Biomolecular Systems Engineering: Unlocking the Potential of Engineered Allostery via the Lactose Repressor Topology

Literature Cited

1. 1. 

   Ahmed MH, Ghatge MS, Safo MK. 2020. Hemoglobin: structure, function and allostery. Subcell Biochem 94:345–82
   [Google Scholar]
2. 2. 

   Alon U. 2007. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8:450–61
   [Google Scholar]
3. 3. 

   Aoki SK, Lillacci G, Gupta A, Baumschlager A, Schweingruber D, Khammash M. 2019. A universal biomolecular integral feedback controller for robust perfect adaptation. Nature 570:533–37
   [Google Scholar]
4. 4. 

   Bell CE, Lewis M. 2000. A closer view of the conformation of the Lac repressor bound to operator. Nat. Struct. Biol. 7:209–14
   [Google Scholar]
5. 5. 

   Cameron DE, Bashor CJ, Collins JJ. 2014. A brief history of synthetic biology. Nat. Rev. Microbiol. 12:381–90
   [Google Scholar]
6. 6. 

   Chan CTY, Lee JW, Cameron DE, Bashor CJ, Collins JJ. 2016.. “ Deadman” and “Passcode” microbial kill switches for bacterial containment. Nat. Chem. Biol. 12:82–86
   [Google Scholar]
7. 7. 

   Chen J, Matthews KS. 1994. Subunit dissociation affects DNA binding in a dimeric lac repressor produced by C-terminal deletion. Biochemistry 33:8728–35
   [Google Scholar]
8. 8. 

   Chen J, Surendran R, Lee JC, Matthews KS. 1994. Construction of a dimeric repressor: dissection of subunit interfaces in Lac repressor. Biochemistry 33:1234–41
   [Google Scholar]
9. 9. 

   Chen Y, Ho JML, Shis DL, Gupta C, Long J et al. 2018. Tuning the dynamic range of bacterial promoters regulated by ligand-inducible transcription factors. Nat. Commun. 9:64
   [Google Scholar]
10. 10. 

    Choi KR, Jang WD, Yang D, Cho JS, Park D, Lee SY 2019. Systems metabolic engineering strategies: integrating systems and synthetic biology with metabolic engineering. Trends Biotechnol 37:817–37
    [Google Scholar]
11. 11. 

    Courtney TM, Deiters A. 2019. Enzyme allostery: now controllable by light. Cell Chem. Biol. 26:1481–83
    [Google Scholar]
12. 12. 

    Coyote-Maestas W, He Y, Myers CL, Schmidt D. 2019. Domain insertion permissibility-guided engineering of allostery in ion channels. Nat. Commun. 10:290
    [Google Scholar]
13. 13. 

    Daber R, Lewis M. 2009. A novel molecular switch. J. Mol. Biol. 391:661–70
    [Google Scholar]
14. 14. 

    Daber R, Sharp K, Lewis M. 2009. One is not enough. J. Mol. Biol. 392:1133–44
    [Google Scholar]
15. 15. 

    Daber R, Stayrook S, Rosenberg A, Lewis M. 2007. Structural analysis of lac repressor bound to allosteric effectors. J. Mol. Biol. 370:609–19
    [Google Scholar]
16. 16. 

    Dahiyat BI, Mayo SL. 1997. De novo protein design: fully automated sequence selection. Science 278:82–87
    [Google Scholar]
17. 17. 

    Elowitz MB, Leibler S. 2000. A synthetic oscillatory network of transcriptional regulators. Nature 403:335–38
    [Google Scholar]
18. 18. 

    Flynn TC, Swint-Kruse L, Kong Y, Booth C, Matthews KS, Ma J. 2003. Allosteric transition pathways in the lactose repressor protein core domains: asymmetric motions in a homodimer. Protein Sci 12:2523–41
    [Google Scholar]
19. 19. 

    Friedman AM, Fischmann TO, Steitz TA. 1995. Crystal structure of lac repressor core tetramer and its implications for DNA looping. Science 268:1721–27
    [Google Scholar]
20. 20. 

    Gordley RM, Bugaj LJ, Lim WA. 2016. Modular engineering of cellular signaling proteins and networks. Curr. Opin. Struct. Biol. 39:106–14
    [Google Scholar]
21. 21. 

    Groseclose TM, Rondon RE, Herde ZD, Aldrete CA, Wilson CJ. 2020. Engineered systems of inducible anti-repressors for the next generation of biological programming. Nat. Commun. 11:4440
    [Google Scholar]
22. 22. 

    Guet CC, Elowitz MB, Hsing W, Leibler S. 2002. Combinatorial synthesis of genetic networks. Science 296:1466–70
    [Google Scholar]
23. 23. 

    Hasty J, Dolnik M, Rottschäfer V, Collins JJ. 2002. Synthetic gene network for entraining and amplifying cellular oscillations. Phys. Rev. Lett. 88:148101
    [Google Scholar]
24. 24. 

    Hooshangi S, Thiberge S, Weiss R. 2005. Ultrasensitivity and noise propagation in a synthetic transcriptional cascade. PNAS 102:3581–86
    [Google Scholar]
25. 25. 

    Howell SC, Inampudi KK, Bean DP, Wilson CJ. 2014. Understanding thermal adaptation of enzymes through the multistate rational design and stability prediction of 100 adenylate kinases. Structure 22:218–29
    [Google Scholar]
26. 26. 

    Huang PS, Boyken SE, Baker D. 2016. The coming of age of de novo protein design. Nature 537:320–27
    [Google Scholar]
27. 27. 

    Kelly JR, Rubin AJ, Davis JH, Ajo-Franklin CM, Cumbers J et al. 2009. Measuring the activity of BioBrick promoters using an in vivo reference standard. J. Biol. Eng. 3:4
    [Google Scholar]
28. 28. 

    Khalil AS, Collins JJ. 2010. Synthetic biology: applications come of age. Nat. Rev. Genet. 11:367–79
    [Google Scholar]
29. 29. 

    Lee J, Natarajan M, Nashine VC, Socolich M, Vo T et al. 2008. Surface sites for engineering allosteric control in proteins. Science 322:438–42
    [Google Scholar]
30. 30. 

    Lewis M, Chang G, Horton NC, Kercher MA, Pace HC et al. 1996. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271:1247–54
    [Google Scholar]
31. 31. 

    Lim WA. 2010. Designing customized cell signalling circuits. Nat. Rev. Mol. Cell Biol. 11:393–403
    [Google Scholar]
32. 32. 

    Lim WA, June CH. 2017. The principles of engineering immune cells to treat cancer. Cell 168:724–40
    [Google Scholar]
33. 33. 

    Lockless SW, Ranganathan R. 1999. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286:295–99
    [Google Scholar]
34. 34. 

    Ma CW, Xiu ZL, Zeng AP. 2015. Exploring signal transduction in heteromultimeric protein based on energy dissipation model. J. Biomol. Struct. Dyn. 33:134–46
    [Google Scholar]
35. 35. 

    Meinhardt S, Manley MW Jr., Becker NA, Hessman JA, Maher LJ 3rd, Swint-Kruse L 2012. Novel insights from hybrid LacI/GalR proteins: family-wide functional attributes and biologically significant variation in transcription repression. Nucleic Acids Res 40:11139–54
    [Google Scholar]
36. 36. 

    Meyer S, Ramot R, Kishore Inampudi K, Luo B, Lin C et al. 2013. Engineering alternate cooperative-communications in the lactose repressor protein scaffold. Protein Eng. Des. Sel. 26:433–43
    [Google Scholar]
37. 37. 

    Michalodimitrakis K, Isalan M. 2009. Engineering prokaryotic gene circuits. FEMS Microbiol. Rev. 33:27–37
    [Google Scholar]
38. 38. 

    Milk L, Daber R, Lewis M 2010. Functional rules for lac repressor–operator associations and implications for protein–DNA interactions. Protein Sci 19:1162–72
    [Google Scholar]
39. 39. 

    Miller JP, Melicher MS, Schepartz A. 2014. Positive allostery in metal ion binding by a cooperatively folded β-peptide bundle. J. Am. Chem. Soc. 136:14726–29
    [Google Scholar]
40. 40. 

    Monod J, Changeux JP, Jacob F 1963. Allosteric proteins and cellular control systems. J. Mol. Biol. 6:306–29
    [Google Scholar]
41. 41. 

    Monod J, Wyman J, Changeux JP. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88–118
    [Google Scholar]
42. 42. 

    Motlagh HN, Wrabl JO, Li J, Hilser VJ. 2014. The ensemble nature of allostery. Nature 508:331–39
    [Google Scholar]
43. 43. 

    Mukhopadhyay A, Redding AM, Rutherford BJ, Keasling JD. 2008. Importance of systems biology in engineering microbes for biofuel production. Curr. Opin. Biotechnol. 19:228–34
    [Google Scholar]
44. 44. 

    Nielsen AAK, Der BS, Shin J, Vaidyanathan P, Paralanov V et al. 2016. Genetic circuit design automation. Science 352:aac7341
    [Google Scholar]
45. 45. 

    Nielsen J, Keasling JD. 2016. Engineering cellular metabolism. Cell 164:1185–97
    [Google Scholar]
46. 46. 

    Nussinov R, Tsai CJ, Xin F, Radivojac P. 2012. Allosteric post-translational modification codes. Trends Biochem. Sci. 37:447–55
    [Google Scholar]
47. 47. 

    Poelwijk FJ, de Vos MGJ, Tans SJ. 2011. Tradeoffs and optimality in the evolution of gene regulation. Cell 146:462–70
    [Google Scholar]
48. 48. 

    Popovych N, Sun S, Ebright RH, Kalodimos CG. 2006. Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 13:831–38
    [Google Scholar]
49. 49. 

    Purnick PE, Weiss R. 2009. The second wave of synthetic biology: from modules to systems. Nat. Rev. Mol. Cell Biol. 10:410–22
    [Google Scholar]
50. 50. 

    Raman AS, White KI, Ranganathan R. 2016. Origins of allostery and evolvability in proteins: a case study. Cell 166:468–80
    [Google Scholar]
51. 51. 

    Richards DH, Meyer S, Wilson CJ. 2017. Fourteen ways to reroute cooperative communications in the lactose repressor: engineering regulatory proteins with alternate repressive functions. ACS Synth. Biol. 6:6–12
    [Google Scholar]
52. 52. 

    Rondon RE, Groseclose TM, Short AE, Wilson CJ. 2019. Transcriptional programming using engineered systems of transcription factors and genetic architectures. Nat. Commun. 10:4784
    [Google Scholar]
53. 53. 

    Rondon RE, Wilson CJ. 2019. Engineering a new class of anti-LacI transcription factors with alternate DNA recognition. ACS Synth. Biol. 8:307–17
    [Google Scholar]
54. 54. 

    Saibil HR, Fenton WA, Clare DK, Horwich AL. 2013. Structure and allostery of the chaperonin GroEL. J. Mol. Biol. 425:1476–87
    [Google Scholar]
55. 55. 

    Sartorius J, Lehming N, Kisters B, von Wilcken-Bergmann B, Müller-Hill B. 1989. lac repressor mutants with double or triple exchanges in the recognition helix bind specifically to lac operator variants with multiple exchanges. EMBO J 8:1265–70
    [Google Scholar]
56. 56. 

    Shis DL, Hussain F, Meinhardt S, Swint-Kruse L, Bennett MR. 2014. Modular, multi-input transcriptional logic gating with orthogonal LacI/GalR family chimeras. ACS Synth. Biol. 3:645–51
    [Google Scholar]
57. 57. 

    Siuti P, Yazbek J, Lu TK. 2013. Synthetic circuits integrating logic and memory in living cells. Nat. Biotechnol. 31:448–52
    [Google Scholar]
58. 58. 

    Sousa FL, Parente DJ, Shis DL, Hessman JA, Chazelle A et al. 2016. AlloRep: a repository of sequence, structural and mutagenesis data for the LacI/GalR transcription regulators. J. Mol. Biol. 428:671–78
    [Google Scholar]
59. 59. 

    Stock G, Hamm P. 2018. A non-equilibrium approach to allosteric communication. Phil. Trans. R. Soc. Lond. B 373:0187
    [Google Scholar]
60. 60. 

    Suckow J, Markiewicz P, Kleina LG, Miller J, Kisters-Woike B, Müller-Hill B. 1996. Genetic studies of the Lac repressor. XV: 4000 single amino acid substitutions and analysis of the resulting phenotypes on the basis of the protein structure. J. Mol. Biol. 261:509–23
    [Google Scholar]
61. 61. 

    Süel GM, Lockless SW, Wall MA, Ranganathan R. 2003. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 10:59–69
    [Google Scholar]
62. 62. 

    Swint-Kruse L, Matthews KS. 2009. Allostery in the LacI/GalR family: variations on a theme. Curr. Opin. Microbiol. 12:129–37
    [Google Scholar]
63. 63. 

    Tamsir A, Tabor JJ, Voigt CA. 2011. Robust multicellular computing using genetically encoded NOR gates and chemical “wires. .” Nature 469:212–15
    [Google Scholar]
64. 64. 

    Taylor ND, Garruss AS, Moretti R, Chan S, Arbing MA et al. 2016. Engineering an allosteric transcription factor to respond to new ligands. Nat. Methods 13:177–83
    [Google Scholar]
65. 65. 

    Tobin PH, Richards DH, Callender RA, Wilson CJ. 2014. Protein engineering: a new frontier for biological therapeutics. Curr. Drug Metab. 15:743–56
    [Google Scholar]
66. 66. 

    Voigt CA. 2006. Genetic parts to program bacteria. Curr. Opin. Biotechnol. 17:548–57
    [Google Scholar]
67. 67. 

    Wehrs M, Tanjore D, Eng T, Lievense J, Pray TR, Mukhopadhyay A. 2019. Engineering robust production microbes for large-scale cultivation. Trends Microbiol 27:524–37
    [Google Scholar]
68. 68. 

    Wilson CJ, Das P, Clementi C, Matthews KS, Wittung-Stafshede P 2005. The experimental folding landscape of monomeric lactose repressor, a large two-domain protein, involves two kinetic intermediates. PNAS 102:14563–68
    [Google Scholar]
69. 69. 

    Wilson CJ, Zhan H, Swint-Kruse L, Matthews KS. 2007. The lactose repressor system: paradigms for regulation, allosteric behavior and protein folding. Cell Mol. Life Sci. 64:3–16
    [Google Scholar]
70. 70. 

    Wilson CJ, Zhan H, Swint-Kruse L, Matthews KS. 2007. Ligand interactions with lactose repressor protein and the repressor–operator complex: the effects of ionization and oligomerization on binding. Biophys. Chem. 126:94–105
    [Google Scholar]
71. 71. 

    Wodak SJ, Paci E, Dokholyan NV, Berezovsky IN, Horovitz A et al. 2019. Allostery in its many disguises: from theory to applications. Structure 27:566–78
    [Google Scholar]
72. 72. 

    Woolston BM, Edgar S, Stephanopoulos G. 2013. Metabolic engineering: past and future. Annu. Rev. Chem. Biomol. Eng. 4:259–88
    [Google Scholar]
73. 73. 

    Wright PE, Dyson HJ. 2015. Intrinsically disordered proteins in cellular signalling and regulation. Nat. Rev. Mol. Cell Biol. 16:18–29
    [Google Scholar]
74. 74. 

    Zhan J, Ding B, Ma R, Ma X, Su X et al. 2010. Develop reusable and combinable designs for transcriptional logic gates. Mol. Syst. Biol. 6:388
    [Google Scholar]