Bacterial invasion of eukaryotic cells can be mediated by actin-hydrolysing metalloproteases grimelysin and protealysin

Cell Biology International

Volumn 35, Issue 2, 2011, Pages 111-118

  Bozhokina, Ekaterina S ^a   Tsaplina, Olga A ^a   Efremova, Tatiana N ^a   Kever, Ludmila V ^a   Demidyuk, Ilya V ^b   Kostrov, Sergey V ^b   Adam, Thomas ^c   Komissarchik, Yan Yu ^a   Khaitlina, Sofia Yu ^a  

^a INSTITUTE OF CYTOLOGY   (Russian Federation)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Actin proteolysis; Bacterial invasion; ECP32; Serratia grimesii; Serratia proteamaculans

Indexed keywords

GRIMELYSIN; METALLOPROTEINASE; PROTEALYSIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CELL INVASION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EUKARYOTIC CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HYDROLYSIS; INTERNALIZATION; LARYNX CARCINOMA; NONHUMAN; PHENOTYPE; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SERRATIA; SERRATIA GRIMESII; SERRATIA PROTEAMACULANS; SPECIES INVASION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; SERRATIA GRIMESII; SERRATIA PROTEAMACULANS;

EID: 78650203309     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1042/CBI20100314     Document Type: Article

References (38)

1. Bollet C, Grimont P, Gainnier M, Geissler A, Sainty JM, De Micco P. Fatal pneumonia due to Serratia proteamaculans subsp. quinovora. J Clin Microbiol 1993;31:444-5.
2. Bozhokina ES, Khaitlina SY, Adam T. Grimelysin, a novel metalloprotease from Serratia grimesii, is similar to ECP32. Biochem Biophys Res Commun 2008;367:888-92.
3. Cossart P, Sansonetti, PJ. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 2004;304:242-8.
4. Demidyuk IV, Gasanov EV, Safina DR, Kostrov SV. Structural organization of precursors of thermolysin-like proteinases. Protein J 2008;27:343-54.
5. Demidyuk IV, Kalashnikov AE, Gromova TY, Gasanov EV, Safina DR, Zabolotskaya MV et al. Cloning, sequencing, expression, and characterization of protealysin, a novel neutral proteinase from Serratia proteamaculans representing a new group of thermolysinlike proteases with short N-terminal region of precursor. Protein Expr Purif 2006;7:551-61.
6. Demidyuk IV, Gromova TY, Polyakov KM, Melik-Adamyan WR, Kuranova IP, Kostrov SV. Crystal structure of protealysin precursor: insights into propeptide function. J Biol Chem 2010;285:2003-13.
7. Eagle RA, Jafferji I, Barrow AD. Beyond stressed self: Evidence for NKG2D ligand expression on healthy cells. Curr Immunol Rev 2009;5:22-34.
8. Efremova TN, Ender NA, Brudnaja MS, Komissarchik YY, Khaitlina SY. Specific Invasion of transformed cells by Escherichia coli A2 strain. Cell Biol Intern 2001;25:557-61.
9. Efremova TN, Gruzdeva IG, Matveyev IV, Bozokina ES, Komissarchik YY, Fedorova ZF et al. Invasive properties of a non-pathogenic Shigella flexneri mutant strain 5a2c produced upon treatment with furazolidon. Bull Exp Biol Med 2004;137:546-50.
10. Ergin A, Bussow K, Sieper J, Thiel A, Duchmann R, Adam T. Homologous high-throughput expression and purification of highly conserved E. coli proteins. Microb Cell Factories 2007;6:18.
11. Filatova NA, Kirpichnikova KM, Gamaley IA. N-acetylcysteine reduces the sensitivity of transformed 3T3-fibroblasts to lysis by natural killer cells. Tsitologia 2006,48:438-41.
12. Filatova NA, Kirpichnikova KM, Gamaley IA. Reorganization of actin cytoskeleton in 3T3 cells and their sensitivity to lysis by natural killer cells. Cell Tissue Biol 2008;2:146-52.
13. Gamaley I, Efremova T, Kirpichnikova K, Kever L, Komissarchik Y, Polozov Y et al. N-Acetylcysteine-induced changes in susceptibility of transformed eukaryotic cells to bacterial invasion. Cell Biol Intern 2006;30:319-25.
14. Goldberg M. Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Revs 2001;65:595-626.
15. Grimont F, Grimont P. The genus Serratia. In M. Dworkin, editor. The prokaryotes. New York: Springer; 2006. p. 219-44.
16. Gromova TY, Demidyuk IV, Kozlovskiy VI, Kuranova IP, Kostrov SV. Processing of protealysin precursor. Biochimie 2009;91:639-45.
17. Hertle R. The family of Serratia type pore forming toxins. Curr Protein Pept Sci 2005;6:313-35.
18. Hertle R, Schwarz H. Serratia marcescens internalization and replication in human bladder epithelial cells. BMC Infect Dis 2004;4:16-30.
19. Khaitlina SY, Strzelecka-Golaszewska H. Role of the DNase-I-binding loop in dynamic properties of actin filament. Biophys J 2002;82:321-34.
20. Khaitlina SY, Strzelecka-Golaszewska H. Effects of tropomyosin on dynamics of actin filaments. Biophys J 2003;84:480a.
21. Khaitlina SY, Collins JH, Kusnetsova IM, Pershina VP, Synakevich IG, Turoverov KK et al. Physico-chemical properties of actin cleaved with bacterial protease from E. coli A2 strain. FEBS Lett 1991;279:49-51.
22. Khaitlina SY, Moraczewska J, Strzelecka-Golaszewska H. The actin-actin interactions involving the N-terminal portion of the DNase I-binding loop are crucial for stabilization of the actin filament. Eur J Biochem 1993;218:911-20.
23. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 1970;227:680-85.
24. Long EO, Rajagopalan S. Stress signals activate natural killer cells. J Exp Med 2002;196:1399-402.
25. Matveyev VV, Usmanova AM, Morozova AB, Khaitlina SY. Purification and characterization of the proteinase ECP-32 from Escherichia coli A2 strain. Biochim Biophys Acta 1996;1296:55-62.
26. Morozova AV, Skovorodkin IN, Khaitlina SY, Malinin AY. Bacterial protease ECP32 and its application for studies on cytoskeleton in vivo. Biochemistry (Moscow) 2001;66:105-13.
27. Okamoto T, Akuta T, Tamura F, van der Vliet A, Akaike T. Molecular mechanism for activation and regulation of matrix metalloproteinases during bacterial infections and respiratory inflammation. Biol Chem 2004;385:997-1006.
28. Rosenshein I, Finley BB. Exploitation of host signal transduction pathways and cytoskeletal functions by invasive bacteria. BioEssays 1993;15:17-24.
29. Sansonetti PJ. Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella, making sense of prokaryote-eukaryote cross-talks. FEMS Microbiol Rev 2001;25:3-14.
30. Schwyter D, Phillips M, Reisler E. Subtilisin-cleaved actin: polymerization and interaction with myosin subfragment 1. Biochemistry 1989;28:5885-95.
31. Spudich JA, Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem 1971;246:4866-71.
32. Stebbins CE, Galán JE. Structural mimicry in bacterial virulence. Nature 2001;412:701-5.
33. Tsaplina OA, Eferemova TN, Kever LV, Komissarchik YY, Demidyuk IV, Kostrov SV et al. Probing for actinase activity of protealysin. Biochemistry (Moscow) (2009);74:648-54.
34. Ursua PR, Unzaga MJ, Melero P, Iturburu I, Ezpeleta C, Cisterna R. Serratia rubidaea as an invasive pathogen. J Clinical Microbiol 1996;1:216-7.
35. Usmanova AM, Khaitlina SY. A specific actin-digesting protease from the bacterial strain E. coli A2. Biochemistry (Moscow) 1989;54: 1074-79.
36. Velge P, Bottreau E, Kaeffer B, Van-Langendonck N. The loss of contact inhibition and anchorage-dependent growth are key steps in the acquisition of Listeria monocytogenes susceptibility phenotype by non-phagocytic cells. Biol Cell 1995;85:55-66.
37. Velge P, Bottreau E, Van-Langendonck N, Kaeffer B. Cell proliferation enhances entry of Listeria monocytogenes into intestinal epithelial cells by two proliferation-dependent entry pathways. J Med Microbiol 1997;46:681-92.
38. Wawro B, Khaitlina SY, Galinska-Rakoczy A, Strzelecka-Golaszewska H. Role of DNase-I-binding loop in myosin subfragment 1-induced actin polymerization. Implications to the polymerization mechanism. Biophys J 2005;88:2883-96.