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Geyvanpittius Mycosins 2002.Pdf (9.113Mb) THE MYCOSINS, A FAMILY OF SECRETED SUBTILISIN-LIKE SERINE PROTEASES ASSOCIATED WITH THE IMMUNOLOGICALLY-IMPORTANT ESAT-6 GENE CLUSTERS OF MYCOBACTERIUM TUBERCULOSIS Nicolaas Claudius Gey van Pittius VI Dissertation presented for the degree of Doctor of Philosophy at the University of Stellenbosch Promoters: Prof. A. D. Beyers and Dr. R. M. W arren Co-promoter: Prof. P. D. van Helden Stellenbosch December 2002 Stellenbosch University http://scholar.sun.ac.za/ Declaration I, the undersigned, hereby declare that the work contained in this dissertation is my own original work, and has not, to my knowledge, previously in its entirety or in part been submitted at any university for a degree. Date Stellenbosch University http://scholar.sun.ac.za/ Summary Pathogenic organisms frequently utilize proteases to perform specific functions related to virulence. There is little information regarding the role of proteolysis in Mycobacterium tuberculosis and no studies on the potential involvement of these enzymes in the pathogenesis of tuberculosis. The present study initially focused on the characterization of a family of membrane anchored, cell wall associated, subtilisin-like serine proteases (mycosins-1 to 5) of Mycobacterium tuberculosis. These proteases were shown to be constitutively expressed in M. tuberculosis, to be located in the cell wall of the organism and to be potentially shed (either actively or passively) from the wall. Relatively high levels of gamma interferon secretion by T-cells in response to these proteases were observed in Mantoux positive individuals. The absence of any detectable protease activity lead to a protein sequence analysis which indicated that the mycosins are probable mycobacterial-specific proprotein processing proteases. To identify possible substrates for these proteases, the genome sequence regions surrounding the mycosin genes were analyzed. This revealed that the mycosin genes are in fact part of a cluster of 6 to 12 genes which have been duplicated multiple times in the genome of M. tuberculosis. Due to the presence of members of the previously described ESAT-6 T-cell antigen family within this duplicated region, the five gene cluster regions were named the ESAT-6 loci. In silico analysis of finished and unfinished genome sequencing data revealed the presence of orthologues of the Mycobacterium tuberculosis H37Rv ESAT-6 loci in the genomes of other mycobacteria, e.g. M. tuberculosis CDC1551, M. tuberculosis 210, M. bovis, M. leprae, M. avium, and the avirulent strain M. smegmatis. Phylogenetic analyses done on the resulting sequences have established the duplication order of the gene clusters and demonstrated that gene cluster region 4 (Rv3444c-3450c) is ancestral. Region 4 is also the only region for which an orthologue could be found in the genomes of Corynebacterium diptheriae and Streptomyces coelicoior. Thus, the comparative genomic analyses revealed that the presence of the ESAT-6 gene cluster seems to be a unique characteristic shared by members of the high G+C gram-positive bacteria and that multiple duplications of this cluster have occurred and have been maintained only within the genomes of members of the genus Mycobacterium. Stellenbosch University http://scholar.sun.ac.za/ The ESAT-6 gene cluster regions were shown to consist of the members of the ESAT-6 gene family (encoding secreted T-cell antigens that lack detectable secretion signals), the mycosins (secreted, cell wall-associated subtilisin-like serine proteases) as well as genes encoding putative ABC transporters, ATP-binding proteins, and other membrane-associated proteins. Thus, from the observation that members of the ESAT-6 family are secreted without the normal sec-dependent secretion signals, it was hypothesized that the membrane-associated and energy-providing proteins function together to form a transport system for the secretion of the members of the ESAT-6 protein family. Supporting this hypothesis, one of the ESAT-6 gene clusters was shown to be expressed as a single polycistronic RNA, forming an operon structure. The promoter for this operon, P e s r e g 3. was also identified and its activity characterized. Subsequent secretion analyses results have shown that secretion of members of the ESAT-6 protein family is dependent on the presence of the proteins encoded by the ESAT-6 gene cluster regions, confirming the putative transport-associated functions of the ESAT-6 gene cluster-encoded proteins. The mycobacterial ESAT-6 gene clusters contain a number of features of quorum sensing and lantibiotic operons, and an extensive review of the literature have led to the hypothesis that the members of the ESAT-6 family may be secreted as signaling molecules and may be involved in the regulation of expression of genes during intracellular residence of the bacterium. In the final part of this study, the evolutionary history of the PE and PPE gene families (members of which is found situated in the ESAT-6 gene clusters) were investigated. This investigation revealed that the expansion of these families are linked to the duplications of the ESAT-6 gene clusters, which is supported by the absence of the multiple copies of the PE and PPE families in the genome of the fast-growing mycobacterium M. smegmatis. Furthermore, dot blot analyses showed that the PPE gene present in ESAT-6 gene cluster region 5 is able to distinguish between mycobacteria belonging to the slow-growing or fast-growing species, indicating a function for the genes of these two families and/or the ESAT-6 gene clusters in the phenotypical differences distinguishing these two groups of mycobacteria. In conclusion, this study has highlighted numerous important aspects of mycobacterial genomics and has greatly contributed to the current body of knowledge concerning the role of proteases, gene duplication and mechanisms of antigen expression and secretion in M. tuberculosis. Stellenbosch University http://scholar.sun.ac.za/ Opsomming Patogeniese organismes gebruik gereeld proteases om spesifieke funksies te verrig wat te doene het met virulensie. Daar is egter baie min inligting beskikbaar aangaande die rol van proteolise in Mycobacterium tuberculosis en geen studies is al gedoen om die invloed van hierdie ensieme in die patogenese van tuberkulose te bestudeer nie. Die huidige studie het oorspronklik gefokus op die karakterisering van 'n familie van membraan-geankerde, selwand-geassosieSrde, subtilisien-agtige serien proteases (mycosins-1 tot 5) van Mycobacterium tuberculosis. Daar is aangetoon dat hierdie proteases deurgans uitgedruk word in M. tuberculosis, dat hulle in die selwand van die organisme geleS is, en dat hulle potensieel afgeskilfer word (of aktief of passief) vanaf die wand. Relatiewe ho6 vlakke van gamma interferon uitskeiding deur T-selle is verkry in respons tot die proteases in Mantoux positiewe persone. Die afwesigheid van enige opspoorbare protease aktiwiteit het gelei tot die analisering van die protein volgordes van hierdie ensieme, wat daarop gedui het dat die mycosins heel moontlik mikobakteri6le-spesifieke proprotein prosesserende proteases is. Die genoom volgorde gebiede random die mycosin gene is geanaliseer om die identiteit van die moontlike substrate van die proteases te identifiseer. Dit het gewys dat die mycosin gene in werklikheid deel vorm van 'n groep van 6 tot 12 gene wat veelvuldiglik in die genoom van M. tuberculosis gedupliseer is. As gevolg van die aanwesigheid van lede van die voorheen beskryfde ESAT-6 T-sel antigeen familie binne hierdie gedupliseerde geen groep, is die vyf geen groep gebiede die ESAT-6 lokusse genoem. In silico analises van voltooide en onvoltooide genoom volgorde data het die teenwoordigheid van ortoloe van die Mycobacterium tuberculosis H37Rv ESAT-6 lokusse in die genome van ander mikobakterie, bv. M. tuberculosis CDC1551, M. tuberculosis 210, M. bovis, M. leprae, M. avium, en die nie-virulente ras M. smegmatis, bevestig. Filogenetiese analises wat op die geenvolgordes uitgevoer is het die volgorde van duplisering van die geen groepe vasgestel, en het aangetoon dat die geen groep gebied 4 (Rv3444c-3450c) die voorouer is van die ander duplikate. Gebied 4 is ook die enigste gebied waarvoor daar ortoloe gebiede in die genome van Corynebacterium diptheriae en Streptomyces coelicolor gevind kon word. Die vergelykende genomiese analises het dus aangetoon dat die teenwoordigheid van die ESAT-6 geen groepe 'n unieke kenmerk is van die lede van die hoe G+C gram-positiewe bakterie en dat die veelvuldige Stellenbosch University http://scholar.sun.ac.za/ V duplisering van hierdie gebiede slegs plaasgevind het en behou is in die genome van die lede van die genus Mikobakterium. Die ESAT-6 geen groep gebiede bestaan uit die gene van die ESAT-6 geen familie (wat kodeer vir gesekreteerde T-sel antigene sonder enige bespeurbare sekreteringsseine), die mycosins (wat gesekreteerde, selwand-geassosieerde subtilisien-agtige serien proteases is) sowel as gene wat kodeer vir moontlike ABC tranporters, ATP-bindingsproteine, en ander membraan-geassosieerde proteine. Aangesien die lede van die ESAT-6 familie gesekreteer word sonder enige normale sec- afhanklike sekreteringsseine, is daar gehipotetiseer dat hierdie membraan-geassosieerde en energie- verskaffende proteine saam funksioneer om 'n transport sisteem te vorm vir die sekretering van die lede van die ESAT-6 protein familie. Hierdie hipotese is ondersteun deur die resultate wat aangedui het dat een van die ESAT-6 geen groep gebiede uitgedruk word as een enkele polisistroniese
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