Proteomic analysis of Chlamydia pneumoniae-infected HL cells reveals extensive degradation of cytoskeletal proteins

FEMS Immunology and Medical Microbiology

Volumn 54, Issue 3, 2008, Pages 375-384

  Savijoki, Kirsi ^a,b   Alvesalo, Joni ^b   Vuorela, Pia ^b,c   Leinonen, Maija ^d   Kalkkinen, Nisse ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c ÅBO AKADEMI UNIVERSITY   (Finland)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

2D DIGE; Chlamydia; Cytoskeleton; HL cells; MALDI TOF; Proteolysis

Indexed keywords

BACTERIAL PROTEIN; BETA TUBULIN; CHLAMYDIAL PROTEASE LIKE ACTIVITY FACTOR; CYTOKERATIN 18; CYTOKERATIN 8; LACTACYSTIN; PROTEOME; UNCLASSIFIED DRUG; VIMENTIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CHLAMYDIASIS; CHLAMYDOPHILA PNEUMONIAE; COMPETITIVE INHIBITION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTERMEDIATE FILAMENT; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEOMICS; SEQUENCE ANALYSIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; CELLS, CULTURED; CHLAMYDOPHILA PNEUMONIAE; CYTOSKELETAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EPITHELIAL CELLS; HUMANS; KERATINS; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PROTEINS; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUBULIN; VIMENTIN;

EID: 56049089861     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2008.00488.x     Document Type: Article

References (47)

1. Airenne S, Surcel HM, Tuukkanen J, Leinonen M Saikku P (2002) Chlamydia pneumoniae inhibits apoptosis in human epithelial and monocyte cell lines. Scand J Immunol 55 : 390 398.
2. Alvesalo J, Greco D, Leinonen M, Raitila T, Vuorela P Auvinen P (2008) Microarray analysis of a Chlamydia pneumoniae-infected human epithelial cell line by use of gene ontology hierarchy. J Infect Dis 197 : 156 162.
3. Baek HY, Lim JW, Kim H, Kim JM, Kim JS, Jung HC Kim KH (2004) Oxidative-stress-related proteome changes in Helicobacter pylori-infected human gastric mucosa. Biochem J 379 : 291 299.
4. Bavoil P, Ohlin A Schachter J (1984) Role of disulfide bonding in outer membrane structure and permeability in Chlamydia trachomatis. Infect Immun 44 : 479 485.
5. Birkelund S, Bini L, Pallini V, Sanchez-Campillo M, Liberatori S, Clausen JD, Ostergaard S, Holm A Christiansen G (1997) Characterization of Chlamydia trachomatis l2-induced tyrosine-phosphorylated HeLa cell proteins by two-dimensional gel electrophoresis. Electrophoresis 18 : 563 567.
6. Boleti H, Benmerah A, Ojcius DM, Cerf-Bensussan N Dautry-Varsat A (1999) Chlamydia infection of epithelial cells expressing dynamin and Eps15 mutants: clathrin independent entry into cells and dynamin-dependent productive growth. J Cell Sci 112 : 1487 1496.
7. Byun Y, Chen F, Chang R, Trivedi M, Green KJ Cryns VL (2001) Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ 8 : 443 450.
8. Campbell LA Kuo CC (2004) Chlamydia pneumoniae - an infectious risk factor for atherosclerosis? Nat Rev Microbiol 2 : 23 32.
9. Campbell LA, Kuo CC Grayston JT (1990) Structural and antigenic analysis of Chlamydia pneumoniae. Infect Immun 58 : 93 97.
10. Carabeo RA, Grieshaber SS, Fischer E Hackstadt T (2002) Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells. Infect Immun 70 : 3793 3803.
11. Caulín C, Salvesen GS Oshima RG (1997) Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J Cell Biol 138 : 1379 1394.
12. Chen PH, Ornelles DA Shenk T (1993) The adenovirus L3 23-kilodalton proteinase cleaves the amino-terminal head domain from cytokeratin 18 and disrupts the cytokeratin network of HeLa cells. J Virol 67 : 3507 3514.
13. Christiansen G, Boesen T, Hjerno K, Daugaard L, Mygind P, Madsen AS, Knudsen K, Falk E Birkelund S (1999) Molecular biology of Chlamydia pneumoniae surface proteins and their role in immunopathogenicity. Am Heart J 138 : 491 495.
14. Clausen JD, Christiansen G, Holst HU Birkelund S (1997) Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol Microbiol 25 : 441 449.
15. Coombes BK Mahony JB (2001) cDNA array analysis of altered gene expression in human endothelial cells in response to Chlamydia pneumoniae Infection. Infect Immun 69 : 1420 1427.
16. Dautry-Varsat A, Subtil A Hackstadt T (2005) Recent insights into the mechanisms of Chlamydia entry. Cell Microbiol 7 : 1714 1722.
17. Dong F, Sharma J, Xiao Y, Zhong Y Zhong G (2004a) Intramolecular dimerization is required for the chlamydia-secreted protease CPAF to degrade host transcriptional factors. Infect Immun 72 : 3869 3875.
18. Dong F, Su H, Huang Y, Zhong Y Zhong G (2004b) Cleavage of host keratin 8 by a Chlamydia-secreted protease. Infect Immun 72 : 3863 3868.
19. Eickhoff M, Thalmann J, Hess S, Martin M, Laue T, Kruppa J, Brandes G Klos A (2007) Host cell responses to Chlamydia pneumoniae in gamma interferon-induced persistence overlap those of productive infection and are linked to genes involved in apoptosis, cell cycle, and metabolism. Infect Immun 75 : 2853 2863.
20. Fan P, Dong F, Huang Y Zhong G (2002) Chlamydia pneumoniae secretion of a protease-like activity factor for degrading host cell transcription factors required for major histocompatibility complex antigen expression. Infect Immun 70 : 345 349.
21. Hatch TP (1996) Disulfide cross-linked envelope protein: the functional equivalent of peptidoglycan in chlamydiae? J Bacteriol 178 : 1 5.
22. Heuer D, Brinkmann V, Meyer TF Szczepek AJ (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.
23. Hogan RJ, Mathews SA, Kutlin A, Hammerschlag MR Timms P (2003) Differential expression of genes encoding membrane proteins between acute and continuous Chlamydia pneumoniae infections. Microb Pathogenesis 34 : 11 16.
24. Jewett TJ, Fischer ER, Mead DJ Hackstadt T (2006) Chlamydial TARP is a bacterial nucleator of actin. P Natl Acad Sci USA 103 : 15599 155604.
25. Kuo CC Grayston JT (1990) A sensitive cell line, HL cells, or isolation and propagation of Chlamydia pneumoniae strain TWAR. J Infect Dis 162 : 755 758.
26. Leinonen M Saikku P (2002) Evidence for infectious agents in cardiovascular disease and atherosclerosis. Lancet Infect Dis 2 : 11 17.
27. Lodish H, Berk A, Matsudaira P, Kaiser CA, Krieger M, Scott MP, Zipursky SL Darnell J (2003) Molecular Cell Biology. W.H. Freeman, New York.
28. Malard V, Prat O, Darrouzet E, Bérenguer F, Sage N Quéméneur E (2005) Proteomic analysis of the response of human lung cells to uranium. Proteomics 5 : 4568 4580.
29. Moll R, Franke WW, Schiller DL, Geiger B Krepler R. (1982) The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31 : 11 24.
30. Omary MB, Ku NO, Liao J Price D (1998) Keratin modifications and solubility properties in epithelial cells and in vitro. Subcell Biochem 31 : 105 140.
31. Pal S, Peterson EM de la Maza LM (2005) Vaccination with the Chlamydia trachomatis major outer membrane protein can elicit an immune response as protective as that resulting from inoculation with live bacteria. Infect Immun 73 : 8153 8160.
32. Pirbhai M, Dong F, Zhong Y, Pan KZ Zhong G (2006) The secreted protease factor CPAF is responsible for degrading proapoptotic BH3/only proteins in C. trachomatis-infected cells. J Biol Chem 281 : 31495 31501.
33. Saba JA, McComb ME, Potts DL, Costello CE Amar S (2007) Proteomic mapping of stimulus-specific signaling pathways involved in THP-1 cells exposed to Porphyromonas gingivalis or its purified components. J Proteome Res 6 : 2211 2221.
34. Schramm N Wyrick PB (1995) Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect Immun 63 : 324 332.
35. Seipelt J, Liebig HD, Sommergruber W, Gerner C Kuechler E (2000) 2A proteinase of human rhinovirus cleaves cytokeratin 8 in infected HeLa cells. J Biol Chem 275 : 20084 20089.
36. Shevchenko A, Wilm M, Vorm O Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68 : 850 858.
37. Solary E, Eymin B, Droin N Haugg M (1998) Proteases, proteolysis, and apoptosis. Cell Biol Toxicol 14 : 121 132.
38. Subtil A, Wyplosz B, Balañá ME Dautry-Varsat A (2004) Analysis of Chlamydia caviae entry sites and involvement of Cdc42 and Rac activity. J Cell Sci 117 : 3923 3933.
39. Todorovic V, Sokic-Milutinovic A, Drndarevic N, Micev M, Mitrovic O, Nikolic I, Wex T, Milosavljevic T Malfertheiner P (2006) Expression of cytokeratins in Helicobacter pylori-associated chronic gastritis of adult patients infected with cagA+strains: an immunohistochemical study. World J Gastroentero 12 : 1865 1873.
40. Vandahl BB, Birkelund S, Demol H, Hoorelbeke B, Christiansen G, Vandekerckhove J Gevaert K (2001) Proteome analysis of the Chlamydia pneumoniae elementary body. Electrophoresis 22 : 1204 1223.
41. Wissel H, Schulz C, Rudiger M, Krull M, Stevens PA Wauer RR (2003) Chlamydia pneumoniae affect surfactant trafficking and secretion due to changes of type II cell cytoskeleton. Am J Resp Cell Mol 29 : 303 313.
42. Wolf K, Fischer E Hackstadt T (2000) Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect Immun 68 : 2379 2385.
43. Wolf K, Fischer E, Mead D, Zhong G, Peeling R, Whitmire B Caldwell HD (2001) Chlamydia pneumoniae major outer membrane protein is a surface-exposed antigen that elicits antibodies primarily directed against conformation- dependent determinants. Infect Immun 69 : 3082 3091.
44. Wyllie S, Longbottom D, Herring AJ Ashley RH (1999) Single channel analysis of recombinant major outer membrane protein porins from Chlamydia psittaci and Chlamydia pneumoniae. FEBS Lett 445 : 192 196.
45. Zhang Y Schneider RJ (1994) Adenovirus inhibition of cell translation facilitates release of virus particles and enhances degradation of the cytokeratin network. J Virol 68 : 2544 2555.
46. Zhong G, Liu L, Fan T, Fan P Ji H (2000) Degradation of transcription factor RFX5 during the inhibition of both constitutive and interferon-inducible major histocompatibility complex class I expression in Chlamydia-infected cells. J Exp Med 191 : 1525 1534.
47. Zhong G, Fan P, Ji H, Dong F Huang Y (2001) Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J Exp Med 193 : 935 942.