I-domain-containing integrins serve as pilus receptors for Neisseria gonorrhoeae adherence to human epithelial cells

Cellular Microbiology

Volumn 7, Issue 8, 2005, Pages 1197-1211

  Edwards, Jennifer L ^a,b   Apicella, Michael A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTEGRIN; ALPHA2 INTEGRIN; INTEGRIN RECEPTOR;

ANTIBODY LABELING; ARTICLE; BACTERIUM ADHERENCE; BACTERIUM PILUS; CELL IMMORTALIZATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM CELL; GONORRHEA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; URETHRA; WESTERN BLOTTING;

ASIALOGLYCOPROTEIN RECEPTOR; BACTERIAL ADHESION; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; IMMUNOPRECIPITATION; INTEGRIN ALPHA CHAINS; MALE; NEISSERIA GONORRHOEAE; PILI, SEX; PROTEIN STRUCTURE, TERTIARY; URETHRA;

NEISSERIA; NEISSERIA GONORRHOEAE;

EID: 22744449495     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00547.x     Document Type: Article

References (79)

1. Aota, S., Nagai, T., and Yamada, K.M. (1991) Characterization of regions of fibronectin besides the arginine-glycine-aspartic acid sequence required for adhesive function of the cell-binding domain using site-directed mutagenesis. J Biol Chem 266: 15938-15943.
2. Apicella, M.A. (1974) Antigenically distinct populations of Neisseria gonorrhoeae: isolation and characterization of the responsible determinants. J Infect Dis 130: 619-625.
3. Arnaout, M.A. (1990) Leukocyte adhesion molecules deficiency: its structural basis, pathophysiology and implications for modulating the inflammatory response. Immunol Rev 114: 145-180.
4. Baricevic, I.L., Vicovac, V., Marinovic, V., and Cuperlovic, M. (2002) Investigation of asialoglycoprotein receptor glycosylation by lectin affinity methods. J Serb Chem Soc 67: 331-338.
5. de Bentzmann, S., Roger, P., and Puchelle, E. (1996a) Pseudomonas aeruginosa adherence to remodelling respiratory epithelium. Eur Respir J 9: 2145-2150.
6. de Bentzmann, S., Roger, P., Dupuit, F., Bajolet-Laudinat, O., Fuchey, C., Plotkowski, M.C., and Puchelle, E. (1996b) Asialo GM1 is a receptor for Pseudomonas aeruginosa adherence to regenerating respiratory epithelial cells. Infect Immun 64: 1582-1588.
7. 1. J Cell Biol 127: 1129-1137.
8. 3 and integrin-associated protein. J Cell Biol 130: 745-754.
9. 3 (platelet GPIIb-IIIa) recognizes multiple sites in fibronectin. J Biol Chem 266: 23323-23328.
10. Bowditch, R.D., Hariharan, M., Tominna, E.F., Smith, J.W., Yamada, K.M., Getzoff, E.D., and Ginsberg, M.H. (1994) Identification of a novel integrin binding site in fibronectin. Differential utilization by beta 3 integrins. J Biol Chem 269: 10856-10863.
11. Cohen, M.S., Cannon, J.G., Jerse, A.E., Charniga, L.M., Isbey, S.F., and Whicker, L.G. (1994) Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J Infect Dis 169: 532-537.
12. v integrin receptors. FEBS Lett 424: 84-88.
13. Dehio, C., Gray-Owen, S.D., and Meyer, T.F. (2000) Host cell invasion by pathogenic Neisseriae. Subcell Biochem 33: 61-96.
14. Dickeson, S.K., and Santoro, S.A. (1998) Ligand recognition by the I domain-containing integrins. Cell Mol Life Sci 54: 556-566.
15. 1 integrins. J Biol Chem 274: 32182-32191.
16. Dillard, J. (1999) A variable pathogenicity island associated with disseminated gonococcal infection. Midwest Microbial Pathogenesis Group, Sixth Annual Midwest Microbial Pathogenesis Meeting, Milwaukee, WI.
17. Dillard, J.P., and Seifert, H.S. (2001) A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41: 263-277.
18. Dudas, K.C., and Apicella, M.A. (1988) Selection and immunochemical analysis of lipooligosaccharide mutants of Neisseria gonorrhoeae. Infect Immun 56: 499-504.
19. Edwards, J.L., and Apicella, M.A. (2002) The role of lipooligosaccharide in Neisseria gonorrhoeae pathogenesis of cervical epithelia: lipid A serves as a C3 acceptor molecule. Cell Microbiol 4: 585-598.
20. Edwards, J.L., and Apicella, M.A. (2004) The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin Microbiol Rev 17: 965-981.
21. Edwards, J.L., Shao, J.Q., Ault, K.A., and Apicella, M.A. (2000) Neisseria gonorrhoeae elicits membrane ruffling and cytoskeletal rearrangements upon infection of primary human endocervical and ectocervical cells. Infect Immun 68: 5354-5363.
22. Edwards, J.L., Brown, E.J., Ault, K.A., and Apicella, M.A. (2001) The role of complement receptor 3 (CR3) in Neisseria gonorrhoeae infection of human cervical epithelia. Cell Microbiol 3: 611-622.
23. Edwards, J.L., Brown, E.J., Uk-Nham, S., Cannon, J.G., Blake, M.S., and Apicella, M.A. (2002) A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells. Cell Microbiol 4: 571-584.
24. Edwards, J.L., Harvey, H.A., and Apicella, M.A. (2004) Neisseria gonarrhoeae: the varying mechanism of pathogenesis in males and females. In Bacterial Invasion of Host Cells. Lamont, R. (ed.). Cambridge: Cambridge University Press, pp. 203-238.
25. Forest, K.T., and Tainer, J.A. (1997) Type-4 pilus-structure: outside to inside and top to bottom - a minireview. Gene 192: 165-69.
26. Forest, K.T., Dunham, S.A., Koomey, M., and Tainer, J.A. (1999) Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 31: 743-752.
27. 3 by using VP7 during cell entry. J Virol 77: 9969-9978.
28. Harvey, H.A., Ketterer, M.R., Preston, A., Lubaroff, D., Williams, R., and Apicella, M.A. (1997) Ultrastructural analysis of primary human urethral epithelial cell cultures infected with Neisseria gonorrhoeae. Infect Immun 65: 2420-2427.
29. Harvey, H.A., Jennings, M.P., Campbell, C.A., Williams, R., and Apicella, M.A. (2001) Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol Microbiol 42: 659-672.
30. Harvey, H.A., Post, D.M., and Apicella, M.A. (2002) Immortalization of human urethral epithelial cells: a model for the study of the pathogenesis of and the inflammatory cytokine response to Neisseria gonorrhoeae infection. Infect Immun 70: 5808-5815.
31. Hasty, L.A., Lambris, J.D., Lessey, B.A., Pruksananonda, K., and Lyttle, C.R. (1994) Hormonal regulation of complement components and receptors throughout the menstrual cycle. Am J Obstet Gynecol 170: 168-175.
32. Hemler, M.E. (1990). VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu Rev Immunol 8: 365-400.
33. Hildreth, J.E., and August, J.T. (1985) The human lymphocyte function-associated (HLFA) antigen and a related macrophage differentiation antigen (HMac-1): functional effects of subunit-specific monoclonal antibodies. J Immunol 134: 3272-3280.
34. Humphries, M.J., and Newham, P. (1998) The structure of cell-adhesion molecules. Trends Cell Biol 8: 78-83.
35. Jerse, A.E., and Rest, R.F. (1997) Adhesion and invasion by the pathogenic Neisseria. Trends Microbiol 5: 217-221.
36. Jones, P.H., and Watt, F.M. (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73: 713-724.
37. Jones, P.H., Harper, S., and Watt, F.M. (1995) Stem cell patterning and fate in human epidermis. Cell 80: 83-93.
38. Källström, H., Liszewski, M.K., Atkinson, J.P., and Jonsson, A.B. (1997) Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol Microbiol 25: 639-647.
39. Kaneko, H., Watanabe, H., Hosokawa, Y., Urata, Y., Hattori, T., Pellicciari, C., and Fukuda, M. (1984) The presence of G1 and G2 populations in normal epithelium of rat urinary bladder. Basic Appl Histochem 28: 41-57.
40. Kimizuka, F., Ohdate, Y., Kawase, Y., Shimojo, T., Taguchi, Y., Hashino, K., et al. (1991) Role of type III homology repeats in cell adhesive function within the cell-binding domain of fibronectin. J Biol Chem 266: 3045-3051.
41. 1) I domain. Identification of two independent virus contact sites distinct from the metal ion-dependent adhesion site. J Biol Chem 272: 28518-28522.
42. Kishimoto, T.K., Larson, R.S., Corbi, A.L., Dustin, M.L., Staunton, D.E., and Springer, T.A. (1989) The leukocyte integrins. Adv Immunol 46: 149-182.
43. Kraus, D., Medof, M.E., and Mold, C. (1998) Complementary recognition of alternative pathway activators by decay-accelerating factor and factor H. Infect Immun 66: 399-405.
44. 2+-Complexed crystal structures. J Cell Biol 143: 1523-1534.
45. Loftus, J.C., and Liddington, R.C. (1997) Cell adhesion in vascular biology. New insights into integrin-ligand interaction. J Clin Invest 99: 2302-2306.
46. Lussier, C., Basora, N., Bouatrouss, Y., and Beaulieu, J,F. (2000) Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa. Microsc Res Tech 51: 169-178.
47. Maisner, A., Liszewski, M.K., Atkinson, J.P., Schwartz-Albiez, R., and Herrler, G. (1996) Two different cytoplasmic tails direct isoforms of the membrane cofactor protein (CD46) to the basolateral surface of Madin-Darby canine kidney cells. J Biol Chem 271: 18853-18858.
48. Merz, A.J., and So, M. (2000) Interactions of pathogenic neisseriae with epithelial cell membranes. Annu Rev Cell Dev Biol 16: 423-457.
49. Mesri, M., Plescia, J., and Altieri, D.C. (1998) Dual regulation of ligand binding by CD11b I domain. Inhibition of intercellular adhesion and monocyte procoagulant activity by a factor X-derived peptide. J Biol Chem 273: 744-748.
50. Miyamoto, S., Akiyama, S.K., and Yamada, K.M. (1995) Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267: 883-885.
51. Modlin, J.F. (2000a) Introduction to picornaviridae. In Principles and Practice of Infectious Disease, 5th edn. Mandell, G.L., Bennett, J.E., and Dolin, R. (eds). Philadelphia, PA: Churchill Livingstone, pp. 1904-1919.
52. Modlin, J.F. (2000b) Coxsackieviruses, echoviruses, and newer enteroviruses. In Principles and Practice of Infectious Disease, 5th edn. Mandell, G.L., Bennett, J.E., and Dolin, R. (eds). Philadelphia, PA: Churchill Livingstone, pp. 1888-1895.
53. Muza-Moons, M.M., Koutsouris, A., and Hecht, G. (2003) Disruption of cell polarity by enteropathogenic Escherichia coli enables basolateral membrane proteins to migrate apically and to potentiate physiological consequences. Infect Immun 71: 7069-7078.
54. Obara, M., Kang, M.S., and Yamada, K.M. (1988) Site-directed mutagenesis of the cell-binding domain of human fibronectin: separable, synergistic sites mediate adhesive function. Cell 153: 649-657.
55. Oglesby, T.J. (1998) The complement system in reproduction. In The Human Complement System in Health and Disease. Volanakis, J. E. and Franks, M. M. (eds). New York: Marcel Dekker, pp. 355-373.
56. Peters, M.J., Ross-Russell, R.I., White, D., Kerr, S.J., Eaton, F.E., Keengwe, I.N., et al. (2001) Early severe neutropenia and thrombocytopenia identifies the highest risk cases of severe meningococcal disease. Pediatr Crit Care Med 2: 225-231.
57. Pietiäinen, V., Marjomaki, V., Upla, P., Pelkmans, L., Helenius, A., and Hyypia, T. (2004) Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 15: 4911-4925.
58. 3. J Biol Chem 272: 2736-2743.
59. Potten, C.S., and Morris, R.J. (1988) Epithelial stem cells in vivo. J Cell Sci Suppl 10: 45-62.
60. + gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol 29: 369-379.
61. 1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur Respir J 13: 1301-1309.
62. 1alpha2beta1-integrin-dependent Src kinase activation. Am J Physiol Gastrointest Liver Physiol 286: G547-G557.
63. Schmid, Y., Grassl, G.A., Buhler, O.T., Skurnik, M., Autenrieth, I.B., and Bohn, E. (2004) Yersinia enterocolitica adhesin A induces production of interleukin-8 in epithelial cells. Infect Immun 72: 6780-6789.
64. Sheppard, D. (1996) Epithelial integrins. Bioessays 18: 655-660.
65. Sheppard, D. (2003) Functions of pulmonary epithelial integrins: from development to disease. Physiol Rev 83: 673-686.
66. Simpson, K.L., Jones, A., Norman, S., and Holmes, C.H. (1997) Expression of the complement regulatory proteins decay accelerating factor (DAF, CD55), membrane cofactor protein (MCP, CD46) and CD59 in the normal human uterine cervix and in premalignant and malignant cervical disease. Am J Pathol 151: 1455-1467.
67. Smyth, C.J., Marron, M.B., Twohig, J.M., and Smith, S.G. (1996) Fimbrial adhesins: similarities and variations in structure and biogenesis. FEMS Immunol Med Microbiol 16: 127-139.
68. Stockert, R.J. (1995) The asialoglycoprotein receptor: relationships between structure, function, and expression. Physiol Rev 75: 591-609.
69. Takada, Y., and Puzon, W. (1993) Identification of a regulatory region of integrin beta 1 subunit using activating and inhibiting antibodies. J Biol Chem 268: 17597-17601.
70. Teuchert, M., Maisner, A., and Herrler, G. (1999) Importance of the carboxyl-terminal FTSL motif of membrane cofactor protein for basolateral sorting and endocytosis. Positive and negative modulation by signals inside and outside the cytoplasmic tail. J Biol Chem 274: 19979-19984.
71. Ulanova, M., Puttagunta, L., Marcet-Palacios, M., Duszyk, M., Steinhoff, U., Duta, F., et al. (2005) Syk tyrosine kinase participates in β1 integrin signaling and inflammatory responses in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 288: L497-507.
72. Ward M.E., Watt, P.J. (1977) The role of specific and non-specific factors in the interaction of gonococci with host cells. In Gonorrhoea: Epidemiology and Pathogenesis. Skinner, F.A., Walker, P.D and Smith, H. (eds). New York: Academic Press, pp. 83-85.
73. Watt, F.M. (1989) Terminal differentiation of epidermal keratinocytes. Curr Opin Cell Biol 1: 1107-1115.
74. Watt, F.M. (2O02) Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J 21: 3919-3926.
75. Wen, K.K., Giardina, P.C., Blake, M.S., Edwards, J., Apicella, M.A., and Rubenstein, P.A. (2000) Interaction of the gonococcal porin P.IB with G- and F-actin. Biochemistry 39: 8638-8647.
76. 1 (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue. Blood 95: 1804-1809.
77. Wicken, A.J. (1985) Bacterial cell walls and surfaces. In Bacterial Adhesion: Mechanisms and Physiological Significance. Savage, D.C and Fletcher, M. (eds). New York: Plenum Press, pp. 45-70.
78. Xiong, J.P., Li, R., Essafi, M., Stehle, T., and Arnaout, M.A. (2000) An isoleucine-based allosteric switch controls affinity and shape shifting in integrin CD11b A-domain. J Biol Chem 275: 38762-38767.
79. 2. J Biol Chem 271: 29953-29957.