1887

Abstract

Non-typable (NTHi) is a common commensal of the human nasopharynx, but causes opportunistic infection when the respiratory tract is compromised by infection or disease. The ability of NTHi to invade epithelial cells has been described, but the underlying molecular mechanisms are poorly characterized. We previously determined that NTHi promotes phosphorylation of the serine-threonine kinase Akt in A549 human lung epithelial cells, and that Akt phosphorylation and NTHi cell invasion are prevented by inhibition of phosphoinositide 3-kinase (PI3K). Because PI3K-Akt signalling is associated with several host cell networks, the purpose of the current study was to identify eukaryotic molecules important for NTHi epithelial invasion. We found that inhibition of Akt activity reduced NTHi internalization; differently, bacterial entry was increased by phospholipase Cγ1 inhibition but was not affected by protein kinase inhibition. We also found that α5 and β1 integrins, and the tyrosine kinases focal adhesion kinase and Src, are important for NTHi A549 cell invasion. NTHi internalization was shown to be favoured by activation of Rac1 guanosine triphosphatase (GTPase), together with the guanine nucleotide exchange factor Vav2 and the effector Pak1. Also, Pak1 might be associated with inactivation of the microtubule destabilizing agent Op18/stathmin, to facilitate microtubule polymerization and NTHi entry. Conversely, inhibition of RhoA GTPase and its effector ROCK increased the number of internalized bacteria. Src and Rac1 were found to be important for NTHi-triggered Akt phosphorylation. An increase in host cyclic AMP reduced bacterial entry, which was linked to protein kinase A. These findings suggest that NTHi finely manipulates host signalling molecules to invade respiratory epithelial cells.

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2012-09-01
2020-01-22
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References

  1. Agarwal V., Asmat T. M., Dierdorf N. I., Hauck C. R., Hammerschmidt S.. ( 2010;). Polymeric immunoglobulin receptor-mediated invasion of Streptococcus pneumoniae into host cells requires a coordinate signaling of SRC family of protein-tyrosine kinases, ERK, and c-Jun N-terminal kinase. J Biol Chem285:35615–35623 [CrossRef][PubMed]
    [Google Scholar]
  2. Agerer F., Michel A., Ohlsen K., Hauck C. R.. ( 2003;). Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J Biol Chem278:42524–42531 [CrossRef][PubMed]
    [Google Scholar]
  3. Agerer F., Lux S., Michel A., Rohde M., Ohlsen K., Hauck C. R.. ( 2005;). Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci118:2189–2200 [CrossRef][PubMed]
    [Google Scholar]
  4. Ahrén I. L., Williams D. L., Rice P. J., Forsgren A., Riesbeck K.. ( 2001;). The importance of a β-glucan receptor in the nonopsonic entry of nontypeable Haemophilus influenzae into human monocytic and epithelial cells. J Infect Dis184:150–158 [CrossRef][PubMed]
    [Google Scholar]
  5. Aiastui A., Pucciarelli M. G., García-del Portillo F.. ( 2010;). Salmonella enterica serovar typhimurium invades fibroblasts by multiple routes differing from the entry into epithelial cells. Infect Immun78:2700–2713 [CrossRef][PubMed]
    [Google Scholar]
  6. Arroyo A. G., Sánchez-Mateos P., Campanero M. R., Martín-Padura I., Dejana E., Sánchez-Madrid F.. ( 1992;). Regulation of the VLA integrin-ligand interactions through the β1 subunit. J Cell Biol117:659–670 [CrossRef][PubMed]
    [Google Scholar]
  7. Arthur W. T., Petch L. A., Burridge K.. ( 2000;). Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol10:719–722 [CrossRef][PubMed]
    [Google Scholar]
  8. Bandi V., Apicella M. A., Mason E., Murphy T. F., Siddiqi A., Atmar R. L., Greenberg S. B.. ( 2001;). Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am J Respir Crit Care Med164:2114–2119[PubMed][CrossRef]
    [Google Scholar]
  9. Barnes P. J.. ( 2006;). Novel signal transduction modulators for the treatment of airway diseases. Pharmacol Ther109:238–245 [CrossRef][PubMed]
    [Google Scholar]
  10. Boettcher J. P., Kirchner M., Churin Y., Kaushansky A., Pompaiah M., Thorn H., Brinkmann V., Macbeath G., Meyer T. F.. ( 2010;). Tyrosine-phosphorylated caveolin-1 blocks bacterial uptake by inducing Vav2-RhoA-mediated cytoskeletal rearrangements. PLoS Biol8:e1000457 [CrossRef][PubMed]
    [Google Scholar]
  11. Bouchet V., Hood D. W., Li J., Brisson J. R., Randle G. A., Martin A., Li Z., Goldstein R., Schweda E. K.. & other authors ( 2003;). Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc Natl Acad Sci U S A100:8898–8903 [CrossRef][PubMed]
    [Google Scholar]
  12. Bower J. M., Eto D. S., Mulvey M. A.. ( 2005;). Covert operations of uropathogenic Escherichia coli within the urinary tract. Traffic6:18–31 [CrossRef][PubMed]
    [Google Scholar]
  13. Bunney T. D., Katan M.. ( 2010;). Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer10:342–352 [CrossRef][PubMed]
    [Google Scholar]
  14. Burrows L., Clark K., Mould A. P., Humphries M. J.. ( 1999;). Fine mapping of inhibitory anti-α5 monoclonal antibody epitopes that differentially affect integrin-ligand binding. Biochem J344:527–533 [CrossRef][PubMed]
    [Google Scholar]
  15. Byrd M. S., Pang B., Mishra M., Swords W. E., Wozniak D. J.. ( 2010;). The Pseudomonas aeruginosa exopolysaccharide Psl facilitates surface adherence and NF-κB activation in A549 cells. MBio1:e00140–e10 [CrossRef][PubMed]
    [Google Scholar]
  16. Campanero M. R., Arroyo A. G., Pulido R., Ursa A., de Matías M. S., Sánchez-Mateos P., Kassner P. D., Chan B. M., Hemler M. E.. & other authors ( 1992;). Functional role of α2/β1 and α4/β1 integrins in leukocyte intercellular adhesion induced through the common β1 subunit. Eur J Immunol22:3111–3119 [CrossRef][PubMed]
    [Google Scholar]
  17. Carabeo R.. ( 2011;). Bacterial subversion of host actin dynamics at the plasma membrane. Cell Microbiol13:1460–1469 [CrossRef][PubMed]
    [Google Scholar]
  18. Caswell P. T., Vadrevu S., Norman J. C.. ( 2009;). Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol10:843–853 [CrossRef][PubMed]
    [Google Scholar]
  19. Chakrabarti A. K., Vipat V. C., Mukherjee S., Singh R., Pawar S. D., Mishra A. C.. ( 2010;). Host gene expression profiling in influenza A virus-infected lung epithelial (A549) cells: a comparative analysis between highly pathogenic and modified H5N1 viruses. Virol J7:219 [CrossRef][PubMed]
    [Google Scholar]
  20. Cho B. A., Cho N. H., Seong S. Y., Choi M. S., Kim I. S.. ( 2010;). Intracellular invasion by Orientia tsutsugamushi is mediated by integrin signaling and actin cytoskeleton rearrangements. Infect Immun78:1915–1923 [CrossRef][PubMed]
    [Google Scholar]
  21. Clementi C., Murphy T. F.. ( 2011;). Non-typable Haemophilus influenzae invasion and persistence in the human respiratory tract. Front Cell Infect Microbiol1:1–9 [CrossRef]
    [Google Scholar]
  22. Cossart P., Sansonetti P. J.. ( 2004;). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science304:242–248 [CrossRef][PubMed]
    [Google Scholar]
  23. del Pozo M. A., Alderson N. B., Kiosses W. B., Chiang H. H., Anderson R. G., Schwartz M. A.. ( 2004;). Integrins regulate Rac targeting by internalization of membrane domains. Science303:839–842 [CrossRef][PubMed]
    [Google Scholar]
  24. Engelman J. A., Luo J., Cantley L. C.. ( 2006;). The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet7:606–619 [CrossRef][PubMed]
    [Google Scholar]
  25. Fang K. M., Shu W. H., Chang H. C., Wang J. J., Mak O. T.. ( 2004;). Study of prostaglandin receptors in mitochondria on apoptosis of human lung carcinoma cell line A549. Biochem Soc Trans32:1078–1080 [CrossRef][PubMed]
    [Google Scholar]
  26. Fink D. L., Green B. A., St Geme J. W. III. ( 2002;). The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect Immun70:4902–4907 [CrossRef][PubMed]
    [Google Scholar]
  27. Forsgren J., Samuelson A., Ahlin A., Jonasson J., Rynnel-Dagöö B., Lindberg A.. ( 1994;). Haemophilus influenzae resides and multiplies intracellularly in human adenoid tissue as demonstrated by in situ hybridization and bacterial viability assay. Infect Immun62:673–679[PubMed]
    [Google Scholar]
  28. Foxwell A. R., Kyd J. M., Cripps A. W.. ( 1998;). Nontypeable Haemophilus influenzae: pathogenesis and prevention. Microbiol Mol Biol Rev62:294–308[PubMed]
    [Google Scholar]
  29. Gilsdorf J. R., Marrs C. F., Foxman B.. ( 2004;). Haemophilus influenzae: genetic variability and natural selection to identify virulence factors. Infect Immun72:2457–2461 [CrossRef][PubMed]
    [Google Scholar]
  30. Guarino M.. ( 2010;). Src signaling in cancer invasion. J Cell Physiol223:14–26[PubMed]
    [Google Scholar]
  31. Guo L., Zhang F., Cai Y., Liu T.. ( 2009;). Expression profiling of integrins in lung cancer cells. Pathol Res Pract205:847–853 [CrossRef][PubMed]
    [Google Scholar]
  32. Hallström T., Singh B., Resman F., Blom A. M., Mörgelin M., Riesbeck K.. ( 2011;). Haemophilus influenzae protein E binds to the extracellular matrix by concurrently interacting with laminin and vitronectin. J Infect Dis204:1065–1074 [CrossRef][PubMed]
    [Google Scholar]
  33. Hammerschmidt S., Wolff S., Hocke A., Rosseau S., Müller E., Rohde M.. ( 2005;). Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun73:4653–4667 [CrossRef][PubMed]
    [Google Scholar]
  34. Heasman S. J., Ridley A. J.. ( 2008;). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol9:690–701 [CrossRef][PubMed]
    [Google Scholar]
  35. Hill D. J., Toleman M. A., Evans D. J., Villullas S., Van Alphen L., Virji M.. ( 2001;). The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol Microbiol39:850–862 [CrossRef][PubMed]
    [Google Scholar]
  36. Hoffmann C., Ohlsen K., Hauck C. R.. ( 2011;). Integrin-mediated uptake of fibronectin-binding bacteria. Eur J Cell Biol90:891–896 [CrossRef][PubMed]
    [Google Scholar]
  37. Howe A. K.. ( 2004;). Regulation of actin-based cell migration by cAMP/PKA. Biochim Biophys Acta1692:159–174 [CrossRef][PubMed]
    [Google Scholar]
  38. Huveneers S., Danen E. H.. ( 2009;). Adhesion signaling - crosstalk between integrins, Src and Rho. J Cell Sci122:1059–1069 [CrossRef][PubMed]
    [Google Scholar]
  39. Ketterer M. R., Shao J. Q., Hornick D. B., Buscher B., Bandi V. K., Apicella M. A.. ( 1999;). Infection of primary human bronchial epithelial cells by Haemophilus influenzae: macropinocytosis as a mechanism of airway epithelial cell entry. Infect Immun67:4161–4170[PubMed]
    [Google Scholar]
  40. Kim D., Chung J.. ( 2002;). Akt: versatile mediator of cell survival and beyond. J Biochem Mol Biol35:106–115 [CrossRef][PubMed]
    [Google Scholar]
  41. Krendel M., Zenke F. T., Bokoch G. M.. ( 2002;). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol4:294–301 [CrossRef][PubMed]
    [Google Scholar]
  42. Maqueda A., Moyano J. V., Gutiérrez-López M. D., Ovalle S., Rodríguez-Frade J. M., Cabañas C., Garcia-Pardo A.. ( 2006;). Activation pathways of α4β1 integrin leading to distinct T-cell cytoskeleton reorganization, Rac1 regulation and Pyk2 phosphorylation. J Cell Physiol207:746–756 [CrossRef][PubMed]
    [Google Scholar]
  43. Marignani P. A., Carpenter C. L.. ( 2001;). Vav2 is required for cell spreading. J Cell Biol154:177–186 [CrossRef][PubMed]
    [Google Scholar]
  44. Martí-Lliteras P., Regueiro V., Morey P., Hood D. W., Saus C., Sauleda J., Agustí A. G., Bengoechea J. A., Garmendia J.. ( 2009;). Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun77:4232–4242 [CrossRef][PubMed]
    [Google Scholar]
  45. Martí-Lliteras P., López-Gómez A., Mauro S., Hood D. W., Viadas C., Calatayud L., Morey P., Servin A., Liñares J.. & other authors ( 2011;). Nontypable Haemophilus influenzae displays a prevalent surface structure molecular pattern in clinical isolates. PLoS ONE6:e21133 [CrossRef][PubMed]
    [Google Scholar]
  46. Martin K. H., Slack J. K., Boerner S. A., Martin C. C., Parsons J. T.. ( 2002;). Integrin connections map: to infinity and beyond. Science296:1652–1653 [CrossRef][PubMed]
    [Google Scholar]
  47. Mata M., Morcillo E., Gimeno C., Cortijo J.. ( 2011;). N-Acetyl-l-cysteine (NAC) inhibit mucin synthesis and pro-inflammatory mediators in alveolar type II epithelial cells infected with influenza virus A and B and with respiratory syncytial virus (RSV). Biochem Pharmacol82:548–555 [CrossRef][PubMed]
    [Google Scholar]
  48. Mejía E., Bliska J. B., Viboud G. I.. ( 2008;). Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog4:e3 [CrossRef][PubMed]
    [Google Scholar]
  49. Mitra S. K., Hanson D. A., Schlaepfer D. D.. ( 2005;). Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol6:56–68 [CrossRef][PubMed]
    [Google Scholar]
  50. Morey P., Cano V., Martí-Lliteras P., López-Gómez A., Regueiro V., Saus C., Bengoechea J. A., Garmendia J.. ( 2011;). Evidence for a non-replicative intracellular stage of nontypable Haemophilus influenzae in epithelial cells. Microbiology157:234–250 [CrossRef][PubMed]
    [Google Scholar]
  51. Muenzner P., Bachmann V., Zimmermann W., Hentschel J., Hauck C. R.. ( 2010;). Human-restricted bacterial pathogens block shedding of epithelial cells by stimulating integrin activation. Science329:1197–1201 [CrossRef][PubMed]
    [Google Scholar]
  52. Murphy T. F., Brauer A. L., Schiffmacher A. T., Sethi S.. ( 2004;). Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am J Respir Crit Care Med170:266–272 [CrossRef][PubMed]
    [Google Scholar]
  53. Nagasawa S. Y., Takuwa N., Sugimoto N., Mabuchi H., Takuwa Y.. ( 2005;). Inhibition of Rac activation as a mechanism for negative regulation of actin cytoskeletal reorganization and cell motility by cAMP. Biochem J385:737–744 [CrossRef][PubMed]
    [Google Scholar]
  54. O’Connor K. L., Mercurio A. M.. ( 2001;). Protein kinase A regulates Rac and is required for the growth factor-stimulated migration of carcinoma cells. J Biol Chem276:47895–47900[PubMed]
    [Google Scholar]
  55. Oviedo-Boyso J., Cortés-Vieyra R., Huante-Mendoza A., Yu H. B., Valdez-Alarcón J. J., Bravo-Patiño A., Cajero-Juárez M., Finlay B. B., Baizabal-Aguirre V. M.. ( 2011;). The phosphoinositide-3-kinase-Akt signaling pathway is important for Staphylococcus aureus internalization by endothelial cells. Infect Immun79:4569–4577 [CrossRef][PubMed]
    [Google Scholar]
  56. Ozeri V., Rosenshine I., Ben-Ze’Ev A., Bokoch G. M., Jou T. S., Hanski E.. ( 2001;). De novo formation of focal complex-like structures in host cells by invading Streptococci. Mol Microbiol41:561–573 [CrossRef][PubMed]
    [Google Scholar]
  57. Pizarro-Cerdá J., Cossart P.. ( 2004;). Subversion of phosphoinositide metabolism by intracellular bacterial pathogens. Nat Cell Biol6:1026–1033 [CrossRef][PubMed]
    [Google Scholar]
  58. Raftopoulou M., Hall A.. ( 2004;). Cell migration: Rho GTPases lead the way. Dev Biol265:23–32 [CrossRef][PubMed]
    [Google Scholar]
  59. Rao V. K., Krasan G. P., Hendrixson D. R., Dawid S., St Geme J. W. III. ( 1999;). Molecular determinants of the pathogenesis of disease due to non-typable Haemophilus influenzae . FEMS Microbiol Rev23:99–129[PubMed][CrossRef]
    [Google Scholar]
  60. Regueiro V., Campos M. A., Morey P., Sauleda J., Agustí A. G., Garmendia J., Bengoechea J. A.. ( 2009;). Lipopolysaccharide-binding protein and CD14 are increased in the bronchoalveolar lavage fluid of smokers. Eur Respir J33:273–281 [CrossRef][PubMed]
    [Google Scholar]
  61. Ridley A. J., Schwartz M. A., Burridge K., Firtel R. A., Ginsberg M. H., Borisy G., Parsons J. T., Horwitz A. R.. ( 2003;). Cell migration: integrating signals from front to back. Science302:1704–1709 [CrossRef][PubMed]
    [Google Scholar]
  62. Sethi S., Murphy T. F.. ( 2001;). Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin Microbiol Rev14:336–363 [CrossRef][PubMed]
    [Google Scholar]
  63. Sethi S., Murphy T. F.. ( 2008;). Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med359:2355–2365 [CrossRef][PubMed]
    [Google Scholar]
  64. Sethi S., Evans N., Grant B. J., Murphy T. F.. ( 2002;). New strains of bacteria and exacerbations of chronic obstructive pulmonary disease. N Engl J Med347:465–471 [CrossRef][PubMed]
    [Google Scholar]
  65. Song J., Bishop B. L., Li G., Duncan M. J., Abraham S. N.. ( 2007;). TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe1:287–298 [CrossRef][PubMed]
    [Google Scholar]
  66. St Geme J. W. III. ( 2002;). Molecular and cellular determinants of non-typeable Haemophilus influenzae adherence and invasion. Cell Microbiol4:191–200 [CrossRef][PubMed]
    [Google Scholar]
  67. St Geme J. W. III, Falkow S.. ( 1990;). Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect Immun58:4036–4044[PubMed]
    [Google Scholar]
  68. Swords W. E., Buscher B. A., Ver Steeg Ii K., Preston A., Nichols W. A., Weiser J. N., Gibson B. W., Apicella M. A.. ( 2000;). Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol Microbiol37:13–27 [CrossRef][PubMed]
    [Google Scholar]
  69. Takesono A., Heasman S. J., Wojciak-Stothard B., Garg R., Ridley A. J.. ( 2010;). Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells. PLoS ONE5:e8774 [CrossRef][PubMed]
    [Google Scholar]
  70. Uliczka F., Kornprobst T., Eitel J., Schneider D., Dersch P.. ( 2009;). Cell invasion of Yersinia pseudotuberculosis by invasin and YadA requires protein kinase C, phospholipase C-γ1 and Akt kinase. Cell Microbiol11:1782–1801 [CrossRef][PubMed]
    [Google Scholar]
  71. Van den Broeke C., Radu M., Chernoff J., Favoreel H. W.. ( 2010;). An emerging role for p21-activated kinases (Paks) in viral infections. Trends Cell Biol20:160–169 [CrossRef][PubMed]
    [Google Scholar]
  72. Vancheri C., Mastruzzo C., Sortino M. A., Crimi N.. ( 2004;). The lung as a privileged site for the beneficial actions of PGE2. Trends Immunol25:40–46 [CrossRef][PubMed]
    [Google Scholar]
  73. Virji M., Kayhty H., Ferguson D. J., Alexandrescu C., Moxon E. R.. ( 1991;). Interactions of Haemophilus influenzae with cultured human endothelial cells. Microb Pathog10:231–245 [CrossRef][PubMed]
    [Google Scholar]
  74. Waschke J., Drenckhahn D., Adamson R. H., Barth H., Curry F. E.. ( 2004;). cAMP protects endothelial barrier functions by preventing Rac-1 inhibition. Am J Physiol Heart Circ Physiol287:H2427–H2433 [CrossRef][PubMed]
    [Google Scholar]
  75. Watabe-Uchida M., John K. A., Janas J. A., Newey S. E., Van Aelst L.. ( 2006;). The Rac activator DOCK7 regulates neuronal polarity through local phosphorylation of stathmin/Op18. Neuron51:727–739 [CrossRef][PubMed]
    [Google Scholar]
  76. Weernink P. A., Meletiadis K., Hommeltenberg S., Hinz M., Ishihara H., Schmidt M., Jakobs K. H.. ( 2004;). Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J Biol Chem279:7840–7849 [CrossRef][PubMed]
    [Google Scholar]
  77. Wittmann T., Bokoch G. M., Waterman-Storer C. M.. ( 2004;). Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem279:6196–6203 [CrossRef][PubMed]
    [Google Scholar]
  78. Wong K. W., Isberg R. R.. ( 2003;). Arf6 and phosphoinositol-4-phosphate-5-kinase activities permit bypass of the Rac1 requirement for beta1 integrin-mediated bacterial uptake. J Exp Med198:603–614 [CrossRef][PubMed]
    [Google Scholar]
  79. Xue Q., Jenkins S. A., Gu C., Smeds E., Liu Q., Vasan R., Russell B. H., Xu Y.. ( 2010;). Bacillus anthracis spore entry into epithelial cells is an actin-dependent process requiring c-Src and PI3K. PLoS ONE5:e11665 [CrossRef][PubMed]
    [Google Scholar]
  80. Yamada M., Tamura Y., Sanzen N., Sato-Nishiuchi R., Hasegawa H., Ashman L. K., Rubinstein E., Yáñez-Mó M., Sánchez-Madrid F., Sekiguchi K.. ( 2008;). Probing the interaction of tetraspanin CD151 with integrin α3β1 using a panel of monoclonal antibodies with distinct reactivities toward the CD151-integrin α3β1 complex. Biochem J415:417–427 [CrossRef][PubMed]
    [Google Scholar]
  81. Yoshida S., Sasakawa C.. ( 2003;). Exploiting host microtubule dynamics: a new aspect of bacterial invasion. Trends Microbiol11:139–143 [CrossRef][PubMed]
    [Google Scholar]
  82. Zimmermann L., Peterhans E., Frey J.. ( 2010;). RGD motif of lipoprotein T, involved in adhesion of Mycoplasma conjunctivae to lamb synovial tissue cells. J Bacteriol192:3773–3779 [CrossRef][PubMed]
    [Google Scholar]
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