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PE-PGRS family protein PE_PGRS33

 PG33_MYCTU              Reviewed;         498 AA.
P9WIF5; L0TAP6; Q50615;
16-APR-2014, integrated into UniProtKB/Swiss-Prot.
16-APR-2014, sequence version 1.
07-JUN-2017, entry version 20.
RecName: Full=PE-PGRS family protein PE_PGRS33 {ECO:0000305};
Name=PE_PGRS33 {ECO:0000312|EMBL:CCP44584.1};
OrderedLocusNames=Rv1818c {ECO:0000312|EMBL:CCP44584.1};
ORFNames=MTCY1A11.25c;
Mycobacterium tuberculosis (strain ATCC 25618 / H37Rv).
Bacteria; Actinobacteria; Corynebacteriales; Mycobacteriaceae;
Mycobacterium; Mycobacterium tuberculosis complex.
NCBI_TaxID=83332;
[1]
NUCLEOTIDE SEQUENCE [LARGE SCALE GENOMIC DNA].
STRAIN=ATCC 25618 / H37Rv;
PubMed=9634230; DOI=10.1038/31159;
Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C.M.,
Harris D.E., Gordon S.V., Eiglmeier K., Gas S., Barry C.E. III,
Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T.,
Connor R., Davies R.M., Devlin K., Feltwell T., Gentles S., Hamlin N.,
Holroyd S., Hornsby T., Jagels K., Krogh A., McLean J., Moule S.,
Murphy L.D., Oliver S., Osborne J., Quail M.A., Rajandream M.A.,
Rogers J., Rutter S., Seeger K., Skelton S., Squares S., Squares R.,
Sulston J.E., Taylor K., Whitehead S., Barrell B.G.;
"Deciphering the biology of Mycobacterium tuberculosis from the
complete genome sequence.";
Nature 393:537-544(1998).
[2]
BIOTECHNOLOGY, AND IMMUNE RESPONSE.
PubMed=11500435; DOI=10.1128/IAI.69.9.5606-5611.2001;
Delogu G., Brennan M.J.;
"Comparative immune response to PE and PE_PGRS antigens of
Mycobacterium tuberculosis.";
Infect. Immun. 69:5606-5611(2001).
[3]
INDUCTION.
PubMed=11967065; DOI=10.1046/j.1365-2958.2002.02813.x;
Banu S., Honore N., Saint-Joanis B., Philpott D., Prevost M.C.,
Cole S.T.;
"Are the PE-PGRS proteins of Mycobacterium tuberculosis variable
surface antigens?";
Mol. Microbiol. 44:9-19(2002).
[4]
SUBCELLULAR LOCATION, AND DOMAIN.
STRAIN=H37Rv;
PubMed=15101979; DOI=10.1111/j.1365-2958.2004.04007.x;
Delogu G., Pusceddu C., Bua A., Fadda G., Brennan M.J., Zanetti S.;
"Rv1818c-encoded PE_PGRS protein of Mycobacterium tuberculosis is
surface exposed and influences bacterial cell structure.";
Mol. Microbiol. 52:725-733(2004).
[5]
INDUCTION.
PubMed=16672626; DOI=10.1128/JB.188.10.3721-3725.2006;
Dheenadhayalan V., Delogu G., Sanguinetti M., Fadda G., Brennan M.J.;
"Variable expression patterns of Mycobacterium tuberculosis PE_PGRS
genes: evidence that PE_PGRS16 and PE_PGRS26 are inversely regulated
in vivo.";
J. Bacteriol. 188:3721-3725(2006).
[6]
BIOTECHNOLOGY, AND INVOLVEMENT IN B-CELL RESPONSE.
PubMed=17687113; DOI=10.1128/CVI.00181-07;
Narayana Y., Joshi B., Katoch V.M., Mishra K.C., Balaji K.N.;
"Differential B-cell responses are induced by Mycobacterium
tuberculosis PE antigens Rv1169c, Rv0978c, and Rv1818c.";
Clin. Vaccine Immunol. 14:1334-1341(2007).
[7]
FUNCTION, INTERACTION WITH TLR2, AND DOMAIN.
STRAIN=H37Rv;
PubMed=17095513; DOI=10.1074/jbc.M604379200;
Basu S., Pathak S.K., Banerjee A., Pathak S., Bhattacharyya A.,
Yang Z., Talarico S., Kundu M., Basu J.;
"Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium
tuberculosis is mediated by Toll-like receptor 2-dependent release of
tumor necrosis factor-alpha.";
J. Biol. Chem. 282:1039-1050(2007).
[8]
FUNCTION IN INDUCTION OF APOPTOSIS, AND SUBCELLULAR LOCATION.
STRAIN=H37Rv;
PubMed=17223373; DOI=10.1016/j.micinf.2006.11.013;
Balaji K.N., Goyal G., Narayana Y., Srinivas M., Chaturvedi R.,
Mohammad S.;
"Apoptosis triggered by Rv1818c, a PE family gene from Mycobacterium
tuberculosis is regulated by mitochondrial intermediates in T cells.";
Microbes Infect. 9:271-281(2007).
[9]
SUBCELLULAR LOCATION, AND DOMAIN.
PubMed=18028308; DOI=10.1111/j.1365-2958.2007.06023.x;
Cascioferro A., Delogu G., Colone M., Sali M., Stringaro A.,
Arancia G., Fadda G., Palu G., Manganelli R.;
"PE is a functional domain responsible for protein translocation and
localization on mycobacterial cell wall.";
Mol. Microbiol. 66:1536-1547(2007).
[10]
SUBCELLULAR LOCATION, AND EXPRESSION IN M.SMEGMATIS.
PubMed=18957600; DOI=10.1099/mic.0.2008/019968-0;
Singh P.P., Parra M., Cadieux N., Brennan M.J.;
"A comparative study of host response to three Mycobacterium
tuberculosis PE_PGRS proteins.";
Microbiology 154:3469-3479(2008).
[11]
INDUCTION.
PubMed=19068228; DOI=10.1016/j.micpath.2008.11.003;
Vallecillo A.J., Espitia C.;
"Expression of Mycobacterium tuberculosis pe_pgrs33 is repressed
during stationary phase and stress conditions, and its transcription
is mediated by sigma factor A.";
Microb. Pathog. 46:119-127(2009).
[12]
SUBCELLULAR LOCATION, AND DOMAIN.
PubMed=21081760; DOI=10.1099/mic.0.041996-0;
Cadieux N., Parra M., Cohen H., Maric D., Morris S.L., Brennan M.J.;
"Induction of cell death after localization to the host cell
mitochondria by the Mycobacterium tuberculosis PE_PGRS33 protein.";
Microbiology 157:793-804(2011).
[13]
SUBCELLULAR LOCATION, EXPORT VIA ESX-5, AND DOMAIN.
PubMed=22110736; DOI=10.1371/journal.pone.0027713;
Cascioferro A., Daleke M.H., Ventura M., Dona V., Delogu G., Palu G.,
Bitter W., Manganelli R.;
"Functional dissection of the PE domain responsible for translocation
of PE_PGRS33 across the mycobacterial cell wall.";
PLoS ONE 6:E27713-E27713(2011).
[14]
FUNCTION, AND DOMAIN.
STRAIN=H37Rv;
PubMed=24106104; DOI=10.1111/2049-632X.12096;
Zumbo A., Palucci I., Cascioferro A., Sali M., Ventura M.,
D'Alfonso P., Iantomasi R., Di Sante G., Ria F., Sanguinetti M.,
Fadda G., Manganelli R., Delogu G.;
"Functional dissection of protein domains involved in the
immunomodulatory properties of PE_PGRS33 of Mycobacterium
tuberculosis.";
Pathog. Dis. 69:232-239(2013).
[15]
BIOTECHNOLOGY, AND IMMUNE RESPONSE.
PubMed=24904584; DOI=10.3389/fimmu.2014.00236;
Cohen I., Parada C., Acosta-Gio E., Espitia C.;
"The PGRS domain from PE_PGRS33 of Mycobacterium tuberculosis is
target of humoral immune response in mice and humans.";
Front. Immunol. 5:236-236(2014).
[16]
REVIEW.
PubMed=25693607; DOI=10.1586/14760584.2015.1015995;
Gastelum-Avina P., Velazquez C., Espitia C., Lares-Villa F.,
Garibay-Escobar A.;
"A PE_PGRS33 protein of Mycobacterium tuberculosis: an ideal target
for future tuberculosis vaccine design.";
Expert Rev. Vaccines 14:699-711(2015).
[17]
FUNCTION, ENZYME REGULATION, INTERACTION WITH TLR2, AND SUBCELLULAR
LOCATION.
PubMed=27483162; DOI=10.1021/acs.biochem.6b00289;
Yeruva V.C., Kulkarni A., Khandelwal R., Sharma Y., Raghunand T.R.;
"The PE_PGRS proteins of Mycobacterium tuberculosis are Ca(2+) binding
mediators of host-pathogen interaction.";
Biochemistry 55:4675-4687(2016).
[18]
FUNCTION, INTERACTION WITH TLR2, DOMAIN, AND DISRUPTION PHENOTYPE.
PubMed=26978522; DOI=10.1371/journal.pone.0150800;
Palucci I., Camassa S., Cascioferro A., Sali M., Anoosheh S.,
Zumbo A., Minerva M., Iantomasi R., De Maio F., Di Sante G., Ria F.,
Sanguinetti M., Palu G., Brennan M.J., Manganelli R., Delogu G.;
"PE_PGRS33 contributes to Mycobacterium tuberculosis entry in
macrophages through interaction with TLR2.";
PLoS ONE 11:E0150800-E0150800(2016).
-!- FUNCTION: Induces TNF-alpha release through human Toll-like
receptor 2 (TLR2) signaling pathway, leading to macrophage
apoptosis (PubMed:17095513, PubMed:17223373, PubMed:24106104). The
signaling pathway involves TLR2-dependent activation of the
mitogen-activated protein kinase kinase kinase 5 (ASK1), which
activates the p38 and JNK MAPKs, leading to enhanced expression of
TNF-alpha and tumor necrosis factor receptor superfamily member 1A
(TNFRI) genes. Signals are amplified through classical caspase 8-
dependent mitochondrial release of cytochrome c, leading to the
activation of caspases 9 and 3 (PubMed:17095513). Mediates Ca(2+)-
dependent up-regulation of the anti-inflammatory cytokine IL-10
(PubMed:27483162). Mediates entry into macrophages in a TLR2-
dependent mechanism and activates the TLR2-dependent pro-adhesive
pathway (PubMed:26978522). {ECO:0000269|PubMed:17095513,
ECO:0000269|PubMed:17223373, ECO:0000269|PubMed:24106104,
ECO:0000269|PubMed:26978522, ECO:0000269|PubMed:27483162}.
-!- ENZYME REGULATION: Binding of Ca(2+) to PE_PGRS33 induces
conformational changes and increases affinity for TLR2.
{ECO:0000269|PubMed:27483162}.
-!- SUBUNIT: Interacts with human TLR2. {ECO:0000269|PubMed:17095513,
ECO:0000269|PubMed:26978522, ECO:0000269|PubMed:27483162}.
-!- SUBCELLULAR LOCATION: Secreted, cell wall
{ECO:0000269|PubMed:15101979, ECO:0000269|PubMed:18028308,
ECO:0000269|PubMed:22110736, ECO:0000269|PubMed:27483162}. Cell
surface {ECO:0000269|PubMed:15101979, ECO:0000269|PubMed:18028308,
ECO:0000269|PubMed:18957600, ECO:0000269|PubMed:22110736,
ECO:0000269|PubMed:27483162}. Cell outer membrane
{ECO:0000269|PubMed:18028308}. Note=Exported to the cell surface
via the ESX-5 / type VII secretion system (T7SS)
(PubMed:22110736). Localizes mostly at the cell poles
(PubMed:15101979). Colocalizes to mitochondria in transfected
eukaryotic cells (PubMed:17223373, PubMed:21081760).
{ECO:0000269|PubMed:15101979, ECO:0000269|PubMed:17223373,
ECO:0000269|PubMed:21081760, ECO:0000269|PubMed:22110736}.
-!- INDUCTION: Constitutively expressed in vitro, suggesting that it
could be an essential gene (PubMed:11967065, PubMed:16672626).
Expression is regulated by SigA. Down-regulated during stationary
phase, under nutrient starvation and oxygen depletion
(PubMed:19068228). {ECO:0000269|PubMed:11967065,
ECO:0000269|PubMed:16672626, ECO:0000269|PubMed:19068228}.
-!- DOMAIN: Contains an N-terminal PE domain, followed by a conserved
linker region and a C-terminal PGRS domain (PubMed:18028308,
PubMed:21081760). The PE domain is responsible for the export and
localization to the cell wall (PubMed:15101979, PubMed:18028308,
PubMed:22110736). The PGRS domain is required for TNF-alpha
secretion and is responsible for the main immunomodulatory
properties of the protein (PubMed:17095513, PubMed:24106104).
Variations within the PGRS domain alter the levels of TNF-alpha
induction and are likely to have an impact on the innate immune
response (PubMed:17095513). PGRS domain is also required to
mediate cell entry into macrophages (PubMed:26978522).
Colocalization to the mitochondria of host cells is dependent on
the linker region and the PGRS domain, but not the PE domain
(PubMed:21081760). {ECO:0000269|PubMed:15101979,
ECO:0000269|PubMed:17095513, ECO:0000269|PubMed:18028308,
ECO:0000269|PubMed:21081760, ECO:0000269|PubMed:22110736,
ECO:0000269|PubMed:24106104, ECO:0000269|PubMed:26978522}.
-!- DISRUPTION PHENOTYPE: Deletion mutant is strongly impaired in its
ability to enter macrophages. Deletion does not affect the
intracellular growth in macrophages.
{ECO:0000269|PubMed:26978522}.
-!- BIOTECHNOLOGY: PE domain induces protective cellular immune
response and PGRS domain induces humoral immune response during
infection in mice, suggesting that this protein is a promising
candidate for the development of M.tuberculosis vaccines
(PubMed:11500435). Immunization of mice with the PE_PGRS33 protein
stimulated CD4(+) and CD8(+) T-cell proliferation as well as IFN-
gamma secretion, supporting the potential use of PE_PGRS33 as a
vaccine candidate for tuberculosis (PubMed:24904584). Elicits a
strong B-cell humoral response among different clinical categories
of both adult and child tuberculosis patients, indicating that it
could be used in the serodiagnosis of tuberculosis
(PubMed:17687113). {ECO:0000269|PubMed:11500435,
ECO:0000269|PubMed:17687113, ECO:0000269|PubMed:24904584}.
-!- MISCELLANEOUS: Expression of this gene in M.smegmatis leads to low
levels of NO and IL-12, increased level of IL-10 and better
survival of recombinant strains in macrophages.
{ECO:0000269|PubMed:18957600}.
-!- SIMILARITY: Belongs to the mycobacterial PE family. PGRS
subfamily. {ECO:0000305}.
-----------------------------------------------------------------------
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Distributed under the Creative Commons Attribution-NoDerivs License
-----------------------------------------------------------------------
EMBL; AL123456; CCP44584.1; -; Genomic_DNA.
PIR; C70720; C70720.
RefSeq; WP_010886133.1; NZ_KK339370.1.
RefSeq; YP_177846.1; NC_000962.3.
ProteinModelPortal; P9WIF5; -.
SMR; P9WIF5; -.
STRING; 83332.Rv1818c; -.
PaxDb; P9WIF5; -.
PRIDE; P9WIF5; -.
EnsemblBacteria; CCP44584; CCP44584; Rv1818c.
GeneID; 885551; -.
KEGG; mtu:Rv1818c; -.
KEGG; mtv:RVBD_1818c; -.
PATRIC; fig|83332.111.peg.2023; -.
TubercuList; Rv1818c; -.
OMA; IAAMSEY; -.
Proteomes; UP000001584; Chromosome.
GO; GO:0009279; C:cell outer membrane; IEA:UniProtKB-SubCell.
GO; GO:0009986; C:cell surface; IEA:UniProtKB-SubCell.
GO; GO:0005618; C:cell wall; IDA:MTBBASE.
GO; GO:0005576; C:extracellular region; IEA:UniProtKB-KW.
GO; GO:0046789; F:host cell surface receptor binding; IPI:MTBBASE.
GO; GO:0052167; P:modulation by symbiont of host innate immune response; IDA:MTBBASE.
GO; GO:0009405; P:pathogenesis; IMP:MTBBASE.
GO; GO:0070482; P:response to oxygen levels; IEP:MTBBASE.
GO; GO:0042594; P:response to starvation; IEP:MTBBASE.
InterPro; IPR000084; PE-PGRS_N.
Pfam; PF00934; PE; 1.
1: Evidence at protein level;
Calcium; Cell outer membrane; Cell wall; Complete proteome; Membrane;
Reference proteome; Secreted; Virulence.
CHAIN 1 498 PE-PGRS family protein PE_PGRS33.
/FTId=PRO_0000216164.
DOMAIN 1 93 PE. {ECO:0000255}.
REGION 1 30 Essential for translocation to the cell
surface. {ECO:0000269|PubMed:22110736}.
REGION 140 260 Interacts with TLR2.
{ECO:0000269|PubMed:26978522}.
SEQUENCE 498 AA; 40755 MW; 4F6F78F2482586BA CRC64;
MSFVVTIPEA LAAVATDLAG IGSTIGTANA AAAVPTTTVL AAAADEVSAA MAALFSGHAQ
AYQALSAQAA LFHEQFVRAL TAGAGSYAAA EAASAAPLEG VLDVINAPAL ALLGRPLIGN
GANGAPGTGA NGGDGGILIG NGGAGGSGAA GMPGGNGGAA GLFGNGGAGG AGGNVASGTA
GFGGAGGAGG LLYGAGGAGG AGGRAGGGVG GIGGAGGAGG NGGLLFGAGG AGGVGGLAAD
AGDGGAGGDG GLFFGVGGAG GAGGTGTNVT GGAGGAGGNG GLLFGAGGVG GVGGDGVAFL
GTAPGGPGGA GGAGGLFGVG GAGGAGGIGL VGNGGAGGSG GSALLWGDGG AGGAGGVGST
TGGAGGAGGN AGLLVGAGGA GGAGALGGGA TGVGGAGGNG GTAGLLFGAG GAGGFGFGGA
GGAGGLGGKA GLIGDGGDGG AGGNGTGAKG GDGGAGGGAI LVGNGGNGGN AGSGTPNGSA
GTGGAGGLLG KNGMNGLP


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