Team:Imperial College London/M2/genes

From 2009.igem.org

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The overexpression of RcsB is akin to fitting a stethoscope to the end of a megaphone. In essence, the sensitivity of the RCS Phosphorelay system becomes such that the smallest of membrane perturbations becomes sufficient to trigger colanic acid production. Thus, the background noise switches the RCS Phosphorelay system on permanently.
The overexpression of RcsB is akin to fitting a stethoscope to the end of a megaphone. In essence, the sensitivity of the RCS Phosphorelay system becomes such that the smallest of membrane perturbations becomes sufficient to trigger colanic acid production. Thus, the background noise switches the RCS Phosphorelay system on permanently.
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There are a total of 19 genes involved in colonic acid biosynthesis, the best characterised of which are shown below.  
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There are numerous genes involved in colonic acid biosynthesis, the best characterised of which are shown below.  
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==Other genes involved in colanic acid biosynthesis are listed below.==
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=====<b><i>wcaF</i> </b>=====
=====<b><i>wcaF</i> </b>=====
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* Predicted colanic acid polymerase
* Predicted colanic acid polymerase
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=====<b><i>wza</i> </b>=====
 
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* This codes for a lipoprotein that is required for colanic acid translocation through the outer membrane. The lipoprotein is a subunit of the capsular polysaccharide export apparatus.
 
=====<b><i>fcl</i> </b>=====
=====<b><i>fcl</i> </b>=====
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===<b>General Protective:</b>===
===<b>General Protective:</b>===
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The following proteins are thought play a role in membrane fortification to confer protection against the rigours of dessication, acid exposure and osmotic stress.
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<area coords="25,20,61,37"  onmouseover="return overlib('RcsB-Pasp trancriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41.5 (ranging from -48 to -35)<br><b>Evidence:</b> Site mutation [DavalosGar01], Gene expression analysis [DavalosGar01], Binding of purified proteins [FrancezCha05]');" onmouseout="return nd();">
<area coords="25,20,61,37"  onmouseover="return overlib('RcsB-Pasp trancriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41.5 (ranging from -48 to -35)<br><b>Evidence:</b> Site mutation [DavalosGar01], Gene expression analysis [DavalosGar01], Binding of purified proteins [FrancezCha05]');" onmouseout="return nd();">
<area coords="19,38,70,55"  onmouseover="return overlib('NhaR-Na+ transcriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41 (ranging from -50 to -32)<br><b>Evidence:</b> Gene expression analysis [Toesca01], Binding of cellular extracts [Sturny03], Site mutation [Toesca01]');" onmouseout="return nd();">
<area coords="19,38,70,55"  onmouseover="return overlib('NhaR-Na+ transcriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41 (ranging from -50 to -32)<br><b>Evidence:</b> Gene expression analysis [Toesca01], Binding of cellular extracts [Sturny03], Site mutation [Toesca01]');" onmouseout="return nd();">
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<area coords="87,42,177,73" onmouseover="return overlib(' <b>Gene:</b>   
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<area coords="87,42,177,73" onmouseover="return overlib(' <b>Gene:</b>  osmC   EG10680    b1482    ECK1476<br><b>Location:</b> 1,554,649 -> 1,555,080  <br> <b>Product:</b> osmotically inducible peroxidase OsmC');" onmouseout="return nd();">
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C   EG10680    b1482    ECK1476<br><b>Location:</b> 1,554,649 -> 1,555,080  <br> <b>Product:</b> osmotically inducible peroxidase OsmC');" onmouseout="return nd();">
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<area coords="19,0,172,90" onmouseover="return overlib('<b>Operon:</b> osmCp1 (Experim. ev.)  <BR><b>Tr.Activators:</b> (NhaR-Na<SUP>+</SUP> phospho-RcsB) <BR><b>Tr.Inhibitors:</b> (Lrp Hns)');" onmouseout="return nd();">
<area coords="19,0,172,90" onmouseover="return overlib('<b>Operon:</b> osmCp1 (Experim. ev.)  <BR><b>Tr.Activators:</b> (NhaR-Na<SUP>+</SUP> phospho-RcsB) <BR><b>Tr.Inhibitors:</b> (Lrp Hns)');" onmouseout="return nd();">
<area coords="0,0,179,90" onmouseover="return overlib('<b>Operon</b>: osmC');" onmouseout="return nd();">
<area coords="0,0,179,90" onmouseover="return overlib('<b>Operon</b>: osmC');" onmouseout="return nd();">
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==Other RcsB induced genes coding for protective proteins are listed below.==
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=====<b><i>ivy</i> (Inhibitor of Vertebrate lysozyme) </b>=====
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=====<b><i>KatE</i> </b>=====
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*Discovered in 2001 as the first bacterial lysozyme inhibitor. This Type-C lysozyme inhibitor resides in the periplasm.<sup>1</sup>
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* Codes for a subunit of heme d synthase / hydroperoxidase. This bacterial catalase protects against osmotic stress.
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=====<b><i>MilC</i> (Membrane-bound lysozyme inhibitor of Type C lysozyme) </b>=====
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{{Imperial/09/Division}}
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*This is a lipoprotein that resides in the membrane. <sup>1</sup>  
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===<b>Host Defence:</b>===
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Humans synthesise a number of enzymes that are able to burst bacterial cells. These enzymes are called lysosymes. RcsB is able to induce a number of proteins that act as lysosyme inhibitors that will prevent the host-mediated lysis of our chassis.
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=====<b><i>ivy</i> (Inhibitor of Vertebrate lysozyme) </b>=====
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=====<b><i>OsmC</i> (Osmotically-inducible protein C) </b>=====
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*Discovered in 2001 as the first bacterial lysozyme inhibitor. This Type-C lysozyme inhibitor resides in the periplasm.<sup>1</sup>
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* This protein provides defense against oxidative stress caused by exposure to organic hydroperoxides. <sup>2</sup> <sup>3</sup>
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=====<b><i>KatE</i> </b>=====
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* Codes for a subunit of heme d synthase / hydroperoxidase. This bacterial catalase protects against osmotic stress.
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=====<b><i>MilC</i> (Membrane-bound lysozyme inhibitor of Type C lysozyme) </b>=====
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*This is a lipoprotein that resides in the membrane. <sup>1</sup>
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<map name="MAP91781">
<map name="MAP91781">
<area coords="17,55,48,72" onmouseover="return overlib('RcsB-Pasp trancriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41.5 (ranging from -35 to -48)<br><b>Evidence:</b> Binding of purified proteins [FrancezCha05], Gene expression analysis [FrancezCha05]');" onmouseout="return nd();">
<area coords="17,55,48,72" onmouseover="return overlib('RcsB-Pasp trancriptional activator activates transcription from associated promoter<br><b>Distance to transcription start site:</b> -41.5 (ranging from -35 to -48)<br><b>Evidence:</b> Binding of purified proteins [FrancezCha05], Gene expression analysis [FrancezCha05]');" onmouseout="return nd();">
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<area coords="165,41,207,72"  onmouseover="return overlib(' <b>Gene:</b>  sra    EG11508    b1480    ECK1474<br><b>Synonyms:</b> rpsV<br><b>Location:</b> 1,553,850 <- 1,553,987  <br> <b>Product:</b> 30S ribosomal subunit protein S22, subunit of ribosome');" onmouseout="return nd();">
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<area coords="165,41,207,72"  onmouseover="return overlib(' <b>Gene:</b>  sra    EG11508    b1480    ECK1474<br><b>Synonyms:</b> rpsV<br><b>Location:</b> 1,553,850 <- 1,553,987  <br> <b>Product:</b> 30S ribosomal subunit protein S22, subunit of ribosome. Sra is more abundant at stationary phase than during log phase growth.  ');" onmouseout="return nd();">
<area coords="75,41,136,72" onmouseover="return overlib(' <b>Gene:</b>  bdm    G6776    b1481    ECK1475<br><b>Synonyms:</b> yddX<br><b>Location:</b> 1,554,089 <- 1,554,304  <br> <b>Product:</b> biofilm-dependent modulation protein');" onmouseout="return nd();">
<area coords="75,41,136,72" onmouseover="return overlib(' <b>Gene:</b>  bdm    G6776    b1481    ECK1475<br><b>Synonyms:</b> yddX<br><b>Location:</b> 1,554,089 <- 1,554,304  <br> <b>Product:</b> biofilm-dependent modulation protein');" onmouseout="return nd();">
<area coords="0,0,103,89" onmouseover="return overlib('<b>Operon:</b> bdmp (Experim. ev.)  <BR><b>Tr.Activators:</b> (phospho-RcsB)');" onmouseout="return nd();">
<area coords="0,0,103,89" onmouseover="return overlib('<b>Operon:</b> bdmp (Experim. ev.)  <BR><b>Tr.Activators:</b> (phospho-RcsB)');" onmouseout="return nd();">
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</html>
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=====<b><i>Sra </i>(stationary-phase-induced ribosome-associated)</b>=====
 
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Sra is a sub-stoichiometric component of the 30S ribosomal subunit that is more abundant at stationary phase than during log phase growth.
 
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=====<b><i>rprA</i> </b>=====
 
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rprA is a gene encoding a small RNA molecule that is involved in the post-transcriptional control of the alternative sigma factor, ("sigma S").
 
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=====<b><i>FtsA</i> </b>=====
 
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FtsA is an essential cell division protein which colocalizes with FtsZ to the septal ring structure.
 
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=====<b><i>FtsZ</i> </b>=====
 
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* Essential cell division protein.
 
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=====<b><i>yfbR</i> </b>=====
 
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* dCMP phosphohydrolase
 
{{Imperial/09/Division}}
{{Imperial/09/Division}}
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===Membrane Proteins:===
 
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=====<b><i>bdm</i> (biofilm-dependent modulation protein) </b>=====
 
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=====<b><i>OsmB</i> </b>=====
 
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* OsmB encodes an outer membrane lipoprotein.
 
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=====<b><i>OsmY</i> </b>=====
 
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Hyperosmotically inducible periplasmic protein
 
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=====<b><i>PhnQ</i> </b>=====
 
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=====<b><i>ycfJ</i> </b>=====
 
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* Uncharacterized putative inner membrane protein.
 
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=====<b><i>ygaC</i> </b>=====
 
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=====<b><i>spy</i> </b>=====
 
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=====<b><i>ymgD</i> </b>=====
 
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* Putative periplasmic protein.
 
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=====<b><i>ypeC</i> </b>=====
 
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* Unknown function
 
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=====<b><i>ymgG</i> </b>=====
 
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=====<b><i>YbaY</i> </b>=====
 
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Predicted outer membrane lipoprotein
 
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{{Imperial/09/Division}}
 
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==Repression:==
==Repression:==
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<hr>  <h3> <b>Interactive Image References</b>
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<hr>  <h3> <b>References</b>
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Note, interactive operons are credited to EcoCyc: Nucleic Acids Research 37:D464-70 2009
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</h3>  <p class="ecoparagraph"> <a name="16606699"></a>
</h3>  <p class="ecoparagraph"> <a name="16606699"></a>
  <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&amp;db=PubMed&amp;list_uids=16606699&amp;dopt=Abstract" class="CITATION-FRAME" onmouseover="return overlib('16606699');" onmouseout="return nd();">  <b>Arifuzzama06</b>: "Large-scale identification of protein-protein interaction of Escherichia coli K-12." Genome Res 16(5);686-91. PMID: 16606699
  <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&amp;db=PubMed&amp;list_uids=16606699&amp;dopt=Abstract" class="CITATION-FRAME" onmouseover="return overlib('16606699');" onmouseout="return nd();">  <b>Arifuzzama06</b>: "Large-scale identification of protein-protein interaction of Escherichia coli K-12." Genome Res 16(5);686-91. PMID: 16606699
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</a>  </p><p class="ecoparagraph"> <a name="10702265"></a>
</a>  </p><p class="ecoparagraph"> <a name="10702265"></a>
  <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&amp;db=PubMed&amp;list_uids=10702265&amp;dopt=Abstract" class="CITATION-FRAME" onmouseover="return overlib('10702265');" onmouseout="return nd();">  <b>Wehland00</b>:  Wehland M, Bernhard F (2000). "The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria." J Biol Chem 2000;275(10);7013-20. PMID: 10702265
  <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&amp;db=PubMed&amp;list_uids=10702265&amp;dopt=Abstract" class="CITATION-FRAME" onmouseover="return overlib('10702265');" onmouseout="return nd();">  <b>Wehland00</b>:  Wehland M, Bernhard F (2000). "The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria." J Biol Chem 2000;275(10);7013-20. PMID: 10702265
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</a> </p><p></p><hr><a href="#" onclick="window.open('feedback.html?' + location, 'bugreport', 'toolbar=no,dependent=yes,height=640,width=620,menubar=no,location=no,scrollbars=yes')">Report Errors or Provide Feedback</a>
 
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<br><font size="-1">Please cite the following article in publications resulting from the use of EcoCyc: <a href="http://nar.oupjournals.org/cgi/content/full/37/suppl_1/D464">Nucleic Acids Research 37:D464-70 2009</a></font>
 
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Latest revision as of 21:47, 21 October 2009

Contents

Regulation for Capsular Synthesis (RCS) Phosphorelay System

RcsB is a transcription factor that forms part of a phosphorelay system. As the name suggests, a phosphorelay system consists of a series of nodes down which a phosphate group is passed. The transfer of this phosphate group down along the Rcs relay system is initiated by membrane stress. Once the phosphate group has been passed to RcsB, it can bind to DNA and act as a transcription factor. Phosphorylated RcsB is thought to regulate ~5% of the E.coli genome 4.

PhosRelay.png

The Rcs phosphorelay is composed of two membrane-anchored proteins, RcsC and RcsD, and a cytoplasmic protein, RcsB. In response to a signal, the sensor kinase RcsC autophosphorylates and the phosphoryl group is transferred to RcsB, via RcsD. RcsB can both homodimerise and heterodimerise with RcsA, these two complexes serve to regulate different operons.


Signal Amplification:

RcsB is able to heterodimerise with the protein RcsA. The RcsB+RcsA complex acts as a transcription factor that induces the expression of a number of genes. One of these genes codes for RcsA, this initiates a positive feedback loop.



Colanic Acid Biosynthesis:

The overexpression of RcsB is akin to fitting a stethoscope to the end of a megaphone. In essence, the sensitivity of the RCS Phosphorelay system becomes such that the smallest of membrane perturbations becomes sufficient to trigger colanic acid production. Thus, the background noise switches the RCS Phosphorelay system on permanently.

There are a total of 19 genes involved in colonic acid biosynthesis, the best characterised of which are shown below.


Other genes involved in colanic acid biosynthesis are listed below.

wcaF
  • Putative colanic acid biosynthesis acetyltransferase 2
gmd

Codes for GDP-mannose 4,6-dehydratase which is a subunit of GDP-mannose 4,6-dehydratase. This enzyme is involved in colanic acid biosynthesis.

wcaD
  • Predicted colanic acid polymerase
fcl
  • Codes for a subunit of GDP-fucose synthase. This enzyme is involved in colanic acid biosynthesis.



General Protective:

The following proteins are thought play a role in membrane fortification to confer protection against the rigours of dessication, acid exposure and osmotic stress.



Other RcsB induced genes coding for protective proteins are listed below.

KatE
  • Codes for a subunit of heme d synthase / hydroperoxidase. This bacterial catalase protects against osmotic stress.


Host Defence:

Humans synthesise a number of enzymes that are able to burst bacterial cells. These enzymes are called lysosymes. RcsB is able to induce a number of proteins that act as lysosyme inhibitors that will prevent the host-mediated lysis of our chassis.


ivy (Inhibitor of Vertebrate lysozyme)
  • Discovered in 2001 as the first bacterial lysozyme inhibitor. This Type-C lysozyme inhibitor resides in the periplasm.1
MilC (Membrane-bound lysozyme inhibitor of Type C lysozyme)
  • This is a lipoprotein that resides in the membrane. 1



Global Regulators:






Repression:

RcsB is also is able to act as a repressor, preventing the expression of both curli and fimbriae. This reduces cell motility and plays a role in biofilm formation.







References

1) [http://www.ncbi.nlm.nih.gov/pubmed/19136591 The Rcs two-component system regulates expression of lysozyme inhibitors and is induced by exposure to lysozyme]

2) [http://www.ncbi.nlm.nih.gov/pubmed/19346340 Gene Expression Induced in Escherichia coli O157:H7 upon Exposure to Model Apple Juice]

3) [http://www.ncbi.nlm.nih.gov/pubmed/14627744 Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC.]

4) [http://www.ncbi.nlm.nih.gov/pubmed/16153174?ordinalpos=5&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_DefaultReportPanel.Pubmed_RVDocSum The Rcs phosphorelay: a complex signal transduction system.]


Interactive Image References

Note, interactive operons are credited to EcoCyc: Nucleic Acids Research 37:D464-70 2009

Arifuzzama06: "Large-scale identification of protein-protein interaction of Escherichia coli K-12." Genome Res 16(5);686-91. PMID: 16606699

Boulanger05: "Multistress regulation in Escherichia coli: expression of osmB involves two independent promoters responding either to sigmaS or to the RcsCDB His-Asp phosphorelay." J Bacteriol 187(9);3282-6. PMID: 15838058

Brill88: "Fine-structure mapping and identification of two regulators of capsule synthesis in Escherichia coli K-12." J Bacteriol 1988;170(6);2599-611. PMID: 2836365

Carballes99: "Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB." Mol Microbiol 1999;34(3);442-50. PMID: 10564486

CastanieCo06: "RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli." J Bacteriol 188(12);4264-70. PMID: 16740933

CastanieCo07: "The glutamate-dependent acid resistance system in Escherichia coli: essential and dual role of the His-Asp phosphorelay RcsCDB/AF." Microbiology 153(Pt 1);238-46. PMID: 17185552

Chen01c: "Characterization of the RcsC-->YojN-->RcsB phosphorelay signaling pathway involved in capsular synthesis in Escherichia coli." Biosci Biotechnol Biochem 65(10);2364-7. PMID: 11758943

Corbett08: "Capsular polysaccharides in Escherichia coli." Adv Appl Microbiol 65;1-26. PMID: 19026860

DavalosGar01: "Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli." J Bacteriol 183(20);5870-6. PMID: 11566985

Dierksen96: "Identification of a second RcsA protein, a positive regulator of colanic acid capsular polysaccharide genes, in Escherichia coli." J Bacteriol 178(16);5053-6. PMID: 8759878

Dominguez01: "Leishmania immune adherence reaction in vertebrates." Parasite Immunol 23(5);259-65. PMID: 11309136

Ebel99: "Escherichia coli RcsA, a positive activator of colanic acid capsular polysaccharide synthesis, functions to activate its own expression." J Bacteriol 1999;181(2);577-84. PMID: 9882673

Ferrieres07: "The yjbEFGH locus in Escherichia coli K-12 is an operon encoding proteins involved in exopolysaccharide production." Microbiology 153(Pt 4);1070-80. PMID: 17379715

FrancezCha03: Francez-Charlot A, Laugel B, Van Gemert A, Dubarry N, Wiorowski F, Castani?-Cornet MP, Gutierrez C, Cam K (2003). "RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli." Mol Microbiol 49(3);823-32. PMID: 12864862

FrancezCha05: Francez-Charlot A, Castanie-Cornet MP, Gutierrez C, Cam K (2005). "Osmotic Regulation of the Escherichia coli bdm (Biofilm-Dependent Modulation) Gene by the RcsCDB His-Asp Phosphorelay." J Bacteriol 187(11);3873-7. PMID: 15901715

Fredericks06: Fredericks CE, Shibata S, Aizawa S, Reimann SA, Wolfe AJ (2006). "Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay." Mol Microbiol 61(3);734-47. PMID: 16776655

Gervais92: Gervais FG, Phoenix P, Drapeau GR (1992). "The rcsB gene, a positive regulator of colanic acid biosynthesis in Escherichia coli, is also an activator of ftsZ expression." J Bacteriol 1992;174(12);3964-71. PMID: 1597415

GOA00: GOA (2000). "Gene Ontology annotation based on Swiss-Prot keyword mapping."

GOA01: GOA, DDB, FB, MGI, ZFIN (2001). "Gene Ontology annotation through association of InterPro records with GO terms."

Gottesman85: Gottesman S, Trisler P, Torres-Cabassa A (1985). "Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes." J Bacteriol 162(3);1111-9. PMID: 3888955

Gottesman91: Gottesman S, Stout V (1991). "Regulation of capsular polysaccharide synthesis in Escherichia coli K12." Mol Microbiol 1991;5(7);1599-606. PMID: 1943696

Gupte97: Gupte G, Woodward C, Stout V (1997). "Isolation and characterization of rcsB mutations that affect colanic acid capsule synthesis in Escherichia coli K-12." J Bacteriol 1997;179(13);4328-35. PMID: 9209051

Hirakawa03: Hirakawa H, Nishino K, Hirata T, Yamaguchi A (2003). "Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli." J Bacteriol 185(6);1851-6. PMID: 12618449

Huang06a: Huang YH, Ferrieres L, Clarke DJ (2006). "The role of the Rcs phosphorelay in Enterobacteriaceae." Res Microbiol 157(3);206-12. PMID: 16427772

Jayaratne93: Jayaratne P, Keenleyside WJ, MacLachlan PR, Dodgson C, Whitfield C (1993). "Characterization of rcsB and rcsC from Escherichia coli O9:K30:H12 and examination of the role of the rcs regulatory system in expression of group I capsular polysaccharides." J Bacteriol 1993;175(17);5384-94. PMID: 8366025

Kuo04: Kuo MS, Chen KP, Wu WF (2004). "Regulation of RcsA by the ClpYQ (HslUV) protease in Escherichia coli." Microbiology 150(Pt 2);437-46. PMID: 14766922

Lee03b: Lee YY, Chang CF, Kuo CL, Chen MC, Yu CH, Lin PI, Wu WF (2003). "Subunit oligomerization and substrate recognition of the Escherichia coli ClpYQ (HslUV) protease implicated by in vivo protein-protein interactions in the yeast two-hybrid system." J Bacteriol 185(8);2393-401. PMID: 12670962

Majdalani02: Majdalani N, Hernandez D, Gottesman S (2002). "Regulation and mode of action of the second small RNA activator of RpoS translation, RprA." Mol Microbiol 46(3);813-26. PMID: 12410838

Majdalani05: Majdalani N, Gottesman S (2005). "The Rcs phosphorelay: a complex signal transduction system." Annu Rev Microbiol 59;379-405. PMID: 16153174

Majdalani05b: Majdalani N, Heck M, Stout V, Gottesman S (2005). "Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli." J Bacteriol 187(19);6770-8. PMID: 16166540

Mouslim03: Mouslim C, Latifi T, Groisman EA (2003). "Signal-dependent requirement for the co-activator protein RcsA in transcription of the RcsB-regulated ugd gene." J Biol Chem 278(50);50588-95. PMID: 14514676

Ogasawara07a: Ogasawara H, Hasegawa A, Kanda E, Miki T, Yamamoto K, Ishihama A (2007). "Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade." J Bacteriol 189(13);4791-9. PMID: 17468243

Pao95: Pao GM, Saier MH (1995). "Response regulators of bacterial signal transduction systems: selective domain shuffling during evolution." J Mol Evol 1995;40(2);136-54. PMID: 7699720

Parkinson92: Parkinson JS, Kofoid EC (1992). "Communication modules in bacterial signaling proteins." Annu Rev Genet 1992;26;71-112. PMID: 1482126

Parkinson93: Parkinson JS (1993). "Signal transduction schemes of bacteria." Cell 1993;73(5);857-71. PMID: 8098993

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