Entry of Bacillus anthracis spores into epithelial cells is mediated by the spore surface protein BclA, integrin α2β1 and complement component C1q

Cellular Microbiology

Volumn 13, Issue 4, 2011, Pages 620-634

  Xue, Qiong ^a   Gu, Chunfang ^a   Rivera, Jose ^a   Höök, Magnus ^a   Chen, Xiwu ^b   Pozzi, Ambra ^b   Xu, Yi ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; COMPLEMENT COMPONENT C1Q; PROTEIN BCLA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2;

ANTHRAX; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL SPORE; BACTERIAL VIRULENCE; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RESPIRATORY EPITHELIUM;

ANIMALS; ANTHRAX; BACILLUS ANTHRACIS; BACTERIAL ADHESION; CELL LINE; CHO CELLS; COMPLEMENT C1Q; CRICETINAE; CRICETULUS; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; INTEGRIN ALPHA2BETA1; MEMBRANE GLYCOPROTEINS; MICE; SPORES, BACTERIAL;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

EID: 79952632061     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01558.x     Document Type: Article

References (57)

1. Bergelson, J.M., Shepley, M.P., Chan, B.M., Hemler, M.E., and Finberg, R.W. (1992) Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 255: 1718-1720.
2. Bourazopoulou, E., Kapsogeorgou, E.K., Routsias, J.G., Manoussakis, M.N., Moutsopoulos, H.M., and Tzioufas, A.G. (2009) Functional expression of the alpha 2-macroglobulin receptor CD91 in salivary gland epithelial cells. J Autoimmun 33: 141-146.
3. Boydston, J.A., Chen, P., Steichen, C.T., and Turnbough, C.L., Jr (2005) Orientation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis. J Bacteriol 187: 5310-5317.
4. Braun, L., Ghebrehiwet, B., and Cossart, P. (2000) gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J 19: 1458-1466.
5. Caswell, C.C., Lukomska, E., Seo, N.S., Hook, M., and Lukomski, S. (2007) Scl1-dependent internalization of group A Streptococcus via direct interactions with the alpha2beta1 integrin enhances pathogen survival and re-emergence. Mol Microbiol 64: 1319-1331.
6. Chakrabarty, K., Wu, W., Booth, J.L., Duggan, E.S., Nagle, N.N., Coggeshall, K.M., and Metcalf, J.P. (2007) Human lung innate immune response to Bacillus anthracis spore infection. Infect Immun 75: 3729-3738.
7. Chen, J., Diacovo, T.G., Grenache, D.G., Santoro, S.A., and Zutter, M.M. (2002) The alpha2 integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol 161: 337-344.
8. Ciarlet, M., Crawford, S.E., Cheng, E., Blutt, S.E., Rice, D.A., Bergelson, J.M., and Estes, M.K. (2002) VLA-2 (alpha2beta1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J Virol 76: 1109-1123.
9. Cleret, A., Quesnel-Hellmann, A., Vallon-Eberhard, A., Verrier, B., Jung, S., Vidal, D., etal. (2007) Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J Immunol 178: 7994-8001.
10. Cote, C.K., Van Rooijen, N., and Welkos, S.L. (2006) Roles of macrophages and neutrophils in the early host response to Bacillus anthracis spores in a mouse model of infection. Infect Immun 74: 469-480.
11. Edelson, B.T., Li, Z., Pappan, L.K., and Zutter, M.M. (2004) Mast cell-mediated inflammatory responses require the alpha 2 beta 1 integrin. Blood 103: 2214-2220.
12. Eisen, D.P. (2010) Mannose-binding lectin deficiency and respiratory tract infection. J Innate Immun 2: 114-122.
13. Emsley, J., King, S.L., Bergelson, J.M., and Liddington, R.C. (1997) Crystal structure of the I domain from integrin alpha2beta1. J Biol Chem 272: 28512-28517.
14. Emsley, J., Knight, C.G., Farndale, R.W., Barnes, M.J., and Liddington, R.C. (2000) Structural basis of collagen recognition by integrin alpha2beta1. Cell 100: 47-56.
15. Evans, S.E., Scott, B.L., Clement, C.G., Larson, D.T., Kontoyiannis, D., Lewis, R.E., etal. (2010) Stimulated innate resistance of lung epithelium protects mice broadly against bacteria and fungi. Am J Respir Cell Mol Biol 42: 40-50.
16. Fowler, T., Wann, E.R., Joh, D., Johansson, S., Foster, T.J., and Hook, M. (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol 79: 672-679.
17. Fraser, D.A., and Tenner, A.J. (2008) Directing an appropriate immune response: the role of defense collagens and other soluble pattern recognition molecules. Curr Drug Targets 9: 113-122.
18. Gaboriaud, C., Thielens, N.M., Gregory, L.A., Rossi, V., Fontecilla-Camps, J.C., and Arlaud, G.J. (2004) Structure and activation of the C1 complex of complement: unraveling the puzzle. Trends Immunol 25: 368-373.
19. Glomski, I.J., Piris-Gimenez, A., Huerre, M., Mock, M., and Goossens, P.L. (2007) Primary involvement of pharynx and Peyer's patch in inhalational and intestinal anthrax. PLoS Pathog 3: e76.
20. Guidi-Rontani, C. (2002) The alveolar macrophage: the Trojan horse of Bacillus anthracis. Trends Microbiol 10: 405-409.
21. Hammerschmidt, S. (2006) Adherence molecules of pathogenic pneumococci. Curr Opin Microbiol 9: 12-20.
22. He, L., Pappan, L.K., Grenache, D.G., Li, Z., Tollefsen, D.M., Santoro, S.A., and Zutter, M.M. (2003) The contributions of the alpha 2 beta 1 integrin to vascular thrombosis in vivo. Blood 102: 3652-3657.
23. Humtsoe, J.O., Kim, J.K., Xu, Y., Keene, D.R., Hook, M., Lukomski, S., and Wary, K.K. (2005) A streptococcal collagen-like protein interacts with the alpha 2beta 1 integrin and induces intracellular signaling. J Biol Chem 280: 13848-13857.
24. Husted, R.F., Hayashi, M., and Stokes, J.B. (1988) Characteristics of papillary collecting duct cells in primary culture. Am J Physiol 255: F1160-F1169.
25. Hynes, R.O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
26. Isberg, R.R., and Leong, J.M. (1990) Multiple beta1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861-871.
27. Joh, D., Wann, E.R., Kreikemeyer, B., Speziale, P., and Hook, M. (1999) Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol 18: 211-223.
28. Jokinen, J., White, D.J., Salmela, M., Huhtala, M., Kapyla, J., Sipila, K., etal. (2010) Molecular mechanism of alpha2beta1 integrin interaction with human echovirus 1. EMBO J 29: 196-208.
29. Kuijpers, M.J., Schulte, V., Bergmeier, W., Lindhout, T., Brakebusch, C., Offermanns, S., etal. (2003) Complementary roles of glycoprotein VI and alpha2beta1 integrin in collagen-induced thrombus formation in flowing whole blood ex vivo. FASEB J 17: 685-687.
30. Lambris, J.D., Ricklin, D., and Geisbrecht, B.V. (2008) Complement evasion by human pathogens. Nat Rev Microbiol 6: 132-142.
31. Legate, K.R., Montanez, E., Kudlacek, O., and Fassler, R. (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7: 20-31.
32. Lu, J.H., Teh, B.K., Wang, L., Wang, Y.N., Tan, Y.S., Lai, M.C., and Reid, K.B. (2008) The classical and regulatory functions of C1q in immunity and autoimmunity. Cell Mol Immunol 5: 9-21.
33. McCall-Culbreath, K.D., Li, Z., and Zutter, M.M. (2008) Crosstalk between the alpha2beta1 integrin and c-met/HGF-R regulates innate immunity. Blood 111: 3562-3570.
34. Massey, R.C., Kantzanou, M.N., Fowler, T., Day, N.P., Schofield, K., Wann, E.R., etal. (2001) Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol 3: 839-851.
35. Mitchell, D.A., Pickering, M.C., Warren, J., Fossati-Jimack, L., Cortes-Hernandez, J., Cook, H.T., etal. (2002) C1q deficiency and autoimmunity: the effects of genetic background on disease expression. J Immunol 168: 2538-2543.
36. Mock, M., and Fouet, A. (2001) Anthrax. Annu Rev Microbiol 55: 647-671.
37. Nayak, A., Ferluga, J., Tsolaki, A.G., and Kishore, U. (2010) The non-classical functions of the classical complement pathway recognition subcomponent C1q. Immunol Lett 131: 139-150.
38. Ogden, C.A., de Cathelineau, A., Hoffmann, P.R., Bratton, D., Ghebrehiwet, B., Fadok, V.A., and Henson, P.M. (2001) C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 194: 781-795.
39. Oliva, C.R., Swiecki, M.K., Griguer, C.E., Lisanby, M.W., Bullard, D.C., Turnbough, C.L., Jr, and Kearney, J.F. (2008) The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc Natl Acad Sci USA 105: 1261-1266.
40. Oliva, C., Turnbough, C.L., Jr, and Kearney, J.F. (2009) CD14-Mac-1 interactions in Bacillus anthracis spore internalization by macrophages. Proc Natl Acad Sci USA 106: 13957-13962.
41. Ozeri, V., Rosenshine, I., Mosher, D.F., Fassler, R., and Hanski, E. (1998a) Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol Microbiol 30: 625-637.
42. Ozeri, V., Rosenshine, I., Mosher, D.F., Fassler, R., and Hanski, E. (1998b) Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol Microbiol 30: 625-637.
43. Rety, S., Salamitou, S., Garcia-Verdugo, I., Hulmes, D.J.S., Le Hegarat, F., Chaby, R., and Lewit-Bentley, A. (2005) The crystal structure of the Bacillus anthracis spore surface protein BclA shows remarkable similarity to mammalian proteins. J Biol Chem 280: 43073-43078.
44. Russell, B.H., Vasan, R., Keene, D.R., and Xu, Y. (2007) Bacillus anthracis internalization by human fibroblasts and epithelial cells. Cell Microbiol 9: 1262-1274.
45. Russell, B.H., Liu, Q., Jenkins, S.A., Tuvim, M.J., Dickey, B.F., and Xu, Y. (2008a) In vivo demonstration and quantification of intracellular Bacillus anthracis in lung epithelial cells. Infect Immun 76: 3975-3983.
46. Russell, B.H., Vasan, R., Keene, D.R., Koehler, T.M., and Xu, Y. (2008b) Potential dissemination of Bacillus anthracis utilizing human lung epithelial cells. Cell Microbiol 10: 945-957.
47. Sarma, V.J., Huber-Lang, M., and Ward, P.A. (2006) Complement in lung disease. Autoimmunity 39: 387-394.
48. Sarratt, K.L., Chen, H., Zutter, M.M., Santoro, S.A., Hammer, D.A., and Kahn, M.L. (2005) GPVI and alpha2beta1 play independent critical roles during platelet adhesion and aggregate formation to collagen under flow. Blood 106: 1268-1277.
49. Seo, N., Russell, B.H., Rivera, J.J., Liang, X., Xu, X., Afshar-Kharghan, V., and Hook, M. (2010) An engineered alpha1 integrin binding collagenous sequence. J Biol Chem 285: 31046-31054.
50. Steichen, C., Chen, P., Kearney, J.F., and Turnbough, C.L., Jr (2003) Identification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium. J Bacteriol 185: 1903-1910.
51. Sylvestre, P., Couture-Tosi, E., and Mock, M. (2002) A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol Microbiol 45: 169-178.
52. Walport, M.J. (2001) Complement. First of two parts. N Engl J Med 344: 1058-1066.
53. Watford, W.T., Ghio, A.J., and Wright, J.R. (2000) Complement-mediated host defense in the lung. Am J Physiol Lung Cell Mol Physiol 279: L790-L798.
54. Xing, L., Huhtala, M., Pietiainen, V., Kapyla, J., Vuorinen, K., Marjomaki, V., etal. (2004) Structural and functional analysis of integrin alpha2I domain interaction with echovirus 1. J Biol Chem 279: 11632-11638.
55. Xu, Y., Gurusiddappa, S., Rich, R.L., Owens, R.T., Keene, D.R., Mayne, R., etal. (2000) Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J Biol Chem 275: 38981-38989.
56. Xue, Q., Jenkins, S.A., Gu, C., Smeds, E., Liu, Q., Vasan, R., etal. (2010) Bacillus anthracis spore entry into epithelial cells is an actin-dependent process requiring c-Src and PI3K. PLoS ONE 5: e11665.
57. Zutter, M.M., and Edelson, B.T. (2007) The alpha2beta1 integrin: a novel collectin/C1q receptor. Immunobiology 212: 343-353.