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. 1997 Dec;92(4):478–486. doi: 10.1046/j.1365-2567.1997.00371.x

Alternatively activated macrophages actively inhibit proliferation of peripheral blood lymphocytes and CD4+ T cells in vitro.

C Schebesch 1, V Kodelja 1, C Müller 1, N Hakij 1, S Bisson 1, C E Orfanos 1, S Goerdt 1
PMCID: PMC1364153  PMID: 9497489

Abstract

We compared the immunological functions of interferon-gamma (IFN-gamma)-induced, classically activated macrophages (caM phi) and of interleukin-4 (IL-4)- and glucocorticoid-induced, alternatively activated macrophages (aaM phi) in a human co-culture system in vitro. Proliferation of peripheral blood leucocytes (PBL) or CD4+ T cells mediated by optimal doses of phytohaemagglutinin (PHA) or concanavalin A (Con A) was only marginally influenced by caM phi, but was strongly inhibited by aaM phi. The degree of lymphocyte proliferation sustained in the presence of caM phi was gradually reduced in a dose-dependent fashion by the addition of aaM phi. Flow cytometric analysis revealed that expression of costimulatory molecules such as CD11a, CD40, CD54, CD58, CD80 and CD86 did not vary significantly between caM phi and aaM phi and was low for CD58, CD80 and CD86. As shown by reverse transcriptase-polymerase chain reaction (RT-PCR) analysis, IL-10 was expressed in caM phi, aaM phi and control macrophages; the level of expression of IL-10 was slightly enhanced in aaM phi. Neither neutralizing anti-IL-10 antibodies, indomethacin nor NG-monomethyl-L-arginine (NMMLA) was able to reverse aaM phi-mediated inhibition of lymphocyte proliferation. Of several agents interfering with various second messenger pathways, cAMP and the Ca(2+)-ionophore A23187 inhibited differentiation of cultured human monocytes into phenotypically mature aaM phi expressing MS-1 high molecular weight protein (MS-1-HMWP) and RM 3/1 antigen, and prevented the suppressive action of aaM phi on lymphocyte proliferation. In conclusion, these results who that aaM phi actively inhibit mitogen-mediated proliferation of PBL and CD4+ T cells independently of the expression of costimulatory molecules and of IL-10, NO or prostaglandin synthesis, and that inhibition of phenotypic differentiation of aaM phi is paralleled by a lack of functional maturation. Thus, fully matured aaM phi may be functional in down-regulating CD4+ T-cell-mediated immune reactions by an as yet unknown mechanism.

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Selected References

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

  1. Asahina A., Moro O., Hosoi J., Lerner E. A., Xu S., Takashima A., Granstein R. D. Specific induction of cAMP in Langerhans cells by calcitonin gene-related peptide: relevance to functional effects. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8323–8327. doi: 10.1073/pnas.92.18.8323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Becker S., Daniel E. G. Antagonistic and additive effects of IL-4 and interferon-gamma on human monocytes and macrophages: effects on Fc receptors, HLA-D antigens, and superoxide production. Cell Immunol. 1990 Sep;129(2):351–362. doi: 10.1016/0008-8749(90)90211-9. [DOI] [PubMed] [Google Scholar]
  3. Beissert S., Hosoi J., Grabbe S., Asahina A., Granstein R. D. IL-10 inhibits tumor antigen presentation by epidermal antigen-presenting cells. J Immunol. 1995 Feb 1;154(3):1280–1286. [PubMed] [Google Scholar]
  4. Boraschi D., Censini S., Tagliabue A. Interferon-gamma reduces macrophage-suppressive activity by inhibiting prostaglandin E2 release and inducing interleukin 1 production. J Immunol. 1984 Aug;133(2):764–768. [PubMed] [Google Scholar]
  5. Buelens C., Verhasselt V., De Groote D., Thielemans K., Goldman M., Willems F. Interleukin-10 prevents the generation of dendritic cells from human peripheral blood mononuclear cells cultured with interleukin-4 and granulocyte/macrophage-colony-stimulating factor. Eur J Immunol. 1997 Mar;27(3):756–762. doi: 10.1002/eji.1830270326. [DOI] [PubMed] [Google Scholar]
  6. Caux C., Massacrier C., Vanbervliet B., Barthelemy C., Liu Y. J., Banchereau J. Interleukin 10 inhibits T cell alloreaction induced by human dendritic cells. Int Immunol. 1994 Aug;6(8):1177–1185. doi: 10.1093/intimm/6.8.1177. [DOI] [PubMed] [Google Scholar]
  7. Chang M. D., Pollard J. W., Khalili H., Goyert S. M., Diamond B. Mouse placental macrophages have a decreased ability to present antigen. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):462–466. doi: 10.1073/pnas.90.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chang Z. L., Bonvini E., Varesio L., Holden H. T., Herberman R. B. Differential in vitro modulation of suppressor and antitumor functions of mouse macrophages by lymphokines and/or endotoxin. Cell Immunol. 1988 Jul;114(2):282–292. doi: 10.1016/0008-8749(88)90322-x. [DOI] [PubMed] [Google Scholar]
  9. Cheung D. L., Hart P. H., Vitti G. F., Whitty G. A., Hamilton J. A. Contrasting effects of interferon-gamma and interleukin-4 on the interleukin-6 activity of stimulated human monocytes. Immunology. 1990 Sep;71(1):70–75. [PMC free article] [PubMed] [Google Scholar]
  10. Clare-Salzler M. J., Brooks J., Chai A., Van Herle K., Anderson C. Prevention of diabetes in nonobese diabetic mice by dendritic cell transfer. J Clin Invest. 1992 Sep;90(3):741–748. doi: 10.1172/JCI115946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Conrad D. J., Kuhn H., Mulkins M., Highland E., Sigal E. Specific inflammatory cytokines regulate the expression of human monocyte 15-lipoxygenase. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):217–221. doi: 10.1073/pnas.89.1.217. [DOI] [PMC free article] [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. Cowan H. B., Vick S., Conary J. T., Shepherd V. L. Dexamethasone up-regulates mannose receptor activity by increasing mRNA levels. Arch Biochem Biophys. 1992 Jul;296(1):314–320. doi: 10.1016/0003-9861(92)90578-k. [DOI] [PubMed] [Google Scholar]
  14. Delespesse G., Sarfati M. An update on human CD23 (Fc epsilon RII). Fc epsilon RII and IgE-BFs (soluble CD23) play an essential role in the regulation of human IgE synthesis. Clin Exp Allergy. 1991 Jan;21 (Suppl 1):153–161. doi: 10.1111/j.1365-2222.1991.tb01720.x. [DOI] [PubMed] [Google Scholar]
  15. Dieter P., Fitzke E. Differential regulation of phospholipase D and phospholipase C by protein kinase C-beta and -delta in liver macrophages. Cell Signal. 1995 Sep;7(7):687–694. doi: 10.1016/0898-6568(95)00038-q. [DOI] [PubMed] [Google Scholar]
  16. Djemadji-Oudjiel N., Goerdt S., Kodelja V., Schmuth M., Orfanos C. E. Immunohistochemical identification of type II alternatively activated dendritic macrophages (RM 3/1+3, MS-1+/-, 25F9-) in psoriatic dermis. Arch Dermatol Res. 1996 Nov;288(12):757–764. doi: 10.1007/BF02505293. [DOI] [PubMed] [Google Scholar]
  17. Enk A. H., Angeloni V. L., Udey M. C., Katz S. I. Inhibition of Langerhans cell antigen-presenting function by IL-10. A role for IL-10 in induction of tolerance. J Immunol. 1993 Sep 1;151(5):2390–2398. [PubMed] [Google Scholar]
  18. Enk A. H., Saloga J., Becker D., Mohamadzadeh M., Knop J. Induction of hapten-specific tolerance by interleukin 10 in vivo. J Exp Med. 1994 Apr 1;179(4):1397–1402. doi: 10.1084/jem.179.4.1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ettensohn D. B., Lalor P. A., Roberts N. J., Jr Human alveolar macrophage suppression of lymphocyte proliferation. Accessory characteristics for the generation and functional expression of con A-induced suppressor cells. Am Rev Respir Dis. 1988 Apr;137(4):765–773. doi: 10.1164/ajrccm/137.4.765. [DOI] [PubMed] [Google Scholar]
  20. Fais S., Burgio V. L., Silvestri M., Capobianchi M. R., Pacchiarotti A., Pallone F. Multinucleated giant cells generation induced by interferon-gamma. Changes in the expression and distribution of the intercellular adhesion molecule-1 during macrophages fusion and multinucleated giant cell formation. Lab Invest. 1994 Nov;71(5):737–744. [PubMed] [Google Scholar]
  21. Fireman E. M., Ben Efraim S., Greif J., Kivity S., Topilsky M. R. Suppressor cell activity of human alveolar macrophages in interstitial lung diseases. Clin Exp Immunol. 1988 Jul;73(1):111–116. [PMC free article] [PubMed] [Google Scholar]
  22. Fujii T., Igarashi T., Kishimoto S. Significance of suppressor macrophages for immunosurveillance of tumor-bearing mice. J Natl Cancer Inst. 1987 Mar;78(3):509–517. [PubMed] [Google Scholar]
  23. Geertsma M. F., Teeuw W. L., Nibbering P. H., van Furth R. Pulmonary surfactant inhibits activation of human monocytes by recombinant interferon-gamma. Immunology. 1994 Jul;82(3):450–456. [PMC free article] [PubMed] [Google Scholar]
  24. Gemsa D., Leser H. G., Deimann W., Resch K. Suppression of T lymphocyte proliferation during lymphoma growth in mice: role of PGE2-producing suppressor macrophages. Immunobiology. 1982 Apr;161(3-4):385–391. doi: 10.1016/s0171-2985(82)80096-x. [DOI] [PubMed] [Google Scholar]
  25. Goerdt S., Bhardwaj R., Sorg C. Inducible expression of MS-1 high-molecular-weight protein by endothelial cells of continuous origin and by dendritic cells/macrophages in vivo and in vitro. Am J Pathol. 1993 May;142(5):1409–1422. [PMC free article] [PubMed] [Google Scholar]
  26. Goerdt S., Kolde G., Bonsmann G., Hamann K., Czarnetzki B., Andreesen R., Luger T., Sorg C. Immunohistochemical comparison of cutaneous histiocytoses and related skin disorders: diagnostic and histogenetic relevance of MS-1 high molecular weight protein expression. J Pathol. 1993 Aug;170(4):421–427. doi: 10.1002/path.1711700404. [DOI] [PubMed] [Google Scholar]
  27. Gosselin D., Turcotte R., Lemieux S. Cellular target of in vitro-induced suppressor cells derived from the spleen of Mycobacterium lepraemurium-infected mice and role of IFN-gamma in their development. J Leukoc Biol. 1995 Jan;57(1):122–128. doi: 10.1002/jlb.57.1.122. [DOI] [PubMed] [Google Scholar]
  28. Hart P. H., Vitti G. F., Burgess D. R., Whitty G. A., Piccoli D. S., Hamilton J. A. Potential antiinflammatory effects of interleukin 4: suppression of human monocyte tumor necrosis factor alpha, interleukin 1, and prostaglandin E2. Proc Natl Acad Sci U S A. 1989 May;86(10):3803–3807. doi: 10.1073/pnas.86.10.3803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hart P. H., Whitty G. A., Burgess D. R., Croatto M., Hamilton J. A. Augmentation of glucocorticoid action on human monocytes by interleukin-4. Lymphokine Res. 1990 Summer;9(2):147–153. [PubMed] [Google Scholar]
  30. Holt P. G., Schon-Hegrad M. A., Oliver J. MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat. Regulation of antigen presentation activity by endogenous macrophage populations. J Exp Med. 1988 Feb 1;167(2):262–274. doi: 10.1084/jem.167.2.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kennard J., Zolla-Pazner S. Origin and function of suppressor macrophages in myeloma. J Immunol. 1980 Jan;124(1):268–273. [PubMed] [Google Scholar]
  32. Kirschmann D. A., He X., Murasko D. M. Inhibition of macrophage-induced, antigen-specific T-cell proliferation by poly I:C role of suppressor macrophages. Immunology. 1994 Jun;82(2):238–243. [PMC free article] [PubMed] [Google Scholar]
  33. Knop J., Malorny U., Macher E. Selective induction of delayed hypersensitivity T-effector and T-suppressor lymphocytes in vitro by haptenized bone marrow-derived macrophages. Cell Immunol. 1984 Oct 15;88(2):411–420. doi: 10.1016/0008-8749(84)90174-6. [DOI] [PubMed] [Google Scholar]
  34. Knop J., Malorny U., Michels E., Sorg C. Selection of the delayed hypersensitivity T effector and T suppressor cell response by antigen-presenting macrophages. Immunobiology. 1984 Dec;168(3-5):246–259. doi: 10.1016/S0171-2985(84)80114-X. [DOI] [PubMed] [Google Scholar]
  35. Knop J., Taborski B., DeMaeyer-Guignard J. Selective inhibition of the generation of T suppressor cells of contact sensitivity in vitro by interferon. J Immunol. 1987 Jun 1;138(11):3684–3687. [PubMed] [Google Scholar]
  36. Kodelja V., Goerdt S. Dissection of macrophage differentiation pathways in cutaneous macrophage disorders and in vitro. Exp Dermatol. 1994 Dec;3(6):257–268. doi: 10.1111/j.1600-0625.1994.tb00287.x. [DOI] [PubMed] [Google Scholar]
  37. Kodelja V., Müller C., Tenorio S., Schebesch C., Orfanos C. E., Goerdt S. Differences in angiogenic potential of classically vs alternatively activated macrophages. Immunobiology. 1997 Nov;197(5):478–493. doi: 10.1016/S0171-2985(97)80080-0. [DOI] [PubMed] [Google Scholar]
  38. Landmann R., Fisscher A. E., Obrecht J. P. Interferon-gamma and interleukin-4 down-regulate soluble CD14 release in human monocytes and macrophages. J Leukoc Biol. 1992 Sep;52(3):323–330. doi: 10.1002/jlb.52.3.323. [DOI] [PubMed] [Google Scholar]
  39. Lemieux S., Gosselin D., Lusignan Y., Turcotte R. Early accumulation of suppressor cell precursors in the spleen of Mycobacterium lepraemurium-infected mice and analysis of their in vitro-induced maturation. Clin Exp Immunol. 1990 Jul;81(1):116–122. doi: 10.1111/j.1365-2249.1990.tb05300.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lichtenstein A., Murahata R., Terpenning M., Cantrell J., Zighelboim J. Activation and mechanism of action of suppressor macrophages. Cell Immunol. 1981 Oct;64(1):150–161. doi: 10.1016/0008-8749(81)90466-4. [DOI] [PubMed] [Google Scholar]
  41. Liew F. Y., Li Y., Severn A., Millott S., Schmidt J., Salter M., Moncada S. A possible novel pathway of regulation by murine T helper type-2 (Th2) cells of a Th1 cell activity via the modulation of the induction of nitric oxide synthase on macrophages. Eur J Immunol. 1991 Oct;21(10):2489–2494. doi: 10.1002/eji.1830211027. [DOI] [PubMed] [Google Scholar]
  42. Marcinkiewicz J., Ptak W. Macrophage suppressor factor in contact sensitivity. Mechanisms of its release and action. Immunology. 1980 Sep;41(1):211–216. [PMC free article] [PubMed] [Google Scholar]
  43. Mills C. D. Molecular basis of "suppressor" macrophages. Arginine metabolism via the nitric oxide synthetase pathway. J Immunol. 1991 Apr 15;146(8):2719–2723. [PubMed] [Google Scholar]
  44. Mitra R. S., Judge T. A., Nestle F. O., Turka L. A., Nickoloff B. J. Psoriatic skin-derived dendritic cell function is inhibited by exogenous IL-10. Differential modulation of B7-1 (CD80) and B7-2 (CD86) expression. J Immunol. 1995 Mar 15;154(6):2668–2677. [PubMed] [Google Scholar]
  45. Mizushima Y., Wepsic H. T., Yamamura Y., Desilva M. A. Tumour-induced suppressor macrophages in rats: differences in their suppressive effects on the Con A and PHA responses. Clin Exp Immunol. 1984 Aug;57(2):371–379. [PMC free article] [PubMed] [Google Scholar]
  46. Modolell M., Corraliza I. M., Link F., Soler G., Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol. 1995 Apr;25(4):1101–1104. doi: 10.1002/eji.1830250436. [DOI] [PubMed] [Google Scholar]
  47. Mues B., Langer D., Zwadlo G., Sorg C. Phenotypic characterization of macrophages in human term placenta. Immunology. 1989 Jul;67(3):303–307. [PMC free article] [PubMed] [Google Scholar]
  48. Murray A. G., Libby P., Pober J. S. Human vascular smooth muscle cells poorly co-stimulate and actively inhibit allogeneic CD4+ T cell proliferation in vitro. J Immunol. 1995 Jan 1;154(1):151–161. [PubMed] [Google Scholar]
  49. Najar H. M., Ruhl S., Bru-Capdeville A. C., Peters J. H. Adenosine and its derivatives control human monocyte differentiation into highly accessory cells versus macrophages. J Leukoc Biol. 1990 May;47(5):429–439. doi: 10.1002/jlb.47.5.429. [DOI] [PubMed] [Google Scholar]
  50. Nakano Y., Nakano K. Non-specific regulatory mechanism of contact sensitivity: induction of macrophage-like suppressor cells and their factors with hapten-conjugated lymphoid cells. Immunology. 1985 Feb;54(2):297–305. [PMC free article] [PubMed] [Google Scholar]
  51. Nestle F. O., Turka L. A., Nickoloff B. J. Characterization of dermal dendritic cells in psoriasis. Autostimulation of T lymphocytes and induction of Th1 type cytokines. J Clin Invest. 1994 Jul;94(1):202–209. doi: 10.1172/JCI117308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Oehler J. R., Herberman R. B., Campbell D. A., Jr, Djeu J. Y. Inhibition of rat mixed lymphocyte cultures by suppressor macrophages. Cell Immunol. 1977 Mar 15;29(2):238–250. doi: 10.1016/0008-8749(77)90319-7. [DOI] [PubMed] [Google Scholar]
  53. Pak A. S., Ip G., Wright M. A., Young M. R. Treating tumor-bearing mice with low-dose gamma-interferon plus tumor necrosis factor alpha to diminish immune suppressive granulocyte-macrophage progenitor cells increases responsiveness to interleukin 2 immunotherapy. Cancer Res. 1995 Feb 15;55(4):885–890. [PubMed] [Google Scholar]
  54. Poulter L. W., Janossy G., Power C., Sreenan S., Burke C. Immunological/physiological relationships in asthma: potential regulation by lung macrophages. Immunol Today. 1994 Jun;15(6):258–261. doi: 10.1016/0167-5699(94)90004-3. [DOI] [PubMed] [Google Scholar]
  55. Pretell J. O., Falchuk Z. M. Generation of suppressor macrophages during the human autologous mixed lymphocyte reaction. Clin Exp Immunol. 1986 Jul;65(1):158–164. [PMC free article] [PubMed] [Google Scholar]
  56. Ptak W., Zembala M., Gershon R. K. Intermediary role of macrophages in the passage of suppressor signals between T-cell subsets. J Exp Med. 1978 Aug 1;148(2):424–434. doi: 10.1084/jem.148.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Saha B., Das G., Vohra H., Ganguly N. K., Mishra G. C. Macrophage-T cell interaction in experimental mycobacterial infection. Selective regulation of co-stimulatory molecules on Mycobacterium-infected macrophages and its implication in the suppression of cell-mediated immune response. Eur J Immunol. 1994 Nov;24(11):2618–2624. doi: 10.1002/eji.1830241108. [DOI] [PubMed] [Google Scholar]
  58. Schlaak J. F., Buslau M., Jochum W., Hermann E., Girndt M., Gallati H., Meyer zum Büschenfelde K. H., Fleischer B. T cells involved in psoriasis vulgaris belong to the Th1 subset. J Invest Dermatol. 1994 Feb;102(2):145–149. doi: 10.1111/1523-1747.ep12371752. [DOI] [PubMed] [Google Scholar]
  59. Sestini P., Tagliabue A., Boraschi D. Modulation of macrophage suppressive activity and prostaglandin release by lymphokines and interferon: comparison of alveolar, pleural and peritoneal macrophages. Clin Exp Immunol. 1984 Dec;58(3):573–580. [PMC free article] [PubMed] [Google Scholar]
  60. Shibata Y., Shibuya E., Ishida N. Relationships between suppressor macrophages and macrophage precursors in the spleens from tumor-bearing mice. Cell Immunol. 1984 Apr 15;85(1):45–57. doi: 10.1016/0008-8749(84)90276-4. [DOI] [PubMed] [Google Scholar]
  61. Spiteri M. A., Knight R. A., Jeremy J. Y., Barnes P. J., Chung K. F. Alveolar macrophage-induced suppression of peripheral blood mononuclear cell responsiveness is reversed by in vitro allergen exposure in bronchial asthma. Eur Respir J. 1994 Aug;7(8):1431–1438. doi: 10.1183/09031936.94.07081431. [DOI] [PubMed] [Google Scholar]
  62. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med. 1992 Jul 1;176(1):287–292. doi: 10.1084/jem.176.1.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Stout R. D., Fisher M. Suppression of lymphocyte proliferative responses: demonstration of two stages occurring in the in vitro generation of suppressor macrophages. J Immunol. 1983 Apr;130(4):1580–1585. [PubMed] [Google Scholar]
  64. Strassmann G., Patil-Koota V., Finkelman F., Fong M., Kambayashi T. Evidence for the involvement of interleukin 10 in the differential deactivation of murine peritoneal macrophages by prostaglandin E2. J Exp Med. 1994 Dec 1;180(6):2365–2370. doi: 10.1084/jem.180.6.2365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sutton L., Gadd M., Mason D. Y., Redman C. W. Cells bearing class II MHC antigens in the human placenta and amniochorion. Immunology. 1986 May;58(1):23–29. [PMC free article] [PubMed] [Google Scholar]
  66. Szczepanik M., Bryniarski K., Pryjma J., Ptak W. Distinct populations of antigen-presenting macrophages are required for induction of effector and regulatory cells in contact sensitivity response in mice. J Leukoc Biol. 1993 Mar;53(3):320–326. doi: 10.1002/jlb.53.3.320. [DOI] [PubMed] [Google Scholar]
  67. Szekanecz Z., Haines G. K., Lin T. R., Harlow L. A., Goerdt S., Rayan G., Koch A. E. Differential distribution of intercellular adhesion molecules (ICAM-1, ICAM-2, and ICAM-3) and the MS-1 antigen in normal and diseased human synovia. Their possible pathogenetic and clinical significance in rheumatoid arthritis. Arthritis Rheum. 1994 Feb;37(2):221–231. doi: 10.1002/art.1780370211. [DOI] [PubMed] [Google Scholar]
  68. Taramelli D., Holden H. T., Varesio L. In vitro induction of tumoricidal and suppressor macrophages by lymphokines: possible feedback regulation. J Immunol. 1981 Jun;126(6):2123–2128. [PubMed] [Google Scholar]
  69. Topoll H. H., Zwadlo G., Lange D. E., Sorg C. Phenotypic dynamics of macrophage subpopulations during human experimental gingivitis. J Periodontal Res. 1989 Mar;24(2):106–112. doi: 10.1111/j.1600-0765.1989.tb00864.x. [DOI] [PubMed] [Google Scholar]
  70. Uyemura K., Yamamura M., Fivenson D. F., Modlin R. L., Nickoloff B. J. The cytokine network in lesional and lesion-free psoriatic skin is characterized by a T-helper type 1 cell-mediated response. J Invest Dermatol. 1993 Nov;101(5):701–705. doi: 10.1111/1523-1747.ep12371679. [DOI] [PubMed] [Google Scholar]
  71. Veit B. C. Immunoregulatory activity of culture-induced suppressor macrophages. Cell Immunol. 1982 Sep 1;72(1):14–27. doi: 10.1016/0008-8749(82)90279-9. [DOI] [PubMed] [Google Scholar]
  72. Vollmer S., Menssen A., Trommler P., Schendel D., Prinz J. C. T lymphocytes derived from skin lesions of patients with psoriasis vulgaris express a novel cytokine pattern that is distinct from that of T helper type 1 and T helper type 2 cells. Eur J Immunol. 1994 Oct;24(10):2377–2382. doi: 10.1002/eji.1830241018. [DOI] [PubMed] [Google Scholar]
  73. Walsh L. J., Goerdt S., Pober J. S., Sueki H., Murphy G. F. MS-1 sinusoidal endothelial antigen is expressed by factor XIIIa+, HLA-DR+ dermal perivascular dendritic cells. Lab Invest. 1991 Dec;65(6):732–741. [PubMed] [Google Scholar]
  74. Webb P. J., Brooks C. G. Macrophage-like suppressor cells in rats. I. Inhibition of natural macrophage-like suppressor cells by red blood cells. Cell Immunol. 1980 Jul 1;52(2):370–380. doi: 10.1016/0008-8749(80)90358-5. [DOI] [PubMed] [Google Scholar]
  75. Wenzel I., Roth J., Sorg C. Identification of a novel surface molecule, RM3/1, that contributes to the adhesion of glucocorticoid-induced human monocytes to endothelial cells. Eur J Immunol. 1996 Nov;26(11):2758–2763. doi: 10.1002/eji.1830261131. [DOI] [PubMed] [Google Scholar]
  76. Zwadlo-Klarwasser G., Bent S., Haubeck H. D., Sorg C., Schmutzler W. Glucocorticoid-induced appearance of the macrophage subtype RM 3/1 in peripheral blood of man. Int Arch Allergy Appl Immunol. 1990;91(2):175–180. doi: 10.1159/000235111. [DOI] [PubMed] [Google Scholar]
  77. Zwadlo G., Voegeli R., Schulze Osthoff K., Sorg C. A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the down-regulatory phase of the inflammatory process. Exp Cell Biol. 1987;55(6):295–304. doi: 10.1159/000163432. [DOI] [PubMed] [Google Scholar]
  78. te Velde A. A., Huijbens R. J., de Vries J. E., Figdor C. G. IL-4 decreases Fc gamma R membrane expression and Fc gamma R-mediated cytotoxic activity of human monocytes. J Immunol. 1990 Apr 15;144(8):3046–3051. [PubMed] [Google Scholar]
  79. van der Pouw Kraan T. C., Boeije L. C., Smeenk R. J., Wijdenes J., Aarden L. A. Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production. J Exp Med. 1995 Feb 1;181(2):775–779. doi: 10.1084/jem.181.2.775. [DOI] [PMC free article] [PubMed] [Google Scholar]

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