-Hill, 1995, p. 3367-3398.
35. Machiedo GW, Powell RJ, Rush BFJ, Swislocki NI, and Dikdan G. The incidence of decreased red blood cell deformability in sepsis and the association with oxygen free radical damage and multiple-system organ failure. Arch Surg 124: 1386-1389, 1989.
36. Nicol CJ, Zielenski J, Tsui LC, and Wells PG. An embryoprotective role for glucose-6-phosphate dehydrogenase in developmental oxidative stress and chemical teratogenesis. FASEB J 14: 111-127, 2000.
37. Nierman DM, Kalb TH, and Schechter CB. In vitro glycolysis of whole blood can detect primed neutrophils in septic ICU patients. Shock 3: 88-95, 1995.
38. Oka S, Kamata H, Kamata K, Yagisawa H, and Hirata H. N-acetyl-cysteine suppresses TNF-induced NF-κB activation through inhibition of IκB kinases. FEBS Lett 472: 196-202, 2000.
39. Picart C, Dalhaimer P, and Discher DE. Actin protofilament orientation in deformation of the erythrocyte membrane skeleton. Biophys J 79: 2987-3000, 2000.
40. Powell RJ, Machiedo GW, and Rush BFJ. Decreased red blood cell deformability and impaired oxygen utilization during human sepsis. Am Surg 59: 65-68, 1993.
41. Richard CA, Wilcox BD, and Loegering DJ. IgG-coated erythrocytes augment LPS-stimulated TNF-α secretion, TNF-α mRNA levels, and TNF-α mRNA stability in macrophages. Biochem Biophys Res Commun 271: 70-74, 2000.
42. Ruwende C and Hill A. Glucose-6-phosphate dehydrogenase deficiency and malaria. J Mol Med 76: 581-588, 1998.
43. Sanders S, Smith DP, Thomas GA, and Williams ED. A glucose-6-phosphate dehydrogenase (G6PD) splice site consensus sequence mutation associated with G6PD enzyme deficiency. Mutat Res 374: 79-87, 1997.
44. Seddon SV, Walker DM, Williams D, and Williams ED. The clonal organization of the squamous epithelium of the tongue. Cell Prolif 25: 115-124, 1992.
45. Shapiro MJ, Gettinger A, Corwin HL, Napolitano L, Levy M, Abraham E, Fink MP, MacIntyre N, Pearl RG, and Shabot MM. Anemia and blood transfusion in trauma patients admitted to the intensive care unit. J Trauma 55: 269-273, 2003.
46. Sloane PJ, Gee MH, Gottlieb JE, Albertine KH, Peters SP, Burns JR, Machiedo G, and Fish JE. A multicenter registry of patients with acute respiratory distress syndrome. Physiology and outcome. Am Rev Respir Dis 146: 419-426, 1992.
47. Spolarics Z. Endotoxemia, pentose cycle, and the oxidant/antioxidant balance in the hepatic sinusoid. J Leukoc Biol 63: 534-541, 1998.
48. Spolarics Z, Siddiqi M, Siegel JH, Garcia ZC, Stein DS, Ong H, Livingston DH, Denny T, and Deitch EA. Increased incidence of sepsis and altered monocyte functions in severely injured type A-glucose-6-phosphate dehydrogenase-deficient African American trauma patients. Crit Care Med 29: 728-736, 2001.
49. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27: 502-522, 1969.
50. Vincent JL, Baron JF, Reinhart K, Gattinoni L, Thijs L, Webb A, Meier-Hellmann A, Nollet G, and Peres-Bota D. Anemia and blood transfusion in critically ill patients. JAMA 288: 1499-1507, 2002.
51. Yang H, Vishnubhakat J, Wang H, Roth J, and Tracey K. Hemoglobin enhances MIF- and interleukin-1-mediated TNF release in murine macrophage-like RAW 264.7 cells. Shock 11: 83, 1999.
52. Zaets SB, Berezina TL, Morgan C, Kamiyama M, Spolarics Z, Xu DZ, Deitch EA, and Machiedo GW. Effect of trauma-hemorrhagic shock on red blood cell deformability and shape. Shock 19: 268-273, 2003.