Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1996 Jul 1;98(1):50–61. doi: 10.1172/JCI118777

Soluble beta-glucan polysaccharide binding to the lectin site of neutrophil or natural killer cell complement receptor type 3 (CD11b/CD18) generates a primed state of the receptor capable of mediating cytotoxicity of iC3b-opsonized target cells.

V Vetvicka 1, B P Thornton 1, G D Ross 1
PMCID: PMC507400  PMID: 8690804

Abstract

When phagocyte CR3 binds to iC3b on bacteria or yeast, phagocytosis and degranulation are triggered because of simultaneous recognition of iC3b via a CD11b I-domain binding site and specific microbial polysaccharides via a lectin site located COOH-terminal to the I-domain. By contrast, when phagocyte or natural killer (NK) cell CR3 adheres to iC3b on erythrocytes or tumor cells that lack CR3-binding membrane polysaccharides, neither lysis nor cytotoxicity are stimulated. This investigation showed that soluble CR3-specific polysaccharides such as beta-glucan induced a primed state of CR3 that could trigger killing of iC3b-target cells that were otherwise resistant to cytotoxicity. Anti-CR3 added before sugars prevented priming, whereas anti-CR3 added after sugars blocked primed CR3 attachment to iC3b-targets. Polysaccharide priming required tyrosine kinase(s) and a magnesium-dependent conformational change of the I-domain that exposed the CBRM1/5 activation epitope. Unlike LPS or cytokines, polysaccharides did not up-regulate neutrophil CR3 expression nor expose the mAb 24 reporter epitope representing the high affinity ICAM-1-binding state. The current data apparently explain the mechanism of tumoricidal beta-glucans used for immunotherapy. These polysaccharides function through binding to phagocyte or NK cell CR3, priming the receptor for cytotoxicity of neoplastic tissues that are frequently targeted with iC3b and sparing normal tissues that lack iC3b.

Full Text

The Full Text of this article is available as a PDF (373.6 KB).

Selected References

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

  1. Akimoto M., Nishihira T., Kasai M. [Modulation of the anti-tumor effect of BRM under various nutritional or endocrine conditions]. Gan To Kagaku Ryoho. 1986 Apr;13(4 Pt 2):1270–1276. [PubMed] [Google Scholar]
  2. Amino M., Noguchi R., Yata J., Matsumura J., Hirayama R., Abe O., Enomoto K., Asato Y. [Studies on the effect of lentinan on human immune system. II. In vivo effect on NK activity, MLR induced killer activity and PHA induced blastic response of lymphocytes in cancer patients]. Gan To Kagaku Ryoho. 1983 Sep;10(9):2000–2006. [PubMed] [Google Scholar]
  3. Ault K. A., Springer T. A. Cross-reaction of a rat-anti-mouse phagocyte-specific monoclonal antibody (anti-Mac-1) with human monocytes and natural killer cells. J Immunol. 1981 Jan;126(1):359–364. [PubMed] [Google Scholar]
  4. BRADNER W. T., CLARKE D. A., STOCK C. C. Stimulation of host defense against experimental cancer. I. Zymosan and sarcoma 180 in mice. Cancer Res. 1958 Apr;18(3):347–351. [PubMed] [Google Scholar]
  5. Baker H. M., Brown R. L., Dobbs A. J., Blackwell L. F., Buckley P. D., Hardman M. J., Hill J. P., Kitson K. E., Kitson T. M., Baker E. N. Crystallization and preliminary X-ray diffraction studies on cytosolic (class 1) aldehyde dehydrogenase from sheep liver. J Mol Biol. 1994 Aug 12;241(2):263–264. doi: 10.1006/jmbi.1994.1494. [DOI] [PubMed] [Google Scholar]
  6. Bayer E. A., Wilchek M. The use of the avidin-biotin complex as a tool in molecular biology. Methods Biochem Anal. 1980;26:1–45. doi: 10.1002/9780470110461.ch1. [DOI] [PubMed] [Google Scholar]
  7. Berger M., O'Shea J., Cross A. S., Folks T. M., Chused T. M., Brown E. J., Frank M. M. Human neutrophils increase expression of C3bi as well as C3b receptors upon activation. J Clin Invest. 1984 Nov;74(5):1566–1571. doi: 10.1172/JCI111572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Berton G., Fumagalli L., Laudanna C., Sorio C. Beta 2 integrin-dependent protein tyrosine phosphorylation and activation of the FGR protein tyrosine kinase in human neutrophils. J Cell Biol. 1994 Aug;126(4):1111–1121. doi: 10.1083/jcb.126.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bohuslav J., Horejsí V., Hansmann C., Stöckl J., Weidle U. H., Majdic O., Bartke I., Knapp W., Stockinger H. Urokinase plasminogen activator receptor, beta 2-integrins, and Src-kinases within a single receptor complex of human monocytes. J Exp Med. 1995 Apr 1;181(4):1381–1390. doi: 10.1084/jem.181.4.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Breard J., Reinherz E. L., Kung P. C., Goldstein G., Schlossman S. F. A monoclonal antibody reactive with human peripheral blood monocytes. J Immunol. 1980 Apr;124(4):1943–1948. [PubMed] [Google Scholar]
  11. Buyon J. P., Abramson S. B., Philips M. R., Slade S. G., Ross G. D., Weissmann G., Winchester R. J. Dissociation between increased surface expression of gp165/95 and homotypic neutrophil aggregation. J Immunol. 1988 May 1;140(9):3156–3160. [PubMed] [Google Scholar]
  12. Cain J. A., Newman S. L., Ross G. D. Role of complement receptor type three and serum opsonins in the neutrophil response to yeast. Complement. 1987;4(2):75–86. doi: 10.1159/000463011. [DOI] [PubMed] [Google Scholar]
  13. Cao D., Mizukami I. F., Garni-Wagner B. A., Kindzelskii A. L., Todd R. F., 3rd, Boxer L. A., Petty H. R. Human urokinase-type plasminogen activator primes neutrophils for superoxide anion release. Possible roles of complement receptor type 3 and calcium. J Immunol. 1995 Feb 15;154(4):1817–1829. [PubMed] [Google Scholar]
  14. Chen J. T., Hasumi K. Activation of peritoneal macrophages in patients with gynecological malignancies by sizofiran and recombinant interferon-gamma. Biotherapy. 1993;6(3):189–194. doi: 10.1007/BF01878080. [DOI] [PubMed] [Google Scholar]
  15. Chihara G. Recent progress in immunopharmacology and therapeutic effects of polysaccharides. Dev Biol Stand. 1992;77:191–197. [PubMed] [Google Scholar]
  16. Czop J. K. The role of beta-glucan receptors on blood and tissue leukocytes in phagocytosis and metabolic activation. Pathol Immunopathol Res. 1986;5(3-5):286–296. doi: 10.1159/000157022. [DOI] [PubMed] [Google Scholar]
  17. DILLER I. C., MANKOWSKI Z. T., FISHER M. E. The effect of yeast polysaccharides on mouse tumors. Cancer Res. 1963 Feb;23:201–208. [PubMed] [Google Scholar]
  18. Di Renzo L., Yefenof E., Klein E. The function of human NK cells is enhanced by beta-glucan, a ligand of CR3 (CD11b/CD18). Eur J Immunol. 1991 Jul;21(7):1755–1758. doi: 10.1002/eji.1830210726. [DOI] [PubMed] [Google Scholar]
  19. Diamond M. S., Springer T. A. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J Cell Biol. 1993 Jan;120(2):545–556. doi: 10.1083/jcb.120.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dransfield I., Cabañas C., Craig A., Hogg N. Divalent cation regulation of the function of the leukocyte integrin LFA-1. J Cell Biol. 1992 Jan;116(1):219–226. doi: 10.1083/jcb.116.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dransfield I., Hogg N. Regulated expression of Mg2+ binding epitope on leukocyte integrin alpha subunits. EMBO J. 1989 Dec 1;8(12):3759–3765. doi: 10.1002/j.1460-2075.1989.tb08552.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Eddy A., Newman S. L., Cosio F., LeBien T., Michael A. The distribution of the CR3 receptor on human cells and tissue as revealed by a monoclonal antibody. Clin Immunol Immunopathol. 1984 Jun;31(3):371–389. doi: 10.1016/0090-1229(84)90090-4. [DOI] [PubMed] [Google Scholar]
  23. Einspahr K. J., Abraham R. T., Binstadt B. A., Uehara Y., Leibson P. J. Tyrosine phosphorylation provides an early and requisite signal for the activation of natural killer cell cytotoxic function. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6279–6283. doi: 10.1073/pnas.88.14.6279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fujimoto T., Omote K., Mai M., Natsuume-Sakai S. Evaluation of basic procedures for adoptive immunotherapy for gastric cancer. Biotherapy. 1992;5(2):153–163. doi: 10.1007/BF02171701. [DOI] [PubMed] [Google Scholar]
  25. Gavioli R., Spisani S., Giuliani A. L., Cosulich E., Risso A., Traniello S. CD16 and CR3 receptors distinguish between the two mechanisms of tumour cytotoxicity in neutrophils. Br J Haematol. 1991 Oct;79(2):170–176. doi: 10.1111/j.1365-2141.1991.tb04518.x. [DOI] [PubMed] [Google Scholar]
  26. Goldman R., Ferber E., Meller R., Zor U. A role for reactive oxygen species in zymosan and beta-glucan induced protein tyrosine phosphorylation and phospholipase A2 activation in murine macrophages. Biochim Biophys Acta. 1994 Jun 30;1222(2):265–276. doi: 10.1016/0167-4889(94)90178-3. [DOI] [PubMed] [Google Scholar]
  27. Gyetko M. R., Sitrin R. G., Fuller J. A., Todd R. F., 3rd, Petty H., Standiford T. J. Function of the urokinase receptor (CD87) in neutrophil chemotaxis. J Leukoc Biol. 1995 Nov;58(5):533–538. doi: 10.1002/jlb.58.5.533. [DOI] [PubMed] [Google Scholar]
  28. Hogg N., Berlin C. Structure and function of adhesion receptors in leukocyte trafficking. Immunol Today. 1995 Jul;16(7):327–330. doi: 10.1016/0167-5699(95)80147-2. [DOI] [PubMed] [Google Scholar]
  29. Kasai S., Fujimoto S., Nitta K., Baba H., Kunimoto T. Antitumor activity of polymorphonuclear leukocytes activated by a beta-1,3-D-glucan. J Pharmacobiodyn. 1991 Sep;14(9):519–525. doi: 10.1248/bpb1978.14.519. [DOI] [PubMed] [Google Scholar]
  30. Kishimoto T. K., Jutila M. A., Berg E. L., Butcher E. C. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science. 1989 Sep 15;245(4923):1238–1241. doi: 10.1126/science.2551036. [DOI] [PubMed] [Google Scholar]
  31. Klein E., Di Renzo L., Yefenof E. Contribution of CR3, CD11b/CD18 to cytolysis by human NK cells. Mol Immunol. 1990 Dec;27(12):1343–1347. doi: 10.1016/0161-5890(90)90041-w. [DOI] [PubMed] [Google Scholar]
  32. Komatsu N., Okubo S., Kikumoto S., Kimura K., Saito G. Host-mediated antitumor action of schizophyllan, a glucan produced by Schizophyllum commune. Gan. 1969 Apr;60(2):137–144. [PubMed] [Google Scholar]
  33. Kotera Y., Fontenot J. D., Pecher G., Metzgar R. S., Finn O. J. Humoral immunity against a tandem repeat epitope of human mucin MUC-1 in sera from breast, pancreatic, and colon cancer patients. Cancer Res. 1994 Jun 1;54(11):2856–2860. [PubMed] [Google Scholar]
  34. Krauss J. C., PooH, Xue W., Mayo-Bond L., Todd R. F., 3rd, Petty H. R. Reconstitution of antibody-dependent phagocytosis in fibroblasts expressing Fc gamma receptor IIIB and the complement receptor type 3. J Immunol. 1994 Aug 15;153(4):1769–1777. [PubMed] [Google Scholar]
  35. Krych M., Atkinson J. P., Holers V. M. Complement receptors. Curr Opin Immunol. 1992 Feb;4(1):8–13. doi: 10.1016/0952-7915(92)90116-v. [DOI] [PubMed] [Google Scholar]
  36. Limb G. A., Hamblin A. S., Wolstencroft R. A., Dumonde D. C. Selective up-regulation of human granulocyte integrins and complement receptor 1 by cytokines. Immunology. 1991 Dec;74(4):696–702. [PMC free article] [PubMed] [Google Scholar]
  37. Lotzová E., Gutterman J. U. Effect of glucan on natural killer (NK) cells: further comparison between NK cell and bone marrow effector cell activities. J Immunol. 1979 Aug;123(2):607–611. [PubMed] [Google Scholar]
  38. Maeda Y. Y., Sakaizumi M., Moriwaki K., Chihara G., Yonekawa H. Genetical control on lentinan-induced acute phase responses and vascular responses. Folia Histochem Cytobiol. 1992;30(4):207–209. [PubMed] [Google Scholar]
  39. Morikawa K., Takeda R., Yamazaki M., Mizuno D. Induction of tumoricidal activity of polymorphonuclear leukocytes by a linear beta-1,3-D-glucan and other immunomodulators in murine cells. Cancer Res. 1985 Apr;45(4):1496–1501. [PubMed] [Google Scholar]
  40. Muto S., Vetvicka V., Ross G. D. CR3 (CD11b/CD18) expressed by cytotoxic T cells and natural killer cells is upregulated in a manner similar to neutrophil CR3 following stimulation with various activating agents. J Clin Immunol. 1993 May;13(3):175–184. doi: 10.1007/BF00919970. [DOI] [PubMed] [Google Scholar]
  41. Myones B. L., Dalzell J. G., Hogg N., Ross G. D. Neutrophil and monocyte cell surface p150,95 has iC3b-receptor (CR4) activity resembling CR3. J Clin Invest. 1988 Aug;82(2):640–651. doi: 10.1172/JCI113643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Naccache P. H., Jean N., Liao N. W., Bator J. M., McColl S. R., Kubes P. Regulation of stimulated integrin surface expression in human neutrophils by tyrosine phosphorylation. Blood. 1994 Jul 15;84(2):616–624. [PubMed] [Google Scholar]
  43. Neuman E., Huleatt J. W., Jack R. M. Granulocyte-macrophage colony-stimulating factor increases synthesis and expression of CR1 and CR3 by human peripheral blood neutrophils. J Immunol. 1990 Nov 15;145(10):3325–3332. [PubMed] [Google Scholar]
  44. Niculescu F., Rus H. G., Retegan M., Vlaicu R. Persistent complement activation on tumor cells in breast cancer. Am J Pathol. 1992 May;140(5):1039–1043. [PMC free article] [PubMed] [Google Scholar]
  45. Oka M., Yoshino S., Hazama S., Shimoda K., Suzuki T. Immunological analysis and clinical effects of intraabdominal and intrapleural injection of lentinan for malignant ascites and pleural effusion. Biotherapy. 1992;5(2):107–112. doi: 10.1007/BF02171695. [DOI] [PubMed] [Google Scholar]
  46. Ortlepp S., Stephens P. E., Hogg N., Figdor C. G., Robinson M. K. Antibodies that activate beta 2 integrins can generate different ligand binding states. Eur J Immunol. 1995 Mar;25(3):637–643. doi: 10.1002/eji.1830250302. [DOI] [PubMed] [Google Scholar]
  47. Pavlović M. D., Colić M., Pejnović N., Tamatani T., Miyasaka M., Dujić A. A novel anti-rat CD18 monoclonal antibody triggers lymphocyte homotypic aggregation and granulocyte adhesion to plastic: different intracellular signaling pathways in resting versus activated thymocytes. Eur J Immunol. 1994 Jul;24(7):1640–1648. doi: 10.1002/eji.1830240728. [DOI] [PubMed] [Google Scholar]
  48. Perlmann H., Perlmann P., Schreiber R. D., Müller-Eberhard H. J. Interaction of target cell-bound C3bi and C3d with human lymphocyte receptors. Enhancement of antibody-mediated cellular cytotoxicity. J Exp Med. 1981 Jun 1;153(6):1592–1603. doi: 10.1084/jem.153.6.1592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Perlmann P., Perlmann H., Müller-Eberhard H. J. Cytolytic lymphocytic cells with complement receptor in human blood. Induction of cytolysis by IgG antibody but not by target cell-bound C3. J Exp Med. 1975 Feb 1;141(2):287–296. doi: 10.1084/jem.141.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Petty H. R., Todd R. F., 3rd Receptor-receptor interactions of complement receptor type 3 in neutrophil membranes. J Leukoc Biol. 1993 Nov;54(5):492–494. doi: 10.1002/jlb.54.5.492. [DOI] [PubMed] [Google Scholar]
  51. Pretus H. A., Ensley H. E., McNamee R. B., Jones E. L., Browder I. W., Williams D. L. Isolation, physicochemical characterization and preclinical efficacy evaluation of soluble scleroglucan. J Pharmacol Exp Ther. 1991 Apr;257(1):500–510. [PubMed] [Google Scholar]
  52. Ramos O. F., Nilsson B., Nilsson K., Eggertsen G., Yefenof E., Klein E. Elevated NK-mediated lysis of Raji and Daudi cells carrying fixed iC3b fragments. Cell Immunol. 1989 Apr 1;119(2):459–469. doi: 10.1016/0008-8749(89)90258-x. [DOI] [PubMed] [Google Scholar]
  53. Robinson M. K., Andrew D., Rosen H., Brown D., Ortlepp S., Stephens P., Butcher E. C. Antibody against the Leu-CAM beta-chain (CD18) promotes both LFA-1- and CR3-dependent adhesion events. J Immunol. 1992 Feb 15;148(4):1080–1085. [PubMed] [Google Scholar]
  54. Ross G. D., Cain J. A., Myones B. L., Newman S. L., Lachmann P. J. Specificity of membrane complement receptor type three (CR3) for beta-glucans. Complement. 1987;4(2):61–74. doi: 10.1159/000463010. [DOI] [PubMed] [Google Scholar]
  55. Roubey R. A., Ross G. D., Merrill J. T., Walton F., Reed W., Winchester R. J., Buyon J. P. Staurosporine inhibits neutrophil phagocytosis but not iC3b binding mediated by CR3 (CD11b/CD18). J Immunol. 1991 May 15;146(10):3557–3562. [PubMed] [Google Scholar]
  56. Sakaguchi T., Watahiki Y., Kosaka A. [A case of breast cancer with thrombosis during treatment of lung metastasis]. Gan To Kagaku Ryoho. 1993 Mar;20(4):525–528. [PubMed] [Google Scholar]
  57. Sanguedolce M. V., Capo C., Bouhamdan M., Bongrand P., Huang C. K., Mege J. L. Zymosan-induced tyrosine phosphorylations in human monocytes. Role of protein kinase C. J Immunol. 1993 Jul 1;151(1):405–414. [PubMed] [Google Scholar]
  58. Sato Y., Sakai T., Okada T., Sasano Y., Ando T., Haruta J., Kanayama K., Kuwahara Y., Tachino H., Tahara H. [A case of unresectable pancreatic cancer that responded to UFT chemotherapy]. Gan No Rinsho. 1990 Sep;36(11):2073–2078. [PubMed] [Google Scholar]
  59. Schulz T. F., Scharfenberger H., Lambris J. D., Rieber P., Riethmüller G., Dierich M. P. Antigenic relationship between the alpha-chain of C3, a leucocyte-surface antigen involved in the activation of phagocytic cells, and a 50,000 MW B-cell antigen. Immunology. 1985 Apr;54(4):791–800. [PMC free article] [PubMed] [Google Scholar]
  60. Sehgal G., Zhang K., Todd R. F., 3rd, Boxer L. A., Petty H. R. Lectin-like inhibition of immune complex receptor-mediated stimulation of neutrophils. Effects on cytosolic calcium release and superoxide production. J Immunol. 1993 May 15;150(10):4571–4580. [PubMed] [Google Scholar]
  61. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
  62. Stöckl J., Majdic O., Pickl W. F., Rosenkranz A., Prager E., Gschwantler E., Knapp W. Granulocyte activation via a binding site near the C-terminal region of complement receptor type 3 alpha-chain (CD11b) potentially involved in intramembrane complex formation with glycosylphosphatidylinositol-anchored Fc gamma RIIIB (CD16) molecules. J Immunol. 1995 May 15;154(10):5452–5463. [PubMed] [Google Scholar]
  63. Sugie K., Nakamura K., Teshigawara K., Diamond M. S., Springer T. A., Nakamura Y., Leonard W. J., Uchida A., Yodoi J. Activation of natural killer cells by the mAb YTA-1 that recognizes leukocyte function-associated antigen-1. Int Immunol. 1995 May;7(5):763–769. doi: 10.1093/intimm/7.5.763. [DOI] [PubMed] [Google Scholar]
  64. Suzuki I., Hashimoto K., Oikawa S., Sato K., Osawa M., Yadomae T. Antitumor and immunomodulating activities of a beta-glucan obtained from liquid-cultured Grifola frondosa. Chem Pharm Bull (Tokyo) 1989 Feb;37(2):410–413. doi: 10.1248/cpb.37.410. [DOI] [PubMed] [Google Scholar]
  65. Taguchi T. Clinical efficacy of lentinan on patients with stomach cancer: end point results of a four-year follow-up survey. Cancer Detect Prev Suppl. 1987;1:333–349. [PubMed] [Google Scholar]
  66. Taguchi T., Furue H., Kimura T., Kondo T., Hattori T., Ogawa N. Clinical efficacy of lentinan on neoplastic diseases. Adv Exp Med Biol. 1983;166:181–187. doi: 10.1007/978-1-4757-1410-4_15. [DOI] [PubMed] [Google Scholar]
  67. Tani M., Tanimura H., Yamaue H., Iwahashi M., Tsunoda T., Tamai M., Noguchi K., Arii K. In vitro generation of activated natural killer cells and cytotoxic macrophages with lentinan. Eur J Clin Pharmacol. 1992;42(6):623–627. doi: 10.1007/BF00265926. [DOI] [PubMed] [Google Scholar]
  68. Tari K., Satake I., Nakagomi K., Ozawa K., Oowada F., Higashi Y., Negishi T., Yamada T., Saito H., Yoshida K. [Effect of lentinan for advanced prostate carcinoma]. Hinyokika Kiyo. 1994 Feb;40(2):119–123. [PubMed] [Google Scholar]
  69. Thornton B. P., Vetvicka V., Pitman M., Goldman R. C., Ross G. D. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol. 1996 Feb 1;156(3):1235–1246. [PubMed] [Google Scholar]
  70. Timonen T., Reynolds C. W., Ortaldo J. R., Herberman R. B. Isolation of human and rat natural killer cells. J Immunol Methods. 1982;51(3):269–277. doi: 10.1016/0022-1759(82)90393-3. [DOI] [PubMed] [Google Scholar]
  71. Williams D. L., Sherwood E. R., Browder I. W., McNamee R. B., Jones E. L., Di Luzio N. R. Pre-clinical safety evaluation of soluble glucan. Int J Immunopharmacol. 1988;10(4):405–414. doi: 10.1016/0192-0561(88)90127-0. [DOI] [PubMed] [Google Scholar]
  72. Wright S. D., Meyer B. C. Phorbol esters cause sequential activation and deactivation of complement receptors on polymorphonuclear leukocytes. J Immunol. 1986 Mar 1;136(5):1759–1764. [PubMed] [Google Scholar]
  73. Wright S. D., Silverstein S. C. Tumor-promoting phorbol esters stimulate C3b and C3b' receptor-mediated phagocytosis in cultured human monocytes. J Exp Med. 1982 Oct 1;156(4):1149–1164. doi: 10.1084/jem.156.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Xue W., Kindzelskii A. L., Todd R. F., 3rd, Petty H. R. Physical association of complement receptor type 3 and urokinase-type plasminogen activator receptor in neutrophil membranes. J Immunol. 1994 May 1;152(9):4630–4640. [PubMed] [Google Scholar]
  75. Yoshino S., Oka M., Hazama S., Suzuki T. [Effect of intrapleural and/or intraperitoneal lentinan therapy in carcinomatous pleuritis and peritonitis]. Gan To Kagaku Ryoho. 1990 Aug;17(8 Pt 2):1588–1591. [PubMed] [Google Scholar]
  76. Zaffran Y., Escallier J. C., Ruta S., Capo C., Mege J. L. Zymosan-triggered association of tyrosine phosphoproteins and lyn kinase with cytoskeleton in human monocytes. J Immunol. 1995 Apr 1;154(7):3488–3497. [PubMed] [Google Scholar]
  77. Zarewych D. M., Kindzelskii A. L., Todd R. F., 3rd, Petty H. R. LPS induces CD14 association with complement receptor type 3, which is reversed by neutrophil adhesion. J Immunol. 1996 Jan 15;156(2):430–433. [PubMed] [Google Scholar]
  78. Zhou M. J., Lublin D. M., Link D. C., Brown E. J. Distinct tyrosine kinase activation and Triton X-100 insolubility upon Fc gamma RII or Fc gamma RIIIB ligation in human polymorphonuclear leukocytes. Implications for immune complex activation of the respiratory burst. J Biol Chem. 1995 Jun 2;270(22):13553–13560. doi: 10.1074/jbc.270.22.13553. [DOI] [PubMed] [Google Scholar]
  79. Zhou M., Todd R. F., 3rd, van de Winkel J. G., Petty H. R. Cocapping of the leukoadhesin molecules complement receptor type 3 and lymphocyte function-associated antigen-1 with Fc gamma receptor III on human neutrophils. Possible role of lectin-like interactions. J Immunol. 1993 Apr 1;150(7):3030–3041. [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES