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Redox- and pH-responsive transcriptional regulator WhiB3

 WHIB3_MYCTU             Reviewed;         102 AA.
P9WF41; F2GEG1; L0TCG8; Q50710; Q7D5K3;
16-APR-2014, integrated into UniProtKB/Swiss-Prot.
16-APR-2014, sequence version 1.
10-MAY-2017, entry version 22.
RecName: Full=Redox- and pH-responsive transcriptional regulator WhiB3;
Name=whiB3; OrderedLocusNames=Rv3416;
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]
FUNCTION, INTERACTION WITH SIGA, AND DISRUPTION PHENOTYPE.
STRAIN=ATCC 25618 / H37Rv;
PubMed=11880648; DOI=10.1073/pnas.052705399;
Steyn A.J., Collins D.M., Hondalus M.K., Jacobs W.R. Jr.,
Kawakami R.P., Bloom B.R.;
"Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host
survival but is dispensable for in vivo growth.";
Proc. Natl. Acad. Sci. U.S.A. 99:3147-3152(2002).
[3]
INDUCTION IN MOUSE INFECTION.
PubMed=16923787; DOI=10.1128/IAI.00190-06;
Banaiee N., Jacobs W.R. Jr., Ernst J.D.;
"Regulation of Mycobacterium tuberculosis whiB3 in the mouse lung and
macrophages.";
Infect. Immun. 74:6449-6457(2006).
[4]
FUNCTION AS A REDOX SENSOR, COFACTOR, DINITROSYLATION, DISRUPTION
PHENOTYPE, AND MUTAGENESIS OF CYS-23; CYS-53; CYS-56 AND CYS-62.
STRAIN=ATCC 25618 / H37Rv;
PubMed=17609386; DOI=10.1073/pnas.0700490104;
Singh A., Guidry L., Narasimhulu K.V., Mai D., Trombley J.,
Redding K.E., Giles G.I., Lancaster J.R. Jr., Steyn A.J.;
"Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via
its [4Fe-4S] cluster and is essential for nutrient starvation
survival.";
Proc. Natl. Acad. Sci. U.S.A. 104:11562-11567(2007).
[5]
FUNCTION AS A DISULFIDE ISOMERASE, COFACTOR, SUBUNIT, AND DISULFIDE
BOND.
STRAIN=ATCC 25618 / H37Rv;
PubMed=18550384; DOI=10.1016/j.pep.2008.04.010;
Suhail Alam M., Agrawal P.;
"Matrix-assisted refolding and redox properties of WhiB3/Rv3416 of
Mycobacterium tuberculosis H37Rv.";
Protein Expr. Purif. 61:83-91(2008).
[6]
FUNCTION, DNA-BINDING, DISULFIDE BONDS, MASS SPECTROMETRY, AND
DISRUPTION PHENOTYPE.
STRAIN=ATCC 25618 / H37Rv;
PubMed=19680450; DOI=10.1371/journal.ppat.1000545;
Singh A., Crossman D.K., Mai D., Guidry L., Voskuil M.I.,
Renfrow M.B., Steyn A.J.;
"Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by
regulating virulence lipid anabolism to modulate macrophage
response.";
PLoS Pathog. 5:E1000545-E1000545(2009).
[7]
FUNCTION, COFACTOR, AND DISULFIDE BOND.
STRAIN=ATCC 25618 / H37Rv;
PubMed=19016840; DOI=10.1111/j.1742-4658.2008.06755.x;
Alam M.S., Garg S.K., Agrawal P.;
"Studies on structural and functional divergence among seven WhiB
proteins of Mycobacterium tuberculosis H37Rv.";
FEBS J. 276:76-93(2009).
[8]
FUNCTION, AND DISRUPTION PHENOTYPE.
STRAIN=H37Rv;
PubMed=26774486; DOI=10.1016/j.celrep.2015.12.056;
Saini V., Cumming B.M., Guidry L., Lamprecht D.A., Adamson J.H.,
Reddy V.P., Chinta K.C., Mazorodze J.H., Glasgow J.N.,
Richard-Greenblatt M., Gomez-Velasco A., Bach H., Av-Gay Y., Eoh H.,
Rhee K., Steyn A.J.;
"Ergothioneine maintains redox and bioenergetic homeostasis essential
for drug susceptibility and virulence of Mycobacterium tuberculosis.";
Cell Rep. 14:572-585(2016).
[9]
FUNCTION, REGULON, INDUCTION BY ACID STRESS, AND DISRUPTION PHENOTYPE.
STRAIN=H37Rv;
PubMed=26637353; DOI=10.1074/jbc.M115.684597;
Mehta M., Rajmani R.S., Singh A.;
"Mycobacterium tuberculosis WhiB3 responds to vacuolar pH-induced
changes in mycothiol redox potential to modulate phagosomal maturation
and virulence.";
J. Biol. Chem. 291:2888-2903(2016).
[10]
REVIEW.
PubMed=22010944; DOI=10.1089/ars.2011.4341;
Saini V., Farhana A., Steyn A.J.;
"Mycobacterium tuberculosis WhiB3: a novel iron-sulfur cluster protein
that regulates redox homeostasis and virulence.";
Antioxid. Redox Signal. 16:687-697(2012).
-!- FUNCTION: A redox-sensitive transcriptional regulator. Maintains
intracellular redox homeostasis by regulating catabolic metabolism
and polyketide biosynthesis (PubMed:17609386, PubMed:19680450).
Regulates expression of the redox buffer ergothioneine (ERG) in a
carbon-source-dependent manner; loss of ERG or mycothiol (MSH, the
other major redox buffer in this bacteria) leads to respiratory
alterations and bioenergetic deficiencies that negatively impact
virulence (PubMed:26774486). In response to low external pH (like
that found in host macrophage phagosomes) alters endogenous gene
expression leading to acid resistance; MSH and WhiB3 are probably
part of a regulatory circuit that mediates gene expression upon
acid stress (PubMed:26637353). Regulates pathogenic lipid
synthesis, coordinating proprionate flux (and other host-derived
fatty acid oxidation intermediates) into methyl-branched fatty
acids (polyacyltrehalose, phthiocerol dimycocerosates,
sulfolipids) and the storage lipid triacylglycerol, functioning as
reductive sink (PubMed:19680450). During intracellular growth
M.tuberculosis uses host fatty acids as an energy source,
generating large quantities of proprionate and NADH/NADPH, which
are toxic and highly reducing respectively. WhiB3 is thought to
help dissipate proprionate and NADH/NADPH by switching to the in
vivo carbon source and via lipid anabolism (PubMed:19680450).
Responds to NO and O(2) (PubMed:17609386). Regulates expression of
genes encoding modular polyketide synthases such as pks2, pks3 and
fbpA (PubMed:19680450). The oxidized apo-form of WhiB3 binds DNA
(with 2 intramolecular disulfide bonds); holo-WhiB3 (with the 4Fe-
4S cluster) binds DNA considerably less well (PubMed:19680450).
Discriminates poorly between specific and non-specific DNA-
binding. Plays a role in virulence and nutritional stress
(PubMed:11880648, PubMed:17609386, PubMed:26637353). In its apo-
form can act as a protein disulfide reductase (PubMed:18550384).
{ECO:0000269|PubMed:11880648, ECO:0000269|PubMed:17609386,
ECO:0000269|PubMed:18550384, ECO:0000269|PubMed:19016840,
ECO:0000269|PubMed:19680450, ECO:0000269|PubMed:26637353,
ECO:0000269|PubMed:26774486}.
-!- FUNCTION: May respond to mycothiol (MSH) redox potential (E-MSH)
which decreases at pH 4.5 for up to 72 hours, indicative of
cellular reductive stress; deletion of whiB3 leads to a lesser E-
MSH at 72 hours, indicative of cellular oxidative stress
(PubMed:26637353). Probably via its effects on production of
polyketide lipids, regulates host gene expression, leading to
blockage of phagosome maturation (PubMed:26637353). Equilibration
of extra- and intracytoplasmic pH kills bacteria
(PubMed:26637353). {ECO:0000269|PubMed:26637353}.
-!- COFACTOR:
Name=[4Fe-4S] cluster; Xref=ChEBI:CHEBI:49883;
Evidence={ECO:0000269|PubMed:17609386,
ECO:0000269|PubMed:18550384, ECO:0000269|PubMed:19016840};
Note=Binds 1 [4Fe-4S] cluster per subunit (PubMed:17609386).
Following nitrosylation of the [4Fe-4S] cluster binds 1 [4Fe-
8(NO)] cluster per subunit (PubMed:17609386).
{ECO:0000269|PubMed:17609386, ECO:0000269|PubMed:18550384,
ECO:0000269|PubMed:19016840};
-!- SUBUNIT: Homodimer (Probable) (PubMed:18550384). Interacts with
the C-terminal 54 residues of sigma factor SigA (RpoV)
(PubMed:11880648). {ECO:0000269|PubMed:11880648,
ECO:0000305|PubMed:18550384}.
-!- INTERACTION:
P9WGI1:sigA; NbExp=3; IntAct=EBI-11859434, EBI-11859464;
-!- SUBCELLULAR LOCATION: Cytoplasm {ECO:0000250|UniProtKB:Q9S426}.
-!- INDUCTION: 100-fold induced in wild-type C57BL/6 mice 2 weeks
after lung infection, RNA levels drop to 30X induced 8 weeks post-
infection (PubMed:16923787). Similar but less dramatic induction
is seen in immunocompromised mice (PubMed:16923787). Rapidly
induced in resting mouse macrophages, remains up-regulated for at
least 60 hours, continuing induction is repressed by interferon
gamma (PubMed:16923787). Induced by growth at acidic pH
(PubMed:26637353). {ECO:0000269|PubMed:16923787,
ECO:0000269|PubMed:26637353}.
-!- PTM: The 4Fe-4S cluster interacts with NO, forming a protein-bound
dinitrosyliron dithiol complex (PubMed:17609386).
{ECO:0000269|PubMed:17609386}.
-!- PTM: The 4Fe-4S cluster interacts with O(2), leading to its
degradation. Cluster loss takes about 2 hours (PubMed:17609386).
Once in the apo-form the cysteines oxidize to form 2
intramolecular disulfide bonds (PubMed:18550384).
{ECO:0000269|PubMed:17609386, ECO:0000269|PubMed:18550384}.
-!- MASS SPECTROMETRY: Mass=14636.76; Method=MALDI; Range=1-102;
Note=Fully reduced protein.;
Evidence={ECO:0000269|PubMed:19680450};
-!- MASS SPECTROMETRY: Mass=14407.22; Method=MALDI; Range=1-102;
Note=Fully oxidized protein.;
Evidence={ECO:0000269|PubMed:19680450};
-!- DISRUPTION PHENOTYPE: Not essential for growth in culture, or
growth in vivo in mouse and guinea pig infections
(PubMed:11880648). Disruption significantly enhances survival of
immunocompetent mice (PubMed:11880648). Decreased bacterial growth
in guinea pig lungs, but not spleen (PubMed:26637353). Growth on
minimal media, glucose or succinate is poor, suggesting WhiB3 is
involved in starvation response (PubMed:17609386). Growth on
acetate is better than wild-type (PubMed:17609386). 55-fold
decreased survival at pH 4.5, no difference at pH 5.5 or 6.6
(PubMed:26637353). Altered expression of genes involved in cell
wall lipid composition, the ESX-1 secretion system and redox
balance, impairs the mycothiol-specific reductive response to acid
stress (PubMed:26637353). Dysfunctional respiration when grown in
pyruvate, increased intracellular ergothioneine (ERG) production
when grown in a number of carbon sources (PubMed:26774486). Upon
infection of human THP-1 macrophage-like cells bacteria are
localized to acidified lysosomes (M.tuberculosis usually blocks
lysosome acidification), do not reduce mycothiol (MSH) and have
significantly decreased survival (PubMed:26637353). Leads to up-
regulation of host innate immunity genes usually repressed by
M.tuberculosis (such as phagosome maturation and TLR signaling)
and down-regulation of genes that inhibit autophagy (such as mTOR)
(PubMed:26637353). Cell size, shape and surface architecture are
perturbed, as is synthesis of cell surface associated virulence
lipids both in culture and in cultured macrophages, or in response
to oxidizing or reducing agents (PubMed:19680450). Disrupted
strains are more resistant to toxic levels of propionate
(PubMed:19680450). {ECO:0000269|PubMed:11880648,
ECO:0000269|PubMed:17609386, ECO:0000269|PubMed:19680450,
ECO:0000269|PubMed:26637353, ECO:0000269|PubMed:26774486}.
-!- SIMILARITY: Belongs to the WhiB family. {ECO:0000305}.
-----------------------------------------------------------------------
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-----------------------------------------------------------------------
EMBL; AL123456; CCP46238.1; -; Genomic_DNA.
PIR; E70737; E70737.
RefSeq; NP_217933.1; NC_000962.3.
RefSeq; WP_003418017.1; NZ_KK339370.1.
ProteinModelPortal; P9WF41; -.
IntAct; P9WF41; 1.
STRING; 83332.Rv3416; -.
PaxDb; P9WF41; -.
EnsemblBacteria; CCP46238; CCP46238; Rv3416.
GeneID; 887598; -.
KEGG; mtu:Rv3416; -.
TubercuList; Rv3416; -.
eggNOG; ENOG4105KIU; Bacteria.
eggNOG; ENOG4111U54; LUCA.
KO; K18955; -.
OMA; WQLHGAC; -.
PhylomeDB; P9WF41; -.
Proteomes; UP000001584; Chromosome.
GO; GO:0005618; C:cell wall; IDA:MTBBASE.
GO; GO:0005737; C:cytoplasm; IEA:UniProtKB-SubCell.
GO; GO:0051539; F:4 iron, 4 sulfur cluster binding; IDA:MTBBASE.
GO; GO:0003677; F:DNA binding; IDA:MTBBASE.
GO; GO:0051536; F:iron-sulfur cluster binding; IDA:MTBBASE.
GO; GO:0046872; F:metal ion binding; IEA:UniProtKB-KW.
GO; GO:0015035; F:protein disulfide oxidoreductase activity; IDA:MTBBASE.
GO; GO:0071766; P:Actinobacterium-type cell wall biogenesis; IDA:MTBBASE.
GO; GO:0045454; P:cell redox homeostasis; IDA:MTBBASE.
GO; GO:0009405; P:pathogenesis; IDA:MTBBASE.
GO; GO:0090034; P:regulation of chaperone-mediated protein complex assembly; IDA:MTBBASE.
GO; GO:0019217; P:regulation of fatty acid metabolic process; IDA:MTBBASE.
GO; GO:0019216; P:regulation of lipid metabolic process; IDA:MTBBASE.
GO; GO:0080134; P:regulation of response to stress; IDA:MTBBASE.
GO; GO:0006355; P:regulation of transcription, DNA-templated; IEA:UniProtKB-KW.
GO; GO:0006351; P:transcription, DNA-templated; IEA:UniProtKB-KW.
HAMAP; MF_01479; WhiB; 1.
InterPro; IPR034768; 4FE4S_WBL.
InterPro; IPR003482; Whib.
Pfam; PF02467; Whib; 1.
PROSITE; PS51674; 4FE4S_WBL; 1.
1: Evidence at protein level;
4Fe-4S; Complete proteome; Cytoplasm; Disulfide bond; DNA-binding;
Iron; Iron-sulfur; Metal-binding; Reference proteome; Stress response;
Transcription; Transcription regulation; Virulence.
CHAIN 1 102 Redox- and pH-responsive transcriptional
regulator WhiB3.
/FTId=PRO_0000420382.
DOMAIN 22 86 4Fe-4S Wbl-type.
METAL 23 23 Dinitrosyliron [4Fe-8(NO)]; alternate.
{ECO:0000305|PubMed:17609386}.
METAL 23 23 Iron-sulfur (4Fe-4S); alternate.
{ECO:0000305|PubMed:17609386}.
METAL 53 53 Dinitrosyliron [4Fe-8(NO)]; alternate.
{ECO:0000305|PubMed:17609386}.
METAL 53 53 Iron-sulfur (4Fe-4S); alternate.
{ECO:0000305|PubMed:17609386}.
METAL 56 56 Dinitrosyliron [4Fe-8(NO)]; alternate.
{ECO:0000305|PubMed:17609386}.
METAL 56 56 Iron-sulfur (4Fe-4S); alternate.
{ECO:0000305|PubMed:17609386}.
METAL 62 62 Dinitrosyliron [4Fe-8(NO)]; alternate.
{ECO:0000305|PubMed:17609386}.
METAL 62 62 Iron-sulfur (4Fe-4S); alternate.
{ECO:0000305|PubMed:17609386}.
MUTAGEN 23 23 C->A: No 4Fe-4S cluster assembly, does
not complement growth defects; when
associated with A-53; A-56 and A-62.
{ECO:0000269|PubMed:17609386}.
MUTAGEN 53 53 C->A: No 4Fe-4S cluster assembly, does
not complement growth defects; when
associated with A-23; A-56 and A-62.
{ECO:0000269|PubMed:17609386}.
MUTAGEN 56 56 C->A: No 4Fe-4S cluster assembly, does
not complement growth defects; when
associated with A-33; A-53 and A-62.
{ECO:0000269|PubMed:17609386}.
MUTAGEN 62 62 C->A: No 4Fe-4S cluster assembly, does
not complement growth defects; when
associated with A-33; A-53 and A-56.
{ECO:0000269|PubMed:17609386}.
SEQUENCE 102 AA; 11612 MW; C38A6774457F71BA CRC64;
MPQPEQLPGP NADIWNWQLQ GLCRGMDSSM FFHPDGERGR ARTQREQRAK EMCRRCPVIE
ACRSHALEVG EPYGVWGGLS ESERDLLLKG TMGRTRGIRR TA


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