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. 1999 Aug;52(4):220–230. doi: 10.1136/mp.52.4.220

Cell adhesion molecules in the pathogenesis of and host defence against microbial infection.

J R Kerr 1
PMCID: PMC395703  PMID: 10694943

Abstract

Eukaryotic cell adhesion molecules (CAMs) are used by various cells and extracellular molecules in host defence against infection. They are involved in many processes including recognition by circulating phagocytes of a site of inflammation, transmigration through the endothelial barrier, diapedesis through basement membrane and extracellular matrix, and release of effector mechanisms at the infected site. CAMs involved in leucocyte-endothelial cell interaction include the selectins, integrins, and members of the immunoglobulin superfamily. However, CAMs are also used by various microorganisms (protozoa, fungi, bacteria, and viruses) during their pathogenesis. For example, bacteria that utilise CAMs include Mycobacterium tuberculosis, Listeria monocytogenes, Yersinia spp, enteropathogenic Escherichia coli, Shigella spp, Neisseria spp, Bordetella spp, and Borrelia burgdorferi. In addition, CAMs are involved in the pathogenetic effects of the RTX toxins of Pasteurella haemolytica, Actinobacillus actinomycetemcomitans, and the superantigen exotoxins of Staphylococcus aureus and Streptococcus pyogenes. A recurrent and topical theme of potential importance within the bacterial group is the intimate relation between CAMs, bacterial protein receptors, and type III secretion systems. For example, the IpaBCD protein complex is secreted by the type III system of Shigella flexneri and interacts with alpha 5 beta 1 integrin on the eukaryotic cell surface, followed by Rho mediated internalisation; this illustrates the relevance of cellular microbiology. CAMs might prove to be novel therapeutic targets. Comparative genomics has provided the knowledge of shared virulence determinants among diverse bacterial genera, and will continue to deepen our understanding of microbial pathogenesis, particularly in the context of the interaction of prokaryotic and eukaryotic molecules.

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Selected References

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  1. Agrez M. V., Shafren D. R., Gu X., Cox K., Sheppard D., Barry R. D. Integrin alpha v beta 6 enhances coxsackievirus B1 lytic infection of human colon cancer cells. Virology. 1997 Dec 8;239(1):71–77. doi: 10.1006/viro.1997.8831. [DOI] [PubMed] [Google Scholar]
  2. Alrutz M. A., Isberg R. R. Involvement of focal adhesion kinase in invasin-mediated uptake. Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13658–13663. doi: 10.1073/pnas.95.23.13658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson D. M., Schneewind O. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science. 1997 Nov 7;278(5340):1140–1143. doi: 10.1126/science.278.5340.1140. [DOI] [PubMed] [Google Scholar]
  4. Autenrieth I. B., Firsching R. Penetration of M cells and destruction of Peyer's patches by Yersinia enterocolitica: an ultrastructural and histological study. J Med Microbiol. 1996 Apr;44(4):285–294. doi: 10.1099/00222615-44-4-285. [DOI] [PubMed] [Google Scholar]
  5. Barnwell J. W., Asch A. S., Nachman R. L., Yamaya M., Aikawa M., Ingravallo P. A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J Clin Invest. 1989 Sep;84(3):765–772. doi: 10.1172/JCI114234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berendt A. R., Simmons D. L., Tansey J., Newbold C. I., Marsh K. Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature. 1989 Sep 7;341(6237):57–59. doi: 10.1038/341057a0. [DOI] [PubMed] [Google Scholar]
  7. Bergelson J. M., Chan M., Solomon K. R., St John N. F., Lin H., Finberg R. W. Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6245–6248. doi: 10.1073/pnas.91.13.6245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bergelson J. M., Cunningham J. A., Droguett G., Kurt-Jones E. A., Krithivas A., Hong J. S., Horwitz M. S., Crowell R. L., Finberg R. W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science. 1997 Feb 28;275(5304):1320–1323. doi: 10.1126/science.275.5304.1320. [DOI] [PubMed] [Google Scholar]
  9. Berlin C., Berg E. L., Briskin M. J., Andrew D. P., Kilshaw P. J., Holzmann B., Weissman I. L., Hamann A., Butcher E. C. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell. 1993 Jul 16;74(1):185–195. doi: 10.1016/0092-8674(93)90305-a. [DOI] [PubMed] [Google Scholar]
  10. Berton G., Laudanna C., Sorio C., Rossi F. Generation of signals activating neutrophil functions by leukocyte integrins: LFA-1 and gp150/95, but not CR3, are able to stimulate the respiratory burst of human neutrophils. J Cell Biol. 1992 Feb;116(4):1007–1017. doi: 10.1083/jcb.116.4.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Briskin M. J., McEvoy L. M., Butcher E. C. MAdCAM-1 has homology to immunoglobulin and mucin-like adhesion receptors and to IgA1. Nature. 1993 Jun 3;363(6428):461–464. doi: 10.1038/363461a0. [DOI] [PubMed] [Google Scholar]
  13. Brown E. J., Lindberg F. P. Leucocyte adhesion molecules in host defence against infection. Ann Med. 1996 Jun;28(3):201–208. doi: 10.3109/07853899609033121. [DOI] [PubMed] [Google Scholar]
  14. Bullock W. E., Wright S. D. Role of the adherence-promoting receptors, CR3, LFA-1, and p150,95, in binding of Histoplasma capsulatum by human macrophages. J Exp Med. 1987 Jan 1;165(1):195–210. doi: 10.1084/jem.165.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  16. Caron E., Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science. 1998 Nov 27;282(5394):1717–1721. doi: 10.1126/science.282.5394.1717. [DOI] [PubMed] [Google Scholar]
  17. Chen T., Belland R. J., Wilson J., Swanson J. Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med. 1995 Aug 1;182(2):511–517. doi: 10.1084/jem.182.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Cinco M., Murgia R., Perticarari S., Presani G. Surface receptors of neutrophils towards B. burgdorferi. Wien Klin Wochenschr. 1998 Dec 23;110(24):866–869. [PubMed] [Google Scholar]
  19. Clark M. A., Hirst B. H., Jepson M. A. M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer's patch M cells. Infect Immun. 1998 Mar;66(3):1237–1243. doi: 10.1128/iai.66.3.1237-1243.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Coburn J., Leong J. M., Erban J. K. Integrin alpha IIb beta 3 mediates binding of the Lyme disease agent Borrelia burgdorferi to human platelets. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7059–7063. doi: 10.1073/pnas.90.15.7059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Colonno R. J., Callahan P. L., Long W. J. Isolation of a monoclonal antibody that blocks attachment of the major group of human rhinoviruses. J Virol. 1986 Jan;57(1):7–12. doi: 10.1128/jvi.57.1.7-12.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Cooper D., Lindberg F. P., Gamble J. R., Brown E. J., Vadas M. A. Transendothelial migration of neutrophils involves integrin-associated protein (CD47). Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3978–3982. doi: 10.1073/pnas.92.9.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Cossart P., Boquet P., Normark S., Rappuoli R. Cellular microbiology emerging. Science. 1996 Jan 19;271(5247):315–316. doi: 10.1126/science.271.5247.315. [DOI] [PubMed] [Google Scholar]
  24. D'Souza S. E., Ginsberg M. H., Plow E. F. Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem Sci. 1991 Jul;16(7):246–250. doi: 10.1016/0968-0004(91)90096-e. [DOI] [PubMed] [Google Scholar]
  25. Dehio C., Gray-Owen S. D., Meyer T. F. The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol. 1998 Dec;6(12):489–495. doi: 10.1016/s0966-842x(98)01365-1. [DOI] [PubMed] [Google Scholar]
  26. Dobrescu D., Ursea B., Pope M., Asch A. S., Posnett D. N. Enhanced HIV-1 replication in V beta 12 T cells due to human cytomegalovirus in monocytes: evidence for a putative herpesvirus superantigen. Cell. 1995 Sep 8;82(5):753–763. doi: 10.1016/0092-8674(95)90472-7. [DOI] [PubMed] [Google Scholar]
  27. Dramsi S., Biswas I., Maguin E., Braun L., Mastroeni P., Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol. 1995 Apr;16(2):251–261. doi: 10.1111/j.1365-2958.1995.tb02297.x. [DOI] [PubMed] [Google Scholar]
  28. Duensing T. D., van Putten J. P. Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect Immun. 1997 Mar;65(3):964–970. doi: 10.1128/iai.65.3.964-970.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ehlers M. R., Daffé M. Interactions between Mycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol. 1998 Aug;6(8):328–335. doi: 10.1016/s0966-842x(98)01301-8. [DOI] [PubMed] [Google Scholar]
  30. Etzioni A., Harlan J. M., Pollack S., Phillips L. M., Gershoni-Baruch R., Paulson J. C. Leukocyte adhesion deficiency (LAD) II: a new adhesion defect due to absence of sialyl Lewis X, the ligand for selectins. Immunodeficiency. 1993;4(1-4):307–308. [PubMed] [Google Scholar]
  31. Evans D. J., Almond J. W. Cell receptors for picornaviruses as determinants of cell tropism and pathogenesis. Trends Microbiol. 1998 May;6(5):198–202. doi: 10.1016/s0966-842x(98)01263-3. [DOI] [PubMed] [Google Scholar]
  32. Everest P., Li J., Douce G., Charles I., De Azavedo J., Chatfield S., Dougan G., Roberts M. Role of the Bordetella pertussis P.69/pertactin protein and the P.69/pertactin RGD motif in the adherence to and invasion of mammalian cells. Microbiology. 1996 Nov;142(Pt 11):3261–3268. doi: 10.1099/13500872-142-11-3261. [DOI] [PubMed] [Google Scholar]
  33. Fernandez R. C., Weiss A. A. Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun. 1994 Nov;62(11):4727–4738. doi: 10.1128/iai.62.11.4727-4738.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Finn T. M., Stevens L. A. Tracheal colonization factor: a Bordetella pertussis secreted virulence determinant. Mol Microbiol. 1995 May;16(4):625–634. doi: 10.1111/j.1365-2958.1995.tb02425.x. [DOI] [PubMed] [Google Scholar]
  35. Fox G., Parry N. R., Barnett P. V., McGinn B., Rowlands D. J., Brown F. The cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). J Gen Virol. 1989 Mar;70(Pt 3):625–637. doi: 10.1099/0022-1317-70-3-625. [DOI] [PubMed] [Google Scholar]
  36. Frankel G., Lider O., Hershkoviz R., Mould A. P., Kachalsky S. G., Candy D. C., Cahalon L., Humphries M. J., Dougan G. The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J Biol Chem. 1996 Aug 23;271(34):20359–20364. doi: 10.1074/jbc.271.34.20359. [DOI] [PubMed] [Google Scholar]
  37. Freemont A. J. Demystified ... adhesion molecules. Mol Pathol. 1998 Aug;51(4):175–184. doi: 10.1136/mp.51.4.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Frydman M., Etzioni A., Eidlitz-Markus T., Avidor I., Varsano I., Shechter Y., Orlin J. B., Gershoni-Baruch R. Rambam-Hasharon syndrome of psychomotor retardation, short stature, defective neutrophil motility, and Bombay phenotype. Am J Med Genet. 1992 Oct 1;44(3):297–302. doi: 10.1002/ajmg.1320440307. [DOI] [PubMed] [Google Scholar]
  39. Gale C. A., Bendel C. M., McClellan M., Hauser M., Becker J. M., Berman J., Hostetter M. K. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science. 1998 Feb 27;279(5355):1355–1358. doi: 10.1126/science.279.5355.1355. [DOI] [PubMed] [Google Scholar]
  40. Gale C., Finkel D., Tao N., Meinke M., McClellan M., Olson J., Kendrick K., Hostetter M. Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):357–361. doi: 10.1073/pnas.93.1.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Gavrilovskaya I. N., Shepley M., Shaw R., Ginsberg M. H., Mackow E. R. beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7074–7079. doi: 10.1073/pnas.95.12.7074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Geng J. G., Bevilacqua M. P., Moore K. L., McIntyre T. M., Prescott S. M., Kim J. M., Bliss G. A., Zimmerman G. A., McEver R. P. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature. 1990 Feb 22;343(6260):757–760. doi: 10.1038/343757a0. [DOI] [PubMed] [Google Scholar]
  43. Geuijen C. A., Willems R. J., Bongaerts M., Top J., Gielen H., Mooi F. R. Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun. 1997 Oct;65(10):4222–4228. doi: 10.1128/iai.65.10.4222-4228.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Gresham H. D., Adams S. P., Brown E. J. Ligand binding specificity of the leukocyte response integrin expressed by human neutrophils. J Biol Chem. 1992 Jul 15;267(20):13895–13902. [PubMed] [Google Scholar]
  45. Gresham H. D., Goodwin J. L., Allen P. M., Anderson D. C., Brown E. J. A novel member of the integrin receptor family mediates Arg-Gly-Asp-stimulated neutrophil phagocytosis. J Cell Biol. 1989 May;108(5):1935–1943. doi: 10.1083/jcb.108.5.1935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  47. Gómez-Duarte O. G., Dehio M., Guzmán C. A., Chhatwal G. S., Dehio C., Meyer T. F. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect Immun. 1997 Sep;65(9):3857–3866. doi: 10.1128/iai.65.9.3857-3866.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Harlan J. M. Leukocyte adhesion deficiency syndrome: insights into the molecular basis of leukocyte emigration. Clin Immunol Immunopathol. 1993 Jun;67(3 Pt 2):S16–S24. doi: 10.1006/clin.1993.1079. [DOI] [PubMed] [Google Scholar]
  49. Henderson I. R., Navarro-Garcia F., Nataro J. P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 1998 Sep;6(9):370–378. doi: 10.1016/s0966-842x(98)01318-3. [DOI] [PubMed] [Google Scholar]
  50. Hengel H., Brune W., Koszinowski U. H. Immune evasion by cytomegalovirus--survival strategies of a highly adapted opportunist. Trends Microbiol. 1998 May;6(5):190–197. doi: 10.1016/s0966-842x(98)01255-4. [DOI] [PubMed] [Google Scholar]
  51. Hodtsev A. S., Choi Y., Spanopoulou E., Posnett D. N. Mycoplasma superantigen is a CDR3-dependent ligand for the T cell antigen receptor. J Exp Med. 1998 Feb 2;187(3):319–327. doi: 10.1084/jem.187.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Huber S. A. VCAM-1 is a receptor for encephalomyocarditis virus on murine vascular endothelial cells. J Virol. 1994 Jun;68(6):3453–3458. doi: 10.1128/jvi.68.6.3453-3458.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Humphries M. J. The molecular basis and specificity of integrin-ligand interactions. J Cell Sci. 1990 Dec;97(Pt 4):585–592. doi: 10.1242/jcs.97.4.585. [DOI] [PubMed] [Google Scholar]
  54. Hyypiä T., Horsnell C., Maaronen M., Khan M., Kalkkinen N., Auvinen P., Kinnunen L., Stanway G. A distinct picornavirus group identified by sequence analysis. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8847–8851. doi: 10.1073/pnas.89.18.8847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
  56. Kansas G. S. Selectins and their ligands: current concepts and controversies. Blood. 1996 Nov 1;88(9):3259–3287. [PubMed] [Google Scholar]
  57. Kaper J. B. EPEC delivers the goods. Trends Microbiol. 1998 May;6(5):169–173. doi: 10.1016/s0966-842x(98)01266-9. [DOI] [PubMed] [Google Scholar]
  58. Kaplan G., Totsuka A., Thompson P., Akatsuka T., Moritsugu Y., Feinstone S. M. Identification of a surface glycoprotein on African green monkey kidney cells as a receptor for hepatitis A virus. EMBO J. 1996 Aug 15;15(16):4282–4296. [PMC free article] [PubMed] [Google Scholar]
  59. Kenny B., DeVinney R., Stein M., Reinscheid D. J., Frey E. A., Finlay B. B. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 1997 Nov 14;91(4):511–520. doi: 10.1016/s0092-8674(00)80437-7. [DOI] [PubMed] [Google Scholar]
  60. Kishimoto T. K., Hollander N., Roberts T. M., Anderson D. C., Springer T. A. Heterogeneous mutations in the beta subunit common to the LFA-1, Mac-1, and p150,95 glycoproteins cause leukocyte adhesion deficiency. Cell. 1987 Jul 17;50(2):193–202. doi: 10.1016/0092-8674(87)90215-7. [DOI] [PubMed] [Google Scholar]
  61. Klotz S. A., Hein R. C., Smith R. L., Rouse J. B. The fibronectin adhesin of Candida albicans. Infect Immun. 1994 Oct;62(10):4679–4681. doi: 10.1128/iai.62.10.4679-4681.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. doi: 10.1016/0968-0004(94)90090-6. [DOI] [PubMed] [Google Scholar]
  63. Koedam J. A., Cramer E. M., Briend E., Furie B., Furie B. C., Wagner D. D. P-selectin, a granule membrane protein of platelets and endothelial cells, follows the regulated secretory pathway in AtT-20 cells. J Cell Biol. 1992 Feb;116(3):617–625. doi: 10.1083/jcb.116.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Lally E. T., Kieba I. R., Sato A., Green C. L., Rosenbloom J., Korostoff J., Wang J. F., Shenker B. J., Ortlepp S., Robinson M. K. RTX toxins recognize a beta2 integrin on the surface of human target cells. J Biol Chem. 1997 Nov 28;272(48):30463–30469. doi: 10.1074/jbc.272.48.30463. [DOI] [PubMed] [Google Scholar]
  65. Lampugnani M. G., Resnati M., Dejana E., Marchisio P. C. The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol. 1991 Feb;112(3):479–490. doi: 10.1083/jcb.112.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Leininger E., Roberts M., Kenimer J. G., Charles I. G., Fairweather N., Novotny P., Brennan M. J. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):345–349. doi: 10.1073/pnas.88.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Levy J. A. Three new human herpesviruses (HHV6, 7, and 8). Lancet. 1997 Feb 22;349(9051):558–563. doi: 10.1016/S0140-6736(97)80119-5. [DOI] [PubMed] [Google Scholar]
  68. Li J., Fairweather N. F., Novotny P., Dougan G., Charles I. G. Cloning, nucleotide sequence and heterologous expression of the protective outer-membrane protein P.68 pertactin from Bordetella bronchiseptica. J Gen Microbiol. 1992 Aug;138(Pt 8):1697–1705. doi: 10.1099/00221287-138-8-1697. [DOI] [PubMed] [Google Scholar]
  69. Li L. J., Dougan G., Novotny P., Charles I. G. P.70 pertactin, an outer-membrane protein from Bordetella parapertussis: cloning, nucleotide sequence and surface expression in Escherichia coli. Mol Microbiol. 1991 Feb;5(2):409–417. doi: 10.1111/j.1365-2958.1991.tb02123.x. [DOI] [PubMed] [Google Scholar]
  70. Lindberg F. P., Gresham H. D., Schwarz E., Brown E. J. Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J Cell Biol. 1993 Oct;123(2):485–496. doi: 10.1083/jcb.123.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Lo S. K., Lee S., Ramos R. A., Lobb R., Rosa M., Chi-Rosso G., Wright S. D. Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD11b/CD18, Mac-1, alpha m beta 2) on human neutrophils. J Exp Med. 1991 Jun 1;173(6):1493–1500. doi: 10.1084/jem.173.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Lundgren E., Carballeira N., Vazquez R., Dubinina E., Bränden H., Persson H., Wolf-Watz H. Invasin of Yersinia pseudotuberculosis activates human peripheral B cells. Infect Immun. 1996 Mar;64(3):829–835. doi: 10.1128/iai.64.3.829-835.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Lusso P., Secchiero P., Crowley R. W., Garzino-Demo A., Berneman Z. N., Gallo R. C. CD4 is a critical component of the receptor for human herpesvirus 7: interference with human immunodeficiency virus. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3872–3876. doi: 10.1073/pnas.91.9.3872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Makhov A. M., Hannah J. H., Brennan M. J., Trus B. L., Kocsis E., Conway J. F., Wingfield P. T., Simon M. N., Steven A. C. Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J Mol Biol. 1994 Aug 5;241(1):110–124. doi: 10.1006/jmbi.1994.1478. [DOI] [PubMed] [Google Scholar]
  75. Malik A. B., Lo S. K. Vascular endothelial adhesion molecules and tissue inflammation. Pharmacol Rev. 1996 Jun;48(2):213–229. [PubMed] [Google Scholar]
  76. Marra A., Isberg R. R. Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer's patch intestinal epithelium. Infect Immun. 1997 Aug;65(8):3412–3421. doi: 10.1128/iai.65.8.3412-3421.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Marth T., Kelsall B. L. Regulation of interleukin-12 by complement receptor 3 signaling. J Exp Med. 1997 Jun 2;185(11):1987–1995. doi: 10.1084/jem.185.11.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Massol P., Montcourrier P., Guillemot J. C., Chavrier P. Fc receptor-mediated phagocytosis requires CDC42 and Rac1. EMBO J. 1998 Nov 2;17(21):6219–6229. doi: 10.1093/emboj/17.21.6219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Mawby W. J., Holmes C. H., Anstee D. J., Spring F. A., Tanner M. J. Isolation and characterization of CD47 glycoprotein: a multispanning membrane protein which is the same as integrin-associated protein (IAP) and the ovarian tumour marker OA3. Biochem J. 1994 Dec 1;304(Pt 2):525–530. doi: 10.1042/bj3040525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
  81. Mengaud J., Lecuit M., Lebrun M., Nato F., Mazie J. C., Cossart P. Antibodies to the leucine-rich repeat region of internalin block entry of Listeria monocytogenes into cells expressing E-cadherin. Infect Immun. 1996 Dec;64(12):5430–5433. doi: 10.1128/iai.64.12.5430-5433.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Mengaud J., Ohayon H., Gounon P., Mege R-M, Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 1996 Mar 22;84(6):923–932. doi: 10.1016/s0092-8674(00)81070-3. [DOI] [PubMed] [Google Scholar]
  83. Meyer D. H., Mintz K. P., Fives-Taylor P. M. Models of invasion of enteric and periodontal pathogens into epithelial cells: a comparative analysis. Crit Rev Oral Biol Med. 1997;8(4):389–409. doi: 10.1177/10454411970080040301. [DOI] [PubMed] [Google Scholar]
  84. Michie C. A., Cohen J. The clinical significance of T-cell superantigens. Trends Microbiol. 1998 Feb;6(2):61–65. doi: 10.1016/S0966-842X(97)01193-1. [DOI] [PubMed] [Google Scholar]
  85. Minnick M. F., Mitchell S. J., McAllister S. J. Cell entry and the pathogenesis of Bartonella infections. Trends Microbiol. 1996 Sep;4(9):343–347. doi: 10.1016/0966-842x(96)10055-x. [DOI] [PubMed] [Google Scholar]
  86. Moore D. A., Henderson D., Gazzard B. G. Neutrophil adhesion molecules in HIV disease. Clin Exp Immunol. 1998 Oct;114(1):73–77. doi: 10.1046/j.1365-2249.1998.00686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Mosser D. M., Edelson P. J. The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. 1987 May 28-Jun 3Nature. 327(6120):329–331. doi: 10.1038/327329b0. [DOI] [PubMed] [Google Scholar]
  88. Muller W. A., Weigl S. A., Deng X., Phillips D. M. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993 Aug 1;178(2):449–460. doi: 10.1084/jem.178.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Newman S. L., Bucher C., Rhodes J., Bullock W. E. Phagocytosis of Histoplasma capsulatum yeasts and microconidia by human cultured macrophages and alveolar macrophages. Cellular cytoskeleton requirement for attachment and ingestion. J Clin Invest. 1990 Jan;85(1):223–230. doi: 10.1172/JCI114416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Newman S. L. Macrophages in host defense against Histoplasma capsulatum. Trends Microbiol. 1999 Feb;7(2):67–71. doi: 10.1016/s0966-842x(98)01431-0. [DOI] [PubMed] [Google Scholar]
  91. Nhieu G. T., Sansonetti P. J. Mechanism of Shigella entry into epithelial cells. Curr Opin Microbiol. 1999 Feb;2(1):51–55. doi: 10.1016/s1369-5274(99)80009-5. [DOI] [PubMed] [Google Scholar]
  92. Ockenhouse C. F., Tandon N. N., Magowan C., Jamieson G. A., Chulay J. D. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science. 1989 Mar 17;243(4897):1469–1471. doi: 10.1126/science.2467377. [DOI] [PubMed] [Google Scholar]
  93. Ockenhouse C. F., Tegoshi T., Maeno Y., Benjamin C., Ho M., Kan K. E., Thway Y., Win K., Aikawa M., Lobb R. R. Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. J Exp Med. 1992 Oct 1;176(4):1183–1189. doi: 10.1084/jem.176.4.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Ohnishi Y., Beppu T., Horinouchi S. Two genes encoding serine protease homologues in Serratia marcescens and characterization of their products in Escherichia coli. J Biochem. 1997 May;121(5):902–913. doi: 10.1093/oxfordjournals.jbchem.a021672. [DOI] [PubMed] [Google Scholar]
  95. Owen P., Meehan M., de Loughry-Doherty H., Henderson I. Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol Med Microbiol. 1996 Dec 1;16(2):63–76. doi: 10.1111/j.1574-695X.1996.tb00124.x. [DOI] [PubMed] [Google Scholar]
  96. Piali L., Hammel P., Uherek C., Bachmann F., Gisler R. H., Dunon D., Imhof B. A. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J Cell Biol. 1995 Jul;130(2):451–460. doi: 10.1083/jcb.130.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Poli G., Pantaleo G., Fauci A. S. Immunopathogenesis of human immunodeficiency virus infection. Clin Infect Dis. 1993 Aug;17 (Suppl 1):S224–S229. [PubMed] [Google Scholar]
  98. Powell R. M., Schmitt V., Ward T., Goodfellow I., Evans D. J., Almond J. W. Characterization of echoviruses that bind decay accelerating factor (CD55): evidence that some haemagglutinating strains use more than one cellular receptor. J Gen Virol. 1998 Jul;79(Pt 7):1707–1713. doi: 10.1099/0022-1317-79-7-1707. [DOI] [PubMed] [Google Scholar]
  99. Pugsley A. P. The complete general secretory pathway in gram-negative bacteria. Microbiol Rev. 1993 Mar;57(1):50–108. doi: 10.1128/mr.57.1.50-108.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Reife R. A., Shapiro R. A., Bamber B. A., Berry K. K., Mick G. E., Darveau R. P. Porphyromonas gingivalis lipopolysaccharide is poorly recognized by molecular components of innate host defense in a mouse model of early inflammation. Infect Immun. 1995 Dec;63(12):4686–4694. doi: 10.1128/iai.63.12.4686-4694.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Reinhold M. I., Lindberg F. P., Plas D., Reynolds S., Peters M. G., Brown E. J. In vivo expression of alternatively spliced forms of integrin-associated protein (CD47). J Cell Sci. 1995 Nov;108(Pt 11):3419–3425. doi: 10.1242/jcs.108.11.3419. [DOI] [PubMed] [Google Scholar]
  102. Roivainen M., Piirainen L., Hovi T., Virtanen I., Riikonen T., Heino J., Hyypiä T. Entry of coxsackievirus A9 into host cells: specific interactions with alpha v beta 3 integrin, the vitronectin receptor. Virology. 1994 Sep;203(2):357–365. doi: 10.1006/viro.1994.1494. [DOI] [PubMed] [Google Scholar]
  103. Rottem S., Naot Y. Subversion and exploitation of host cells by mycoplasmas. Trends Microbiol. 1998 Nov;6(11):436–440. doi: 10.1016/s0966-842x(98)01358-4. [DOI] [PubMed] [Google Scholar]
  104. Sandros J., Tuomanen E. Attachment factors of Bordetella pertussis: mimicry of eukaryotic cell recognition molecules. Trends Microbiol. 1993 Aug;1(5):192–196. doi: 10.1016/0966-842x(93)90090-e. [DOI] [PubMed] [Google Scholar]
  105. Santoni G., Gismondi A., Liu J. H., Punturieri A., Santoni A., Frati L., Piccoli M., Djeu J. Y. Candida albicans expresses a fibronectin receptor antigenically related to alpha 5 beta 1 integrin. Microbiology. 1994 Nov;140(Pt 11):2971–2979. doi: 10.1099/13500872-140-11-2971. [DOI] [PubMed] [Google Scholar]
  106. Shafren D. R., Bates R. C., Agrez M. V., Herd R. L., Burns G. F., Barry R. D. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol. 1995 Jun;69(6):3873–3877. doi: 10.1128/jvi.69.6.3873-3877.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Sherman I. W., Crandall I. E., Guthrie N., Land K. M. The sticky secrets of sequestration. Parasitol Today. 1995 Oct;11(10):378–384. doi: 10.1016/0169-4758(95)80006-9. [DOI] [PubMed] [Google Scholar]
  108. Shevchenko D. V., Akins D. R., Robinson E., Li M., Popova T. G., Cox D. L., Radolf J. D. Molecular characterization and cellular localization of TpLRR, a processed leucine-rich repeat protein of Treponema pallidum, the syphilis spirochete. J Bacteriol. 1997 May;179(10):3188–3195. doi: 10.1128/jb.179.10.3188-3195.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Sinclair J. P., Shearer W. T. Current Status of CD4-Based Therapies for Prophylaxis and Treatment of HIV Infection. BioDrugs. 1997 Aug;8(2):128–138. doi: 10.2165/00063030-199708020-00006. [DOI] [PubMed] [Google Scholar]
  110. 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]
  111. Staunton D. E., Merluzzi V. J., Rothlein R., Barton R., Marlin S. D., Springer T. A. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell. 1989 Mar 10;56(5):849–853. doi: 10.1016/0092-8674(89)90689-2. [DOI] [PubMed] [Google Scholar]
  112. Stockbauer K. E., Magoun L., Liu M., Burns E. H., Jr, Gubba S., Renish S., Pan X., Bodary S. C., Baker E., Coburn J. A natural variant of the cysteine protease virulence factor of group A Streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins alphavbeta3 and alphaIIbbeta3. Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):242–247. doi: 10.1073/pnas.96.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Stone D. M., Norton L. K., Davis W. C. Modulation of bovine leukemia virus-associated spontaneous lymphocyte proliferation by monoclonal antibodies to lymphocyte surface molecules. Clin Immunol Immunopathol. 1997 May;83(2):156–164. doi: 10.1006/clin.1997.4340. [DOI] [PubMed] [Google Scholar]
  114. Summerford C., Bartlett J. S., Samulski R. J. AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat Med. 1999 Jan;5(1):78–82. doi: 10.1038/4768. [DOI] [PubMed] [Google Scholar]
  115. Tedder T. F., Steeber D. A., Chen A., Engel P. The selectins: vascular adhesion molecules. FASEB J. 1995 Jul;9(10):866–873. [PubMed] [Google Scholar]
  116. 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]
  117. Varki A. Selectin ligands: will the real ones please stand up? J Clin Invest. 1997 Jan 15;99(2):158–162. doi: 10.1172/JCI119142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Verdegaal M. E., Zegveld S. T., van Furth R. Heat shock protein 65 induces CD62e, CD106, and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J Immunol. 1996 Jul 1;157(1):369–376. [PubMed] [Google Scholar]
  119. Vines R. R., Ramakrishnan G., Rogers J. B., Lockhart L. A., Mann B. J., Petri W. A., Jr Regulation of adherence and virulence by the Entamoeba histolytica lectin cytoplasmic domain, which contains a beta2 integrin motif. Mol Biol Cell. 1998 Aug;9(8):2069–2079. doi: 10.1091/mbc.9.8.2069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Wang J. F., Kieba I. R., Korostoff J., Guo T. L., Yamaguchi N., Rozmiarek H., Billings P. C., Shenker B. J., Lally E. T. Molecular and biochemical mechanisms of Pasteurella haemolytica leukotoxin-induced cell death. Microb Pathog. 1998 Dec;25(6):317–331. doi: 10.1006/mpat.1998.0236. [DOI] [PubMed] [Google Scholar]
  121. Ward T., Pipkin P. A., Clarkson N. A., Stone D. M., Minor P. D., Almond J. W. Decay-accelerating factor CD55 is identified as the receptor for echovirus 7 using CELICS, a rapid immuno-focal cloning method. EMBO J. 1994 Nov 1;13(21):5070–5074. doi: 10.1002/j.1460-2075.1994.tb06836.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Warren A. P., Owens C. N., Borysiewicz L. K., Patel K. Down-regulation of integrin alpha 1/beta 1 expression and association with cell rounding in human cytomegalovirus-infected fibroblasts. J Gen Virol. 1994 Dec;75(Pt 12):3319–3325. doi: 10.1099/0022-1317-75-12-3319. [DOI] [PubMed] [Google Scholar]
  123. Watarai M., Funato S., Sasakawa C. Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med. 1996 Mar 1;183(3):991–999. doi: 10.1084/jem.183.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Williams-Bouyer N. M., Hill E. M. Involvement of host cell tyrosine phosphorylation in the invasion of HEp-2 cells by Bartonella bacilliformis. FEMS Microbiol Lett. 1999 Feb 15;171(2):191–201. doi: 10.1111/j.1574-6968.1999.tb13432.x. [DOI] [PubMed] [Google Scholar]
  125. Wong W. S., Luk J. M. Signaling mechanisms of pertussis toxin-induced myelomonocytic cell adhesion: role of tyrosine phosphorylation. Biochem Biophys Res Commun. 1997 Jul 18;236(2):479–482. doi: 10.1006/bbrc.1997.6986. [DOI] [PubMed] [Google Scholar]
  126. Wright S. D., Silverstein S. C. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J Exp Med. 1983 Dec 1;158(6):2016–2023. doi: 10.1084/jem.158.6.2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Zhou M., Brown E. J. Leukocyte response integrin and integrin-associated protein act as a signal transduction unit in generation of a phagocyte respiratory burst. J Exp Med. 1993 Oct 1;178(4):1165–1174. doi: 10.1084/jem.178.4.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. van Putten J. P., Duensing T. D., Cole R. L. Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol. 1998 Jul;29(1):369–379. doi: 10.1046/j.1365-2958.1998.00951.x. [DOI] [PubMed] [Google Scholar]
  129. van Putten J. P., Paul S. M. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 1995 May 15;14(10):2144–2154. doi: 10.1002/j.1460-2075.1995.tb07208.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. van't Wout J., Burnette W. N., Mar V. L., Rozdzinski E., Wright S. D., Tuomanen E. I. Role of carbohydrate recognition domains of pertussis toxin in adherence of Bordetella pertussis to human macrophages. Infect Immun. 1992 Aug;60(8):3303–3308. doi: 10.1128/iai.60.8.3303-3308.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. von Andrian U. H., Berger E. M., Ramezani L., Chambers J. D., Ochs H. D., Harlan J. M., Paulson J. C., Etzioni A., Arfors K. E. In vivo behavior of neutrophils from two patients with distinct inherited leukocyte adhesion deficiency syndromes. J Clin Invest. 1993 Jun;91(6):2893–2897. doi: 10.1172/JCI116535. [DOI] [PMC free article] [PubMed] [Google Scholar]

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