The role of serine proteases in the pathogenesis of bacterial infections

COMMENTARY ON THE LAW

The role of serine proteases in the pathogenesis of bacterial infections

Ewa Burchacka 1 , Danuta Witkowska 2

1. Politechnika Wrocławska, Wydział Chemiczny, Zakład Chemii Medycznej i Mikrobiologii, Wrocław
2. Instytut Immunologii i Terapii Doświadczalnej PAN im. L. Hirszfelda we Wrocławiu

Published: 2016-06-30
DOI: 10.5604/17322693.1208011
GICID: 01.3001.0009.6847
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2016; 70 : 678-694

 

Abstract

An increasing resistance of pathogenic bacterial species has been considered as one of the major health problems worldwide. The discovery of novel protein targets and development of effective anti-bacterial therapeutics is of high need since for some extremely resistant pathogens we are simply left unarmed. One of new promising therapeutic strategy is the application of specific inhibitors targeting bacterial serine proteases. Pathogenic microorganisms secrete abroad range of hydrolases, including serine proteases which lead to activation of various virulence factors. Herein, we review the specific bacteria serine proteases which have an influence on pathogenicity of bacterial infection as well as we introduce the reader with a brief history of the subject.

References

  • 1. Akopian T., Kandror O., Raju R.M., Unnikrishnan M., Rubin E.J.,Goldberg A.L.: The active ClpP protease from M. tuberculosis is a complexcomposed of a heptameric ClpP1 and a ClpP2 ring. EMBO J.,2012; 31: 1529-1541
    Google Scholar
  • 2. Al-Hasani K., Henderson I.R., Sakellaris H., Rajakumar K., GrantT., Nataro J.P., Robins-Browne R., Adler B.: The sigA gene which isborne on the she pathogenicity island of Shigella flexneri 2a encodesan exported cytopathic protease involved in intestinal fluid accumulation.Infect. Immun., 2000; 68: 2457-2463
    Google Scholar
  • 3. Allsop A.E., Brooks G., Bruton G., Coulton S., Edwards P.D., HattonI.K., Kaura A.C., Mc Lean S.D., Pearson N.D., Smar T.C., Southgate R.:Penem inhibitors of bacterial signal peptidase. Bioorg. Med. Chem.Lett., 1995; 5: 443-448
    Google Scholar
  • 4. Barrett A.J., Rawlings N.D.: Families and clans of serine peptidases.Arch. Biochem. Biophys., 1995; 318: 247-250
    Google Scholar
  • 5. Benjelloun-Touimi Z., Si Tahar M., Montecucco C., Sansonetti P.J.,Parsot C.: SepA, the 110 kDa protein secreted by Shigella flexneri: two-domainstructure and proteolytic activity. Microbiol., 1998; 144: 1815-1822
    Google Scholar
  • 6. Bolhuis A., Venema G., Quax W.J., Bron S., van Dijl J. M.: Functionalanalysis of paralogous thiol-disulfide oxidoreductases in Bacillussubtilis. J. Biol. Chem., 1999; 274: 24531-24538
    Google Scholar
  • 7. Brannon J.R., Burk D.L., Leclerc J.M., Thomassin J.L., Portt A.,Berghuis A.M., Gruenheid S., Le Moual H.: Inhibition of outer membraneproteases of the omptin family by aprotinin. Infect. Immun.,2015; 83: 2300-2311
    Google Scholar
  • 8. Burchacka E., Sieńczyk M., Frick I.M., Wysocka M., Lesner A.,Oleksyszyn J.: Substrate profiling of Finegoldia magna SufA protease,inhibitor screening and application to prevent human fibrinogen degradationand bacteria growth in vitro. Biochimie, 2014; 103: 137-143
    Google Scholar
  • 9. Burns D.L.: Biochemistry of type IV secretion. Curr. Opin. Microbiol.,1999; 2: 25-29
    Google Scholar
  • 10. Buzder-Lantos P., Bocksteal K., Anné J., Herdewijn P.: Substratebased peptide aldehyde inhibits bacterial type I signal peptidase.Bioorg. Med. Chem. Lett., 2009; 19: 2880-2883
    Google Scholar
  • 11. Carmona C., Gray G.L.: Nucleotide sequence of the serine proteasegene of Staphylococcus aureus, strain V8. Nucleic Acids Res., 1987; 15: 6757
    Google Scholar
  • 12. Casey J., Pichichero M.E.: Changes in frequency and pathogenscausing acute otitis media in 1995-2003. Pediatr. Infect. Dis.J., 2004; 23: 824-828
    Google Scholar
  • 13. Chagnot C., Zorgani M.A., Astruc T., Desvaux M.: Proteinaceousdeterminants of surface colonization in bacteria: bacterial adhesionand biofilm formation from a protein secretion perspective. Front.Microbiol., 2013; 4: 303
    Google Scholar
  • 14. Conelly M.B., Young G.M., Sloma A.: Extracellular proteolyticactivity plays a central role in swarming motility in Bacillus subtilis.J. Bacteriol., 2004; 186: 4159-4167
    Google Scholar
  • 15. Cregg K.M., Wilding I., Black M.T.: Molecular cloning and expressionof the spsB gene encoding an essential type I signal peptidasefrom Staphylococcus aureus. J. Bacteriol., 1996; 178: 5712-5718
    Google Scholar
  • 16. Date T.: Demonstration by a novel genetic technique that leaderpeptidase is an essential enzyme of Escherichia coli. J. Bacteriol.,1983; 154: 76-83
    Google Scholar
  • 17. Date T., Wicker W.: Isolation of the Escherichia coli leader peptidasegene and effects of leader peptidase overproduction in vivo.Proc. Natl. Asad. Sci. USA, 1981; 78: 6106-6110
    Google Scholar
  • 18. Dave J.A., Gey van Pittius N.C., Beyers A.D., Ehlers M.R., BrownG.D.: Mycosin-1, a subtilisin-like serine protease of Mycobacteriumtuberculosis, is cell wall-associated and expressed during infectionof macrophages. BMC Microbiol., 2002; 2: 30
    Google Scholar
  • 19. Derrick S.C., Morris S.L.: The ESAT6 protein of Mycobacteriumtuberculosis induces apoptosis of macrophages by activating caspaseexpression. Cell Microbiol., 2007; 9: 1547-1555
    Google Scholar
  • 20. Desvaux M., Hébraud M., Talon R., Henderson I.R.: Secretion andsubcellular localizations of bacterial proteins: a semantic awarenessissue. Trends Microbiol., 2009; 17: 139-145
    Google Scholar
  • 21. Dubin G., Stec-Niemczyk J., Kisielewska M., Pustelny K., PopowiczG.M., Bista M., Kantyka T., Boulware K.T., Stennicke H.R., CzarnaA., Phopaisarn M., Doughtery P.S., Thogersen I.B., Enghlid J.J., ThornberryN. i wsp.: Enzymatic activity of the Staphylococcus aureus SpIBserine protease is induced by substrates containing the sequenceTrp-Glu-Leu-Gln. J. Mol. Biol., 2008; 379: 343-356
    Google Scholar
  • 22. Eslava C., Navarro-Garcia F., Czeczulin J.R., Henderson I.R., CravitoA., Nataro J.P.: Pet, an autotransporter enterotoxin from enteroaggregativeEscherichia coli. Infect Immun., 1998; 66: 3155-3163
    Google Scholar
  • 23. European Commission. Communication From The CommissionOn A Community Strategy Against Antimicrobial Resistance, Brussels,2001, 1, COM 333
    Google Scholar
  • 24. Feng X., Akiyoshi D.E., Widmer G., Tzipori S.: Characterizationof subtilas protease in Cryptosporidium parvum and C. hominis. J. Parasitol.,2007; 93: 619-626
    Google Scholar
  • 25. Fernandes R.M., Carbonare S.B., Carneiro-Sampaio M.N., TrabulsiL.R.: Inhibition of enteroaggregative Escherichia coli adhesion toHep-2 cells by secretory immunoglobulin A from human colostrum.Pediatr. Infect. Dis. J., 2001; 20: 672-678
    Google Scholar
  • 26. Fink D.L., Cope L.D., Hansen E.J., Geme J.W.3rd: The Hemophilusinfluenzae Hap autotransporter is a chymotrypsin clan serine proteaseand undergoes autoproteolysis via an intermolecular mechanism.J. Biol. Chem., 2001; 276: 39492-39500
    Google Scholar
  • 27. Girard M.P., Steele D., Chaignat C.L., Kieny M.P.: A review of vaccineresearch and development: human enteric infections. Vaccine,2006; 24: 2732-2750
    Google Scholar
  • 28. Gonzalez C.T., Maheswaran S.K., Murtaugh M.P.: Pasteurella haemolyticaserotype 2 contains the gene for a noncapsular serotype1-specific antigen. Infect. Immun., 1995; 63: 1340-1348
    Google Scholar
  • 29. Goodyear C.S., Silverman G.J.: Death by a B cell superantigen invivo VH-targeted apoptotic supraclonal B cell deletion by a Staphylococcaltoxin. J. Exp. Med., 2003; 197: 1125-1139
    Google Scholar
  • 30. Guyer D.M., Henderson I.R., Nataro J.P., Mobley H.L.: Identificationof sat, an autotransporter toxin produced by uropathogenicEscherichia coli. Mol. Microbiol., 2000; 38: 53-66
    Google Scholar
  • 31. Guyer D.M., Radulovic S., Jones F.E., Mobley H.L.: Sat, the secretedautotransporter toxin of uropathogenic Escherichia coli, is a vacuolatingcytotoxin for bladder and kidney epithelial cells. Infect.Immun., 2002; 70: 4539-4546
    Google Scholar
  • 32. Hauck C.R., Meyer T.F.: The lysosomal/phagosomal membraneprotein h-lamp-1 is a target of the IgA1 protease of Neisseria gonorrhoeae.FEBS Lett., 1997; 405: 86-90
    Google Scholar
  • 33. Hauske P., Meltzer M., Ottman C., Krojer T., Clausen T., EhrmannM., Kaiser M.: Selectivity profiling of DegP substrates and inhibitors.Bioorg. Med. Chem., 2009; 17: 2920-2924
    Google Scholar
  • 34. Henderson I.R., Czeczulin J., Eslava C., Noriega F., Nataro J.P.:Characterization of pic, a secreted protease of Shigella flexneriand enteroaggregative Escherichia coli. Infect. Immun., 1999; 67:5587-5596
    Google Scholar
  • 35. Henderson I.R., Hicks S., Navarro-Garcia F., Elias W.P., PhilipsA.D., Nataro J.P.: Involvement of the enteroaggregative Escherichiacoli plasmid-encoded toxin in causing human intestinal damage.Infect. Immun., 1999; 67: 5338-5344
    Google Scholar
  • 36. Henderson I.R., Nataro J.P.: Virulence functions of autotransporterproteins. Infect. Immun., 2001; 69: 1231-1243
    Google Scholar
  • 37. Henderson I.R., Navarro-Garcia F., Nataro J.P.: The great escape:structure and function of the autotransporter proteins. TrendsMicrobiol., 1998; 6: 370-378
    Google Scholar
  • 38. Hendrixson D.R., de la Morena M.L., Stathopoulos C., St. GemeIII J.W.: Structural determinants of processing and secretion of theHaemophilus influenzae hap protein. Mol. Microbiol., 1997; 26: 505-518
    Google Scholar
  • 39. Hendrixson D.R., St. Geme III J.W.: The Haemophilus influenzae Hapserine protease promotes adherence and microcolony formation,potentiated by a soluble host protein. Mol. Cell., 1998; 2: 841-850
    Google Scholar
  • 40. Hirasava Y., Takai T., Nakamura T., Mitsuishi K., Gunavan H.,Suto H., Ogawa T., Wang X.L., Ikeda S., Okumura K., Ogawa H.: Staphylococcusaureus extracellular protease causes epidermal barrierdysfunction. J. Invest. Dermatol., 2010; 130: 614-617
    Google Scholar
  • 41. Hoy B., Löwer M., Weyding C., Carra G., Tegtmeyer N., Geppert T.,Schröder P., Sewald N., Backert S., Schneider G., Wessler S.: Helicobacterpylori HtrA is a new secreted virulence factor that cleaves E-cadherin todisrupt intercellular adhesion. EMBO Rep., 2010; 11: 798-804
    Google Scholar
  • 42. Imamura T., Pike R.N., Potempa J., Travis J.: Pathogenesis of periodontitis:a major arginine-specific cysteine proteinase from Porphyromonasgingivalis induces vascular permeability enhancementthrough activation of the kallikrein/kinin pathway. J. Clin. Invest.,1994; 94: 361-367
    Google Scholar
  • 43. Jacobson M., Sali A.: Comparative protein structure modeling and itsapplication to drug discovery. Annu. Rep. Med. Chem., 2004; 39: 259-276
    Google Scholar
  • 44. Jarząb A., Górska-Frączek S., Rybka J., Witkowska D.: Zakażenia pa-łeczkami jelitowymi – diagnostyka, oporność na antybiotyki i profilaktyka.Postępy Hig. Med. Dośw., 2011; 65: 55-72
    Google Scholar
  • 45. Jennison A.V., Verma N.K.: Shigella flexneri infection: pathogenesisand vaccine development. FEMS Microbiol. Rev., 2004; 28: 43-58
    Google Scholar
  • 46. Karlsson C., Andersson M.L., Collin M., Schmidtchen A., BjörckL., Frick I.M.: SufA-a novel subtilisin-like serine proteinase of Finegoldiamagna. Microbiology, 2007; 153: 4208-4218
    Google Scholar
  • 47. Kawai E., Idei A., Kumura H., Shimazaki K., Akatsuka H., OmoriK.: The ABC-exporter genes involved in the lipase secretion areclustered with the genes for lipase, alkaline protease, and serineprotease homologues in Pseudomonas fluorescens no. 33. Biochim.Biophys Acta, 1999; 1446: 377-382
    Google Scholar
  • 48. Kennan R.M., Dhungyel O.P., Whittington R.J., Egerton J.R., RoodJ.I.: The type IV fimbrial subunit gene (fimA) of Dichelobacter nodosusis essential for virulence, protease secretion, and natural competence.J. Bacteriol., 2001; 183: 4451-4458
    Google Scholar
  • 49. Kim D.Y., Kim K.K.: Structure and function of HtrA family proteins,the key players in protein quality control. J. Biochem. Mol. Biol., 2005;38: 266-274
    Google Scholar
  • 50. Klenotic P.A., Carlos J.L., Samuelson J.C., Schuenemann T.A.,Tschantz W.R., Paetzel M., Strynadka N.C., Dalbey R.E.: The role ofthe conserved box E residues in the active site of the Escherichia colitype I signal peptidase. J. Biol. Chem., 2000; 275: 6490-6498
    Google Scholar
  • 51. Kostakioti M., Newman C.L., Thanassi D.G., Stathopoulos C.: Mechanismsof protein export across the bacterial outer membrane. J.Bacteriol., 2005; 187: 4306-4314
    Google Scholar
  • 52. Kostakioti M., Stathopoulos C.: Functional analysis of the Tshautotransporter from an avian pathogenic Escherichia coli strain.Infect. Immun., 2004; 72: 5548-5554
    Google Scholar
  • 53. Kramer R.A., Dekker N., Egmond M.R.: Identification of active siteserine and hisitidine residues in Escherichia coli outer membane proteaseOmpT. FEBS Lett., 2000, 468: 220-224
    Google Scholar
  • 54. Kramer R.A., Zandwijken D., Egmond M.R., Dekker N.: In vitro folding,purification and characterization of Escherichia coli outer membraneprotease ompT. Eur. J. Biochem., 2000; 267: 885-893
    Google Scholar
  • 55. Kulanthaivel P., Kreuzamn A.J., Strege M.A., Belvo M.D., Smitka T.A.,Clemens M., Swartling J.R., Minton K.L., Zheng F., Angleton E.L., MullenD, Jungheim L.N., Klimkowski V.J., Nicas T.I., Thompson R.C., Peng S.B.:Novel lipoglycopeptides as inhibitors of bacterial signal peptidase I. J.Biol. Chem., 2004; 279: 36250-36258
    Google Scholar
  • 56. Kuroda M., Ohta T., Uchiyama I., Baba T., Yuzawa H., KobayashiI., Cui L., Oguchi A., Aoki K., Nagai Y., Lian J., Ito T., Kanamori M., MatsumaruH., Maruyama A. i wsp.: Whole genome sequencing of meticillin-resistantStaphylococcus aureus. Lancet., 2001; 357: 1225-1240
    Google Scholar
  • 57. Lilley G.G., Rifkin M.C., Stewart D.J., Kortt A.A.: Nucleotide and deducedprotein sequence of the extracellular, serine basic protease gene(bprB) from Dichelobacter nodosus strain 305: comparison with the basicprotease gene (bprV) from virulent strain 198. Biochem. Mol. Biol. Int.,1995; 36: 101-111
    Google Scholar
  • 58. Lindsay J.A., Holden M.T.: Staphylococcus aureus: superbug, supergenome? Trends Microbiol., 2004; 12: 378-385
    Google Scholar
  • 59. Lorenzen D.R., Düx F., Wölk U., Tsirpouchtsidis A., Haas G., MeyerT.F.: Immunoglobulin A1 protease, an exoenzyme of pathogenicNeisseriae, is a potent inducer of proinflammatory cytokines. J. Exp.Med., 1999; 190: 1049-1058
    Google Scholar
  • 60. Löwer M., Weydig C., Metzler D., Reuter A., Starzinski-Powitz A., WesslerS., Schneider G.: Prediction of extracellular proteases of the humanpathogen Helicobacter pylori reveals proteolytic activity of the Hp1018/19protein HtrA. PLoS One, 2008; 3: 3510
    Google Scholar
  • 61. Luo Y., Pfuetzner R.A., Mosimann S., Paetzel M., Frey E.A., CherneyM., Kim B., Little J.W., Strynadka N.C.: Crystal structure of LexA:a conformational switch for regulation of self-cleavage. Cell, 2001;106: 585-594
    Google Scholar
  • 62. Maeda H., Yamamoto T.: Pathogenic mechanisms induced by microbialproteases in microbial infections. Biol Chem Hoppe Seyler.,1996; 377: 217-226
    Google Scholar
  • 63. Mellies J.L., Navarro-Garcia F., Okeke I., Frederickson J., NataroJ.P., Kaper J.B.: espC pathogenicity island of enteropathogenic Escherichiacoli encodes an enterotoxin. Infect. Immun., 2001; 69: 315-324
    Google Scholar
  • 64. Mertz D., Frei R., Periat N., Zimmerli M., Battegay M., FlückigerU., Widmer A.F.: Exclusive Staphylococcus aureus throat carriage: at–risk populations. Arch. Intern. Med., 2009; 169: 172-178
    Google Scholar
  • 65. Michaelis S., Beckwith J.: Mechanism of incorporation of cellenvelope proteins in Escherichia coli. Annu. Rev. Microbiol., 1982;36: 435-465
    Google Scholar
  • 66. Milstein C., Brownlee G.G., Harrison T.M., Mathews M.B.: A possibleprecursor of immunoglobulin light chains. Nat. New Biol.,1972; 239: 117-120
    Google Scholar
  • 67. Molla A., Yamamoto T., Akaike T., Miyoshi S., Maeda H.: Activationof Hageman factor and prekallikrein and generation of kininby various microbial proteinases. J. Biol. Chem., 1989; 264: 10589-10594
    Google Scholar
  • 68. Natale P., Brüser T., Driessen A.J.: Sec- and Tat-mediated proteinsecretion across the bacterial cytoplasmic membrane – distincttranslocases and mechanisms. Biochim. Biophys. Acta, 2008; 1778:1735-1756
    Google Scholar
  • 69. Nataro J.P., Deng D.R., Meneval A.L., German A.L., Martin W.C.,Levine M.M.: Aggregative adherence fimbriae I of enteroaggregativeEscherichia coli mediate adherence to HEp-2 cells and hemagglutinationof human erythrocytes. Infect. Immun., 1992; 60: 2297-2304
    Google Scholar
  • 70. Navarro-Garcia F., Eslava C., Villaseca J.M., Lopez-Revilla R., CzeczulinJ.R., Srinivas S., Nataro J.P., Cravioto A.: In vitro effects of a high-molecular-weightheat-labile enterotoxin from enteroaggregative Escherichiacoli. Infect. Immun., 1998; 66: 3149-3154
    Google Scholar
  • 71. Nielsen H., Engelbrecht J., Brunak S., von Hejne G.: Identification ofprokaryotic and eukaryotic signal peptides and prediction of their cleavagesites. Protein Eng., 1997; 10: 1-6
    Google Scholar
  • 72. Ohnishi Y., Beppu T., Horinouchi S.: Two genes encoding serine proteasehomologues in Serratia marcescens and characterization of theirproducts in Escherichia coli. J. Biochem., 1997; 121: 902-913
    Google Scholar
  • 73. Otto B.R., Sijbrandi R., Luirink J., Oudega B., Heddle J.G., Mizutani K.,Park S.Y., Tame J.R.: Crystal structure of hemoglobin protease, a hemebinding autotransporter protein from pathogenic Escherichia coli. J. Biol.Chem., 2005; 280: 17339-17345
    Google Scholar
  • 74. Otto M.: Staphylococcus epidermidis – the “accidental” pathogen.Nat. Rev. Microbiol., 2009; 7: 555-567
    Google Scholar
  • 75. Paetzel M., Dalbey R.E., Strynadka N.C.: Crystal structure ofa bacterial signal peptidase in complex with a beta-lactam inhibitor.Nature, 1998; 396: 186-190
    Google Scholar
  • 76. Paetzel M., Karla A., Strynadka N.C., Dalbey R.E.: Signal peptidases.Chem. Rev., 2002; 102: 4549-4580
    Google Scholar
  • 77. Parham N.J., Pollard S.J., Desvaux M., Scott-Tucker A., Liu C., FivianA., Henderson I.R.: Distribution of the serine protease autotransportersof the Enterobacteriaceae among extraintestinal clinical isolates of Escherichiacoli. J. Clin. Microbiol., 2005; 43: 4076-4082
    Google Scholar
  • 78. Park R.Y., Sun H.Y., Choi M.H., Bai Y.H., Chung Y.Y., Shin S.H.:Proteases of a Bacillus subtilis clinical isolate facilitate swarming andsiderophore-mediated iron uptake via proteolytic cleavage of transferrin.Biol. Pharm. Bull., 2006; 29: 850-853
    Google Scholar
  • 79. Parreira V.R., Gyles C.L.: A novel pathogenicity island integratedadjacent to the thrW tRNA gene of avian pathogenic Escherichiacoli encodes a vacuolating autotransporter toxin. Infect. Immun.,2003; 71: 5087-5096
    Google Scholar
  • 80. Parro V., Schacht S., Anné J., Mellado R.P.: Four genes encodingdifferent type I signal peptidases are organized in a cluster in Streptomyceslividans TK21. Microbiology, 1999; 145: 2255-2263
    Google Scholar
  • 81. Paton A.W., Beddoe T., Thorpe C.M., Whisstock J.C., Wilce M.C.,Rossjohn J., Talbot U.M., Paton J.C.: AB5 subtilase cytotoxin inactivatesthe endoplasmic reticulum chaperone BiP. Nature, 2006; 443: 548-552
    Google Scholar
  • 82. Peng S.B., Wang L., Moomaw J., Peery R.B., Sun P.M., Johnson R.B.,Lu J., Treadway P., Skatrud P.L., Wang Q.M.: Biochemical characterizationof signal peptidase I from Gram-positive Streptococcus pneumoniae.J. Bacteriol., 2001; 183: 621-627
    Google Scholar
  • 83. Peng X., Sun J.: Mechanism ESAT-6 membrane interaction and its rolesin pathogenesis Mycobacterium tuberculosis. Toxicon., 2016; 116: 29-34
    Google Scholar
  • 84. Pohlner J., Halter R., Beyreuther K., Meyer T.F.: Gene structureand extracellular secretion of Neisseria gonorrhoeae IgA protease.Nature, 1987; 325: 458-462
    Google Scholar
  • 85. Popowicz G.M., Dubin G., Stec-Niemczyk J., Czarny A., DubinA., Potempa J., Holak T.A.: Functional and structural characterizationof Spl proteases from Staphylococcus aureus. J. Mol. Biol., 2006;358: 270-279
    Google Scholar
  • 86. Potempa J., Watorek W., Travis J.: The inactivation of humanplasma α1-proteinase inhibitor by proteinases from Staphylococcusaureus. J. Biol. Chem., 1986; 261: 14330-14334
    Google Scholar
  • 87. Pugsley A.P., Francetic O., Hardie K., Possot O.M., SauvonnetN., Seydel A.: Pullulanase: model protein substrate for the generalsecretory pathway of gram-negative bacteria. Folia. Microbiol.,1997; 42: 184-192
    Google Scholar
  • 88. Raviglione M.C., O‘Brien R.J.: Tuberculosis. W: Harrison‘s Principlesof Internal Medicine, 16th., red.: D.L Kasper, E. Braunwald,A.S. Fauci, S.L. Hauser, D.L. Longo, L. Jameson. McGraw-Hill, NewYork 2005, 953-966
    Google Scholar
  • 89. Reineck K., Renneberg J., Diamant M., Gutschik E., Bendtzen K.:Molecular cloning and expression of a novel Staphylococcus aureusantigen. Biochim. Biophys. Acta, 1997; 1350: 128-132
    Google Scholar
  • 90. Rodríguez-Lainz A., Hird D.W., Walker R.L., Read D.H.: Papillomatousdigital dermatitis in 458 dairies. J. Am. Vet. Med. Assoc.,1996; 209: 1464-1467
    Google Scholar
  • 91. Roy F., Vanterpool E., Fletcher H.M.: HtrA in Porphyromonasgingivalis can regulate growth and gingipain activity under stressfulenvironmental conditions. Microbiology, 2006; 152: 3391-3398
    Google Scholar
  • 92. Ryan M.H., Petrone D., Nemeth J.F., Barnathan E., Björck L., JordanR.E.: Proteolysis of purified IgGs by human and bacterial enzymesin vitro and the detection of specific proteolytic fragmentsof endogenous IgG in rheumatoid synovial fluid. Mol. Immunol.,2008; 45: 1837-1846
    Google Scholar
  • 93. Schimana J., Gebhardt K., Höltzel A., Schmid D.G., Süssmuth R., MüllerJ., Pukall R., Fiedler H.P.: Arylomycins A and B, new biaryl-bridgedlipopeptide antibiotics produced by Streptomyces sp. Tü 6075. I. Taxonomy,fermentation, isolation and biological activities. J. Antibiot., 2002;55: 565-570
    Google Scholar
  • 94. Siezen R.J., de Vos W.M., Leunissen J.A., Dijkstra B.W.: Homologymodelling and protein engineering strategy of subtilases, the familyof subtilisin-like serine proteinases. Protein Eng., 1991; 4: 719-737
    Google Scholar
  • 95. Siezen R.J., Leunissen J.A.: Subtilases: the superfamily of subtilisin-likeserine proteases. Protein Sci., 1997; 6: 501-523
    Google Scholar
  • 96. Solomonson M., Huesgen P.F., Wasney G.A., Watanabe N., GruningerR.J., Prehna G., Overall C.M., Strynadka N.C.: Structure of themycosin-1 protease mycobacterial ESX-1 protein typeVII secretionsystem. J. Biol. Chem., 2013; 288: 17782-17790
    Google Scholar
  • 97. Stanley P., Koronakis V., Hughes C.: Acylation of Escherichia coli hemolysin:a unique protein lipidation mechanism underlying toxin function.Microbiol. Mol. Biol. Rev., 1998; 62: 309-333
    Google Scholar
  • 98. Stec-Niemczyk J., Pustelny K., Kisielewska M., Bista M., Boulware K.T.,Stennicke H.R., Thogersen I.B., Daughtery P.S., Enghild J.J., Baczynski K.,Popowicz G.M., Dubin A., Potempa J., Dubin G.: Structural and functionalcharacterization of SplA, an exclusively specific protease of Staphylococcusaureus. Biochem. J., 2009; 419: 555-564
    Google Scholar
  • 99. Steiner T.S., Lima A.A., Nataro J.P., Guerrant R.L.: EnteroaggregativeEscherichia coli produce intestinal inflammation and growth impairmentand cause interleukin-8 release from intestinal epithelial cells. J. Infect.Dis., 1998; 177: 88-96
    Google Scholar
  • 100. Stephens P., Wall I.B., Wilson M.J., Hill K.E., Davies C.E., HillC.M., Harding K.G., Thomas D.W.: Anaerobic cocci populating thedeep tissues of chronic wounds impair cellular wound healing responsesin vitro. Br. J. Dermatol., 2003; 148: 456-466
    Google Scholar
  • 101. Sung M., Dalbey R.E., Identification of potential active-siteresidues in the Escherichia coli leader peptidase. J. Biol. Chem., 1992;267: 13154-13159
    Google Scholar
  • 102. Supuran C.T., Scozzafava A., Clare B.W.: Bacterial protease inhibitors.Med. Res. Rev., 2002; 22: 329-372
    Google Scholar
  • 103. Tanaka M., Hanioka T., Takaya K., Shizukuishi S.: Association of oxygentension in human periodontal pockets with gingival inflammation.J. Periodontol., 1998; 69: 1127-1130
    Google Scholar
  • 104. Tjalsma H., Bolhuis A., Jongbloed J.D., Bron S., van Dijl J.M.:Signal peptide-dependent protein transport in Bacillus subtilis: a genome-basedsurvey of the secretome. Microbiol. Mol. Biol. Rev.,2000; 64: 515-547
    Google Scholar
  • 105. Tjalsma H., van den Dolder J., Meijer W.J., Venema G., Bron S.,van Dijl J.M.: The plasmid-encoded signal peptidase SipP can functionallyreplace the major signal peptidases SipS and SipT of Bacillussubtilis. J. Bacteriol., 1999; 181: 2448-2454
    Google Scholar
  • 106. Travis J., Potempa J.: Bacterial proteinases as targets for thedevelopment of second-generation antibiotics. Biochim. Biophys.Acta, 2000; 1477: 35-50
    Google Scholar
  • 107. Travis J., Potempa J., Maeda H.: Are bacterial proteinases pathogenicfactors? Trends Microbiol., 1995; 3: 405-407
    Google Scholar
  • 108. Travis J., Shieh B.H., Potempa J.: The functional role of acutephase plasma proteinase inhibitors. Tokai J. Exp. Clin. Med., 1988;13: 313-320
    Google Scholar
  • 109. Tuteja R.: Type I signal peptidase: an overview. Arch. Biochem Biophys.,2005; 441: 107-111
    Google Scholar
  • 110. van Klompenburg W., Paetzel M., de Jong J.M., Dalbey R.E.,Demel R.A., von Heijne G., de Kruijff B.: Phosphatidylethanolaminemediates insertion of the catalytic domain of leader peptidase inmembranes. FEBS Lett., 1998; 431: 75-79
    Google Scholar
  • 111. Vandeputte-Rutten L., Kramer R.A., Kroon J., Dekker N., EgmondM.R., Gros P.: Crystal structure of the outer membrane proteaseOmpT from Escherichia coli suggests a novel catalytic site.EMBO J., 2001; 20: 5033-5039
    Google Scholar
  • 112. Vinothkumar K.R., Pierrat O.A., Large J.M., Freeman M.: Structureof rhomboid protease in complex with β-lactam inhibitors defines theS2′ cavity. Structure, 2013; 21: 1051-1058
    Google Scholar
  • 113. von Heijne G.: Patterns of amino acids near signal-sequencecleavage sites. Eur. J. Biochem., 1983; 133: 17-21
    Google Scholar
  • 114. Vrba A., Kwiatkowska S.: Mycobacterium tuberculosis jako przykładpatogenu wewnątrzkomórkowego. Wzajemne relacje międzymikro- i makroorganizmem. Pol. Merk Lek., 2009; 27: 508-513
    Google Scholar
  • 115. Wang H., Paton J.C., Paton A.W.: Pathologic changes in miceinduced by subtilase cytotoxin, a potent new Escherichia coli AB5toxin that targets the endoplasmic reticulum. J. Infect. Dis., 2007;196: 1093-1101
    Google Scholar
  • 116. Westers H. Westers L., Darmon E., van Dijl J.M., Quax W.J., ZanenG.: The CssRS two-component regulatory system controls a generalsecretion stress response in Bacillus subtilis. FEBS J., 2006; 273:3816-3827
    Google Scholar
  • 117. Wolfe P.B., Wickner W., Goodman J.M.: Sequence of the leaderpeptidase gene of Escherichia coli and the orientation of leader peptidasein the bacterial envelope. J. Biol. Chem., 1983; 258: 12073-12080
    Google Scholar
  • 118. Yu A.Y., Houry W.A.: ClpP: a distinctive family of cilindricalenergy-dependet serine proteasess. FEBS Lett., 2007; 581: 3749-3757
    Google Scholar
  • 119. Yuan L., Rodrigues P., Bélanger M., Dunn W.A. Jr, Progulske-FoxA.:Porphyromonas gingivalis htrA is involved in cellular invasion and invivo survival. Microbiology, 2008; 154: 1161-1169
    Google Scholar
  • 120. Zhang Y.B., Greenberg B., Lacks S.A.: Analysis of a Streptococcuspneumoniae gene encoding signal peptidase I and overproduction ofthe enzyme. Gene, 1997; 194: 249-255
    Google Scholar
  • 121. Zwizinski C., Wickner W.: Purification and characterization ofleader (signal) peptidase from Escherichia coli. J. Biol. Chem., 1980;255: 7973-7977
    Google Scholar

Full text

Skip to content