Trp operon

Last updated
Structure of the trp operon Trpoperon.svg
Structure of the trp operon

The trp operon is a group of genes that are transcribed together, encoding the enzymes that produce the amino acid tryptophan in bacteria. The trp operon was first characterized in Escherichia coli, and it has since been discovered in many other bacteria. [1] The operon is regulated so that, when tryptophan is present in the environment, the genes for tryptophan synthesis are repressed.

Contents

The trp operon contains five structural genes: trpE, trpD, trpC, trpB, and trpA, which encode the enzymes needed to synthesize tryptophan. It also contains a repressive regulator gene called trpR. When tryptophan is present, the trpR protein binds to the operator, blocking transcription of the trp operon by RNA polymerase.

This operon is an example of repressible negative regulation of gene expression. The repressor protein binds to the operator in the presence of tryptophan (repressing transcription) and is released from the operon when tryptophan is absent (allowing transcription to proceed). The trp operon additionally uses attenuation to control expression of the operon, a second negative feedback control mechanism.

The trp operon is well-studied and is commonly used as an example of gene regulation in bacteria alongside the lac operon.

Genes

The composition of the genes within the trp operon among three specific bacterial species. Trp operon organization across three different bacterial species.png
The composition of the genes within the trp operon among three specific bacterial species.

trp operon contains five structural genes. The roles of their products are:

Reactions catalyzed by the enzymes synthesized from the trp operon. Tryptophan biosynthesis (en).svg
Reactions catalyzed by the enzymes synthesized from the trp operon.

Repression

Trp repressor dimer bound to operator DNA Trp repressor dimer and operator.png
Trp repressor dimer bound to operator DNA

The operon operates by a negative repressible feedback mechanism. The repressor for the trp operon is produced upstream by the trpR gene, which is constitutively expressed at a low level. Synthesized trpR monomers associate into dimers. When tryptophan is present, these tryptophan repressor dimers bind to tryptophan, causing a change in the repressor conformation, allowing the repressor to bind to the operator. This prevents RNA polymerase from binding to and transcribing the operon, so tryptophan is not produced from its precursor. When tryptophan is not present, the repressor is in its inactive conformation and cannot bind the operator region, so transcription is not inhibited by the repressor.

Attenuation

Mechanism of transcriptional attenuation of the trp operon. Trp operon attenuation.svg
Mechanism of transcriptional attenuation of the trp operon.

Attenuation is a second mechanism of negative feedback in the trp operon. The repression system targets the intracellular trp concentration whereas the attenuation responds to the concentration of charged tRNAtrp. [2] Thus, the trpR repressor decreases gene expression by altering the initiation of transcription, while attenuation does so by altering the process of transcription that's already in progress. [2] While the TrpR repressor decreases transcription by a factor of 70, attenuation can further decrease it by a factor of 10, thus allowing accumulated repression of about 700-fold. [3] Attenuation is made possible by the fact that in prokaryotes (which have no nucleus), the ribosomes begin translating the mRNA while RNA polymerase is still transcribing the DNA sequence. This allows the process of translation to affect transcription of the operon directly.

At the beginning of the transcribed genes of the trp operon is a sequence of at least 130 nucleotides termed the leader transcript (trpL; P0AD92 ). [4] Lee and Yanofsky (1977) found that the attenuation efficiency is correlated with the stability of a secondary structure embedded in trpL, [5] and the 2 constituent hairpins of the terminator structure were later elucidated by Oxender et al. (1979). [6] This transcript includes four short sequences designated 1–4, each of which is partially complementary to the next one. Thus, three distinct secondary structures (hairpins) can form: 1–2, 2–3 or 3–4. The hybridization of sequences 1 and 2 to form the 1–2 structure is rare because the RNA polymerase waits for a ribosome to attach before continuing transcription past sequence 1, however if the 1–2 hairpin were to form it would prevent the formation of the 2–3 structure (but not 3–4). The formation of a hairpin loop between sequences 2–3 prevents the formation of hairpin loops between both 1–2 and 3–4. The 3–4 structure is a transcription termination sequence (abundant in G/C and immediately followed by several uracil residues), once it forms RNA polymerase will disassociate from the DNA and transcription of the structural genes of the operon can not occur (see below for a more detailed explanation). The functional importance of the 2nd hairpin for the transcriptional termination is illustrated by the reduced transcription termination frequency observed in experiments destabilizing the central G+C pairing of this hairpin. [5] [7] [8] [9]

Part of the leader transcript codes for a short polypeptide of 14 amino acids, termed the leader peptide. This peptide contains two adjacent tryptophan residues, which is unusual, since tryptophan is a fairly uncommon amino acid (about one in a hundred residues in a typical E. coli protein is tryptophan). The strand 1 in trpL encompasses the region encoding the trailing residues of the leader peptide: Trp, Trp, Arg, Thr, Ser; [2] conservation is observed in these 5 codons whereas mutating the upstream codons do not alter the operon expression. [2] [10] [11] [12] If the ribosome attempts to translate this peptide while tryptophan levels in the cell are low, it will stall at either of the two trp codons. While it is stalled, the ribosome physically shields sequence 1 of the transcript, preventing the formation of the 1–2 secondary structure. Sequence 2 is then free to hybridize with sequence 3 to form the 2–3 structure, which then prevents the formation of the 3–4 termination hairpin, which is why the 2–3 structure is called an anti-termination hairpin. In the presence of the 2–3 structure, RNA polymerase is free to continue transcribing the operon. Mutational analysis and studies involving complementary oligonucleotides demonstrate that the stability of the 2–3 structure corresponds to the operon expression level. [10] [13] [14] [15] If tryptophan levels in the cell are high, the ribosome will translate the entire leader peptide without interruption and will only stall during translation termination at the stop codon. At this point the ribosome physically shields both sequences 1 and 2. Sequences 3 and 4 are thus free to form the 3–4 structure which terminates transcription. This terminator structure forms when no ribosome stalls in the vicinity of the Trp tandem (i.e. Trp or Arg codon): either the leader peptide is not translated or the translation proceeds smoothly along the strand 1 with abundant charged tRNAtrp. [2] [10] More over, the ribosome is proposed to only block about 10 nts downstream, thus ribosome stalling in either the upstream Gly or further downstream Thr do not seem to affect the formation of the termination hairpin. [2] [10] The end result is that the operon will be transcribed only when tryptophan is unavailable for the ribosome, while the trpL transcript is constitutively expressed.

This attenuation mechanism is experimentally supported. First, the translation of the leader peptide and ribosomal stalling are directly evidenced to be necessary for inhibiting the transcription termination. [13] Moreover, mutational analysis destabilizing or disrupting the base-pairing of the antiterminator hairpin results in increased termination of several folds; consistent with the attenuation model, this mutation fails to relieve attenuation even with starved Trp. [10] [13] In contrast, complementary oligonucleotides targeting strand 1 increases the operon expression by promoting the antiterminator formation. [10] [14] Furthermore, in histidine operon, compensatory mutation shows that the pairing ability of strands 2–3 matters more than their primary sequence in inhibiting attenuation. [10] [15]

In attenuation, where the translating ribosome is stalled determines whether the termination hairpin will be formed. [10] In order for the transcribing polymerase to concomitantly capture the alternative structure, the time scale of the structural modulation must be comparable to that of the transcription. [2] To ensure that the ribosome binds and begins translation of the leader transcript immediately following its synthesis, a pause site exists in the trpL sequence. Upon reaching this site, RNA polymerase pauses transcription and apparently waits for translation to begin. This mechanism allows for synchronization of transcription and translation, a key element in attenuation.

A similar attenuation mechanism regulates the synthesis of histidine, phenylalanine and threonine.

Regulation of trp operon in Bacillus subtilis

The arrangement of the trp operon in E. coli and Bacillus subtilis differs. There are 5 structural genes in E. coli that are found under a single transcriptional unit. In Bacillus subtilis, there are 6 structural genes that are situated within a supraoperon. Three of these genes are found upstream while the other three genes are found downstream of the trp operon. [16] There is a 7th gene in Bacillus subtilis's operon called trpG or pabA which is responsible for protein synthesis of tryptophan and folate. [17] Regulation of trp operons in both organisms depends on the amount of trp present in the cell. However, the primary regulation of tryptophan biosynthesis in B. subtilis is via attenuation, rather than repression, of transcription. [18] In B. subtilis, tryptophan binds to the eleven-subunit tryptophan-activated RNA-binding attenuation protein (TRAP), which activates TRAP's ability to bind to the trp leader RNA. [19] [20] Binding of trp-activated TRAP to leader RNA results in the formation of a terminator structure that causes transcription termination. [18] In addition, the activated TRAP inhibits the initiation of translation of trpP, trpE, trpG and ycbK genes. The gene trpP plays a role in trp transportation, while the gene trpG is utilized in the folate operon, and the gene ycbK is involved in synthesis of an efflux protein. The activated TRAP protein is regulated by an anti-TRAP protein and AT synthesis. AT can inactive TRAP to lower the transcription of tryptophan. [21]

Related Research Articles

<span class="mw-page-title-main">Lambda phage</span> Bacteriophage that infects Escherichia coli

Enterobacteria phage λ is a bacterial virus, or bacteriophage, that infects the bacterial species Escherichia coli. It was discovered by Esther Lederberg in 1950. The wild type of this virus has a temperate life cycle that allows it to either reside within the genome of its host through lysogeny or enter into a lytic phase, during which it kills and lyses the cell to produce offspring. Lambda strains, mutated at specific sites, are unable to lysogenize cells; instead, they grow and enter the lytic cycle after superinfecting an already lysogenized cell.

In genetics, an operon is a functioning unit of DNA containing a cluster of genes under the control of a single promoter. The genes are transcribed together into an mRNA strand and either translated together in the cytoplasm, or undergo splicing to create monocistronic mRNAs that are translated separately, i.e. several strands of mRNA that each encode a single gene product. The result of this is that the genes contained in the operon are either expressed together or not at all. Several genes must be co-transcribed to define an operon.

<span class="mw-page-title-main">Rho factor</span> Prokaryotic protein

A ρ factor is a bacterial protein involved in the termination of transcription. Rho factor binds to the transcription terminator pause site, an exposed region of single stranded RNA after the open reading frame at C-rich/G-poor sequences that lack obvious secondary structure.

<span class="mw-page-title-main">Tryptophan repressor</span> Transcription factor

Tryptophan repressor is a transcription factor involved in controlling amino acid metabolism. It has been best studied in Escherichia coli, where it is a dimeric protein that regulates transcription of the 5 genes in the tryptophan operon. When the amino acid tryptophan is plentiful in the cell, it binds to the protein, which causes a conformational change in the protein. The repressor complex then binds to its operator sequence in the genes it regulates, shutting off the genes.

Charles Yanofsky was an American geneticist on the faculty of Stanford University who contributed to the establishment of the one gene-one enzyme hypothesis and discovered attenuation, a riboswitch mechanism in which messenger RNA changes shape in response to a small molecule and thus alters its binding ability for the regulatory region of a gene or operon.

In molecular biology, a termination factor is a protein that mediates the termination of RNA transcription by recognizing a transcription terminator and causing the release of the newly made mRNA. This is part of the process that regulates the transcription of RNA to preserve gene expression integrity and are present in both eukaryotes and prokaryotes, although the process in bacteria is more widely understood. The most extensively studied and detailed transcriptional termination factor is the Rho (ρ) protein of E. coli.

Bacterial translation is the process by which messenger RNA is translated into proteins in bacteria.

In genetics, attenuation is a regulatory mechanism for some bacterial operons that results in premature termination of transcription. The canonical example of attenuation used in many introductory genetics textbooks, is ribosome-mediated attenuation of the trp operon. Ribosome-mediated attenuation of the trp operon relies on the fact that, in bacteria, transcription and translation proceed simultaneously. Attenuation involves a provisional stop signal (attenuator), located in the DNA segment that corresponds to the leader sequence of mRNA. During attenuation, the ribosome becomes stalled (delayed) in the attenuator region in the mRNA leader. Depending on the metabolic conditions, the attenuator either stops transcription at that point or allows read-through to the structural gene part of the mRNA and synthesis of the appropriate protein.

Gene structure is the organisation of specialised sequence elements within a gene. Genes contain most of the information necessary for living cells to survive and reproduce. In most organisms, genes are made of DNA, where the particular DNA sequence determines the function of the gene. A gene is transcribed (copied) from DNA into RNA, which can either be non-coding (ncRNA) with a direct function, or an intermediate messenger (mRNA) that is then translated into protein. Each of these steps is controlled by specific sequence elements, or regions, within the gene. Every gene, therefore, requires multiple sequence elements to be functional. This includes the sequence that actually encodes the functional protein or ncRNA, as well as multiple regulatory sequence regions. These regions may be as short as a few base pairs, up to many thousands of base pairs long.

<span class="mw-page-title-main">Amino acid synthesis</span> The set of biochemical processes by which amino acids are produced

Amino acid synthesis is the set of biochemical processes by which the amino acids are produced. The substrates for these processes are various compounds in the organism's diet or growth media. Not all organisms are able to synthesize all amino acids. For example, humans can synthesize 11 of the 20 standard amino acids. These 11 are called the non-essential amino acids).

<span class="mw-page-title-main">Tryptophan operon leader</span>

The Tryptophan operon leader is an RNA element found at the 5′ of some bacterial tryptophan operons. The leader sequence can form two different structures known as the terminator and the anti-terminator, based on the Tryptophan amounts in the cell. The leader also codes for very short peptide sequence that is rich in tryptophan. The terminator structure is recognised as a termination signal for RNA polymerase and the operon is not transcribed. This structure forms when the cell has an excess of tryptophan and ribosome movement over the leader transcript is not impeded. When there is a deficiency of the charged tryptophanyl tRNA the ribosome translating the leader peptide stalls and the antiterminator structure can form. This allows RNA polymerase to transcribe the operon.

<span class="mw-page-title-main">5S ribosomal RNA</span> RNA component of the large subunit of the ribosome

The 5S ribosomal RNA is an approximately 120 nucleotide-long ribosomal RNA molecule with a mass of 40 kDa. It is a structural and functional component of the large subunit of the ribosome in all domains of life, with the exception of mitochondrial ribosomes of fungi and animals. The designation 5S refers to the molecule's sedimentation velocity in an ultracentrifuge, which is measured in Svedberg units (S).

<span class="mw-page-title-main">Leucine operon leader</span>

The Leucine operon leader is an RNA element found upstream of the first gene in the Leucine biosynthetic operon. The leader sequence can assume two different secondary structures known as the terminator and the anti-terminator structure. The leader also codes for very short peptide sequence that is rich in leucine amino acid. The terminator structure is recognised as a termination signal for RNA polymerase and the operon is not transcribed. This structure forms when the cell has an excess of leucine and ribosome movement over the leader transcript is not impeded. When there is a deficiency of the charged leucyl tRNA the ribosome translating the leader peptide stalls and the antiterminator structure can form. This allows RNA polymerase to transcribe the operon. At least 6 amino acid operons are known to be regulated by attenuation.

<span class="mw-page-title-main">PreQ1 riboswitch</span>

The PreQ1-I riboswitch is a cis-acting element identified in bacteria which regulates expression of genes involved in biosynthesis of the nucleoside queuosine (Q) from GTP. PreQ1 (pre-queuosine1) is an intermediate in the queuosine pathway, and preQ1 riboswitch, as a type of riboswitch, is an RNA element that binds preQ1. The preQ1 riboswitch is distinguished by its unusually small aptamer, compared to other riboswitches. Its atomic-resolution three-dimensional structure has been determined, with the PDB ID 2L1V.

<span class="mw-page-title-main">Histidine operon leader</span>

The Histidine operon leader is an RNA element found in the bacterial histidine operon. At least 6 amino acid operons are known to be regulated by attenuation. In each a leader sequence of 150–200 bp is found upstream of the first gene in the operon. This leader sequence can assume two different secondary structures known as the terminator and the anti-terminator structure. In each case the leader also codes for very short peptide sequence that is rich in the end product amino acid of the operon. The terminator structure is recognised as a termination signal for RNA polymerase and the operon is not transcribed. This structure forms when the cell has an excess of the regulatory amino acid and ribosome movement over the leader transcript is not impeded. When there is a deficiency of the charged tRNA of the regulatory amino acid the ribosome translating the leader peptide stalls and the antiterminator structure can form. This allows RNA polymerase to transcribe the operon.

<span class="mw-page-title-main">Threonine operon leader</span>

The threonine operon leader is an RNA element. Threonine is one of at least 6 amino acid operons are known to be regulated by attenuation. In each a leader sequence of 150–200 bp is found upstream of the first gene in the operon. This leader sequence can assume two different secondary structures known as the terminator and the anti-terminator structure. In each case the leader also codes for very short peptide sequence that is rich in the end product amino acid of the operon. The terminator structure is recognised as a termination signal for RNA polymerase and the operon is not transcribed. This structure forms when the cell has an excess of the regulatory amino acid and ribosome movement over the leader transcript is not impeded. When there is a deficiency of the charged tRNA of the regulatory amino acid the ribosome translating the leader peptide stalls and the antiterminator structure can form. This allows RNA polymerase to transcribe the operon.

<span class="mw-page-title-main">Intrinsic termination</span>

Intrinsic, or rho-independent termination, is a process in prokaryotes to signal the end of transcription and release the newly constructed RNA molecule. In prokaryotes such as E. coli, transcription is terminated either by a rho-dependent process or rho-independent process. In the Rho-dependent process, the rho-protein locates and binds the signal sequence in the mRNA and signals for cleavage. Contrarily, intrinsic termination does not require a special protein to signal for termination and is controlled by the specific sequences of RNA. When the termination process begins, the transcribed mRNA forms a stable secondary structure hairpin loop, also known as a Stem-loop. This RNA hairpin is followed by multiple uracil nucleotides. The bonds between uracil and adenine are very weak. A protein bound to RNA polymerase (nusA) binds to the stem-loop structure tightly enough to cause the polymerase to temporarily stall. This pausing of the polymerase coincides with transcription of the poly-uracil sequence. The weak adenine-uracil bonds lower the energy of destabilization for the RNA-DNA duplex, allowing it to unwind and dissociate from the RNA polymerase. Overall, the modified RNA structure is what terminates transcription.

<span class="mw-page-title-main">Paul Babitzke</span>

Paul Babitzke is a Professor of Biochemistry and Molecular Biology and Director of the Center for RNA Molecular Biology at Pennsylvania State University.

Transcription-translation coupling is a mechanism of gene expression regulation in which synthesis of an mRNA (transcription) is affected by its concurrent decoding (translation). In prokaryotes, mRNAs are translated while they are transcribed. This allows communication between RNA polymerase, the multisubunit enzyme that catalyzes transcription, and the ribosome, which catalyzes translation. Coupling involves both direct physical interactions between RNA polymerase and the ribosome, as well as ribosome-induced changes to the structure and accessibility of the intervening mRNA that affect transcription.

Catherine Louise Kearney Squires was a microbiologist known for her work on ribosomal RNA using Escherichia coli as a model organism. She was an elected fellow of the American Academy of Microbiology and the American Association for the Advancement of Science.

References

  1. ↑ Merino, Enrique; Jensen, Roy A; Yanofsky, Charles (April 2008). "Evolution of bacterial trp operons and their regulation". Current Opinion in Microbiology. 11 (2): 78–86. doi:10.1016/j.mib.2008.02.005. ISSN   1369-5274. PMC   2387123 . PMID   18374625.
  2. 1 2 3 4 5 6 7 Yanofsky C (February 1981). "Attenuation in the control of expression of bacterial operons". Nature. 289 (5800): 751–8. Bibcode:1981Natur.289..751Y. doi:10.1038/289751a0. PMID   7007895. S2CID   4364204.
  3. ↑ Lehninger AL, Nelson DL, Cox MM (2008). Principles of Biochemistry (5th ed.). New York, NY: W.H. Freeman and Company. p.  1128. ISBN   978-0-7167-7108-1.
  4. ↑ Bertrand K, Squires C, Yanofsky C (May 1976). "Transcription termination in vivo in the leader region of the tryptophan operon of Escherichia coli". Journal of Molecular Biology. 103 (2): 319–37. doi:10.1016/0022-2836(76)90315-6. PMID   781269.
  5. 1 2 Lee F, Yanofsky C (October 1977). "Transcription termination at the trp operon attenuators of Escherichia coli and Salmonella typhimurium: RNA secondary structure and regulation of termination". Proceedings of the National Academy of Sciences of the United States of America. 74 (10): 4365–9. Bibcode:1977PNAS...74.4365L. doi: 10.1073/pnas.74.10.4365 . PMC   431942 . PMID   337297.
  6. ↑ Oxender DL, Zurawski G, Yanofsky C (November 1979). "Attenuation in the Escherichia coli tryptophan operon: role of RNA secondary structure involving the tryptophan codon region". Proceedings of the National Academy of Sciences of the United States of America. 76 (11): 5524–8. Bibcode:1979PNAS...76.5524O. doi: 10.1073/pnas.76.11.5524 . PMC   411681 . PMID   118451.
  7. ↑ Stroynowski I, Yanofsky C (July 1982). "Transcript secondary structures regulate transcription termination at the attenuator of S. marcescens tryptophan operon". Nature. 298 (5869): 34–8. Bibcode:1982Natur.298...34S. doi:10.1038/298034a0. PMID   7045685. S2CID   4347442.
  8. ↑ Zurawski G, Yanofsky C (September 1980). "Escherichia coli tryptophan operon leader mutations, which relieve transcription termination, are cis-dominant to trp leader mutations, which increase transcription termination". Journal of Molecular Biology. 142 (1): 123–9. doi:10.1016/0022-2836(80)90210-7. PMID   6159477.
  9. ↑ Stauffer GV, Zurawski G, Yanofsky C (October 1978). "Single base-pair alterations in the Escherichia coli trp operon leader region that relieve transcription termination at the trp attenuator". Proceedings of the National Academy of Sciences of the United States of America. 75 (10): 4833–7. Bibcode:1978PNAS...75.4833S. doi: 10.1073/pnas.75.10.4833 . PMC   336215 . PMID   368800.
  10. 1 2 3 4 5 6 7 8 Kolter R, Yanofsky C (1982). "Attenuation in amino acid biosynthetic operons". Annual Review of Genetics. 16: 113–34. doi:10.1146/annurev.ge.16.120182.000553. PMID   6186194.
  11. ↑ Lee F, Bertrand K, Bennett G, Yanofsky C (May 1978). "Comparison of the nucleotide sequences of the initial transcribed regions of the tryptophan operons of Escherichia coli and Salmonella typhimurium". Journal of Molecular Biology. 121 (2): 193–217. doi:10.1016/s0022-2836(78)80005-9. PMID   351195.
  12. ↑ Miozzari G, Yanofsky C (November 1978). "Naturally occurring promoter down mutation: nucleotide sequence of the trp promoter/operator/leader region of Shigella dysenteriae 16". Proceedings of the National Academy of Sciences of the United States of America. 75 (11): 5580–4. Bibcode:1978PNAS...75.5580M. doi: 10.1073/pnas.75.11.5580 . PMC   393010 . PMID   364484.
  13. 1 2 3 Zurawski G, Elseviers D, Stauffer GV, Yanofsky C (December 1978). "Translational control of transcription termination at the attenuator of the Escherichia coli tryptophan operon". Proceedings of the National Academy of Sciences of the United States of America. 75 (12): 5988–92. Bibcode:1978PNAS...75.5988Z. doi: 10.1073/pnas.75.12.5988 . PMC   393102 . PMID   366606.
  14. 1 2 Winkler ME, Mullis K, Barnett J, Stroynowski I, Yanofsky C (April 1982). "Transcription termination at the tryptophan operon attenuator is decreased in vitro by an oligomer complementary to a segment of the leader transcript". Proceedings of the National Academy of Sciences of the United States of America. 79 (7): 2181–5. Bibcode:1982PNAS...79.2181W. doi: 10.1073/pnas.79.7.2181 . PMC   346154 . PMID   6179092.
  15. 1 2 Johnston HM, Roth JR (February 1981). "DNA sequence changes of mutations altering attenuation control of the histidine operon of Salmonella typhimurium". Journal of Molecular Biology. 145 (4): 735–56. doi:10.1016/0022-2836(81)90312-0. PMID   6167727.
  16. ↑ Yanofsky, Charles (2004). "The different roles of tryptophan transfer RNA in regulating trp operon expression in E. coli versus B. subtilis". Trends in Genetics. 20 (8): 367–374. doi:10.1016/j.tig.2004.06.007.
  17. ↑ Yang, Wen-Jen; Yanofsky, Charles (2005-03-15). "Effects of Tryptophan Starvation on Levels of the trp RNA-Binding Attenuation Protein (TRAP) and Anti-TRAP Regulatory Protein and Their Influence on trp Operon Expression in Bacillus subtilis". Journal of Bacteriology. 187 (6): 1884–1891. doi:10.1128/JB.187.6.1884-1891.2005. ISSN   0021-9193. PMC   1064063 . PMID   15743934.
  18. 1 2 Gollnick P, Babitzke P, Antson A, Yanofsky C (2005-11-14). "Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis". Annual Review of Genetics. 39 (1): 47–68. doi:10.1146/annurev.genet.39.073003.093745. PMID   16285852.
  19. ↑ Elliott MB, Gottlieb PA, Gollnick P (January 2001). "The mechanism of RNA binding to TRAP: initiation and cooperative interactions". RNA. 7 (1): 85–93. doi:10.1017/S135583820100173X. PMC   1370072 . PMID   11214184.
  20. ↑ Antson AA, Otridge J, Brzozowski AM, Dodson EJ, Dodson GG, Wilson KS, et al. (April 1995). "The structure of trp RNA-binding attenuation protein". Nature. 374 (6524): 693–700. Bibcode:1995Natur.374..693A. doi:10.1038/374693a0. PMID   7715723. S2CID   4340136.
  21. ↑ Cruz-Vera, Luis R.; Gong, Ming; Yanofsky, Charles (2008-03-15). "Physiological Effects of Anti-TRAP Protein Activity and tRNA Trp Charging on trp Operon Expression in Bacillus subtilis". Journal of Bacteriology. 190 (6): 1937–1945. doi:10.1128/JB.01820-07. ISSN   0021-9193. PMC   2258860 . PMID   18178730.

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.