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. 1996 Jun;148(6):1935–1948.

Cytokine secretion and adhesion molecule expression by granuloma T lymphocytes in Mycobacterium avium infection.

R E Sacco 1, R J Jensen 1, C O Thoen 1, M Sandor 1, J Weinstock 1, R G Lynch 1, M O Dailey 1
PMCID: PMC1861647  PMID: 8669479

Abstract

Mice experimentally infected with Mycobacterium avium develop a chronic disease characterized by widespread noncaseating granulomas. In this report, we describe the phenotype and cytokine secretion profile of these granuloma-infiltrating effector T lymphocytes. In response to specific antigen, granuloma T cells and, to a lesser extent, spleen cells secrete interferon-gamma, but no interleukin-4 or -5. The importance of this Th1-like response to the host was demonstrated by the massively increased bacterial load and lethal disease in interferon-gamma knockout mice. One function of localized cytokine secretion is to recruit inflammatory T cells bearing surface adhesion molecules complementary to counter-receptors on vascular endothelial cells. Granuloma T cells express high levels of these pro-inflammatory adhesion molecules but have down-regulated their expression of L-selectin (CD62L). The expression of these adhesion molecules on granuloma-infiltrating T lymphocytes would alter the migration pathway of these cells and is likely to be important in facilitating the traffic of effector T cells to the granulomatous inflammatory site. In addition, T cells from Schistosoma mansoni granulomas express the same set of adhesion molecules, showing that this phenotype is not specifically dependent upon the Th1 pattern of cytokine secretion.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amiri P., Locksley R. M., Parslow T. G., Sadick M., Rector E., Ritter D., McKerrow J. H. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature. 1992 Apr 16;356(6370):604–607. doi: 10.1038/356604a0. [DOI] [PubMed] [Google Scholar]
  2. Appelberg R., Castro A. G., Pedrosa J., Silva R. A., Orme I. M., Minóprio P. Role of gamma interferon and tumor necrosis factor alpha during T-cell-independent and -dependent phases of Mycobacterium avium infection. Infect Immun. 1994 Sep;62(9):3962–3971. doi: 10.1128/iai.62.9.3962-3971.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bermudez L. E., Champsi J. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect Immun. 1993 Jul;61(7):3093–3097. doi: 10.1128/iai.61.7.3093-3097.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bermudez L. E. Production of transforming growth factor-beta by Mycobacterium avium-infected human macrophages is associated with unresponsiveness to IFN-gamma. J Immunol. 1993 Mar 1;150(5):1838–1845. [PubMed] [Google Scholar]
  5. Bermudez L. E., Stevens P., Kolonoski P., Wu M., Young L. S. Treatment of experimental disseminated Mycobacterium avium complex infection in mice with recombinant IL-2 and tumor necrosis factor. J Immunol. 1989 Nov 1;143(9):2996–3000. [PubMed] [Google Scholar]
  6. Bermudez L. E., Young L. S. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-gamma, is associated with macrophage killing of Mycobacterium avium complex. J Immunol. 1988 May 1;140(9):3006–3013. [PubMed] [Google Scholar]
  7. Boyd A. W., Wawryk S. O., Burns G. F., Fecondo J. V. Intercellular adhesion molecule 1 (ICAM-1) has a central role in cell-cell contact-mediated immune mechanisms. Proc Natl Acad Sci U S A. 1988 May;85(9):3095–3099. doi: 10.1073/pnas.85.9.3095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Butcher E. C., Scollay R. G., Weissman I. L. Lymphocyte adherence to high endothelial venules: characterization of a modified in vitro assay, and examination of the binding of syngeneic and allogeneic lymphocyte populations. J Immunol. 1979 Nov;123(5):1996–2003. [PubMed] [Google Scholar]
  9. Chan J., Xing Y., Magliozzo R. S., Bloom B. R. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med. 1992 Apr 1;175(4):1111–1122. doi: 10.1084/jem.175.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chensue S. W., Otterness I. G., Higashi G. I., Forsch C. S., Kunkel S. L. Monokine production by hypersensitivity (Schistosoma mansoni egg) and foreign body (Sephadex bead)-type granuloma macrophages. Evidence for sequential production of IL-1 and tumor necrosis factor. J Immunol. 1989 Feb 15;142(4):1281–1286. [PubMed] [Google Scholar]
  11. Chin Y. H., Cai J. P., Xu X. M. Transforming growth factor-beta 1 and IL-4 regulate the adhesiveness of Peyer's patch high endothelial venule cells for lymphocytes. J Immunol. 1992 Feb 15;148(4):1106–1112. [PubMed] [Google Scholar]
  12. Cooper A. M., Dalton D. K., Stewart T. A., Griffin J. P., Russell D. G., Orme I. M. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993 Dec 1;178(6):2243–2247. doi: 10.1084/jem.178.6.2243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dalton D. K., Pitts-Meek S., Keshav S., Figari I. S., Bradley A., Stewart T. A. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science. 1993 Mar 19;259(5102):1739–1742. doi: 10.1126/science.8456300. [DOI] [PubMed] [Google Scholar]
  14. Damle N. K., Klussman K., Linsley P. S., Aruffo A., Ledbetter J. A. Differential regulatory effects of intercellular adhesion molecule-1 on costimulation by the CD28 counter-receptor B7. J Immunol. 1992 Oct 15;149(8):2541–2548. [PubMed] [Google Scholar]
  15. Dang L. H., Michalek M. T., Takei F., Benaceraff B., Rock K. L. Role of ICAM-1 in antigen presentation demonstrated by ICAM-1 defective mutants. J Immunol. 1990 Jun 1;144(11):4082–4091. [PubMed] [Google Scholar]
  16. Denis M., Ghadirian E. IL-10 neutralization augments mouse resistance to systemic Mycobacterium avium infections. J Immunol. 1993 Nov 15;151(10):5425–5430. [PubMed] [Google Scholar]
  17. Denis M. Involvement of cytokines in determining resistance and acquired immunity in murine tuberculosis. J Leukoc Biol. 1991 Nov;50(5):495–501. doi: 10.1002/jlb.50.5.495. [DOI] [PubMed] [Google Scholar]
  18. Denis M. Modulation of Mycobacterium avium growth in vivo by cytokines: involvement of tumour necrosis factor in resistance to atypical mycobacteria. Clin Exp Immunol. 1991 Mar;83(3):466–471. doi: 10.1111/j.1365-2249.1991.tb05662.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dustin M. L., Rothlein R., Bhan A. K., Dinarello C. A., Springer T. A. Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol. 1986 Jul 1;137(1):245–254. [PubMed] [Google Scholar]
  20. Elices M. J., Osborn L., Takada Y., Crouse C., Luhowskyj S., Hemler M. E., Lobb R. R. VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell. 1990 Feb 23;60(4):577–584. doi: 10.1016/0092-8674(90)90661-w. [DOI] [PubMed] [Google Scholar]
  21. Ellner J. J., Daniel T. M. Immunosuppression by mycobacterial arabinomannan. Clin Exp Immunol. 1979 Feb;35(2):250–257. [PMC free article] [PubMed] [Google Scholar]
  22. Farhi D. C., Mason U. G., 3rd, Horsburgh C. R., Jr Pathologic findings in disseminated Mycobacterium avium-intracellulare infection. A report of 11 cases. Am J Clin Pathol. 1986 Jan;85(1):67–72. doi: 10.1093/ajcp/85.1.67. [DOI] [PubMed] [Google Scholar]
  23. Flynn J. L., Chan J., Triebold K. J., Dalton D. K., Stewart T. A., Bloom B. R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993 Dec 1;178(6):2249–2254. doi: 10.1084/jem.178.6.2249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fournie J. J., Adams E., Mullins R. J., Basten A. Inhibition of human lymphoproliferative responses by mycobacterial phenolic glycolipids. Infect Immun. 1989 Nov;57(11):3653–3659. doi: 10.1128/iai.57.11.3653-3659.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Freemont A. J., Ford W. L. Functional and morphological changes in post-capillary venules in relation to lymphocytic infiltration into BCG-induced granulomata in rat skin. J Pathol. 1985 Sep;147(1):1–12. doi: 10.1002/path.1711470102. [DOI] [PubMed] [Google Scholar]
  26. Gallatin W. M., Weissman I. L., Butcher E. C. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 1983 Jul 7;304(5921):30–34. doi: 10.1038/304030a0. [DOI] [PubMed] [Google Scholar]
  27. Harp J. A., Whitmire W. M., Sacco R. In vitro proliferation and production of gamma interferon by murine CD4+ cells in response to Cryptosporidium parvum antigen. J Parasitol. 1994 Feb;80(1):67–72. [PubMed] [Google Scholar]
  28. Havell E. A. Evidence that tumor necrosis factor has an important role in antibacterial resistance. J Immunol. 1989 Nov 1;143(9):2894–2899. [PubMed] [Google Scholar]
  29. Hawkins C. C., Gold J. W., Whimbey E., Kiehn T. E., Brannon P., Cammarata R., Brown A. E., Armstrong D. Mycobacterium avium complex infections in patients with the acquired immunodeficiency syndrome. Ann Intern Med. 1986 Aug;105(2):184–188. doi: 10.7326/0003-4819-105-2-184. [DOI] [PubMed] [Google Scholar]
  30. Holzmann B., Weissman I. L. Peyer's patch-specific lymphocyte homing receptors consist of a VLA-4-like alpha chain associated with either of two integrin beta chains, one of which is novel. EMBO J. 1989 Jun;8(6):1735–1741. doi: 10.1002/j.1460-2075.1989.tb03566.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Huygen K., Abramowicz D., Vandenbussche P., Jacobs F., De Bruyn J., Kentos A., Drowart A., Van Vooren J. P., Goldman M. Spleen cell cytokine secretion in Mycobacterium bovis BCG-infected mice. Infect Immun. 1992 Jul;60(7):2880–2886. doi: 10.1128/iai.60.7.2880-2886.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Issekutz T. B., Chin W., Hay J. B. The characterization of lymphocytes migrating through chronically inflamed tissues. Immunology. 1982 May;46(1):59–66. [PMC free article] [PubMed] [Google Scholar]
  33. Issekutz T. B. Dual inhibition of VLA-4 and LFA-1 maximally inhibits cutaneous delayed-type hypersensitivity-induced inflammation. Am J Pathol. 1993 Nov;143(5):1286–1293. [PMC free article] [PubMed] [Google Scholar]
  34. Kamijo R., Le J., Shapiro D., Havell E. A., Huang S., Aguet M., Bosland M., Vilcek J. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guérin and subsequent challenge with lipopolysaccharide. J Exp Med. 1993 Oct 1;178(4):1435–1440. doi: 10.1084/jem.178.4.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kilshaw P. J., Baker K. C. A unique surface antigen on intraepithelial lymphocytes in the mouse. Immunol Lett. 1988 Jun;18(2):149–154. doi: 10.1016/0165-2478(88)90056-9. [DOI] [PubMed] [Google Scholar]
  36. Kilshaw P. J., Murant S. J. Expression and regulation of beta 7(beta p) integrins on mouse lymphocytes: relevance to the mucosal immune system. Eur J Immunol. 1991 Oct;21(10):2591–2597. doi: 10.1002/eji.1830211041. [DOI] [PubMed] [Google Scholar]
  37. Kindler V., Sappino A. P., Grau G. E., Piguet P. F., Vassalli P. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell. 1989 Mar 10;56(5):731–740. doi: 10.1016/0092-8674(89)90676-4. [DOI] [PubMed] [Google Scholar]
  38. Klatt E. C., Jensen D. F., Meyer P. R. Pathology of Mycobacterium avium-intracellulare infection in acquired immunodeficiency syndrome. Hum Pathol. 1987 Jul;18(7):709–714. doi: 10.1016/s0046-8177(87)80242-3. [DOI] [PubMed] [Google Scholar]
  39. Lee W. T., Vitetta E. S. The differential expression of homing and adhesion molecules on virgin and memory T cells in the mouse. Cell Immunol. 1991 Jan;132(1):215–222. doi: 10.1016/0008-8749(91)90020-c. [DOI] [PubMed] [Google Scholar]
  40. Lukacs N. W., Boros D. L. Lymphokine regulation of granuloma formation in murine schistosomiasis mansoni. Clin Immunol Immunopathol. 1993 Jul;68(1):57–63. doi: 10.1006/clin.1993.1095. [DOI] [PubMed] [Google Scholar]
  41. Lukacs N. W., Chensue S. W., Strieter R. M., Warmington K., Kunkel S. L. Inflammatory granuloma formation is mediated by TNF-alpha-inducible intercellular adhesion molecule-1. J Immunol. 1994 Jun 15;152(12):5883–5889. [PubMed] [Google Scholar]
  42. Metwali A., Blum A., Mathew R., Sandor M., Lynch R. G., Weinstock J. V. Modulation of T lymphocyte proliferation in mice infected with Schistosoma mansoni: VIP suppresses mitogen- and antigen-induced T cell proliferation possibly by inhibiting IL-2 production. Cell Immunol. 1993 Jun;149(1):11–23. doi: 10.1006/cimm.1993.1132. [DOI] [PubMed] [Google Scholar]
  43. Metwali A., Elliott D., Mathew R., Blum A., Weinstock J. V. IL-2 contributes to the IL-5 response in granulomas from mice infected with Schistosoma mansoni. J Immunol. 1993 Jan 15;150(2):536–542. [PubMed] [Google Scholar]
  44. Mobley J. L., Dailey M. O. Regulation of adhesion molecule expression by CD8 T cells in vivo. I. Differential regulation of gp90MEL-14 (LECAM-1), Pgp-1, LFA-1, and VLA-4 alpha during the differentiation of cytotoxic T lymphocytes induced by allografts. J Immunol. 1992 Apr 15;148(8):2348–2356. [PubMed] [Google Scholar]
  45. Murray H. W., Squires K. E., Miralles C. D., Stoeckle M. Y., Granger A. M., Granelli-Piperno A., Bogdan C. Acquired resistance and granuloma formation in experimental visceral leishmaniasis. Differential T cell and lymphokine roles in initial versus established immunity. J Immunol. 1992 Mar 15;148(6):1858–1863. [PubMed] [Google Scholar]
  46. Mustafa A. S., Godal T. BCG-induced suppressor T cells optimal conditions for in vitro induction and mode of action. Clin Exp Immunol. 1985 Dec;62(3):474–481. [PMC free article] [PubMed] [Google Scholar]
  47. Oppenheimer-Marks N., Davis L. S., Lipsky P. E. Human T lymphocyte adhesion to endothelial cells and transendothelial migration. Alteration of receptor use relates to the activation status of both the T cell and the endothelial cell. J Immunol. 1990 Jul 1;145(1):140–148. [PubMed] [Google Scholar]
  48. Orme I. M., Roberts A. D., Griffin J. P., Abrams J. S. Cytokine secretion by CD4 T lymphocytes acquired in response to Mycobacterium tuberculosis infection. J Immunol. 1993 Jul 1;151(1):518–525. [PubMed] [Google Scholar]
  49. Pearce E. J., Caspar P., Grzych J. M., Lewis F. A., Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991 Jan 1;173(1):159–166. doi: 10.1084/jem.173.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Picker L. J. Mechanisms of lymphocyte homing. Curr Opin Immunol. 1992 Jun;4(3):277–286. doi: 10.1016/0952-7915(92)90077-r. [DOI] [PubMed] [Google Scholar]
  51. Rothlein R., Kishimoto T. K., Mainolfi E. Cross-linking of ICAM-1 induces co-signaling of an oxidative burst from mononuclear leukocytes. J Immunol. 1994 Mar 1;152(5):2488–2495. [PubMed] [Google Scholar]
  52. 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]
  53. Salgame P., Abrams J. S., Clayberger C., Goldstein H., Convit J., Modlin R. L., Bloom B. R. Differing lymphokine profiles of functional subsets of human CD4 and CD8 T cell clones. Science. 1991 Oct 11;254(5029):279–282. doi: 10.1126/science.254.5029.279. [DOI] [PubMed] [Google Scholar]
  54. Saunders B. M., Cheers C. Inflammatory response following intranasal infection with Mycobacterium avium complex: role of T-cell subsets and gamma interferon. Infect Immun. 1995 Jun;63(6):2282–2287. doi: 10.1128/iai.63.6.2282-2287.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Schumacher J. H., O'Garra A., Shrader B., van Kimmenade A., Bond M. W., Mosmann T. R., Coffman R. L. The characterization of four monoclonal antibodies specific for mouse IL-5 and development of mouse and human IL-5 enzyme-linked immunosorbent. J Immunol. 1988 Sep 1;141(5):1576–1581. [PubMed] [Google Scholar]
  56. Semnani R. T., Nutman T. B., Hochman P., Shaw S., van Seventer G. A. Costimulation by purified intercellular adhesion molecule 1 and lymphocyte function-associated antigen 3 induces distinct proliferation, cytokine and cell surface antigen profiles in human "naive" and "memory" CD4+ T cells. J Exp Med. 1994 Dec 1;180(6):2125–2135. doi: 10.1084/jem.180.6.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sher A., Coffman R. L., Hieny S., Scott P., Cheever A. W. Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc Natl Acad Sci U S A. 1990 Jan;87(1):61–65. doi: 10.1073/pnas.87.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sher A., Fiorentino D., Caspar P., Pearce E., Mosmann T. Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. J Immunol. 1991 Oct 15;147(8):2713–2716. [PubMed] [Google Scholar]
  59. Shimizu Y., Newman W., Gopal T. V., Horgan K. J., Graber N., Beall L. D., van Seventer G. A., Shaw S. Four molecular pathways of T cell adhesion to endothelial cells: roles of LFA-1, VCAM-1, and ELAM-1 and changes in pathway hierarchy under different activation conditions. J Cell Biol. 1991 Jun;113(5):1203–1212. doi: 10.1083/jcb.113.5.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. Sohn C. C., Schroff R. W., Kliewer K. E., Lebel D. M., Fligiel S. Disseminated Mycobacterium avium-intracellulare infection in homosexual men with acquired cell-mediated immunodeficiency: a histologic and immunologic study of two cases. Am J Clin Pathol. 1983 Feb;79(2):247–252. doi: 10.1093/ajcp/79.2.247. [DOI] [PubMed] [Google Scholar]
  62. Stenger S., Solbach W., Röllinghoff M., Bogdan C. Cytokine interactions in experimental cutaneous leishmaniasis. II. Endogenous tumor necrosis factor-alpha production by macrophages is induced by the synergistic action of interferon (IFN)-gamma and interleukin (IL) 4 and accounts for the antiparasitic effect mediated by IFN-gamma and IL 4. Eur J Immunol. 1991 Jul;21(7):1669–1675. doi: 10.1002/eji.1830210713. [DOI] [PubMed] [Google Scholar]
  63. Sullivan L., Sano S., Pirmez C., Salgame P., Mueller C., Hofman F., Uyemura K., Rea T. H., Bloom B. R., Modlin R. L. Expression of adhesion molecules in leprosy lesions. Infect Immun. 1991 Nov;59(11):4154–4160. doi: 10.1128/iai.59.11.4154-4160.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Suttles J., Schwarting G. A., Stout R. D. Flow cytometric analysis reveals the presence of asialo GM1 on the surface membrane of alloimmune cytotoxic T lymphocytes. J Immunol. 1986 Mar 1;136(5):1586–1591. [PubMed] [Google Scholar]
  65. 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]
  66. Vella A. T., Hulsebosch M. D., Pearce E. J. Schistosoma mansoni eggs induce antigen-responsive CD44-hi T helper 2 cells and IL-4-secreting CD44-lo cells. Potential for T helper 2 subset differentiation is evident at the precursor level. J Immunol. 1992 Sep 1;149(5):1714–1722. [PubMed] [Google Scholar]
  67. Vella A. T., Pearce E. J. CD4+ Th2 response induced by Schistosoma mansoni eggs develops rapidly, through an early, transient, Th0-like stage. J Immunol. 1992 Apr 1;148(7):2283–2290. [PubMed] [Google Scholar]
  68. Wacholtz M. C., Patel S. S., Lipsky P. E. Leukocyte function-associated antigen 1 is an activation molecule for human T cells. J Exp Med. 1989 Aug 1;170(2):431–448. doi: 10.1084/jem.170.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wadee A. A., Sher R., Rabson A. R. Production of a suppressor factor by human adherent cells treated with mycobacteria. J Immunol. 1980 Sep;125(3):1380–1386. [PubMed] [Google Scholar]
  70. Yamamura M., Uyemura K., Deans R. J., Weinberg K., Rea T. H., Bloom B. R., Modlin R. L. Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science. 1991 Oct 11;254(5029):277–279. doi: 10.1126/science.254.5029.277. [DOI] [PubMed] [Google Scholar]
  71. Young L. S. Mycobacterium avium complex infection. J Infect Dis. 1988 May;157(5):863–867. doi: 10.1093/infdis/157.5.863. [DOI] [PubMed] [Google Scholar]
  72. van Seventer G. A., Newman W., Shimizu Y., Nutman T. B., Tanaka Y., Horgan K. J., Gopal T. V., Ennis E., O'Sullivan D., Grey H. Analysis of T cell stimulation by superantigen plus major histocompatibility complex class II molecules or by CD3 monoclonal antibody: costimulation by purified adhesion ligands VCAM-1, ICAM-1, but not ELAM-1. J Exp Med. 1991 Oct 1;174(4):901–913. doi: 10.1084/jem.174.4.901. [DOI] [PMC free article] [PubMed] [Google Scholar]

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