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. 1995 Jan;63(1):126–133. doi: 10.1128/iai.63.1.126-133.1995

Immunomodulatory spectrum of lipids associated with Mycobacterium avium serovar 8.

W W Barrow 1, T L Davis 1, E L Wright 1, V Labrousse 1, M Bachelet 1, N Rastogi 1
PMCID: PMC172968  PMID: 7806348

Abstract

Lipid fractions obtained from Mycobacterium avium serovar 8 were assessed for the ability to affect various immune functions of human peripheral blood mononuclear cells (PBM). Lipids included a total lipid fraction and fractions eluted from silicic acid column separation of that total lipid fraction, using chloroform and chloroform-methanol combinations. Lipid fractions were assayed for total carbohydrate and total 6-deoxyhexose content and were assessed for the ability to influence human macrophage function and the capacity to induce secretion of prostaglandin E2 (PGE2) and tumor necrosis factor alpha in PBM. The total lipid and serovar-specific glycopeptidolipid (GPL) fractions both induced significant levels of tumor necrosis factor alpha, as well as PGE2, in PBM exposed to a sublethal concentration of 100 micrograms lipid per 2 x 10(6) cells. In addition, the same concentrations of the 5 to 7% and GPL fractions induced significant levels of leukotriene B4 in PBM. Comparison of carbohydrate and 6-deoxyhexose contents of each fraction suggested a relationship to carbohydrate content and ability of fractions to induce immune modulator secretion. Analysis of GPL fractions from M. avium serovars 4 and 20 revealed that those GPL lacked the ability to induce PGE2. These results are explained by considering the difference in the carbohydrate residues of the oligosaccharide moieties.

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Selected References

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  1. Barrow W. W. Contributing factors of pathogenesis in the Mycobacterium avium complex. Res Microbiol. 1991 May;142(4):427–433. doi: 10.1016/0923-2508(91)90115-q. [DOI] [PubMed] [Google Scholar]
  2. Barrow W. W., Ullom B. P., Brennan P. J. Peptidoglycolipid nature of the superficial cell wall sheath of smooth-colony-forming mycobacteria. J Bacteriol. 1980 Nov;144(2):814–822. doi: 10.1128/jb.144.2.814-822.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrow W. W., Wright E. L., Goh K. S., Rastogi N. Activities of fluoroquinolone, macrolide, and aminoglycoside drugs combined with inhibitors of glycosylation and fatty acid and peptide biosynthesis against Mycobacterium avium. Antimicrob Agents Chemother. 1993 Apr;37(4):652–661. doi: 10.1128/aac.37.4.652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barrow W. W., de Sousa J. P., Davis T. L., Wright E. L., Bachelet M., Rastogi N. Immunomodulation of human peripheral blood mononuclear cell functions by defined lipid fractions of Mycobacterium avium. Infect Immun. 1993 Dec;61(12):5286–5293. doi: 10.1128/iai.61.12.5286-5293.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belisle J. T., Brennan P. J. Molecular basis of colony morphology in Mycobacterium avium. Res Microbiol. 1994 Mar-Apr;145(3):237–242. doi: 10.1016/0923-2508(94)90024-8. [DOI] [PubMed] [Google Scholar]
  6. Belisle J. T., McNeil M. R., Chatterjee D., Inamine J. M., Brennan P. J. Expression of the core lipopeptide of the glycopeptidolipid surface antigens in rough mutants of Mycobacterium avium. J Biol Chem. 1993 May 15;268(14):10510–10516. [PubMed] [Google Scholar]
  7. Bray M. A., Ford-Hutchinson A. W., Smith M. J. Leukotriene B4: an inflammatory mediator in vivo. Prostaglandins. 1981 Aug;22(2):213–222. doi: 10.1016/0090-6980(81)90036-8. [DOI] [PubMed] [Google Scholar]
  8. Brennan P. J., Goren M. B. Structural studies on the type-specific antigens and lipids of the mycobacterium avium. Mycobacterium intracellulare. Mycobacterium scrofulaceum serocomplex. Mycobacterium intracellulare serotype 9. J Biol Chem. 1979 May 25;254(10):4205–4211. [PubMed] [Google Scholar]
  9. Brennan P. J. Structure of mycobacteria: recent developments in defining cell wall carbohydrates and proteins. Rev Infect Dis. 1989 Mar-Apr;11 (Suppl 2):S420–S430. doi: 10.1093/clinids/11.supplement_2.s420. [DOI] [PubMed] [Google Scholar]
  10. Brownback P. E., Barrow W. W. Modified lymphocyte response to mitogens after intraperitoneal injection of glycopeptidolipid antigens from Mycobacterium avium complex. Infect Immun. 1988 May;56(5):1044–1050. doi: 10.1128/iai.56.5.1044-1050.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Denis M., Gregg E. O. Modulation of Mycobacterium avium growth in murine macrophages: reversal of unresponsiveness to interferon-gamma by indomethacin or interleukin-4. J Leukoc Biol. 1991 Jan;49(1):65–72. doi: 10.1002/jlb.49.1.65. [DOI] [PubMed] [Google Scholar]
  12. Dimitrijevich S. D., Johnson M. M., Barrow W. W. One-step column chromatographic procedure for purification of mycobacterial glycopeptidolipid antigens. J Chromatogr. 1986 Apr 25;377:345–349. doi: 10.1016/s0378-4347(00)80791-4. [DOI] [PubMed] [Google Scholar]
  13. Draper P. The mycoside capsule of Mycobacterium Avium 357. J Gen Microbiol. 1974 Aug;83(2):431–433. doi: 10.1099/00221287-83-2-431. [DOI] [PubMed] [Google Scholar]
  14. Edwards C. K., 3rd, Hedegaard H. B., Zlotnik A., Gangadharam P. R., Johnston R. B., Jr, Pabst M. J. Chronic infection due to Mycobacterium intracellulare in mice: association with macrophage release of prostaglandin E2 and reversal by injection of indomethacin, muramyl dipeptide, or interferon-gamma. J Immunol. 1986 Mar 1;136(5):1820–1827. [PubMed] [Google Scholar]
  15. Ellner J. J., Goldberger M. J., Parenti D. M. Mycobacterium avium infection and AIDS: a therapeutic dilemma in rapid evolution. J Infect Dis. 1991 Jun;163(6):1326–1335. doi: 10.1093/infdis/163.6.1326. [DOI] [PubMed] [Google Scholar]
  16. Ferreri N. R., Millet I., Paliwal V., Herzog W., Solomon D., Ramabhadran R., Askenase P. W. Induction of macrophage TNF alpha, IL-1, IL-6, and PGE2 production by DTH-initiating factors. Cell Immunol. 1991 Oct 15;137(2):389–405. doi: 10.1016/0008-8749(91)90088-s. [DOI] [PubMed] [Google Scholar]
  17. Ferreri N. R., Sarr T., Askenase P. W., Ruddle N. H. Molecular regulation of tumor necrosis factor-alpha and lymphotoxin production in T cells. Inhibition by prostaglandin E2. J Biol Chem. 1992 May 5;267(13):9443–9449. [PubMed] [Google Scholar]
  18. Fieren M. W., van den Bemd G. J., Ben-Efraim S., Bonta I. L. Prostaglandin E2 inhibits the release of tumor necrosis factor-alpha, rather than interleukin 1 beta, from human macrophages. Immunol Lett. 1992 Jan;31(1):85–90. doi: 10.1016/0165-2478(92)90015-g. [DOI] [PubMed] [Google Scholar]
  19. Fletcher J. R., Collins J. N., Graves E. D., 3rd, Luterman A., Williams M. D., Izenberg S. D., Rodning C. B. Tumor necrosis factor-induced mortality is reversed with cyclooxygenase inhibition. Ann Surg. 1993 Jun;217(6):668–675. doi: 10.1097/00000658-199306000-00008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Flick D. A., Gifford G. E. Comparison of in vitro cell cytotoxic assays for tumor necrosis factor. J Immunol Methods. 1984 Mar 30;68(1-2):167–175. doi: 10.1016/0022-1759(84)90147-9. [DOI] [PubMed] [Google Scholar]
  21. Gagnon L., Filion L. G., Dubois C., Rola-Pleszczynski M. Leukotrienes and macrophage activation: augmented cytotoxic activity and enhanced interleukin 1, tumor necrosis factor and hydrogen peroxide production. Agents Actions. 1989 Jan;26(1-2):141–147. doi: 10.1007/BF02126587. [DOI] [PubMed] [Google Scholar]
  22. Goldman G., Welbourn R., Kobzik L., Valeri C. R., Shepro D., Hechtman H. B. Lavage with leukotriene B4 induces lung generation of tumor necrosis factor-alpha that in turn mediates neutrophil diapedesis. Surgery. 1993 Mar;113(3):297–303. [PubMed] [Google Scholar]
  23. Gustafson-Svärd C., Tagesson C., Boll R. M., Kald B. Tumor necrosis factor-alpha potentiates phospholipase A2-stimulated release and metabolism of arachidonic acid in cultured intestinal epithelial cells (INT 407). Scand J Gastroenterol. 1993 Apr;28(4):323–330. doi: 10.3109/00365529309090250. [DOI] [PubMed] [Google Scholar]
  24. Hayakawa M., Oku N., Takagi T., Hori T., Shibamoto S., Yamanaka Y., Takeuchi K., Tsujimoto M., Ito F. Involvement of prostaglandin-producing pathway in the cytotoxic action of tumor necrosis factor. Cell Struct Funct. 1991 Aug;16(4):333–340. doi: 10.1247/csf.16.333. [DOI] [PubMed] [Google Scholar]
  25. Hooper L. C., Barrow W. W. Decreased mitogenic response of murine spleen cells following intraperitoneal injection of serovar-specific glycopeptidolipid antigens from the Mycobacterium avium complex. Adv Exp Med Biol. 1988;239:309–325. doi: 10.1007/978-1-4757-5421-6_31. [DOI] [PubMed] [Google Scholar]
  26. Hooper L. C., Johnson M. M., Khera V. R., Barrow W. W. Macrophage uptake and retention of radiolabeled glycopeptidolipid antigens associated with the superficial L1 layer of Mycobacterium intracellulare serovar 20. Infect Immun. 1986 Oct;54(1):133–141. doi: 10.1128/iai.54.1.133-141.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McNeil M., Tsang A. Y., Brennan P. J. Structure and antigenicity of the specific oligosaccharide hapten from the glycopeptidolipid antigen of Mycobacterium avium serotype 4, the dominant Mycobacterium isolated from patients with acquired immune deficiency syndrome. J Biol Chem. 1987 Feb 25;262(6):2630–2635. [PubMed] [Google Scholar]
  28. Merino J., Casado J. A., Cid J., Sánchez-Ibarrola A., Subirá M. L. The measurement of transforming growth factor type beta (TGF beta) levels produced by peripheral blood mononuclear cells requires the efficient elimination of contaminating platelets. J Immunol Methods. 1992 Aug 30;153(1-2):151–159. doi: 10.1016/0022-1759(92)90317-m. [DOI] [PubMed] [Google Scholar]
  29. Molloy R. G., O'Riordain M., Holzheimer R., Nestor M., Collins K., Mannick J. A., Rodrick M. L. Mechanism of increased tumor necrosis factor production after thermal injury. Altered sensitivity to PGE2 and immunomodulation with indomethacin. J Immunol. 1993 Aug 15;151(4):2142–2149. [PubMed] [Google Scholar]
  30. Pourshafie M., Ayub Q., Barrow W. W. Comparative effects of Mycobacterium avium glycopeptidolipid and lipopeptide fragment on the function and ultrastructure of mononuclear cells. Clin Exp Immunol. 1993 Jul;93(1):72–79. doi: 10.1111/j.1365-2249.1993.tb06499.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rastogi N., Bachelet M., Carvalho de Sousa J. P. Intracellular growth of Mycobacterium avium in human macrophages is linked to the increased synthesis of prostaglandin E2 and inhibition of the phagosome-lysosome fusions. FEMS Microbiol Immunol. 1992 Jul;4(5):273–279. doi: 10.1111/j.1574-6968.1992.tb05006.x. [DOI] [PubMed] [Google Scholar]
  32. Rastogi N., Barrow W. W. Cell envelope constituents and the multifaceted nature of Mycobacterium avium pathogenicity and drug resistance. Res Microbiol. 1994 Mar-Apr;145(3):243–261. doi: 10.1016/0923-2508(94)90025-6. [DOI] [PubMed] [Google Scholar]
  33. Rastogi N., Labrousse V., Goh K. S., De Sousa J. P. Antimycobacterial spectrum of sparfloxacin and its activities alone and in association with other drugs against Mycobacterium avium complex growing extracellularly and intracellularly in murine and human macrophages. Antimicrob Agents Chemother. 1991 Dec;35(12):2473–2480. doi: 10.1128/aac.35.12.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rola-Pleszczynski M., Stanková J. Leukotriene B4 enhances interleukin-6 (IL-6) production and IL-6 messenger RNA accumulation in human monocytes in vitro: transcriptional and posttranscriptional mechanisms. Blood. 1992 Aug 15;80(4):1004–1011. [PubMed] [Google Scholar]
  35. Rulong S., Aguas A. P., da Silva P. P., Silva M. T. Intramacrophagic Mycobacterium avium bacilli are coated by a multiple lamellar structure: freeze fracture analysis of infected mouse liver. Infect Immun. 1991 Nov;59(11):3895–3902. doi: 10.1128/iai.59.11.3895-3902.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shiratsuchi H., Johnson J. L., Ellner J. J. Bidirectional effects of cytokines on the growth of Mycobacterium avium within human monocytes. J Immunol. 1991 May 1;146(9):3165–3170. [PubMed] [Google Scholar]
  37. Shiratsuchi H., Toossi Z., Mettler M. A., Ellner J. J. Colonial morphotype as a determinant of cytokine expression by human monocytes infected with Mycobacterium avium. J Immunol. 1993 Apr 1;150(7):2945–2954. [PubMed] [Google Scholar]
  38. Sirois P. Pharmacology of the leukotrienes. Adv Lipid Res. 1985;21:79–101. doi: 10.1016/b978-0-12-024921-3.50009-5. [DOI] [PubMed] [Google Scholar]
  39. Sors H., Pradelles P., Dray F., Rigaud M., Maclouf J., Bernard P. Analytical methods for thromboxane B2 measurement and validation of radioimmunoassay by gas liquid chromatography-mass spectrometry. Prostaglandins. 1978 Aug;16(2):277–290. doi: 10.1016/0090-6980(78)90030-8. [DOI] [PubMed] [Google Scholar]
  40. Stanková J., Dupuis G., Gagnon N., Thivierge M., Turcotte S., Rola-Pleszczynski M. Priming of human monocytes with leukotriene B4 enhances their sensitivity in IL-2-driven tumor necrosis factor-alpha production. Transcriptional and post-transcriptional up-regulation of IL-2 receptors. J Immunol. 1993 May 1;150(9):4041–4051. [PubMed] [Google Scholar]
  41. Stout R. D., Ferguson K. P., Li Y. N., Lambe D. W., Jr Staphylococcal exopolysaccharides inhibit lymphocyte proliferative responses by activation of monocyte prostaglandin production. Infect Immun. 1992 Mar;60(3):922–927. doi: 10.1128/iai.60.3.922-927.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Takayama T. K., Miller C., Szabo G. Elevated tumor necrosis factor alpha production concomitant to elevated prostaglandin E2 production by trauma patients' monocytes. Arch Surg. 1990 Jan;125(1):29–35. doi: 10.1001/archsurg.1990.01410130031004. [DOI] [PubMed] [Google Scholar]
  43. Tassell S. K., Pourshafie M., Wright E. L., Richmond M. G., Barrow W. W. Modified lymphocyte response to mitogens induced by the lipopeptide fragment derived from Mycobacterium avium serovar-specific glycopeptidolipids. Infect Immun. 1992 Feb;60(2):706–711. doi: 10.1128/iai.60.2.706-711.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tereletsky M. J., Barrow W. W. Postphagocytic detection of glycopeptidolipids associated with the superficial L1 layer of Mycobacterium intracellulare. Infect Immun. 1983 Sep;41(3):1312–1321. doi: 10.1128/iai.41.3.1312-1321.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tomioka H., Saito H., Yamada Y. Characteristics of immunosuppressive macrophages induced in spleen cells by Mycobacterium avium complex infections in mice. J Gen Microbiol. 1990 May;136(5):965–973. doi: 10.1099/00221287-136-5-965. [DOI] [PubMed] [Google Scholar]
  46. Tsuyuguchi I., Kawasumi H., Takashima T., Tsuyuguchi T., Kishimoto S. Mycobacterium avium-Mycobacterium intracellular complex-induced suppression of T-cell proliferation in vitro by regulation of monocyte accessory cell activity. Infect Immun. 1990 May;58(5):1369–1378. doi: 10.1128/iai.58.5.1369-1378.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Valone S. E., Rich E. A., Wallis R. S., Ellner J. J. Expression of tumor necrosis factor in vitro by human mononuclear phagocytes stimulated with whole Mycobacterium bovis BCG and mycobacterial antigens. Infect Immun. 1988 Dec;56(12):3313–3315. doi: 10.1128/iai.56.12.3313-3315.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wallis R. S., Ellner J. J., Shiratsuchi H. Macrophages, mycobacteria and HIV: the role of cytokines in determining mycobacterial virulence and regulating viral replication. Res Microbiol. 1992 May;143(4):398–405. doi: 10.1016/0923-2508(92)90053-q. [DOI] [PubMed] [Google Scholar]
  49. Woodbury J. L., Barrow W. W. Radiolabelling of Mycobacterium avium oligosaccharide determinant and use in macrophage studies. J Gen Microbiol. 1989 Jul;135(7):1875–1884. doi: 10.1099/00221287-135-7-1875. [DOI] [PubMed] [Google Scholar]
  50. Wright E. L., Barrow W. W. Inhibition of glycopeptidolipid synthesis resulting from treatment of Mycobacterium avium with 2-deoxy-D-glucose. Res Microbiol. 1991 Jun;142(5):597–608. doi: 10.1016/0923-2508(91)90193-e. [DOI] [PubMed] [Google Scholar]
  51. Yakrus M. A., Good R. C. Geographic distribution, frequency, and specimen source of Mycobacterium avium complex serotypes isolated from patients with acquired immunodeficiency syndrome. J Clin Microbiol. 1990 May;28(5):926–929. doi: 10.1128/jcm.28.5.926-929.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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