Determination of the order of mutational sites governing l-arabinose utilization in Escherichia coli by transduction with phage P1bt

Gross, Jürgen H.; Englesberg, Ellis

doi:10.1016/0042-6822(59)90125-4

Cited by 125 publications

(84 citation statements)

References 15 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…AraC was first identified in 1959 by virtue of the requirement of araC for the metabolism of L-arabinose (2) and is the first-described positive regulator of transcription (3,4). E. coli AraC activates transcription of the araBAD, araFGH, araE, and araJ transcripts in the presence of its inducer, L-arabinose (5).…”

mentioning

confidence: 99%

Genome-Scale Analyses of Escherichia coli and Salmonella enterica AraC Reveal Noncanonical Targets and an Expanded Core Regulon

et al. 2014

View full text Add to dashboard Cite

c Escherichia coli AraC is a well-described transcription activator of genes involved in arabinose metabolism. Using complementary genomic approaches, chromatin immunoprecipitation (ChIP)-chip, and transcription profiling, we identify direct regulatory targets of AraC, including five novel target genes: ytfQ, ydeN, ydeM, ygeA, and polB. Strikingly, only ytfQ has an established connection to arabinose metabolism, suggesting that AraC has a broader function than previously described. We demonstrate arabinose-dependent repression of ydeNM by AraC, in contrast to the well-described arabinose-dependent activation of other target genes. We also demonstrate unexpected read-through of transcription at the Rho-independent terminators downstream of araD and araE, leading to significant increases in the expression of polB and ygeA, respectively. AraC is highly conserved in the related species Salmonella enterica. We use ChIP sequencing (ChIP-seq) and RNA sequencing (RNA-seq) to map the AraC regulon in S. enterica. A comparison of the E. coli and S. enterica AraC regulons, coupled with a bioinformatic analysis of other related species, reveals a conserved regulatory network across the family Enterobacteriaceae comprised of 10 genes associated with arabinose transport and metabolism.

show abstract

mentioning

confidence: 99%

Genome-Scale Analyses of Escherichia coli and Salmonella enterica AraC Reveal Noncanonical Targets and an Expanded Core Regulon

et al. 2014

View full text Add to dashboard Cite

show abstract

“…L-Ribulose-5-phosphate and D-xylulose-5-phosphate are substrates for the pentose phosphate pathway, which produces glycolytic intermediates ( Figure S2). L-Arabinose isomerase, ribulokinase, and L-ribulose-5-phosphate-4-epimerase are encoded by the araA, araB, and araD genes, respectively (Englesberg 1961;Englesberg et al 1962), arranged in a single transcriptional unit, the araBAD operon (Gross and Englesberg 1959;Englesberg 1961;Englesberg et al 1962;Lee et al 1984). Expression of the araBAD operon and the araE gene is induced by L-arabinose (Lee et al 1980(Lee et al , 1982 and requires the transcriptional regulator AraC (Englesberg et al 1965;Lee et al 1981).…”

mentioning

confidence: 99%

Virulence Gene Regulation by l-Arabinose in Salmonella enterica

López‐Garrido

Puerta-Fernández

Cota³

et al. 2015

Genetics

View full text Add to dashboard Cite

Invasion of the intestinal epithelium is a critical step in Salmonella enterica infection and requires functions encoded in the gene cluster known as Salmonella Pathogenicity Island 1 (SPI-1). Expression of SPI-1 genes is repressed by L-arabinose, and not by other pentoses. Transport of L-arabinose is necessary to repress SPI-1; however, repression is independent of L-arabinose metabolism and of the L-arabinose-responsive regulator AraC. SPI-1 repression by L-arabinose is exerted at a single target, HilD, and the mechanism appears to be post-translational. As a consequence of SPI-1 repression, L-arabinose reduces translocation of SPI-1 effectors to epithelial cells and decreases Salmonella invasion in vitro. These observations reveal a hitherto unknown role of L-arabinose in gene expression control and raise the possibility that Salmonella may use L-arabinose as an environmental signal.KEYWORDS Salmonella pathogenicity island 1; Salmonella invasion; L-arabinose; HilD I NVASION of epithelial cells by Salmonella enterica requires the expression of genes located in a 40-kb region known as Salmonella pathogenicity island 1 (SPI-1) (Lostroh and Lee 2001;Altier 2005;Jones 2005). SPI-1 is a cluster of 40 genes organized in several transcriptional units that encodes a Type 3 Secretion System (TTSS) and effector proteins that are translocated into epithelial cells (Lostroh and Lee 2001). Inside the epithelial cell, the effector proteins trigger cytoskeleton rearrangements necessary for Salmonella invasion (Darwin and Miller 1999a). SPI-1 also encodes transcriptional activators responsible for its own expression: HilA, HilC, HilD, and InvF (Lostroh and Lee 2001;Ellermeier and Slauch 2007). HilA is a transcriptional activator of the OmpR/ToxR family (Lee et al. 1992;Bajaj et al. 1995) and activates transcription of genes encoding components of the TTSS and the transcriptional activator InvF (Bajaj et al. 1996). In association with the SicA chaperone, InvF boosts transcription of the sicA/sip operon, which encodes effector proteins (Darwin and Miller 1999b;Eichelberg and Galan 1999). Transcription of hilA is directly activated by HilC and HilD, both members of the AraC/XylS family of transcriptional regulators (Schechter and Lee 2001). HilC and HilD relieve repression of the hilA promoter by the nucleoid proteins H-NS and Hha (Olekhnovich and Kadner 2006) and can activate expression of the invF and sicA/sip transcriptional units independently of HilA (Rakeman et al. 1999;Akbar et al. 2003). Furthermore, HilD activates transcription of hilC and of hilD itself (Ellermeier et al. 2005) by direct binding to both promoters (Olekhnovich and Kadner 2002). Together with a transcriptional activator encoded outside SPI-1, RtsA (Ellermeier and Slauch 2003), SPI-1 transcription factors form a regulatory network that governs SPI-1 expression in response to environmental and physiological factors (Supporting Information, Figure S1) (Jones 2005;Ellermeier and Slauch 2007).During passage through the digestive tract, Salmonella en...

show abstract

“…Englesberg, who had a great interest in carbohydrate metabolism, was no novice at bacterial genetics, having done his Ph.D. with Roger Stanier at Berkeley on inducible enzyme formation. In 1959, while at the Long Island Biological Laboratories in Cold Spring Harbor, New York, he collaborated with graduate student Julian Gross on the genetics of arabinose utilization (Gross and Englesberg 1959). According to Englesberg, "we picked the arabinose system to test the operon theory and negative control because it was completely different from the lactose operon, not because we had some insight into whether it would be under positive or negative control" (Fogle 1991, p. 68).…”

mentioning

confidence: 99%

Ellis Englesberg and the Discovery of Positive Control in Gene Regulation

Hahn

2014

Genetics

View full text Add to dashboard Cite

Based on his work with the Escherichia coli L-arabinose operon, Ellis Englesberg proposed in 1965 that the regulatory gene araC was an "activator gene" required for positive control of the ara operon. This challenged the widely held belief in a universal mechanism of negative regulation proposed earlier by Jacob and Monod. For years, Englesberg's model was met with deep skepticism. Despite much frustration with complex ad hoc explanations used to challenge his model, Englesberg persisted until the evidence for positive control in ara and other systems became overwhelming. Englesberg's pioneering work enriched the original operon model and had a lasting impact in opening new and exciting ways of thinking about transcriptional regulation. ELLIS Englesberg was one of the pioneers in deciphering mechanisms of gene regulation (Figure 1). In 1965, Englesberg and colleagues Joseph Irr, Joseph Power, and Nancy Lee published an article now widely recognized as a landmark in understanding the mechanisms of transcriptional control (Englesberg et al. 1965). Examining regulation of the L-arabinose (ara) operon in Escherichia coli, their work led them to conclude that the regulatory gene araC is a new type of gene, termed an "activator gene," that has a positive role in expression of the structural genes of the ara operon. They noted that their results were "in sharp contrast to the negative or repressor control" mechanism of Jacob and Monod as exemplified in the bacterial b-galactosidase (lac) operon and bacteriophage lambda. Today, the logic of Englesberg's 1965 approach and the interpretation of his experiments demonstrating positive control seem elegant and clear-cut. However, the reaction of the molecular biology community at the time was one of deep skepticism, and resulted in both scientific and personal criticism of Englesberg until the early 1970s. Englesberg did not wither under this criticism, but persisted until evidence for positive control from ara and other unrelated systems was so overwhelming that it could not be dismissed.Today we believe that positive control is probably the most widely used mechanism to regulate transcription in all forms of life and plays key roles in fundamental processes such as cell-type specificity, cell growth, development, and stress response. Significantly, when altered or misexpressed, transcription activator proteins can cause many human diseases. To understand why Englesberg's pioneering work was so important in opening new ways of thinking about gene regulation, we first need to revisit the thinking of the field in 1965 and how his work overturned a key aspect of a widely accepted and highly influential paradigm.After the discovery of DNA structure by Watson and Crick, arguably the next most influential work in 20th century molecular biology was the operon model of gene regulation proposed by Jacob and Monod. In 1961, they summarized their revolutionary work conducted over the preceding decade . Importantly, they also outlined the methodology and logic they developed f...

show abstract

Determination of the order of mutational sites governing l-arabinose utilization in Escherichia coli by transduction with phage P1bt

Cited by 125 publications

References 15 publications

Genome-Scale Analyses of Escherichia coli and Salmonella enterica AraC Reveal Noncanonical Targets and an Expanded Core Regulon

Genome-Scale Analyses of Escherichia coli and Salmonella enterica AraC Reveal Noncanonical Targets and an Expanded Core Regulon

Virulence Gene Regulation by l-Arabinose in Salmonella enterica

Ellis Englesberg and the Discovery of Positive Control in Gene Regulation

Contact Info

Product

Resources

About