The Role of Focal Adhesion Kinase Signaling Pathway in the Bacterial Invasion of Non-phagocytic Cells

doi:10.13560/j.cnki.biotech.bull.1985.2016.07.004

Abstract

Abstract: The adhesion and invasion into eukaryotic cells are major steps in bacterial pathogenesis. In order to further study the entire process and molecular mechanisms of bacteria invading non-phagocytic cells,we reviewed the bacterial adhesion and invasion of non-phagocytic cells and the regulatory mechanisms of focal adhesion kinase（FAK）in this process. During the adhesion process,the interaction of surface adhesive molecules and special structures of bacteria with receptors of host cells activates the FAK to regulate the cytoskeletal rearrangement through FAK/Src-Cortactin-Arp2/3 and FAK/PI3K-Rac pathways,which promotes the bacterial invasion of non-phagocytic cells.

Key words: bacteria, adhesion, invasion, focal adhesion kinase, signaling pathway

JIA Xiao-yang FU Yu WANG Xiao-nan WANG Zhi-gang HAO Hui-fang. The Role of Focal Adhesion Kinase Signaling Pathway in the Bacterial Invasion of Non-phagocytic Cells[J]. Biotechnology Bulletin, 2016, 32(7): 28-33.

References

[1] 郭晓奎, 童善庆. 细胞微生物学[M]. 上海：第二军医大学出版社, 2004：94-96.
[2] Kline KA, Fälker S, Dahlberg S, et al. Bacterial adhesins in host-microbe interactions[J]. Cell Host Microbe, 2009, 6：580-592.
[3] Pizarro-Cerdá J, Cossart P. Bacterial adhesion and entry into host cells[J]. Cell, 2006, 124（4）：720-727.
[4] Hultgren SJ, Normark S, Abraham SN. Chaperoneassisted assembly and molecular architecture of adhesive pili[J]. Annu Rev Microbiol, 1991, 45：383-415.
[5] Wolfgang M, van Putten JP, Hayes SF, et al. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili[J]. EMBO J, 2000, 19（23）：6408-6418.
[6] Foster TJ, Geoghegan JA, Ganesh VK, et al. Adhesion, invasion and evasion：The many functions of the surface proteins of Staphylococcus aureus[J]. Nat Rev Microbiol, 2014, 1：49-62.
[7] Stones DH, Krachler AM. Fatal attraction：how bacterial adhesins affect host signaling and what we can learn from them[J]. Int J Mol Sci, 2015, 16（2）：2626-2640.
[8] Bölin I, Wolf-Watz H. Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis[J]. Infect Immun, 1984, 43（1）：72-78.
[9] Juliano RL. Signal transduction by cell adhesion receptors and the cytoskeleton：functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members[J]. Annu Rev Pharmacol Toxicol, 2002, 42：283-323.
[10] El Tahir Y, Skurnik M. YadA, the multifaceted Yersinia adhesion [J]. Int J Med Microbiol, 2001, 291（3）：209-218.
[11] Isberg RR, Barnes P. Subversion of integrins by enteropathogenic Yersinia[J]. J Cell Sci, 2001, 114（1）：21-28.
[12] Boyle EC, Finlay BB. Bacterial pathogenesis：exploiting cellular adherence[J]. Curr Opin Cell Biol, 2003, 15（5）：633-639.
[13] Pizarro-Cerdá J, et al. Entry of Listeria monocytogenes in mammalian epithelial cells：an updated view[J]. Cold Spring Harb Perspect in Med, 2012, 2（11）. pii：a010009.
[14] Isberg RR, Leong JM. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells[J]. Cell, 1990, 60（5）：861-871.
[15] Nägele V, Heesemann J, Schielke S, et al. Neisseria meningitids adhesin NadA targets β1 integrins：functional similarity to Yersinia invasin[J]. J Biol Chem, 2011, 286（23）：20536-20546.
[16] Hoffmann C, et al. Integrin-mediated uptake of fibronectin-binding bacteria[J]. Eur J Cell Biol, 2011, 90（11）：891-896.
[17] Campellone KG, Leong JM. Nck-independent actin assembly is mediated by two phosphorylated tyrosines within enteropathogenic Escherichia coli Tir[J]. Mol Microbiol, 2005, 56（2）：416-432.
[18] 张湘燕, 郭晓奎, 刘晶星, 等. 细菌利用宿主肌动蛋白细胞骨架进入非吞噬细胞的机制[J]. 细胞生物学杂志, 2002, 24（3）：155-158.
[19] Swanson JA, Baer SC. Phagocytosis by zippers and triggers[J]. Trends Cell Biol. 1995, 5（3）：89-93.
[20] Alva-Murillo N, López-Meza JE, Ochoa-Zarzosa A. Nonprofessional Phagocytic Cell Receptors Involved in Staphylococcus aureus Internalization[J]. Biomed Res Int, 2014, 2014：538-546.
[21] Hardt WD, Chen LM, Schuebel KE, et al. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells[J]. Cell, 1998, 5：815-826.
[22] Kim M, Ogawa M, Mimuro H, et al. Reinforcement of epithelial cell adhesion to basement membrane by a bacterial pathogen as a new infectious stratagem[J]. Virulence, 2010, 1（1）：52-55.
[23] Parsons JT, Parsons SJ. Src family protein tyrosine kinases：cooperating with growth factor and adhesion signaling pathways[J]. Curr Opin Cell Biol, 1997, 9（2）：187-192.
[24] Sasaki H, Nagura K, Ishino M, et al. Cloning and kinase characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion subfamily[J]. J Biol Chem, 1995, 270（36）：21206-21219.
[25] Lev S, Moreno H, Martinez R, et al. Protein tyrosine kinase PYK2 involved in Ca 2+ -induced regulation of ion channel and MAP kinase functions[J]. Nature, 1995, 376（6543）：737-745.
[26] Avraham S, London R, Fu Y, et al：Identification and characterization of a novel related adhesion focal tyrosine kinase（RAFTK）from megakaryocytes and brain[J]. J Biol Chem, 1995, 270：27742-27751.
[27] Yu H, Li X, Marchetto GS, et al. Activation of a novel calcium-dependent protein-tyrosine kinase. Correlation with c-Jun N-terminal kinase but not mitogen-activated protein kinase activation[J]. J Biol Chem, 1996, 271（47）：29993-29998.
[28] Calalb MB, et al. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity：a role for Src family kinases[J]. Mol Cell Biol, 1995, 2：954-963.
[29] Schlaepfer DD, Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases[J]. Mol Cell Biol, 1996, 16（10）：5623-5633.
[30] Burgaya F, Toutant M, Studler JM, et al. Alternatively spliced focal adhesion kinase in rat brain with increased autophosphorylation activity[J]. J Biol Chem, 1997, 272（45）：28720-28725.
[31] Schwartz MA, et al. Integrins：emerging paradigms of signal transduction[J]. Annu Rev Cell Dev Biol, 1995, 11：549-599.
[32] Brown MC, et al. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding[J]. J Cell Biol, 1996, 135（4）：1109-1123.
[33] Chen HC, Appeddu PA, Parsons JT, et al. Interaction of focal adhesion kinase with cytoskeletal protein talin[J]. J Biol Chem, 1995, 270（28）：16995-16999.
[34] Hildebrand JD, Taylor JM, Parsons JT. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase[J]. Mol Cell Biol, 1996, 16（6）：3169-3178.
[35] Ohba T, Ishino M, Aoto H, et al. Interaction of two proline-rich sequences of cell adhesion kinase beta with SH3 domains of p130Cas-related proteins and a GTPase-activating protein[J]. Biochem J, 1998, 330（Pt 3）：1249-1254.
[36] Eto DS, Jones TA, Sundsbak JL, et al. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli[J]. PLoS Pathog, 2007, 3（7）：e100.
[37] Martinez JJ, Hultgren SJ. Requirement of Rho-family GTPases in the invasion of Type 1-piliated uropathogenic Escherichia coli[J]. Cell Microbiol, 2002, 4（1）：19-28.
[38] Shoelson SE, Sivaraja M, Williams KP, et al. Specific phosphopeptide binding regulates a conformational change in the PI 3-kinase SH2 domain associated with enzyme activation[J]. EMBO J, 1993, 12（2）：795-802.
[39] Yin HL, Janmey PA. Phosphoinositide regulation of the actin cytoskeleton[J]. Annu Rev Physiol, 2003, 65：761-789.
[40] Hartwig JH, Bokoch GM, Carpenter CL, et al. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets[J]. Cell, 1995, 82（4）：643-653.
[41] Joh D, Wann ER, Kreikemeyer B, et al. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells[J]. Matrix Biol, 1999, 18（3）：211-223.
[42] Dziewanowska K, Carson AR, Patti JM, et al. Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins：role in internalization by epithelial cells[J]. Infect Immun, 2000, 68（11）：6321-6328.
[43] Agerer F, Lux S, Michel A, et al. Cellular invasion by Staphyloco-ccus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalization[J]. J Cell Sci 2005, 118：2189-2200.
[44] Agerer F, Lux S, Michel A, et al. Cellular invasion by Staphyloco-ccus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation[J]. J Cell Sci, 2005, 118（10）：2189-2200.
[45] Martinez-Quiles N, et al. Erk/Src phospho-rylation of cortactin acts as a switch on-switch off mechanism that controls its ability to acti-vate N-WASP[J]. Mol Cell Biol, 2004, 12：5269-5280.
[46] Pollard TD, Cooper JA. Actin, a central player in cell shape and movement[J]. Science, 2009, 326（5957）：1208-1212.
[47] Kurisu S, Takenawa T. The WASP and WAVE family proteins[J]. Genome Biol, 2009, 10（6）：226.
[48] Martinez-Quiles N, Ho HY, Kirschner MW, et al. Erk/Src phosphorylation of cortactin acts as a switch on switch off mechanism that controls its ability to activate N-WASP[J]. Mol Cell Biol, 2004, 24（12）：5269-5280.