Display options
Cite
Taggart JC, Lalanne JB, Li GW. Quantitative Control for Stoichiometric Protein Synthesis. Annu Rev Microbiol. 2021;75:243-267doi: 10.1146/annurev-micro-041921-012646.
Taggart, J. C., Lalanne, J. B., & Li, G. W. (2021). Quantitative Control for Stoichiometric Protein Synthesis. Annual review of microbiology, 75243-267. https://doi.org/10.1146/annurev-micro-041921-012646
Taggart, James C, et al. "Quantitative Control for Stoichiometric Protein Synthesis." Annual review of microbiology vol. 75 (2021): 243-267. doi: https://doi.org/10.1146/annurev-micro-041921-012646
Taggart JC, Lalanne JB, Li GW. Quantitative Control for Stoichiometric Protein Synthesis. Annu Rev Microbiol. 2021 Oct 08;75:243-267. doi: 10.1146/annurev-micro-041921-012646. Epub 2021 Aug 03. PMID: 34343023; PMCID: PMC8720029.
Copy Download .nbib Format: NLM
Share it on

Annu Rev Microbiol. 2021 Oct 08;75:243-267. doi: 10.1146/annurev-micro-041921-012646. Epub 2021 Aug 03.

Quantitative Control for Stoichiometric Protein Synthesis.

Annual review of microbiology

James C Taggart, Jean-Benoît Lalanne, Gene-Wei Li

Affiliations

  1. Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA; email: [email protected], [email protected].
  2. Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
  3. Current affiliation: Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA; email: [email protected].

PMID: 34343023 PMCID: PMC8720029 DOI: 10.1146/annurev-micro-041921-012646

Abstract

Bacterial protein synthesis rates have evolved to maintain preferred stoichiometries at striking precision, from the components of protein complexes to constituents of entire pathways. Setting relative protein production rates to be well within a factor of two requires concerted tuning of transcription, RNA turnover, and translation, allowing many potential regulatory strategies to achieve the preferred output. The last decade has seen a greatly expanded capacity for precise interrogation of each step of the central dogma genome-wide. Here, we summarize how these technologies have shaped the current understanding of diverse bacterial regulatory architectures underpinning stoichiometric protein synthesis. We focus on the emerging expanded view of bacterial operons, which encode diverse primary and secondary mRNA structures for tuning protein stoichiometry. Emphasis is placed on how quantitative tuning is achieved. We discuss the challenges and open questions in the application of quantitative, genome-wide methodologies to the problem of precise protein production.

Keywords: differential RNA stability; differential translation; expression stoichiometry; operon mRNA isoform; proportional synthesis

References

  1. Elife. 2020 Sep 23;9: - PubMed
  2. Nat Rev Genet. 2020 Oct;21(10):630-644 - PubMed
  3. Mol Cell. 2017 Jan 5;65(1):39-51 - PubMed
  4. J Biol Chem. 2015 Apr 10;290(15):9478-86 - PubMed
  5. Cell Syst. 2018 Dec 26;7(6):580-589.e4 - PubMed
  6. Genes Dev. 2012 Dec 15;26(24):2696-708 - PubMed
  7. Mol Cell. 2019 Apr 18;74(2):284-295.e5 - PubMed
  8. J Bacteriol. 2011 Nov;193(22):6384-6 - PubMed
  9. Proc Natl Acad Sci U S A. 2016 Jan 19;113(3):602-7 - PubMed
  10. Cell Syst. 2020 Feb 26;10(2):125-132 - PubMed
  11. RNA. 2021 Apr 29;: - PubMed
  12. Annu Rev Genet. 2014;48:537-59 - PubMed
  13. Nature. 1995 Mar 16;374(6519):287-90 - PubMed
  14. Synth Biol (Oxf). 2019 Oct 29;4(1):ysz026 - PubMed
  15. Nature. 2010 Mar 11;464(7286):250-5 - PubMed
  16. PLoS One. 2009 Oct 19;4(10):e7526 - PubMed
  17. Nat Commun. 2020 Sep 24;11(1):4827 - PubMed
  18. J Bacteriol. 1985 Sep;163(3):991-9 - PubMed
  19. Nat Microbiol. 2020 Aug;5(8):995-1001 - PubMed
  20. Curr Opin Genet Dev. 2005 Apr;15(2):116-24 - PubMed
  21. Mol Cell. 2018 Jun 7;70(5):785-799 - PubMed
  22. Genome Res. 2020 May;30(5):711-723 - PubMed
  23. Mol Cell. 2018 Jun 7;70(5):894-905.e5 - PubMed
  24. PLoS Comput Biol. 2019 Feb 4;15(2):e1006226 - PubMed
  25. Mol Cell. 2017 Jul 6;67(1):44-54.e6 - PubMed
  26. Trends Genet. 1990 Mar;6(3):78-85 - PubMed
  27. Biochemistry. 2019 Mar 19;58(11):1539-1551 - PubMed
  28. Cell. 2001 Nov 16;107(4):437-49 - PubMed
  29. Proc Natl Acad Sci U S A. 1959 Oct;45(10):1453-61 - PubMed
  30. Nucleic Acids Res. 2017 May 19;45(9):5437-5448 - PubMed
  31. J Bacteriol. 2012 Nov;194(22):6233-9 - PubMed
  32. J Mol Biol. 1992 Apr 20;224(4):949-66 - PubMed
  33. Elife. 2017 May 12;6: - PubMed
  34. J Mol Biol. 1992 Aug 5;226(3):581-96 - PubMed
  35. Elife. 2019 Feb 06;8: - PubMed
  36. Nat Commun. 2019 Jan 8;10(1):68 - PubMed
  37. Mol Cell. 2017 Jan 19;65(2):207-219 - PubMed
  38. J Mol Biol. 1996 Aug 2;260(5):649-63 - PubMed
  39. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2307-11 - PubMed
  40. Nucleic Acids Res. 2016 Apr 7;44(6):2554-63 - PubMed
  41. Nat Rev Genet. 2020 Nov;21(11):699-714 - PubMed
  42. Elife. 2016 May 20;5: - PubMed
  43. Nat Microbiol. 2016 Jan 11;1:15007 - PubMed
  44. Nat Rev Mol Cell Biol. 2015 Nov;16(11):651-64 - PubMed
  45. Science. 2009 Nov 27;326(5957):1268-71 - PubMed
  46. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5439-43 - PubMed
  47. J Mol Biol. 2003 Aug 29;331(5):981-9 - PubMed
  48. Cell Syst. 2019 Mar 27;8(3):212-225.e9 - PubMed
  49. Elife. 2020 Sep 21;9: - PubMed
  50. Structure. 2011 Sep 7;19(9):1252-61 - PubMed
  51. Annu Rev Biochem. 2016 Jun 2;85:319-47 - PubMed
  52. Cell Rep. 2013 Sep 12;4(5):938-44 - PubMed
  53. Crit Rev Biochem Mol Biol. 2019 Jun;54(3):242-300 - PubMed
  54. Cell. 2013 Apr 11;153(2):426-37 - PubMed
  55. Cell. 1982 Oct;30(3):865-71 - PubMed
  56. BMC Genomics. 2013 Jul 30;14:520 - PubMed
  57. Annu Rev Microbiol. 2016 Sep 8;70:25-44 - PubMed
  58. Mol Cell. 2015 Dec 17;60(6):953-65 - PubMed
  59. EMBO J. 2009 Nov 18;28(22):3523-33 - PubMed
  60. Nat Commun. 2019 Dec 4;10(1):5536 - PubMed
  61. Nature. 1986 Jul 17-23;322(6076):273-5 - PubMed
  62. Nat Biotechnol. 2018 Nov;36(10):1005-1015 - PubMed
  63. Annu Rev Genomics Hum Genet. 2019 Aug 31;20:99-127 - PubMed
  64. Proc Natl Acad Sci U S A. 2018 Jun 12;115(24):E5585-E5594 - PubMed
  65. J Mol Biol. 1968 Feb 14;31(3):519-40 - PubMed
  66. J Bacteriol. 2013 May;195(10):2340-8 - PubMed
  67. Genes Dev. 1999 Sep 15;13(18):2449-61 - PubMed
  68. Mol Syst Biol. 2019 Aug;15(8):e8875 - PubMed
  69. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342-6 - PubMed
  70. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2516-20 - PubMed
  71. J Am Chem Soc. 2016 Jun 8;138(22):7016-23 - PubMed
  72. Cell. 2018 Mar 22;173(1):181-195.e18 - PubMed
  73. Mol Cell. 2011 Sep 16;43(6):940-9 - PubMed
  74. Science. 2009 Apr 10;324(5924):218-23 - PubMed
  75. Mol Syst Biol. 2015 Jan 12;11(1):781 - PubMed
  76. Proc Natl Acad Sci U S A. 2018 May 22;115(21):E4796-E4805 - PubMed
  77. J Mol Biol. 1961 Jun;3:318-56 - PubMed
  78. Cell Syst. 2016 Dec 21;3(6):563-571.e6 - PubMed
  79. PLoS One. 2012;7(11):e48542 - PubMed
  80. Sci STKE. 2003 Jun 03;2003(185):pe22 - PubMed
  81. PLoS Genet. 2018 Apr 18;14(4):e1007354 - PubMed
  82. Nucleic Acids Res. 1996 Aug 1;24(15):3065-70 - PubMed
  83. Genome Res. 2005 Jun;15(6):809-19 - PubMed
  84. J Biol Chem. 1994 Apr 8;269(14):10790-6 - PubMed
  85. Nature. 2014 Jan 30;505(7485):701-5 - PubMed
  86. Mol Syst Biol. 2021 Apr;17(4):e10302 - PubMed
  87. Cell. 2018 Apr 19;173(3):749-761.e38 - PubMed
  88. Mol Cell. 2001 Jan;7(1):185-92 - PubMed
  89. Science. 2016 Oct 28;354(6311): - PubMed
  90. PLoS Genet. 2012;8(3):e1002520 - PubMed
  91. Annu Rev Genet. 2015;49:367-94 - PubMed
  92. PLoS One. 2010 Dec 31;5(12):e15628 - PubMed
  93. Nat Commun. 2018 Sep 10;9(1):3676 - PubMed
  94. Nucleic Acids Res. 2016 Apr 20;44(7):3373-89 - PubMed
  95. mBio. 2014 Jul 08;5(4):e01442-14 - PubMed
  96. J Mol Biol. 1977 Jul;114(1):1-21 - PubMed
  97. Cell Syst. 2020 Aug 26;11(2):121-130.e6 - PubMed
  98. Nat Commun. 2020 Jun 29;11(1):3268 - PubMed
  99. Mol Microbiol. 2011 Sep;81(6):1459-73 - PubMed
  100. Nucleic Acids Res. 1993 Sep 25;21(19):4599-603 - PubMed
  101. Science. 2003 May 2;300(5620):801-5 - PubMed
  102. Nat Biotechnol. 2009 Nov;27(11):1043-9 - PubMed
  103. Proc Natl Acad Sci U S A. 2013 May 28;110(22):8864-9 - PubMed
  104. PLoS Genet. 2014 Jul 31;10(7):e1004463 - PubMed
  105. Annu Rev Genet. 2011;45:61-79 - PubMed
  106. Nucleic Acids Res. 2014 Oct;42(18):11733-51 - PubMed
  107. Nat Rev Genet. 2020 Apr;21(4):227-242 - PubMed
  108. Science. 2009 Apr 10;324(5924):255-8 - PubMed
  109. Elife. 2018 Dec 20;7: - PubMed
  110. Nat Methods. 2013 Jul;10(7):659-64 - PubMed
  111. Mol Syst Biol. 2019 May 3;15(5):e8719 - PubMed
  112. Biochim Biophys Acta Gene Regul Mech. 2020 May;1863(5):194505 - PubMed
  113. Methods Enzymol. 2018;612:361-391 - PubMed
  114. Cell Rep. 2018 Aug 14;24(7):1890-1901.e8 - PubMed
  115. Mol Microbiol. 2012 Sep;85(5):817-32 - PubMed
  116. Nucleic Acids Res. 2017 Jun 2;45(10):5980-5994 - PubMed
  117. PLoS Genet. 2015 Oct 16;11(10):e1005577 - PubMed
  118. Elife. 2017 Jan 31;6: - PubMed
  119. Nucleic Acids Res. 2014 Oct;42(18):11383-92 - PubMed
  120. PLoS Genet. 2011 Jun;7(6):e1002155 - PubMed
  121. Curr Opin Microbiol. 2007 Jun;10(3):271-8 - PubMed
  122. Cell. 1983 Feb;32(2):335-49 - PubMed
  123. Curr Opin Microbiol. 2015 Feb;23:133-40 - PubMed
  124. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 - PubMed
  125. Metab Eng. 2020 Nov;62:10-19 - PubMed
  126. J Mol Biol. 2011 Feb 11;406(1):29-43 - PubMed
  127. Science. 2003 Jun 13;300(5626):1718-22 - PubMed
  128. Mol Cell. 2009 Jul 31;35(2):247-53 - PubMed
  129. Nucleic Acids Res. 1985 Oct 25;13(20):7307-26 - PubMed
  130. Mol Microbiol. 2016 Jan;99(2):425-37 - PubMed
  131. Nat Methods. 2013 Apr;10(4):354-60 - PubMed
  132. Nucleic Acids Res. 1990 Apr 11;18(7):1725-9 - PubMed
  133. Nucleic Acids Res. 2011 Apr;39(8):3188-203 - PubMed
  134. Mol Cell. 2018 Oct 18;72(2):275-285.e4 - PubMed
  135. Mol Syst Biol. 2013 Jun 18;9:675 - PubMed
  136. Trends Biochem Sci. 2020 Jan;45(1):42-57 - PubMed
  137. Annu Rev Genet. 1996;30:507-28 - PubMed
  138. J Bacteriol. 2006 Jul;188(14):5145-52 - PubMed
  139. Nat Microbiol. 2016 Dec 12;2:16231 - PubMed
  140. Elife. 2020 Feb 17;9: - PubMed
  141. Science. 2012 Nov 23;338(6110):1088-93 - PubMed
  142. Nat Commun. 2020 Mar 27;11(1):1587 - PubMed
  143. Science. 2013 Oct 25;342(6157):475-9 - PubMed
  144. Proc Natl Acad Sci U S A. 1990 May;87(10):3713-7 - PubMed
  145. Nucleic Acids Res. 2013 May;41(9):5139-48 - PubMed
  146. Nucleic Acids Res. 2012 Oct;40(18):8979-92 - PubMed
  147. Annu Rev Biochem. 1984;53:75-117 - PubMed
  148. Microbiology (Reading). 1997 Jun;143 ( Pt 6):2071-2078 - PubMed
  149. Cell. 2019 Sep 19;179(1):106-119.e16 - PubMed
  150. Nature. 1968 Oct 26;220(5165):345-50 - PubMed
  151. Nature. 2020 Sep;585(7823):124-128 - PubMed
  152. Nature. 2016 Jan 21;529(7586):358-363 - PubMed
  153. Front Microbiol. 2015 Jul 02;6:636 - PubMed
  154. mBio. 2018 Sep 11;9(5): - PubMed
  155. PLoS One. 2013;8(1):e54062 - PubMed
  156. FEMS Microbiol Lett. 2013 Jul;344(2):104-13 - PubMed
  157. Sci Prog. 2006;89(Pt 3-4):151-66 - PubMed
  158. Nat Commun. 2019 Dec 18;10(1):5774 - PubMed
  159. Mol Cell Proteomics. 2009 Jun;8(6):1350-60 - PubMed
  160. J Mol Biol. 2019 Sep 20;431(20):4040-4066 - PubMed
  161. Cell. 2014 Apr 24;157(3):624-35 - PubMed
  162. J Mol Biol. 1966 Dec 28;22(2):235-47 - PubMed
  163. Gigascience. 2020 Feb 1;9(2): - PubMed
  164. Elife. 2021 Apr 09;10: - PubMed
  165. J Biol Chem. 1978 Mar 10;253(5):1738-42 - PubMed
  166. Genes Cells. 2005 Jul;10(7):733-41 - PubMed
  167. Nat Microbiol. 2019 Nov;4(11):1907-1918 - PubMed
  168. Nature. 2016 Sep 14;537(7620):347-55 - PubMed
  169. Biochem Biophys Res Commun. 1962 Jun 4;7:419-24 - PubMed
  170. Cell. 2010 Apr 16;141(2):344-54 - PubMed
  171. PLoS Comput Biol. 2012;8(12):e1002811 - PubMed
  172. Proc Natl Acad Sci U S A. 2010 May 18;107(20):9158-63 - PubMed
  173. Nat Chem Biol. 2005 Aug;1(3):159-66 - PubMed
  174. Cell. 2014 Nov 20;159(5):1200-1211 - PubMed
  175. PLoS Genet. 2015 Oct 23;11(10):e1005613 - PubMed
  176. J Mol Biol. 2004 Dec 3;344(4):965-76 - PubMed
  177. Science. 1963 Oct 25;142(3591):493-7 - PubMed
  178. Nature. 2008 Jan 17;451(7176):355-8 - PubMed
  179. J Bacteriol. 1987 Jun;169(6):2872-5 - PubMed
  180. Science. 2016 Apr 8;352(6282):aad9822 - PubMed
  181. Cell. 2016 Aug 25;166(5):1282-1294.e18 - PubMed
  182. Cell. 1978 Mar;13(3):427-34 - PubMed
  183. Cell. 2016 Jun 2;165(6):1493-1506 - PubMed
  184. Science. 2015 Nov 6;350(6261):678-80 - PubMed
  185. Curr Opin Microbiol. 2015 Apr;24:66-71 - PubMed

Publication Types

Grant support