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. 1992 May;88(2):269–274. doi: 10.1111/j.1365-2249.1992.tb03072.x

Intracellular hydrogen peroxide production by peripheral phagocytes from diabetic patients. Dissociation between polymorphonuclear leucocytes and monocytes.

M Noritake 1, Y Katsura 1, N Shinomiya 1, M Kanatani 1, Y Uwabe 1, N Nagata 1, S Tsuru 1
PMCID: PMC1554292  PMID: 1572091

Abstract

Although the standard assays for reactive oxygen species have been based on the measurement of those released into the extracellular environment, the microbicidal capacity to the engulfed microorganisms is mainly dependent on those released into the intracellular environment, such as phagosomes. We studied intracellular oxidative activities of individual phagocytes by dichlorofluorescein (DCFH) oxidation assay to investigate the relationship between the reactive oxygen species released intracellularly and the impaired microbicidal capacity in diabetic patients. Time courses of intracellular production of hydrogen peroxide by polymorphonuclear leucocytes (PMNL) and monocytes were observed at the resting condition and after the stimulation with phorbol myristate acetate (PMA; 160 nM) by flow cytometry. Thirty-four patients with non-insulin-dependent diabetes mellitus (NIDDM) and 23 age-matched healthy volunteers were subjected to the studies. PMNL from patients with NIDDM showed a significantly decreased capacity to produce hydrogen peroxide after the stimulation (P less than 0.05 at 15 min, P less than 0.01 at 30 and 45 min). By contrast, intracellular hydrogen peroxide production by monocytes at the resting condition and an early stimulatory phase (8 min after the stimulation) was significantly (P less than 0.01) enhanced in patients with NIDDM compared with that in controls. Both the changes of intracellular hydrogen peroxide production observed in PMNL and monocytes from patients with NIDDM were in association with an increased haemoglobin Alc level in erythrocytes, but did not relate to total cholesterol and triglyceride levels in the serum. The possible mechanisms of these dissociated changes in hydrogen peroxide producing capacity of phagocytes from patients with NIDDM are discussed.

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Selected References

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  1. Babior B. M. Oxygen-dependent microbial killing by phagocytes (first of two parts). N Engl J Med. 1978 Mar 23;298(12):659–668. doi: 10.1056/NEJM197803232981205. [DOI] [PubMed] [Google Scholar]
  2. Baehner R. L., Johnston R. B., Jr Monocyte function in children with neutropenia and chronic infections. Blood. 1972 Jul;40(1):31–41. [PubMed] [Google Scholar]
  3. Bass D. A., Parce J. W., Dechatelet L. R., Szejda P., Seeds M. C., Thomas M. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol. 1983 Apr;130(4):1910–1917. [PubMed] [Google Scholar]
  4. Brownlee M., Vlassara H., Cerami A. Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann Intern Med. 1984 Oct;101(4):527–537. doi: 10.7326/0003-4819-101-4-527. [DOI] [PubMed] [Google Scholar]
  5. Esmann V. The diabetic leukocyte. Enzyme. 1972;13(1):32–55. [PubMed] [Google Scholar]
  6. Gilcrease M. Z., Hoover R. L. Activated human monocytes exhibit receptor-mediated adhesion to a non-enzymatically glycosylated protein substrate. Diabetologia. 1990 Jun;33(6):329–333. doi: 10.1007/BF00404635. [DOI] [PubMed] [Google Scholar]
  7. Hiramatsu K., Arimori S. Increased superoxide production by mononuclear cells of patients with hypertriglyceridemia and diabetes. Diabetes. 1988 Jun;37(6):832–837. doi: 10.2337/diab.37.6.832. [DOI] [PubMed] [Google Scholar]
  8. Hostetter M. K. Handicaps to host defense. Effects of hyperglycemia on C3 and Candida albicans. Diabetes. 1990 Mar;39(3):271–275. doi: 10.2337/diab.39.3.271. [DOI] [PubMed] [Google Scholar]
  9. Johnston R. B., Jr, Lehmeyer J. E., Guthrie L. A. Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. J Exp Med. 1976 Jun 1;143(6):1551–1556. doi: 10.1084/jem.143.6.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kador P. F. The role of aldose reductase in the development of diabetic complications. Med Res Rev. 1988 Jul-Sep;8(3):325–352. doi: 10.1002/med.2610080302. [DOI] [PubMed] [Google Scholar]
  11. Kirstein M., Brett J., Radoff S., Ogawa S., Stern D., Vlassara H. Advanced protein glycosylation induces transendothelial human monocyte chemotaxis and secretion of platelet-derived growth factor: role in vascular disease of diabetes and aging. Proc Natl Acad Sci U S A. 1990 Nov;87(22):9010–9014. doi: 10.1073/pnas.87.22.9010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kitagawa S., Takaku F., Sakamoto S. A comparison of the superoxide-releasing response in human polymorphonuclear leukocytes and monocytes. J Immunol. 1980 Jul;125(1):359–364. [PubMed] [Google Scholar]
  13. Kitahara M., Eyre H. J., Lynch R. E., Rallison M. L., Hill H. R. Metabolic activity of diabetic monocytes. Diabetes. 1980 Apr;29(4):251–256. doi: 10.2337/diab.29.4.251. [DOI] [PubMed] [Google Scholar]
  14. Klebanoff S. J., Rosen H. The role of myeloperoxidase in the microbicidal activity of polymorphonuclear leukocytes. Ciba Found Symp. 1978 Jun 6;(65):263–284. doi: 10.1002/9780470715413.ch15. [DOI] [PubMed] [Google Scholar]
  15. Kobzik L., Godleski J. J., Brain J. D. Oxidative metabolism in the alveolar macrophage: analysis by flow cytometry. J Leukoc Biol. 1990 Apr;47(4):295–303. [PubMed] [Google Scholar]
  16. Lopes-Virella M. F., Klein R. L., Lyons T. J., Stevenson H. C., Witztum J. L. Glycosylation of low-density lipoprotein enhances cholesteryl ester synthesis in human monocyte-derived macrophages. Diabetes. 1988 May;37(5):550–557. doi: 10.2337/diab.37.5.550. [DOI] [PubMed] [Google Scholar]
  17. Ludwig P. W., Hunninghake D. B., Hoidal J. R. Increased leucocyte oxidative metabolism in hyperlipoproteinaemia. Lancet. 1982 Aug 14;2(8294):348–350. doi: 10.1016/s0140-6736(82)90546-3. [DOI] [PubMed] [Google Scholar]
  18. Miller J. A., Gravallese E., Bunn H. F. Nonenzymatic glycosylation of erythrocyte membrane proteins. Relevance to diabetes. J Clin Invest. 1980 Apr;65(4):896–901. doi: 10.1172/JCI109743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mohsenin V., Latifpour J. Respiratory burst in alveolar macrophages of diabetic rats. J Appl Physiol (1985) 1990 Jun;68(6):2384–2390. doi: 10.1152/jappl.1990.68.6.2384. [DOI] [PubMed] [Google Scholar]
  20. Rayfield E. J., Ault M. J., Keusch G. T., Brothers M. J., Nechemias C., Smith H. Infection and diabetes: the case for glucose control. Am J Med. 1982 Mar;72(3):439–450. doi: 10.1016/0002-9343(82)90511-3. [DOI] [PubMed] [Google Scholar]
  21. Robinson J. P., Bruner L. H., Bassoe C. F., Hudson J. L., Ward P. A., Phan S. H. Measurement of intracellular fluorescence of human monocytes relative to oxidative metabolism. J Leukoc Biol. 1988 Apr;43(4):304–310. doi: 10.1002/jlb.43.4.304. [DOI] [PubMed] [Google Scholar]
  22. Rossi F. The O2- -forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function. Biochim Biophys Acta. 1986 Nov 4;853(1):65–89. doi: 10.1016/0304-4173(86)90005-4. [DOI] [PubMed] [Google Scholar]
  23. Sasada M., Johnston R. B., Jr Macrophage microbicidal activity. Correlation between phagocytosis-associated oxidative metabolism and the killing of Candida by macrophages. J Exp Med. 1980 Jul 1;152(1):85–98. doi: 10.1084/jem.152.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shah S. V., Wallin J. D., Eilen S. D. Chemiluminescence and superoxide anion production by leukocytes from diabetic patients. J Clin Endocrinol Metab. 1983 Aug;57(2):402–409. doi: 10.1210/jcem-57-2-402. [DOI] [PubMed] [Google Scholar]
  25. Steigbigel R. T., Lambert L. H., Jr, Remington J. S. Phagocytic and bacterial properties of normal human monocytes. J Clin Invest. 1974 Jan;53(1):131–142. doi: 10.1172/JCI107531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tsuru S., Shinomiya N., Nomoto K. Depression of early protection against influenza virus infection by cyclophosphamide and its restoration by Y-19995 [2,4'-bis(1-methyl-2-dimethyl-aminoethoxyl)-3-benzoylpyridine dimaleate]. Nat Immun Cell Growth Regul. 1991;10(1):1–11. [PubMed] [Google Scholar]
  27. Vlassara H., Valinsky J., Brownlee M., Cerami C., Nishimoto S., Cerami A. Advanced glycosylation endproducts on erythrocyte cell surface induce receptor-mediated phagocytosis by macrophages. A model for turnover of aging cells. J Exp Med. 1987 Aug 1;166(2):539–549. doi: 10.1084/jem.166.2.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wierusz-Wysocka B., Wysocki H., Wykretowicz A., Szczepanik A., Siekierka H. Phagocytosis, bactericidal capacity, and superoxide anion (O2-) production by polymorphonuclear neutrophils from patients with diabetes mellitus. Folia Haematol Int Mag Klin Morphol Blutforsch. 1985;112(5):658–668. [PubMed] [Google Scholar]
  29. Zeller J. M., Rothberg L., Landay A. L. Evaluation of human monocyte oxidative metabolism utilizing a flow cytometric assay. Clin Exp Immunol. 1989 Oct;78(1):91–96. [PMC free article] [PubMed] [Google Scholar]

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