Loss and gain of GroEL in the Mollicutes

Biochemistry and Cell Biology

Volumn 88, Issue 2, 2010, Pages 185-194

  Clark, Gregory W ^a   Tillier, Elisabeth R M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

GroEL; Invasin; Lateral gene transfer; Mycoplasma

Indexed keywords

ADHESIN; GROEL; HOST TISSUES; PHYLOGENETIC ANALYSIS; PROTEOBACTERIA;

GENE TRANSFER;

ADHESIN; CHAPERONE; INVASIN; PROTEIN GROEL; RIBOSOME RNA; THIAMINE; UNCLASSIFIED DRUG; CHAPERONIN 60;

BACTERIAL GENOME; BIOSYNTHESIS; BURKHOLDERIA CENOCEPACIA; CELL INVASION; CHLAMYDIA TRACHOMATIS; CONFERENCE PAPER; GENE TRANSFER; HELICOBACTER PYLORI; HOST CELL; HOST PATHOGEN INTERACTION; MOLLICUTES; MYCOPLASMA; NONHUMAN; PHYLOGENY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEOBACTERIA; RHIZOBIUM; CHEMISTRY; GENETICS; METABOLISM;

BACTERIA (MICROORGANISMS); MOLLICUTES; MYCOPLASMA; MYCOPLASMA PENETRANS; PROTEOBACTERIA;

CHAPERONIN 60; PHYLOGENY; TENERICUTES;

EID: 77950621338     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O09-157     Document Type: Conference Paper

References (85)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215(3): 403-410. PMID:2231712.
2. Barreiro, C., Gonzalez-Lavado, E., Brand, S., Tauch, A., and Martin, J.F. 2005. Heat shock proteome analysis of wild-type Corynebacterium glutamicum ATCC 13032 and a spontaneous mutant lacking GroEL1, a dispensable chaperone. J. Bacteriol. 187: 884-889.
3. Bencina, D., Slavec, B., and Narat, M. 2005. Antibody response to GroEL varies in patients with acute Mycoplasma pneumoniae infection. FEMS Immunol. Med. Microbiol. 43(3): 399-406. doi:10.1016/j.femsim.2004.10.009. PMID:15708314.
4. Bittner, A.N., Foltz, A., and Oke, V. 2007. Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti. J. Bacteriol. 189: 1884-1889.
5. Brennan, P.C., and Feinstein, R.N. 1969. Relationship of hydrogen peroxide production by Mycoplasma pulmonis to virulence for catalase-deficient mice. J. Bacteriol. 98(3): 1036-1040. PMID:5788695.
6. Chang, L.J., Chen, W.H., Minion, F.C., and Shiuan, D. 2008. Mycoplasmas regulate the expression of heat-shock protein genes through CIRCE-HrcA interactions. Biochem. Biophys. Res. Commun. 367(1): 213-218. doi:10.1016/j.bbrc.2007.12.124. PMID:18164681.
7. Chatellier, J., Hill, F., Lund, P.A., and Fersht, A.R. 1998. In vivo activities of GroEL minichaperones. Proc. Natl. Acad. Sci. U.S.A. 95(17): 9861-9866. doi:10.1073/pnas.95.17.9861. PMID:9707566.
8. Cohen, G., and Somerson, N.L. 1969. Glucose-dependent secretion and destruction of hydrogen peroxide by Mycoplasma pneumoniae. J. Bacteriol. 98(2): 547-551. PMID:5784211.
9. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37(Database issue): D141-D145. doi:10.1093/nar/gkn879. PMID:19004872.
10. Dallo, S.F., and Baseman, J.B. 2000. Intracellular DNA replication and long-term survival of pathogenic mycoplasmas. Microb. Pathog. 29(5): 301-309. doi:10.1006/mpat.2000.0395. PMID:11031124.
11. Dallo, S.F., Chavoya, A., and Baseman, J.B. 1990. Characterization of the gene for a 30-kilodalton adhesion-related protein of Mycoplasma pneumoniae. Infect. Immun. 58(12): 4163-4165. PMID:2123834.
12. de Souza, C.P. 2003. Pathogenicity mechanisms of prokaryotic cells: an evolutionary view. Braz. J. Infect. Dis. 7(1): 23-31. PMID:12807689.
13. dos Reis, M., Wernisch, L., and Savva, R. 2003. Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res. 31(23): 6976-6985. doi:10.1093/nar/gkg897. PMID:14627830.
14. Dusanić, D., Bercic, R.L., Cizelj, I., Salmic, S., Narat, M., and Bencina, D. 2009. Mycoplasma synoviae invades non-phagocytic chicken cells in vitro. Vet. Microbiol. 138(1-2): 114-119. doi:10.1016/j.vetmic.2009.02.014. PMID:19321273.
15. Ellis, R.J. 2005. Chaperomics: in vivo GroEL function defined. Curr. Biol. 15(17): R661-R663. doi:10.1016/j.cub.2005.08.025. PMID:16139196.
16. Fayet, O., Ziegelhoffer, T., and Georgopoulos, C. 1989. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol. 171(3): 1379-1385. PMID:2563997.
17. Felsenstein, J. 2005. PHYLIP (phylogeny inference package) (version 3.6 ed.) [Computer Software]. Department of Genome Sciences, University of Washington, Seattle, Wash.
18. Garduño, R.A., Garduño, E., and Hoffman, P.S. 1998. Surface-associated hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66(10): 4602-4610. PMID:9746556.
19. Glass, J.I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M.R., Maruf, M., et al. 2006. Essential genes of a minimal bacterium. Proc. Natl. Acad. Sci. U.S.A. 103(2): 425-430. doi:10.1073/pnas.0510013103. PMID:16407165.
20. Goyal, K., Qamra, R., and Mande, S.C. 2006. Multiple gene duplication and rapid evolution in the groEL gene: functional implications. J. Mol. Evol. 63(6): 781-787. doi:10.1007/s00239-006-0037-7. PMID:17103057.
21. Groebel, K., Hoelzle, K., Wittenbrink, M.M., Ziegler, U., and Hoelzle, L.E. 2009. Mycoplasma suis invades porcine erythrocytes. Infect. Immun. 77(2): 576-584. doi:10.1128/IAI.00773-08. PMID:19015255.
22. Hatchel, J.M., Balish, R.S., Duley, M.L., and Balish, M.F. 2006. Ultrastructure and gliding motility of Mycoplasma amphoriforme, a possible human respiratory pathogen. Microbiology, 152(Pt 7): 2181-2189. doi:10.1099/mic.0. 28905-0. PMID:16804191.
23. Henderson, B., Allan, E., and Coates, A.R. 2006. Stress wars: the direct role of host and bacterial molecular chaperones in bacterial infection. Infect. Immun. 74(7): 3693-3706. doi:10.1128/IAI.01882-05. PMID:16790742.
24. Hennequin, C., Porcheray, F., Waligora-Dupriet, A., Collignon, A., Barc, M., Bourlioux, P., and Karjalainen, T. 2001. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology, 147(Pt 1): 87-96. PMID:11160803.
25. Hoelzle, L.E., Hoelzle, K., Harder, A., Ritzmann, M., Aupperle, H., Schoon, H.A., et al. 2007. First identification and functional characterization of an immunogenic protein in unculturable haemotrophic Mycoplasmas (Mycoplasma suis HspA1). FEMS Immunol. Med. Microbiol. 49(2): 215-223. doi:10.1111/j.1574- 695X.2006.00184.x. PMID:17328755.
26. Hoffman, P.S., and Garduno, R.A. 1999. Surface-associated heat shock proteins of Legionella pneumophila and Helicobacter pylori: roles in pathogenesis and immunity. Infect. Dis. Obstet. Gynecol. 7(1-2): 58-63. doi:10.1002/(SICI)1098-0997(1999)7:1/2〈58::AID-IDOG12〉3.0.CO;2-A. PMID:10231011.
27. Horwich, A.L., Farr, G.W., and Fenton, W.A. 2006. GroEL-GroES-mediated protein folding. Chem. Rev. 106(5): 1917-1930. doi:10.1021/cr040435v. PMID:16683761.
28. Houry, W.A., Frishman, D., Eckerskorn, C., Lottspeich, F., and Hartl, F.U. 1999. Identification of in vivo substrates of the chaperonin GroEL. Nature, 402(6758): 147-154. doi:10.1038/45977. PMID:10647006.
29. Hu, Y., Henderson, B., Lund, P.A., Tormay, P., Ahmed, M.T., Gurcha, S.S., et al. 2008. A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable but fails to induce an inflammatory response in animal models of infection. Infect. Immun. 76(4): 1535-1546. doi:10.1128/IAI.01078-07. PMID:18227175.
30. Hutchison, C.A., III, Peterson, S.N., Gill, S.R., Cline, R.T., White, O., Fraser, C.M., et al. 1999. Global transposon mutagenesis and a minimal Mycoplasma genome. Science, 286(5447): 2165-2169. doi:10.1126/science.286.5447. 2165. PMID:10591650.
31. Jensen, J.S., Blom, J., and Lind, K. 1994. Intracellular location of Mycoplasma genitalium in cultured Vero cells as demonstrated by electron microscopy. Int. J. Exp. Pathol. 75(2): 91-98. PMID:8199010.
32. Kandror, O., Busconi, L., Sherman, M., and Goldberg, A.L. 1994. Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES. J. Biol. Chem. 269(38): 23575-23582. PMID:7916344.
33. Kannan, T.R., Musatovova, O., Gowda, P., and Baseman, J.B. 2008. Characterization of a unique ClpB protein of Mycoplasma pneumoniae and its impact on growth. Infect. Immun. 76(11): 5082-5092. doi:10.1128/IAI.00698-08. PMID:18779336.
34. Kerner, M.J., Naylor, D.J., Ishihama, Y., Maier, T., Chang, H.C., Stines, A.P., et al. 2005. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell, 122(2): 209-220. doi:10.1016/j.cell.2005.05. 028. PMID:16051146.
35. Kobayashi, K., Ehrlich, S.D., Albertini, A., Amati, G., Andersen, K.K., Arnaud, M., et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U.S.A. 100(8): 4678-4683. doi:10.1073/pnas.0730515100. PMID:12682299.
36. Koonin, E.V. 2000. How many genes can make a cell: the minimal-gene-set concept. Annu. Rev. Genomics Hum. Genet. 1(1): 99-116. doi:10.1146/annurev. genom.1.1.99. PMID:11701626.
37. Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y., and Ito, K. 1989. Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J. 8: 3517-3521.
38. Lee, W.T., Terlesky, K.C., and Tabita, F.R. 1997. Cloning and characterization of two groESL operons of Rhodobacter sphaeroides: transcriptional regulation of the heat-induced groESL operon. J. Bacteriol. 179(2): 487-495. PMID:8990302.
39. Li, M., and Wong, S.L. 1992. Cloning and characterization of the groESL operon from Bacillus subtilis. J. Bacteriol. 174(12): 3981-3992. PMID:1350776.
40. Lund, P.A. 2009. Multiple chaperonins in bacteria - why so many? FEMS Microbiol. Rev. 33(4): 785-800. doi:10.1111/j.1574-6976.2009.00178.x. PMID:19416363.
41. Melkani, G.C., McNamara, C., Zardeneta, G., and Mendoza, J.A. 2004. Hydrogen peroxide induces the dissociation of GroEL into monomers that can facilitate the reactivation of oxidatively inactivated rhodanese. Int. J. Biochem. Cell Biol. 36(3): 505-518. doi:10.1016/j.biocel.2003.08.012. PMID:14687928.
42. Mernaugh, G.R., Dallo, S.F., Holt, S.C., and Baseman, J.B. 1993. Properties of adhering and nonadhering populations of Mycoplasma genitalium. Clin. Infect. Dis. 17(Suppl 1): S69-S78. PMID:8399942.
43. Meseguer, M.A., Alvarez, A., Rejas, M.T., Sánchez, C., Pérez-Díaz, J.C., and Baquero, F. 2003. Mycoplasma pneumoniae: a reduced-genome intracellular bacterial pathogen. Infect. Genet. Evol. 3(1): 47-55. doi:10.1016/S1567-1348(02)00151-X. PMID:12797972.
44. Moran, N.A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell, 108(5): 583-586. doi:10.1016/S0092-8674(02)00665-7. PMID:11893328.
45. Morett, E., Korbel, J.O., Rajan, E., Saab-Rincon, G., Olvera, L., Olvera, M., et al. 2003. Systematic discovery of analogous enzymes in thiamin biosynthesis. Nat. Biotechnol. 21(7): 790-795. doi:10.1038/nbt834. PMID:12794638.
46. Musatovova, O., Dhandayuthapani, S., and Baseman, J.B. 2006. Transcriptional heat shock response in the smallest known self-replicating cell, Mycoplasma genitalium. J. Bacteriol. 188(8): 2845-2855. doi:10.1128/JB.188.8. 2845-2855.2006. PMID:16585746.
47. Narberhaus, F. 1999. Negative regulation of bacterial heat shock genes. Mol. Microbiol. 31(1): 1-8. doi:10.1046/j.1365-2958. 1999.01166.x. PMID:9987104.
48. Noivirt-Brik, O., Unger, R., and Horovitz, A. 2007. Low folding propensity and high translation efficiency distinguish in vivo substrates of GroEL from other Escherichia coli proteins. Bioinformatics, 23(24): 3276-3279. doi:10.1093/bioinformatics/btm513. PMID:18006553.
49. O'Keefe, F.R., and Wagner, P.J. 2001. Inferring and testing hypotheses of cladistic character dependence by using character compatibility. Syst. Biol. 50(5): 657-675. doi:10.1080/106351501753328794. PMID:12116937.
50. Pellegrini, M., Marcotte, E.M., Thompson, M.J., Eisenberg, D., and Yeates, T.O. 1999. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc. Natl. Acad. Sci. U.S.A. 96(8): 4285-4288. doi:10.1073/pnas.96.8.4285. PMID:10200254.
51. Petersen, A.M., Blom, J., Andersen, L.P., and Krogfelt, K.A. 2000. Role of strain type, AGS cells and fetal calf serum in Helicobacter pylori adhesion and invasion assays. FEMS Immunol. Med. Microbiol. 29(1): 59-67. doi:10.1111/j.1574-695X.2000.tb01506.x. PMID:10967262.
52. Prilusky, J., Felder, C.E., Zeev-Ben-Mordehai, T., Rydberg, E.H., Man, O., Beckmann, J.S., et al. 2005. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics, 21(16): 3435-3438. doi:10.1093/bioinformatics/bti537. PMID:15955783.
53. Ranford, J.C., Coates, A.R., and Henderson, B. 2000. Chaperonins are cell-signalling proteins: the unfolding biology of molecular chaperones. Expert Rev. Mol. Med. 2(8): 1-17. doi:10.1017/S1462399400002015. PMID:14585136.
54. Razin, S., Yogev, D., and Naot, Y. 1998. Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62(4): 1094-1156. PMID:9841667.
55. Reading, D.S., Hallberg, R.L., and Myers, A.M. 1989. Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor.. Nature, 337: 655-661.
56. Reischl, S., Wiegert, T., and Schumann, W. 2002. Isolation and analysis of mutant alleles of the Bacillus subtilis HrcA repressor with reduced dependency on GroE function. J. Biol. Chem. 277(36): 32659-32667. doi:10.1074/jbc.M201372200. PMID:12082092.
57. Reynolds, D.J., and Pearce, J.H. 1991. Endocytic mechanisms utilized by chlamydiae and their influence on induction of productive infection. Infect. Immun. 59(9): 3033-3039. PMID:1879929.
58. Rodríguez-Quiñones, F., Maguire, M., Wallington, E.J., Gould, P.S., Yerko, V., Downie, J.A., and Lund, P.A. 2005. Two of the three groEL homologues in Rhizobium leguminosarum are dispensable for normal growth. Arch. Microbiol. 183(4): 253-265. doi:10.1007/s00203-005-0768-7. PMID:15830189.
59. Rottem, S., and Naot, Y. 1998. Subversion and exploitation of host cells by mycoplasmas. Trends Microbiol. 6(11): 436-440. doi:10.1016/S0966-842X(98) 01358-4. PMID:9846360.
60. Scherm, B., Gerlach, G.F., and Runge, M. 2002. Analysis of heat shock protein 60 encoding genes of mycoplasmas and investigations concerning their role in immunity and infection. Vet. Microbiol. 89(2-3): 141-150. doi:10.1016/S0378-1135(02)00158-X. PMID:12243891.
61. Segal, E.D., Falkow, S., and Tompkins, L.S. 1996. Helicobacter pylori attachment to gastric cells induces cytoskeletal rearrangements and tyrosine phosphorylation of host cell proteins. Proc. Natl. Acad. Sci. U.S.A. 93(3): 1259-1264. doi:10.1073/pnas.93.3.1259. PMID:8577751.
62. Servant, P., Thompson, C., and Mazodier, P. 1993. Use of new Escherichia coli/Streptomyces conjugative vectors to probe the functions of the two groEL-like genes of Streptomyces albus G by gene disruption. Gene, 134(1): 25-32. doi:10.1016/0378-1119(93)90170-8. PMID:7902308.
63. Seto, S., and Miyata, M. 1998. Cell reproduction and morphological changes in Mycoplasma capricolum. J. Bacteriol. 180(2): 256-264. PMID:9440514.
64. Sheppard, M., Webb, C., Heath, F., Mallows, V., Emilianus, R., Maskell, D., and Mastroeni, P. 2003. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell. Microbiol. 5(9): 593-600. doi:10.1046/j.1462-5822. 2003.00296.x. PMID:12925129.
65. Sirand-Pugnet, P., Lartigue, C., Marenda, M., Jacob, D., Barré, A., Barbe, V., et al. 2007. Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet. 3(5): e75. doi:10.1371/journal.pgen.0030075. PMID:17511520.
66. Søndergård-Andersen, J., Jensen, J.S., Uldum, S.A., and Lind, K. 1990. Heat-shock protein in Mycoplasma pneumoniae shown by immunoblotting to be related to the bacterial common antigen. J. Infect. Dis. 161(5): 1039-1040. PMID:2109019.
67. Su, C.J., Chavoya, A., and Baseman, J.B. 1989. Spontaneous mutation results in loss of the cytadhesin (P1) of Mycoplasma pneumoniae. Infect. Immun. 57(10): 3237-3239. PMID:2506134.
68. Su, H.C., Hutchison, C.A., 3rd, and Giddings, M.C. 2007. Mapping phosphoproteins in Mycoplasma genitalium and Mycoplasma pneumoniae. BMC Microbiol. 7(1): 63. doi:10.1186/1471-2180-7-63. PMID:17605819.
69. Taguchi, H., Makino, Y., and Yoshida, M. 1994. Monomeric chaperonin-60 and its 50-kDa fragment possess the ability to interact with non-native proteins, to suppress aggregation, and to promote protein folding. J. Biol. Chem. 269(11): 8529-8534. PMID:7907593.
70. Tarshis, M., Yavlovich, A., Katzenell, A., Ginsburg, I., and Rottem, S. 2004. Intracellular location and survival of Mycoplasma penetrans within HeLa cells. Curr. Microbiol. 49(2): 136-140. doi:10.1007/s00284-004-4298-3. PMID:15297920.
71. Taylor-Robinson, D., Davies, H.A., Sarathchandra, P., and Furr, P.M. 1991. Intracellular location of mycoplasmas in cultured cells demonstrated by immunocytochemistry and electron microscopy. Int. J. Exp. Pathol. 72(6): 705-714. PMID:1768615.
72. Terebiznik, M.R., Vazquez, C.L., Torbicki, K., Banks, D., Wang, T., Hong, W., et al. 2006. Helicobacter pylori VacA toxin promotes bacterial intracellular survival in gastric epithelial cells. Infect. Immun. 74(12): 6599-6614. doi:10.1128/IAI.01085-06. PMID:17000720.
73. Theodoropoulos, C., Wong, T.H., O'Brien, M., and Stenzel, D. 2001. Plesiomonas shigelloides enters polarized human intestinal Caco-2 cells in an in vitro model system. Infect. Immun. 69(4): 2260-2269. doi:10.1128/IAI.69.4.2260- 2269.2001. PMID:11254582.
74. van Eden, W., Koets, A., van Kooten, P., Prakken, B., and van der Zee, R. 2003. Immunopotentiating heat shock proteins: negotiators between innate danger and control of autoimmunity. Vaccine, 21(9-10): 897-901. doi:10.1016/S0264- 410X(02)00538-8. PMID:12547600.
75. van Eden, W., van der Zee, R., and Prakken, B. 2005. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat. Rev. Immunol. 5(4): 318-330. doi:10.1038/nri1593. PMID:15803151.
76. Vasconcelos, A.T., Ferreira, H.B., Bizarro, C.V., Bonatto, S.L., Carvalho, M.O., Pinto, P.M., et al. 2005. Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J. Bacteriol. 187(16): 5568-5577. doi:10.1128/JB.187.16.5568-5577.2005. PMID:16077101.
77. Vogl, G., Plaickner, A., Szathmary, S., Stipkovits, L., Rosengarten, R., and Szostak, M.P. 2008. Mycoplasma gallisepticum invades chicken erythrocytes during infection. Infect. Immun. 76(1): 71-77. doi:10.1128/IAI.00871-07. PMID:17954728.
78. Waites, K.B., Balish, M.F., and Atkinson, T.P. 2008. New insights into the pathogenesis and detection of Mycoplasma pneumoniae infections. Future Microbiol. 3(6): 635-648. doi:10.2217/17460913.3.6.635. PMID:19072181.
79. Wilson, A.C., Wu, C.C., Yates, J.R., 3rd, and Tan, M. 2005. Chlamydial GroEL autoregulates its own expression through direct interactions with the HrcA repressor protein. J. Bacteriol. 187(21): 7535-7542. doi:10.1128/JB.187.21. 7535-7542.2005. PMID:16237037.
80. Winner, F., Rosengarten, R., and Citti, C. 2000. In vitro cell invasion of Mycoplasma gallisepticum. Infect. Immun. 68(7): 4238-4244. doi:10.1128/IAI.68.7.4238-4244.2000. PMID:10858241.
81. Wong, P., and Houry, W.A. 2004. Chaperone networks in bacteria: analysis of protein homeostasis in minimal cells. J. Struct. Biol. 146(1-2): 79-89. doi:10.1016/j.jsb.2003.11.006. PMID:15037239.
82. Wuppermann, F.N., Mölleken, K., Julien, M., Jantos, C.A., and Hegemann, J.H. 2008. Chlamydia pneumoniae GroEL1 protein is cell surface associated and required for infection of HEp-2 cells. J. Bacteriol. 190(10): 3757-3767. doi:10.1128/JB.01638-07. PMID:18310329.
83. Yamaguchi, H., Osaki, T., Kurihara, N., Taguchi, H., Hanawa, T., Yamamoto, T., and Kamiya, S. 1997. Heat-shock protein 60 homologue of Helicobacter pylori is associated with adhesion of H. pylori to human gastric epithelial cells. J. Med. Microbiol. 46(10): 825-831. doi:10.1099/00222615-46- 10-825. PMID:9364138.
84. Yavlovich, A., and Rottem, S. 2007. Binding of host extracellular matrix proteins to Mycoplasma fermentans and its effect on adherence to, and invasion of HeLa cells. FEMS Microbiol. Lett. 266(2): 158-162. doi:10.1111/j.1574-6968. 2006.00534.x. PMID:17233726.
85. Yavlovich, A., Tarshis, M., and Rottem, S. 2004. Internalization and intracellular survival of Mycoplasma pneumoniae by non-phagocytic cells. FEMS Microbiol. Lett. 233(2): 241-246. doi:10.1111/j.1574-6968.2004.tb09488.x. PMID:15063492.