Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Dec 1;109(6):3169–3182. doi: 10.1083/jcb.109.6.3169

Adhesomes: specific granules containing receptors for laminin, C3bi/fibrinogen, fibronectin, and vitronectin in human polymorphonuclear leukocytes and monocytes

PMCID: PMC2115924  PMID: 2480353

Abstract

We have localized several major extracellular matrix protein receptors in the specific granules of human polymorphonuclear (PMN) and monocytic leukocytes using double label immunoelectron microscopy (IEM) with ultrathin frozen sections and colloidal-gold conjugates. Rabbit antibodies to 67-kD human laminin receptor (LNR) were located on the inner surface of the specific granule membrane and within its internal matrix. LNR antigens co-distributed with lactoferrin, a marker of specific granules, but did not co-localize with elastase in azurophilic granules of PMNs. Further, CD11b/CD18 (leukocyte receptor for C3bi, fibrinogen, endothelial cells, and endotoxin), mammalian fibronectin receptor (FNR), and vitronectin receptor (VNR) antigens were also co- localized with LNR in PMN specific granules. A similar type of granule was found in monocytes which stained for LNR, FNR, VNR, CD18, and lysozyme. Activation of PMNs with either PMA, f-met-leu-phe (fMLP), tumor necrosis factor (TNF), or monocytic leukocytes with lipopolysaccharide (LPS), induced fusion of specific granules with the cell membrane and expression of both LNR and CD18 antigens on the outer cell surface. Further, stimulation led to augmented PMN adhesion on LN substrata, and six- to eightfold increases in specific binding of soluble LN that was inhibited by LNR antibody. These results indicate that four types of extracellular matrix receptors are located in leukocyte specific granules, and suggest that up-regulation of these receptors during inflammation may mediate leukocyte adhesion and extravasation. We have thus termed leukocyte specific granules adhesomes.

Full Text

The Full Text of this article is available as a PDF (7.3 MB).

Selected References

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

  1. Anderson D. C., Springer T. A. Leukocyte adhesion deficiency: an inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. Annu Rev Med. 1987;38:175–194. doi: 10.1146/annurev.me.38.020187.001135. [DOI] [PubMed] [Google Scholar]
  2. Aumailley M., Nurcombe V., Edgar D., Paulsson M., Timpl R. The cellular interactions of laminin fragments. Cell adhesion correlates with two fragment-specific high affinity binding sites. J Biol Chem. 1987 Aug 25;262(24):11532–11538. [PubMed] [Google Scholar]
  3. Bainton D. F., Miller L. J., Kishimoto T. K., Springer T. A. Leukocyte adhesion receptors are stored in peroxidase-negative granules of human neutrophils. J Exp Med. 1987 Dec 1;166(6):1641–1653. doi: 10.1084/jem.166.6.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barsky S. H., Rao C. N., Williams J. E., Liotta L. A. Laminin molecular domains which alter metastasis in a murine model. J Clin Invest. 1984 Sep;74(3):843–848. doi: 10.1172/JCI111501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beatty P. G., Ledbetter J. A., Martin P. J., Price T. H., Hansen J. A. Definition of a common leukocyte cell-surface antigen (Lp95-150) associated with diverse cell-mediated immune functions. J Immunol. 1983 Dec;131(6):2913–2918. [PubMed] [Google Scholar]
  6. 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]
  7. Bergmann J. E., Singer S. J. Immunoelectron microscopic studies of the intracellular transport of the membrane glycoprotein (G) of vesicular stomatitis virus in infected Chinese hamster ovary cells. J Cell Biol. 1983 Dec;97(6):1777–1787. doi: 10.1083/jcb.97.6.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bevilacqua M. P., Pober J. S., Mendrick D. L., Cotran R. S., Gimbrone M. A., Jr Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9238–9242. doi: 10.1073/pnas.84.24.9238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bevilacqua M. P., Stengelin S., Gimbrone M. A., Jr, Seed B. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science. 1989 Mar 3;243(4895):1160–1165. doi: 10.1126/science.2466335. [DOI] [PubMed] [Google Scholar]
  10. Bohnsack J. F., Kleinman H. K., Takahashi T., O'Shea J. J., Brown E. J. Connective tissue proteins and phagocytic cell function. Laminin enhances complement and Fc-mediated phagocytosis by cultured human macrophages. J Exp Med. 1985 May 1;161(5):912–923. doi: 10.1084/jem.161.5.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Boonstra J., van Maurik P., Defize L. H., de Laat S. W., Leunissen J. L., Verkley A. J. Visualization of epidermal growth factor receptor in cryosections of cultured A431 cells by immuno-gold labeling. Eur J Cell Biol. 1985 Mar;36(2):209–216. [PubMed] [Google Scholar]
  12. Borregaard N., Heiple J. M., Simons E. R., Clark R. A. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J Cell Biol. 1983 Jul;97(1):52–61. doi: 10.1083/jcb.97.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Bryant G., Rao C. N., Brentani M., Martins W., Lopes J. D., Martin S. E., Liotta L. A., Schiffmann E. A role for the laminin receptor in leukocyte chemotaxis. J Leukoc Biol. 1987 Mar;41(3):220–227. doi: 10.1002/jlb.41.3.220. [DOI] [PubMed] [Google Scholar]
  15. Burn P., Kupfer A., Singer S. J. Dynamic membrane-cytoskeletal interactions: specific association of integrin and talin arises in vivo after phorbol ester treatment of peripheral blood lymphocytes. Proc Natl Acad Sci U S A. 1988 Jan;85(2):497–501. doi: 10.1073/pnas.85.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Chen W. T., Greve J. M., Gottlieb D. I., Singer S. J. Immunocytochemical localization of 140 kD cell adhesion molecules in cultured chicken fibroblasts, and in chicken smooth muscle and intestinal epithelial tissues. J Histochem Cytochem. 1985 Jun;33(6):576–586. doi: 10.1177/33.6.3889142. [DOI] [PubMed] [Google Scholar]
  18. Detmers P. A., Wright S. D., Olsen E., Kimball B., Cohn Z. A. Aggregation of complement receptors on human neutrophils in the absence of ligand. J Cell Biol. 1987 Sep;105(3):1137–1145. doi: 10.1083/jcb.105.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gabig T. G., Schervish E. W., Santinga J. T. Functional relationship of the cytochrome b to the superoxide-generating oxidase of human neutrophils. J Biol Chem. 1982 Apr 25;257(8):4114–4119. [PubMed] [Google Scholar]
  20. Gehlsen K. R., Dillner L., Engvall E., Ruoslahti E. The human laminin receptor is a member of the integrin family of cell adhesion receptors. Science. 1988 Sep 2;241(4870):1228–1229. doi: 10.1126/science.2970671. [DOI] [PubMed] [Google Scholar]
  21. Hand P. H., Thor A., Schlom J., Rao C. N., Liotta L. Expression of laminin receptor in normal and carcinomatous human tissues as defined by a monoclonal antibody. Cancer Res. 1985 Jun;45(6):2713–2719. [PubMed] [Google Scholar]
  22. Hayman E. G., Pierschbacher M. D., Ohgren Y., Ruoslahti E. Serum spreading factor (vitronectin) is present at the cell surface and in tissues. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4003–4007. doi: 10.1073/pnas.80.13.4003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Horwitz A., Duggan K., Greggs R., Decker C., Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985 Dec;101(6):2134–2144. doi: 10.1083/jcb.101.6.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Huard T. K., Malinoff H. L., Wicha M. S. Macrophages express a plasma membrane receptor for basement membrane laminin. Am J Pathol. 1986 May;123(2):365–370. [PMC free article] [PubMed] [Google Scholar]
  25. Humes J. L., Opas E. E., Galavage M., Soderman D., Bonney R. J. Regulation of macrophage eicosanoid production by hydroperoxy-and hydroxy-eicosatetraenoic acids. Biochem J. 1986 Jan 1;233(1):199–206. doi: 10.1042/bj2330199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  27. Ignatius M. J., Reichardt L. F. Identification of a neuronal laminin receptor: an Mr 200K/120K integrin heterodimer that binds laminin in a divalent cation-dependent manner. Neuron. 1988 Oct;1(8):713–725. doi: 10.1016/0896-6273(88)90170-5. [DOI] [PubMed] [Google Scholar]
  28. Kishimoto T. K., O'Connor K., Lee A., Roberts T. M., Springer T. A. Cloning of the beta subunit of the leukocyte adhesion proteins: homology to an extracellular matrix receptor defines a novel supergene family. Cell. 1987 Feb 27;48(4):681–690. doi: 10.1016/0092-8674(87)90246-7. [DOI] [PubMed] [Google Scholar]
  29. Kleinman H. K., Ogle R. C., Cannon F. B., Little C. D., Sweeney T. M., Luckenbill-Edds L. Laminin receptors for neurite formation. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1282–1286. doi: 10.1073/pnas.85.4.1282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lesot H., Kühl U., Mark K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J. 1983;2(6):861–865. doi: 10.1002/j.1460-2075.1983.tb01514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Liotta L. A., Rao C. N., Wewer U. M. Biochemical interactions of tumor cells with the basement membrane. Annu Rev Biochem. 1986;55:1037–1057. doi: 10.1146/annurev.bi.55.070186.005133. [DOI] [PubMed] [Google Scholar]
  32. Lo S. K., Detmers P. A., Levin S. M., Wright S. D. Transient adhesion of neutrophils to endothelium. J Exp Med. 1989 May 1;169(5):1779–1793. doi: 10.1084/jem.169.5.1779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Luedke E. S., Humes J. L. Effect of tumor necrosis factor on granule release and LTB4 production in adherent human polymorphonuclear leukocytes. Agents Actions. 1989 Jun;27(3-4):451–454. doi: 10.1007/BF01972850. [DOI] [PubMed] [Google Scholar]
  34. Marlin S. D., Springer T. A. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell. 1987 Dec 4;51(5):813–819. doi: 10.1016/0092-8674(87)90104-8. [DOI] [PubMed] [Google Scholar]
  35. Martin G. R., Timpl R. Laminin and other basement membrane components. Annu Rev Cell Biol. 1987;3:57–85. doi: 10.1146/annurev.cb.03.110187.000421. [DOI] [PubMed] [Google Scholar]
  36. Mercurio A. M., Shaw L. M. Macrophage interactions with laminin: PMA selectively induces the adherence and spreading of mouse macrophages on a laminin substratum. J Cell Biol. 1988 Nov;107(5):1873–1880. doi: 10.1083/jcb.107.5.1873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Miller L. J., Bainton D. F., Borregaard N., Springer T. A. Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface. J Clin Invest. 1987 Aug;80(2):535–544. doi: 10.1172/JCI113102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Nathan C. F. Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J Clin Invest. 1987 Dec;80(6):1550–1560. doi: 10.1172/JCI113241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nathan C., Srimal S., Farber C., Sanchez E., Kabbash L., Asch A., Gailit J., Wright S. D. Cytokine-induced respiratory burst of human neutrophils: dependence on extracellular matrix proteins and CD11/CD18 integrins. J Cell Biol. 1989 Sep;109(3):1341–1349. doi: 10.1083/jcb.109.3.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nermut M. V., Green N. M., Eason P., Yamada S. S., Yamada K. M. Electron microscopy and structural model of human fibronectin receptor. EMBO J. 1988 Dec 20;7(13):4093–4099. doi: 10.1002/j.1460-2075.1988.tb03303.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. O'Flaherty J. T., Showell H. J., Becker E. L., Ward P. A. Substances which aggregate neutrophils. Mechanism of action. Am J Pathol. 1978 Jul;92(1):155–166. [PMC free article] [PubMed] [Google Scholar]
  42. Paulsson M., Aumailley M., Deutzmann R., Timpl R., Beck K., Engel J. Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur J Biochem. 1987 Jul 1;166(1):11–19. doi: 10.1111/j.1432-1033.1987.tb13476.x. [DOI] [PubMed] [Google Scholar]
  43. Philips M. R., Buyon J. P., Winchester R., Weissmann G., Abramson S. B. Up-regulation of the iC3b receptor (CR3) is neither necessary nor sufficient to promote neutrophil aggregation. J Clin Invest. 1988 Aug;82(2):495–501. doi: 10.1172/JCI113623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pommier C. G., Inada S., Fries L. F., Takahashi T., Frank M. M., Brown E. J. Plasma fibronectin enhances phagocytosis of opsonized particles by human peripheral blood monocytes. J Exp Med. 1983 Jun 1;157(6):1844–1854. doi: 10.1084/jem.157.6.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Rao N. C., Barsky S. H., Terranova V. P., Liotta L. A. Isolation of a tumor cell laminin receptor. Biochem Biophys Res Commun. 1983 Mar 29;111(3):804–808. doi: 10.1016/0006-291x(83)91370-0. [DOI] [PubMed] [Google Scholar]
  46. Rollins T. E., Springer M. S. Identification of the polymorphonuclear leukocyte C5a receptor. J Biol Chem. 1985 Jun 25;260(12):7157–7160. [PubMed] [Google Scholar]
  47. Ruoslahti E. Fibronectin and its receptors. Annu Rev Biochem. 1988;57:375–413. doi: 10.1146/annurev.bi.57.070188.002111. [DOI] [PubMed] [Google Scholar]
  48. Ruoslahti E., Pierschbacher M. D. New perspectives in cell adhesion: RGD and integrins. Science. 1987 Oct 23;238(4826):491–497. doi: 10.1126/science.2821619. [DOI] [PubMed] [Google Scholar]
  49. Sandborg R. R., Smolen J. E. Early biochemical events in leukocyte activation. Lab Invest. 1988 Sep;59(3):300–320. [PubMed] [Google Scholar]
  50. Schwartz B. R., Ochs H. D., Beatty P. G., Harlan J. M. A monoclonal antibody-defined membrane antigen complex is required for neutrophil-neutrophil aggregation. Blood. 1985 Jun;65(6):1553–1556. [PubMed] [Google Scholar]
  51. Segui-Real B., Rhodes C., Yamada Y. The human genome contains a pseudogene for the Mr=32,000 laminin binding protein. Nucleic Acids Res. 1989 Feb 11;17(3):1257–1257. doi: 10.1093/nar/17.3.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Singer I. I. Association of fibronectin and vinculin with focal contacts and stress fibers in stationary hamster fibroblasts. J Cell Biol. 1982 Feb;92(2):398–408. doi: 10.1083/jcb.92.2.398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Singer I. I., Scott S., Hall G. L., Limjuco G., Chin J., Schmidt J. A. Interleukin 1 beta is localized in the cytoplasmic ground substance but is largely absent from the Golgi apparatus and plasma membranes of stimulated human monocytes. J Exp Med. 1988 Feb 1;167(2):389–407. doi: 10.1084/jem.167.2.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Singer I. I., Scott S., Kawka D. W., Kazazis D. M., Gailit J., Ruoslahti E. Cell surface distribution of fibronectin and vitronectin receptors depends on substrate composition and extracellular matrix accumulation. J Cell Biol. 1988 Jun;106(6):2171–2182. doi: 10.1083/jcb.106.6.2171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Singer I. I. The fibronexus: a transmembrane association of fibronectin-containing fibers and bundles of 5 nm microfilaments in hamster and human fibroblasts. Cell. 1979 Mar;16(3):675–685. doi: 10.1016/0092-8674(79)90040-0. [DOI] [PubMed] [Google Scholar]
  56. Smalheiser N. R., Schwartz N. B. Cranin: a laminin-binding protein of cell membranes. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6457–6461. doi: 10.1073/pnas.84.18.6457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sonnenberg A., Modderman P. W., Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 1988 Dec 1;336(6198):487–489. doi: 10.1038/336487a0. [DOI] [PubMed] [Google Scholar]
  58. Terranova V. P., DiFlorio R., Hujanen E. S., Lyall R. M., Liotta L. A., Thorgeirsson U., Siegal G. P., Schiffmann E. Laminin promotes rabbit neutrophil motility and attachment. J Clin Invest. 1986 Apr;77(4):1180–1186. doi: 10.1172/JCI112419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Terranova V. P., Rao C. N., Kalebic T., Margulies I. M., Liotta L. A. Laminin receptor on human breast carcinoma cells. Proc Natl Acad Sci U S A. 1983 Jan;80(2):444–448. doi: 10.1073/pnas.80.2.444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Todd R. F., 3rd, Arnaout M. A., Rosin R. E., Crowley C. A., Peters W. A., Babior B. M. Subcellular localization of the large subunit of Mo1 (Mo1 alpha; formerly gp 110), a surface glycoprotein associated with neutrophil adhesion. J Clin Invest. 1984 Oct;74(4):1280–1290. doi: 10.1172/JCI111538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tomaselli K. J., Damsky C. H., Reichardt L. F. Purification and characterization of mammalian integrins expressed by a rat neuronal cell line (PC12): evidence that they function as alpha/beta heterodimeric receptors for laminin and type IV collagen. J Cell Biol. 1988 Sep;107(3):1241–1252. doi: 10.1083/jcb.107.3.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Tonnesen M. G., Anderson D. C., Springer T. A., Knedler A., Avdi N., Henson P. M. Adherence of neutrophils to cultured human microvascular endothelial cells. Stimulation by chemotactic peptides and lipid mediators and dependence upon the Mac-1, LFA-1, p150,95 glycoprotein family. J Clin Invest. 1989 Feb;83(2):637–646. doi: 10.1172/JCI113928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Vedder N. B., Harlan J. M. Increased surface expression of CD11b/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium. J Clin Invest. 1988 Mar;81(3):676–682. doi: 10.1172/JCI113372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Wallis W. J., Hickstein D. D., Schwartz B. R., June C. H., Ochs H. D., Beatty P. G., Klebanoff S. J., Harlan J. M. Monoclonal antibody-defined functional epitopes on the adhesion-promoting glycoprotein complex (CDw18) of human neutrophils. Blood. 1986 Apr;67(4):1007–1013. [PubMed] [Google Scholar]
  65. Wencel-Drake J. D., Plow E. F., Kunicki T. J., Woods V. L., Keller D. M., Ginsberg M. H. Localization of internal pools of membrane glycoproteins involved in platelet adhesive responses. Am J Pathol. 1986 Aug;124(2):324–334. [PMC free article] [PubMed] [Google Scholar]
  66. Wewer U. M., Liotta L. A., Jaye M., Ricca G. A., Drohan W. N., Claysmith A. P., Rao C. N., Wirth P., Coligan J. E., Albrechtsen R. Altered levels of laminin receptor mRNA in various human carcinoma cells that have different abilities to bind laminin. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7137–7141. doi: 10.1073/pnas.83.19.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Wewer U. M., Taraboletti G., Sobel M. E., Albrechtsen R., Liotta L. A. Role of laminin receptor in tumor cell migration. Cancer Res. 1987 Nov 1;47(21):5691–5698. [PubMed] [Google Scholar]
  68. Wicker L. S., Boltz R. C., Jr, Nichols E. A., Miller B. J., Sigal N. H., Peterson L. B. Large, activated B cells are the primary B-cell target of 8-bromoguanosine and 8-mercaptoguanosine. Cell Immunol. 1987 May;106(2):318–329. doi: 10.1016/0008-8749(87)90175-4. [DOI] [PubMed] [Google Scholar]
  69. Wright S. D., Craigmyle L. S., Silverstein S. C. Fibronectin and serum amyloid P component stimulate C3b- and C3bi-mediated phagocytosis in cultured human monocytes. J Exp Med. 1983 Oct 1;158(4):1338–1343. doi: 10.1084/jem.158.4.1338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wright S. D., Detmers P. A. Adhesion-promoting receptors on phagocytes. J Cell Sci Suppl. 1988;9:99–120. doi: 10.1242/jcs.1988.supplement_9.5. [DOI] [PubMed] [Google Scholar]
  71. Wright S. D., Levin S. M., Jong M. T., Chad Z., Kabbash L. G. CR3 (CD11b/CD18) expresses one binding site for Arg-Gly-Asp-containing peptides and a second site for bacterial lipopolysaccharide. J Exp Med. 1989 Jan 1;169(1):175–183. doi: 10.1084/jem.169.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wright S. D., Licht M. R., Craigmyle L. S., Silverstein S. C. Communication between receptors for different ligands on a single cell: ligation of fibronectin receptors induces a reversible alteration in the function of complement receptors on cultured human monocytes. J Cell Biol. 1984 Jul;99(1 Pt 1):336–339. doi: 10.1083/jcb.99.1.336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wright S. D., Meyer B. C. Fibronectin receptor of human macrophages recognizes the sequence Arg-Gly-Asp-Ser. J Exp Med. 1985 Aug 1;162(2):762–767. doi: 10.1084/jem.162.2.762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wright S. D., Rao P. E., Van Voorhis W. C., Craigmyle L. S., Iida K., Talle M. A., Westberg E. F., Goldstein G., Silverstein S. C. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5699–5703. doi: 10.1073/pnas.80.18.5699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Wright S. D., Weitz J. I., Huang A. J., Levin S. M., Silverstein S. C., Loike J. D. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7734–7738. doi: 10.1073/pnas.85.20.7734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Yoon P. S., Boxer L. A., Mayo L. A., Yang A. Y., Wicha M. S. Human neutrophil laminin receptors: activation-dependent receptor expression. J Immunol. 1987 Jan 1;138(1):259–265. [PubMed] [Google Scholar]
  77. Yow H. K., Wong J. M., Chen H. S., Lee C. G., Davis S., Steele G. D., Jr, Chen L. B. Increased mRNA expression of a laminin-binding protein in human colon carcinoma: complete sequence of a full-length cDNA encoding the protein. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6394–6398. doi: 10.1073/pnas.85.17.6394. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES