Tarp regulates early Chlamydia-induced host cell survival through interactions with the human adaptor protein SHC1

Journal of Cell Biology

Volumn 190, Issue 1, 2010, Pages 143-157

  Mehlitz, Adrian ^a,b   Banhart, Sebastian ^a   Mäurer, André P ^a   Kaushansky, Alexis ^c   Gordus, Andrew G ^c   Zielecki, Julia ^a   MacBeath, Gavin ^c   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BACTERIAL PROTEIN; PHOSPHOPEPTIDE; PROTEIN SHC; PROTEIN TARP; TRANSCRIPTOME; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; GENE CONTROL; HOST CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

APOPTOSIS; BACTERIAL PROTEINS; CELL SURVIVAL; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); CHLAMYDIA; CHLAMYDIA TRACHOMATIS;

EID: 77954746346     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200909095     Document Type: Article

References (71)

1. Arora, S., Y. Wang, Z. Jia, S. Vardar-Sengul, A. Munawar, K.S. Doctor, M. Birrer, M. McClelland, E. Adamson, and D. Mercola. 2008. Egr1 regulates the coordinated expression of numerous EGF receptor target genes as identified by ChIP-on-chip. Genome Biol. 9:R166. doi:10.1186/gb-2008-9-11-r166
2. Asahi, M., T. Azuma, S. Ito, Y. Ito, H. Suto, Y. Nagai, M. Tsubokawa, Y. Tohyama, S. Maeda, M. Omata, et al. 2000. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191:593-602. doi:10.1084/jem.191.4.593
3. Backert, S., S.M. Feller, and S. Wessler. 2008. Emerging roles of Abl family tyrosine kinases in microbial pathogenesis. Trends Biochem. Sci. 33:80-90.
4. Barilá, D., R. Mangano, S. Gonfloni, J. Kretzschmar, M. Moro, D. Bohmann, and G. Superti-Furga. 2000. A nuclear tyrosine phosphorylation circuit: c-Jun as an activator and substrate of c-Abl and JNK. EMBO J. 19:273-281. doi:10.1093/emboj/19.2.273 (Pubitemid 30042709)
5. Brunham, R.C., and J. Rey-Ladino. 2005. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat. Rev. Immunol. 5:149-161. doi:10.1038/nri1551 (Pubitemid 40208904)
6. Buchholz, K.R., and R.S. Stephens. 2008. The cytosolic pattern recognition receptor NOD1 induces inflammatory interleukin-8 during Chlamydia trachomatis infection. Infect. Immun. 76:3150-3155. doi:10.1128/IAI.00104-08
7. Chen, X.M., P.L. Splinter, P.S. Tietz, B.Q. Huang, D.D. Billadeau, and N.F. LaRusso. 2004. Phosphatidylinositol 3-kinase and frabin mediate Cryptosporidium parvum cellular invasion via activation of Cdc42. J. Biol. Chem. 279:31671-31678. doi:10.1074/jbc.M401592200 (Pubitemid 39037838)
8. Christie, P.J., K. Atmakuri, V. Krishnamoorthy, S. Jakubowski, and E. Cascales. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485. doi:10.1146/annurev.micro. 58.030603.123630 (Pubitemid 41507439)
9. Churin, Y., L. Al-Ghoul, O. Kepp, T.F. Meyer, W. Birchmeier, and M. Naumann. 2003. Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J. Cell Biol. 161:249-255. doi:10.1083/jcb. 200208039 (Pubitemid 36529844)
10. Clifton, D.R., K.A. Fields, S.S. Grieshaber, C.A. Dooley, E.R. Fischer, D.J. Mead, R.A. Carabeo, and T. Hackstadt. 2004. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc. Natl. Acad. Sci. USA. 101:10166-10171. doi:10.1073/pnas.0402829101
11. Clifton, D.R., C.A. Dooley, S.S. Grieshaber, R.A. Carabeo, K.A. Fields, and T. Hackstadt. 2005. Tyrosine phosphorylation of the chlamydial effector protein Tarp is species specific and not required for recruitment of actin. Infect. Immun. 73:3860-3868. doi:10.1128/IAI.73.7.3860-3868.2005
12. Elwell, C.A., A. Ceesay, J.H. Kim, D. Kalman, and J.N. Engel. 2008. RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog. 4:e1000021. doi:10.1371/journal.ppat.1000021
13. Fagiani, E., G. Giardina, L. Luzi, M. Cesaroni, M. Quarto, M. Capra, G. Germano, M. Bono, M. Capillo, P. Pelicci, and L. Lanfrancone. 2007. RaLP, a new member of the Src homology and collagen family, regulates cell migration and tumor growth of metastatic melanomas. Cancer Res. 67:3064-3073. doi:10.1158/0008-5472.CAN-06-2301
14. Fan, T., H. Lu, H. Hu, L. Shi, G.A. McClarty, D.M. Nance, A.H. Greenberg, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487-496. doi:10.1084/jem.187.4.487 (Pubitemid 28093351)
15. Fischer, S.F., J. Vier, S. Kirschnek, A. Klos, S. Hess, S. Ying, and G. Häcker. 2004. Chlamydia inhibit host cell apoptosis by degradation of proapoptotic BH3-only proteins. J. Exp. Med. 200:905-916. doi:10.1084/jem. 20040402
16. Goraca, A. 2002. New views on the role of endothelin (minireview). Endocr. Regul. 36:161-167.
17. Gordus, A., and G. MacBeath. 2006. Circumventing the problems caused by protein diversity in microarrays: implications for protein interaction networks. J. Am. Chem. Soc. 128:13668-13669. doi:10.1021/ja065381g (Pubitemid 44632829)
18. Gregorc, U., S. Ivanova, M. Thomas, E. Guccione, B. Glaunsinger, R. Javier, V. Turk, L. Banks, and B. Turk. 2007. Cleavage of MAGI-1, a tight junction PDZ protein, by caspases is an important step for cell-cell detachment in apoptosis. Apoptosis. 12:343-354. doi:10.1007/s10495-006-0579-6 (Pubitemid 46169915)
19. Guo, W., and F.G. Giancotti. 2004. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5:816-826. doi:10.1038/nrm1490
20. Gurumurthy, R.K., A.P. Mäurer, N. Machuy, S. Hess, K.-P. Pleissner, J. Schuchhardt, T. Rudel, and T.F. Meyer. 2010. A loss-of-function screen reveals Rasand Raf-independent MEK-ERK signaling during Chlamydia trachomatis infection. Sci. Signal. 3:ra21. doi:10.1126/scisignal.2000651
21. Hantschel, O., B. Nagar, S. Guettler, J. Kretzschmar, K. Dorey, J. Kuriyan, and G. Superti-Furga. 2003. A myristoyl/phosphotyrosine switch regulates c-Abl. Cell. 112:845-857. doi:10.1016/S0092-8674(03)00191-0
22. Hatakeyama, M. 2008. SagA of CagA in Helicobacter pylori pathogenesis. Curr. Opin. Microbiol. 11:30-37. doi:10.1016/j.mib.2007.12.003
23. Heuer, D., V. Brinkmann, T.F. Meyer, and A.J. Szczepek. 2003. Expression and translocation of chlamydial protease during acute and persistent infection of the epithelial HEp-2 cells with Chlamydophila (Chlamydia) pneumoniae. Cell. Microbiol. 5:315-322. doi:10.1046/j.1462-5822.2003.00278.x (Pubitemid 37009909)
24. Higashi, H., R. Tsutsumi, A. Fujita, S. Yamazaki, M. Asaka, T. Azuma, and M. Hatakeyama. 2002. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc. Natl. Acad. Sci. USA. 99:14428-14433. doi:10.1073/pnas.222375399 (Pubitemid 35257688)
25. Hueck, C.J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433. (Pubitemid 28270280)
26. Jewett, T.J., E.R. Fischer, D.J. Mead, and T. Hackstadt. 2006. Chlamydial TARP is a bacterial nucleator of actin. Proc. Natl. Acad. Sci. USA. 103:15599-15604. doi:10.1073/pnas.0603044103
27. Jewett, T.J., C.A. Dooley, D.J. Mead, and T. Hackstadt. 2008. Chlamydia trachomatis tarp is phosphorylated by src family tyrosine kinases. Biochem. Biophys. Res. Commun. 371:339-344. doi:10.1016/j.bbrc.2008.04.089
28. Jones, N., and D.J. Dumont. 2000. Tek/Tie2 signaling: new and old partners. Cancer Metastasis Rev. 19:13-17. doi:10.1023/A:1026555121511 (Pubitemid 32004687)
29. Jones, R.B., A. Gordus, J.A. Krall, and G. MacBeath. 2006. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature. 439:168-174. doi:10.1038/nature04177 (Pubitemid 43083134)
30. Juban, G., G. Giraud, B. Guyot, S. Belin, J.J. Diaz, J. Starck, C. Guillouf, F. Moreau-Gachelin, and F. Morlé. 2009. Spi-1 and Fli-1 directly activate common target genes involved in ribosome biogenesis in Friend erythroleukemic cells. Mol. Cell. Biol. 29:2852-2864. doi:10.1128/MCB.01435-08
31. Keates, S., A.C. Keates, M. Warny, R.M. Peek Jr., P.G. Murray, and C.P. Kelly. 1999. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J. Immunol. 163:5552-5559.
32. Kenny, B., R. DeVinney, M. Stein, D.J. Reinscheid, E.A. Frey, and B.B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 91:511-520. doi:10.1016/S0092- 8674(00)80437-7 (Pubitemid 27508240)
33. Lane, B.J., C. Mutchler, S. Al Khodor, S.S. Grieshaber, and R.A. Carabeo. 2008. Chlamydial entry involves TARP binding of guanine nucleotide exchange factors. PLoS Pathog. 4:e1000014. doi:10.1371/journal.ppat.1000014
34. Lewis, J.M., and M.A. Schwartz. 1998. Integrins regulate the association and phosphorylation of paxillin by c-Abl. J. Biol. Chem. 273:14225-14230. doi:10.1074/jbc.273.23.14225
35. Luzi, L., S. Confalonieri, P.P. Di Fiore, and P.G. Pelicci. 2000. Evolution of Shc functions from nematode to human. Curr. Opin. Genet. Dev. 10:668-674. doi:10.1016/S0959-437X(00)00146-5
36. MacBeath, G., and S.L. Schreiber. 2000. Printing proteins as microarrays for high-throughput function determination. Science. 289:1760-1763.
37. Mao, X., and X. Chen. 2005. Crystallization and X-ray crystallographic analysis of human STAT1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61:666-668. doi:10.1107/S1744309105017392 (Pubitemid 44210822)
38. Mathews, S.A., K.M. Volp, and P. Timms. 1999. Development of a quantitative gene expression assay for Chlamydia trachomatis identified temporal expression of sigma factors. FEBS Lett. 458:354-358. doi:10.1016/S0014-5793(99) 01182-5
39. McDowall, M., N.M. Edwards, C.A. Jahoda, and P.I. Hynd. 2008. The role of activins and follistatins in skin and hair follicle development and function. Cytokine Growth Factor Rev. 19:415-426. doi:10.1016/j.cytogfr.2008.08.005
40. Mehlitz, A., S. Banhart, S. Hess, M. Selbach, and T.F. Meyer. 2008. Complex kinase requirements for Chlamydia trachomatis Tarp phosphorylation. FEMS Microbiol. Lett. 289:233-240. doi:10.1111/j.1574-6968.2008.01390.x
41. Meng, W., S. Sawasdikosol, S.J. Burakoff, and M.J. Eck. 1999. Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature. 398:84-90. doi:10.1038/18050
42. Mimuro, H., T. Suzuki, J. Tanaka, M. Asahi, R. Haas, and C. Sasakawa. 2002. Grb2 is a key mediator of helicobacter pylori CagA protein activities. Mol. Cell. 10:745-755. doi:10.1016/S1097-2765(02)00681-0 (Pubitemid 35335631)
43. Muñoz, E., D. Xu, M. Kemp, F. Zhang, J. Liu, and R.J. Linhardt. 2006. Affinity, kinetic, and structural study of the interaction of 3-O-sulfotransferase isoform 1 with heparan sulfate. Biochemistry. 45:5122-5128. doi:10.1021/bi052403n
44. Nagar, B., O. Hantschel, M.A. Young, K. Scheffzek, D. Veach, W. Bornmann, B. Clarkson, G. Superti-Furga, and J. Kuriyan. 2003. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell. 112:859-871. doi:10.1016/S0092- 8674(03)00194-6 (Pubitemid 36378887)
45. Neef, R., M.A. Kuske, E. Pröls, and J.P. Johnson. 2002. Identification of the human PHLDA1/TDAG51 gene: down-regulation in metastatic melanoma contributes to apoptosis resistance and growth deregulation. Cancer Res. 62:5920-5929. (Pubitemid 35204755)
46. Oh, E.S., and J.R. Couchman. 2004. Syndecans-2 and -4; close cousins, but not identical twins. Mol. Cells. 17:181-187.
47. Paland, N., L. Böhme, R.K. Gurumurthy, A. Mäurer, A.J. Szczepek, and T. Rudel. 2008. Reduced display of tumor necrosis factor receptor I at the host cell surface supports infection with Chlamydia trachomatis. J. Biol. Chem. 283:6438-6448. doi:10.1074/jbc.M708422200
48. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P.G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell. 70:93-104. doi:10.1016/0092-8674(92)90536-L
49. Perfettini, J.L., M. Gissot, P. Souque, and D.M. Ojcius. 2002. Modulation of apoptosis during infection with Chlamydia. Methods Enzymol. 358:334-344. doi:10.1016/S0076-6879(02)58099-X
50. Poppe, M., S.M. Feller, G. Römer, and S. Wessler. 2007. Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene. 26:3462-3472. doi:10.1038/sj.onc.1210139 (Pubitemid 46816757)
51. Rajalingam, K., M. Sharma, C. Lohmann, M. Oswald, O. Thieck, C.J. Froelich, and T. Rudel. 2008. Mcl-1 is a key regulator of apoptosis resistance in Chlamydia trachomatis-infected cells. PLoS One. 3:e3102. doi:10.1371/journal. pone.0003102
52. Ravichandran, K.S. 2001. Signaling via Shc family adapter proteins. Oncogene. 20:6322-6330. doi:10.1038/sj.onc.1204776
53. Reutershan, J., and K. Ley. 2004. Bench-to-bedside review: acute respiratory distress syndrome - how neutrophils migrate into the lung. Crit. Care. 8:453-461. doi:10.1186/cc2881 (Pubitemid 40073680)
54. Rozen, S., and H.J. Skaltesky. 2000. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology. S. Krawetz and S. Misener, editors. Humana Press, Totowa, NJ. 365-386.
55. Sambrook, J., and D.W. Russel. 2001. Molecular Cloning: A Laboratory Manual. Third edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 2,334 pp.
56. Schlessinger, J., and M.A. Lemmon. 2003. SH2 and PTB domains in tyrosine kinase signaling. Sci. STKE. 2003:RE12. doi:10.1126/stke.2003.191.re12
57. Schubbert, S., K. Shannon, and G. Bollag. 2007. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer. 7:295-308. doi:10.1038/nrc2109 (Pubitemid 46480970)
58. Selbach, M., F.E. Paul, S. Brandt, P. Guye, O. Daumke, S. Backert, C. Dehio, and M. Mann. 2009. Host cell interactome of tyrosine-phosphorylated bacterial proteins. Cell Host Microbe. 5:397-403. doi:10.1016/j.chom.2009.03.004
59. Su, H., G. McClarty, F. Dong, G.M. Hatch, Z.K. Pan, and G. Zhong. 2004. Activation of Raf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J. Biol. Chem. 279:9409-9416. doi:10.1074/jbc.M312008200 (Pubitemid 38296007)
60. Sudol, M. 1998. From Src Homology domains to other signaling modules: proposal of the 'protein recognition code'. Oncogene. 17:1469-1474. doi:10.1038/sj.onc.1202182
61. Suzuki, M., H. Mimuro, T. Suzuki, M. Park, T. Yamamoto, and C. Sasakawa. 2005. Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J. Exp. Med. 202:1235-1247. doi:10.1084/jem.20051027 (Pubitemid 41586954)
62. Swimm, A., B. Bommarius, Y. Li, D. Cheng, P. Reeves, M. Sherman, D. Veach, W. Bornmann, and D. Kalman. 2004. Enteropathogenic Escherichia coli use redundant tyrosine kinases to form actin pedestals. Mol. Biol. Cell. 15:3520-3529. doi:10.1091/mbc.E04-02-0093 (Pubitemid 38989693)
63. Tammer, I., S. Brandt, R. Hartig, W. König, and S. Backert. 2007. Activation of Abl by Helicobacter pylori: a novel kinase for CagA and crucial mediator of host cell scattering. Gastroenterology. 132:1309-1319. doi:10.1053/j.gastro.2007.01.050 (Pubitemid 46627580)
64. Tapinos, N., and A. Rambukkana. 2005. Insights into regulation of human Schwann cell proliferation by Erk1/2 via a MEK-independent and p56Lck-dependent pathway from leprosy bacilli. Proc. Natl. Acad. Sci. USA. 102:9188-9193. doi:10.1073/pnas.0501196102 (Pubitemid 40923539)
65. Thomas, J.O., and A.A. Travers. 2001. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 26:167-174. doi:10.1016/S0968-0004(01)01801-1
66. Tse, S.M., D. Mason, R.J. Botelho, B. Chiu, M. Reyland, K. Hanada, R.D. Inman, and S. Grinstein. 2005. Accumulation of diacylglycerol in the Chlamydia inclusion vacuole: possible role in the inhibition of host cell apoptosis. J. Biol. Chem. 280:25210-25215. doi:10.1074/jbc.M501980200
67. Valdivia, R.H. 2008. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr. Opin. Microbiol. 11:53-59. doi:10.1016/j.mib.2008.01.003
68. van der Geer, P., S. Wiley, G.D. Gish, and T. Pawson. 1996. The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr. Biol. 6:1435-1444. doi:10.1016/S0960-9822(96)00748-8
69. Willis, S.N., and J.M. Adams. 2005. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17:617-625. doi:10.1016/j.ceb.2005.10.001
70. Wright, H.R., A. Turner, and H.R. Taylor. 2008. Trachoma. Lancet. 371:1945-1954. doi:10.1016/S0140-6736(08)60836-3
71. Zhao, J., K.A. Kim, and A. Abo. 2009. Tipping the balance: modulating the Wnt pathway for tissue repair. Trends Biotechnol. 27:131-136. doi:10.1016/j.tibtech.2008.11.007