5hzh › Citations

Engineering extrinsic disorder to control protein activity in living cells.

Dagliyan O, Tarnawski M, Chu PH, Shirvanyants D, Schlichting I, Dokholyan NV, Hahn KM
Science 354 1441-1444 (2016)
Related entries: 5hzi, 5hzj, 5hzk

Cited: 102 times
EuropePMC logo PMID: 27980211

Abstract

Optogenetic and chemogenetic control of proteins has revealed otherwise inaccessible facets of signaling dynamics. Here, we use light- or ligand-sensitive domains to modulate the structural disorder of diverse proteins, thereby generating robust allosteric switches. Sensory domains were inserted into nonconserved, surface-exposed loops that were tight and identified computationally as allosterically coupled to active sites. Allosteric switches introduced into motility signaling proteins (kinases, guanosine triphosphatases, and guanine exchange factors) controlled conversion between conformations closely resembling natural active and inactive states, as well as modulated the morphodynamics of living cells. Our results illustrate a broadly applicable approach to design physiological protein switches.

Articles - 5hzh mentioned but not cited (1)

  1. Engineering extrinsic disorder to control protein activity in living cells. Dagliyan O, Tarnawski M, Chu PH, Shirvanyants D, Schlichting I, Dokholyan NV, Hahn KM. Science 354 1441-1444 (2016)


Reviews citing this publication (37)

  1. Advances in protein structure prediction and design. Kuhlman B, Bradley P. Nat Rev Mol Cell Biol 20 681-697 (2019)
  2. Allostery in Its Many Disguises: From Theory to Applications. Wodak SJ, Paci E, Dokholyan NV, Berezovsky IN, Horovitz A, Li J, Hilser VJ, Bahar I, Karanicolas J, Stock G, Hamm P, Stote RH, Eberhardt J, Chebaro Y, Dejaegere A, Cecchini M, Changeux JP, Bolhuis PG, Vreede J, Faccioli P, Orioli S, Ravasio R, Yan L, Brito C, Wyart M, Gkeka P, Rivalta I, Palermo G, McCammon JA, Panecka-Hofman J, Wade RC, Di Pizio A, Niv MY, Nussinov R, Tsai CJ, Jang H, Padhorny D, Kozakov D, McLeish T. Structure 27 566-578 (2019)
  3. Blue-Light Receptors for Optogenetics. Losi A, Gardner KH, Möglich A. Chem Rev 118 10659-10709 (2018)
  4. Optogenetically controlled protein kinases for regulation of cellular signaling. Leopold AV, Chernov KG, Verkhusha VV. Chem Soc Rev 47 2454-2484 (2018)
  5. A bright future: optogenetics to dissect the spatiotemporal control of cell behavior. Goglia AG, Toettcher JE. Curr Opin Chem Biol 48 106-113 (2019)
  6. Optophysiology: Illuminating cell physiology with optogenetics. Tan P, He L, Huang Y, Zhou Y. Physiol Rev 102 1263-1325 (2022)
  7. Engineering genetically-encoded tools for optogenetic control of protein activity. Liu Q, Liu Q, Tucker CL. Curr Opin Chem Biol 40 17-23 (2017)
  8. Biomechanical Contributions to Macrophage Activation in the Tumor Microenvironment. Hoffmann EJ, Ponik SM. Front Oncol 10 787 (2020)
  9. Engineered control of enzyme structural dynamics and function. Boehr DD, D'Amico RN, O'Rourke KF. Protein Sci 27 825-838 (2018)
  10. Unleashing the Power of Bond Cleavage Chemistry in Living Systems. Wang J, Wang X, Fan X, Chen PR. ACS Cent Sci 7 929-943 (2021)
  11. CRAC channel-based optogenetics. Nguyen NT, Ma G, Lin E, D'Souza B, Jing J, He L, Huang Y, Zhou Y. Cell Calcium 75 79-88 (2018)
  12. Signaling, Deconstructed: Using Optogenetics to Dissect and Direct Information Flow in Biological Systems. Farahani PE, Reed EH, Underhill EJ, Aoki K, Toettcher JE. Annu Rev Biomed Eng 23 61-87 (2021)
  13. Controlling protein conformation with light. Dagliyan O, Hahn KM. Curr Opin Struct Biol 57 17-22 (2019)
  14. Lights, cytoskeleton, action: Optogenetic control of cell dynamics. Wittmann T, Dema A, van Haren J. Curr Opin Cell Biol 66 1-10 (2020)
  15. Engineering an Allosteric Control of Protein Function. Vishweshwaraiah YL, Chen J, Dokholyan NV. J Phys Chem B 125 1806-1814 (2021)
  16. Experimentally-driven protein structure modeling. Dokholyan NV. J Proteomics 220 103777 (2020)
  17. New approaches for solving old problems in neuronal protein trafficking. Bourke AM, Bowen AB, Kennedy MJ. Mol Cell Neurosci 91 48-66 (2018)
  18. Lighting the way: Recent insights into the structure and regulation of phototropin blue light receptors. Hart JE, Gardner KH. J Biol Chem 296 100594 (2021)
  19. Optogenetic Modulation of Intracellular Signalling and Transcription: Focus on Neuronal Plasticity. Eleftheriou C, Cesca F, Maragliano L, Benfenati F, Maya-Vetencourt JF. J Exp Neurosci 11 1179069517703354 (2017)
  20. Self-Referential Encoding on Modules of Anticodon Pairs-Roots of the Biological Flow System. Cardoso Guimarães R. Life (Basel) 7 E16 (2017)
  21. Optogenetics for transcriptional programming and genetic engineering. Lan TH, He L, Huang Y, Zhou Y. Trends Genet 38 1253-1270 (2022)
  22. Approaches to Manipulate Ephrin-A:EphA Forward Signaling Pathway. Baudet S, Bécret J, Nicol X. Pharmaceuticals (Basel) 13 E140 (2020)
  23. A guide to the optogenetic regulation of endogenous molecules. Manoilov KY, Verkhusha VV, Shcherbakova DM. Nat Methods 18 1027-1037 (2021)
  24. Optically inducible membrane recruitment and signaling systems. Hannanta-Anan P, Glantz ST, Chow BY. Curr Opin Struct Biol 57 84-92 (2019)
  25. Plant Synthetic Biology: Quantifying the "Known Unknowns" and Discovering the "Unknown Unknowns". Wright RC, Nemhauser J. Plant Physiol 179 885-893 (2019)
  26. Nanoscale programming of cellular and physiological phenotypes: inorganic meets organic programming. Dokholyan NV. NPJ Syst Biol Appl 7 15 (2021)
  27. Advances, Perspectives and Potential Engineering Strategies of Light-Gated Phosphodiesterases for Optogenetic Applications. Tian Y, Yang S, Gao S. Int J Mol Sci 21 E7544 (2020)
  28. Induction of Signal Transduction by Using Non-Channelrhodopsin-Type Optogenetic Tools. Ueda Y, Sato M. Chembiochem 19 1217-1231 (2018)
  29. A light way for nuclear cell biologists. Forlani G, Di Ventura B. J Biochem 169 273-286 (2021)
  30. Design and engineering of allosteric communications in proteins. Chen J, Vishweshwaraiah YL, Dokholyan NV. Curr Opin Struct Biol 73 102334 (2022)
  31. Molecular perturbation strategies to examine spatiotemporal features of Rho GEF and Rho GTPase activity in living cells. Goedhart J, van Unen J. Small GTPases 10 178-186 (2019)
  32. Optogenetic Techniques for Manipulating and Sensing G Protein-Coupled Receptor Signaling. Abreu N, Levitz J. Methods Mol Biol 2173 21-51 (2020)
  33. Optogenetics: The Art of Illuminating Complex Signaling Pathways. Shaaya M, Fauser J, Karginov AV. Physiology (Bethesda) 36 52-60 (2021)
  34. Why Proteins are Big: Length Scale Effects on Equilibria and Kinetics. Rubinson KA. Protein J 38 95-119 (2019)
  35. Dual Systems for Enhancing Control of Protein Activity through Induced Dimerization Approaches. Pearce S, Tucker CL. Adv Biol (Weinh) 5 e2000234 (2021)
  36. Light-regulated gene expression in Bacteria: Fundamentals, advances, and perspectives. Ohlendorf R, Möglich A. Front Bioeng Biotechnol 10 1029403 (2022)
  37. Engineering Light-Control in Biology. Baumschlager A. Front Bioeng Biotechnol 10 901300 (2022)

Articles citing this publication (64)

  1. Engineered anti-CRISPR proteins for optogenetic control of CRISPR-Cas9. Bubeck F, Hoffmann MD, Harteveld Z, Aschenbrenner S, Bietz A, Waldhauer MC, Börner K, Fakhiri J, Schmelas C, Dietz L, Grimm D, Correia BE, Eils R, Niopek D. Nat Methods 15 924-927 (2018)
  2. Optical control of cell signaling by single-chain photoswitchable kinases. Zhou XX, Zhou XX, Fan LZ, Li P, Shen K, Lin MZ. Science 355 836-842 (2017)
  3. Mapping allosteric communications within individual proteins. Wang J, Jain A, McDonald LR, Gambogi C, Lee AL, Dokholyan NV. Nat Commun 11 3862 (2020)
  4. Optogenetic control of protein binding using light-switchable nanobodies. Gil AA, Carrasco-López C, Zhu L, Zhao EM, Ravindran PT, Wilson MZ, Goglia AG, Avalos JL, Toettcher JE. Nat Commun 11 4044 (2020)
  5. Computational design of chemogenetic and optogenetic split proteins. Dagliyan O, Krokhotin A, Ozkan-Dagliyan I, Deiters A, Der CJ, Hahn KM, Dokholyan NV. Nat Commun 9 4042 (2018)
  6. Local control of intracellular microtubule dynamics by EB1 photodissociation. van Haren J, Charafeddine RA, Ettinger A, Wang H, Hahn KM, Wittmann T. Nat Cell Biol 20 252-261 (2018)
  7. Encoding optical control in LCK kinase to quantitatively investigate its activity in live cells. Liaunardy-Jopeace A, Murton BL, Mahesh M, Chin JW, James JR. Nat Struct Mol Biol 24 1155-1163 (2017)
  8. Engineering a far-red light-activated split-Cas9 system for remote-controlled genome editing of internal organs and tumors. Yu Y, Wu X, Guan N, Shao J, Li H, Chen Y, Ping Y, Li D, Ye H. Sci Adv 6 eabb1777 (2020)
  9. Spatiotemporal dynamics of GEF-H1 activation controlled by microtubule- and Src-mediated pathways. Azoitei ML, Noh J, Marston DJ, Roudot P, Marshall CB, Daugird TA, Lisanza SL, Sandí MJ, Ikura M, Sondek J, Rottapel R, Hahn KM, Danuser G. J Cell Biol 218 3077-3097 (2019)
  10. Engineering proteins for allosteric control by light or ligands. Dagliyan O, Dokholyan NV, Hahn KM. Nat Protoc 14 1863-1883 (2019)
  11. A viral fusogen hijacks the actin cytoskeleton to drive cell-cell fusion. Chan KMC, Son S, Schmid EM, Fletcher DA. Elife 9 e51358 (2020)
  12. RecV recombinase system for in vivo targeted optogenomic modifications of single cells or cell populations. Yao S, Yuan P, Ouellette B, Zhou T, Mortrud M, Balaram P, Chatterjee S, Wang Y, Daigle TL, Tasic B, Kuang X, Gong H, Luo Q, Zeng S, Curtright A, Dhaka A, Kahan A, Gradinaru V, Chrapkiewicz R, Schnitzer M, Zeng H, Cetin A. Nat Methods 17 422-429 (2020)
  13. Optogenetic control of cofilin and αTAT in living cells using Z-lock. Stone OJ, Pankow N, Liu B, Sharma VP, Eddy RJ, Wang H, Putz AT, Teets FD, Kuhlman B, Condeelis JS, Hahn KM. Nat Chem Biol 15 1183-1190 (2019)
  14. Modifications to the Framework Regions Eliminate Chimeric Antigen Receptor Tonic Signaling. Landoni E, Fucá G, Wang J, Chirasani VR, Yao Z, Dukhovlinova E, Ferrone S, Savoldo B, Hong LK, Shou P, Musio S, Padelli F, Finocchiaro G, Droste M, Kuhlman B, Shamshiev A, Pellegatta S, Dokholyan NV, Dotti G. Cancer Immunol Res 9 441-453 (2021)
  15. Islet Amyloid Polypeptide Promotes Amyloid-Beta Aggregation by Binding-Induced Helix-Unfolding of the Amyloidogenic Core. Ge X, Yang Y, Sun Y, Cao W, Ding F. ACS Chem Neurosci 9 967-975 (2018)
  16. Profiling cellular morphodynamics by spatiotemporal spectrum decomposition. Ma X, Dagliyan O, Hahn KM, Danuser G. PLoS Comput Biol 14 e1006321 (2018)
  17. Development of light-responsive protein binding in the monobody non-immunoglobulin scaffold. Carrasco-López C, Zhao EM, Gil AA, Alam N, Toettcher JE, Avalos JL. Nat Commun 11 4045 (2020)
  18. Engineering Pak1 Allosteric Switches. Dagliyan O, Karginov AV, Yagishita S, Gale ME, Wang H, DerMardirossian C, Wells CM, Dokholyan NV, Kasai H, Hahn KM. ACS Synth Biol 6 1257-1262 (2017)
  19. Light-regulated allosteric switch enables temporal and subcellular control of enzyme activity. Shaaya M, Fauser J, Zhurikhina A, Conage-Pough JE, Huyot V, Brennan M, Flower CT, Matsche J, Khan S, Natarajan V, Rehman J, Kota P, White FM, Tsygankov D, Karginov AV. Elife 9 e60647 (2020)
  20. Rational design and implementation of a chemically inducible heterotrimerization system. Wu HD, Kikuchi M, Dagliyan O, Aragaki AK, Nakamura H, Dokholyan NV, Umehara T, Inoue T. Nat Methods 17 928-936 (2020)
  21. Minimally disruptive optical control of protein tyrosine phosphatase 1B. Hongdusit A, Zwart PH, Sankaran B, Fox JM. Nat Commun 11 788 (2020)
  22. Optical control of protein phosphatase function. Courtney TM, Deiters A. Nat Commun 10 4384 (2019)
  23. Editorial An engineered photoswitchable mammalian pyruvate kinase. Gehrig S, Macpherson JA, Driscoll PC, Symon A, Martin SR, MacRae JI, Kleinjung J, Fraternali F, Anastasiou D. FEBS J 284 2955-2980 (2017)
  24. Differential Substrate Recognition by Maltose Binding Proteins Influenced by Structure and Dynamics. Shukla S, Bafna K, Gullett C, Myles DAA, Agarwal PK, Cuneo MJ. Biochemistry 57 5864-5876 (2018)
  25. β-Methylamino-L-alanine substitution of serine in SOD1 suggests a direct role in ALS etiology. Proctor EA, Mowrey DD, Dokholyan NV. PLoS Comput Biol 15 e1007225 (2019)
  26. Structurally distributed surface sites tune allosteric regulation. McCormick JW, Russo MA, Thompson S, Blevins A, Reynolds KA. Elife 10 e68346 (2021)
  27. Engineering allosteric regulation in protein kinases. Pincus D, Pandey JP, Feder ZA, Creixell P, Resnekov O, Reynolds KA. Sci Signal 11 eaar3250 (2018)
  28. Two-input protein logic gate for computation in living cells. Vishweshwaraiah YL, Chen J, Chirasani VR, Tabdanov ED, Dokholyan NV. Nat Commun 12 6615 (2021)
  29. Optogenetic control of Neisseria meningitidis Cas9 genome editing using an engineered, light-switchable anti-CRISPR protein. Hoffmann MD, Mathony J, Upmeier Zu Belzen J, Harteveld Z, Aschenbrenner S, Stengl C, Grimm D, Correia BE, Eils R, Niopek D. Nucleic Acids Res 49 e29 (2021)
  30. Probing ion channel functional architecture and domain recombination compatibility by massively parallel domain insertion profiling. Coyote-Maestas W, Nedrud D, Suma A, He Y, Matreyek KA, Fowler DM, Carnevale V, Myers CL, Schmidt D. Nat Commun 12 7114 (2021)
  31. Deep phylogeny of cancer drivers and compensatory mutations. Rochman ND, Wolf YI, Koonin EV. Commun Biol 3 551 (2020)
  32. Disorder driven allosteric control of protein activity. Tee WV, Guarnera E, Berezovsky IN. Curr Res Struct Biol 2 191-203 (2020)
  33. Domain insertion permissibility-guided engineering of allostery in ion channels. Coyote-Maestas W, He Y, Myers CL, Schmidt D. Nat Commun 10 290 (2019)
  34. Increasing spatial resolution of photoregulated GTPases through immobilized peripheral membrane proteins. Van Geel O, Hartsuiker R, Gadella TWJ. Small GTPases 11 441-450 (2020)
  35. Repurposing Protein Degradation for Optogenetic Modulation of Protein Activities. Mondal P, Krishnamurthy VV, Sharum SR, Haack N, Zhou H, Cheng J, Yang J, Zhang K. ACS Synth Biol 8 2585-2592 (2019)
  36. Engineering a switchable single-chain TEV protease to control protein maturation in living neurons. Renna P, Ripoli C, Dagliyan O, Pastore F, Rinaudo M, Re A, Paciello F, Grassi C. Bioeng Transl Med 7 e10292 (2022)
  37. Engineering and exploiting synthetic allostery of NanoLuc luciferase. Guo Z, Parakra RD, Xiong Y, Johnston WA, Walden P, Edwardraja S, Moradi SV, Ungerer JPJ, Ai HW, Phillips JJ, Alexandrov K. Nat Commun 13 789 (2022)
  38. Targeted insertional mutagenesis libraries for deep domain insertion profiling. Coyote-Maestas W, Nedrud D, Okorafor S, He Y, Schmidt D. Nucleic Acids Res 48 e11 (2020)
  39. A Split-Abl Kinase for Direct Activation in Cells. Diaz JE, Morgan CW, Minogue CE, Hebert AS, Coon JJ, Wells JA. Cell Chem Biol 24 1250-1258.e4 (2017)
  40. Excited State Vibrations of Isotopically Labeled FMN Free and Bound to a Light-Oxygen-Voltage (LOV) Protein. Iuliano JN, Hall CR, Green D, Jones GA, Lukacs A, Illarionov B, Bacher A, Fischer M, French JB, Tonge PJ, Meech SR. J Phys Chem B 124 7152-7165 (2020)
  41. Inter-Active Site Communication Mediated by the Dimer Interface β-Sheet in the Half-the-Sites Enzyme, Thymidylate Synthase. Sapienza PJ, Popov KI, Mowrey DD, Falk BT, Dokholyan NV, Lee AL. Biochemistry 58 3302-3313 (2019)
  42. Optogenetic Control of Microtubule Dynamics. van Haren J, Adachi LS, Wittmann T. Methods Mol Biol 2101 211-234 (2020)
  43. Optogenetic Reconstitution for Determining the Form and Function of Membraneless Organelles. Dine E, Toettcher JE. Biochemistry 57 2432-2436 (2018)
  44. Structure-based design of a photoswitchable affibody scaffold. Woloschuk RM, Reed PMM, Jaikaran ASI, Demmans KZ, Youn J, Kanelis V, Uppalapati M, Woolley GA. Protein Sci 30 2359-2372 (2021)
  45. Analysis of Three Architectures for Controlling PTP1B with Light. Hongdusit A, Liechty ET, Fox JM. ACS Synth Biol 11 61-68 (2022)
  46. Biosensors based on peptide exposure show single molecule conformations in live cells. Liu B, Stone OJ, Pablo M, Herron JC, Nogueira AT, Dagliyan O, Grimm JB, Lavis LD, Elston TC, Hahn KM. Cell 184 5670-5685.e23 (2021)
  47. Prefusion spike protein stabilization through computational mutagenesis. Zhang DY, Wang J, Dokholyan NV. Proteins 89 399-408 (2021)
  48. Advances in the Computational Design of Small-Molecule-Controlled Protein-Based Circuits for Synthetic Biology. Kretschmer S, Kortemme T. Proc IEEE Inst Electr Electron Eng 110 659-674 (2022)
  49. Allosteric inactivation of an engineered optogenetic GTPase. Jain A, Dokholyan NV, Lee AL. Proc Natl Acad Sci U S A 120 e2219254120 (2023)
  50. The Next Frontier for Designing Switchable Proteins: Rational Enhancement of Kinetics. Bogetti AT, Presti MF, Loh SN, Chong LT. J Phys Chem B 125 9069-9077 (2021)
  51. Two Engineered OBPs with opposite temperature-dependent affinities towards 1-aminoanthracene. Gonçalves F, Castro TG, Azoia NG, Ribeiro A, Silva C, Cavaco-Paulo A. Sci Rep 8 14844 (2018)
  52. Z-DNA and Z-RNA: Methods-Past and Future. Herbert A. Methods Mol Biol 2651 295-329 (2023)
  53. A computational method for the design of nested proteins by loop-directed domain insertion. Blacklock KM, Yang L, Mulligan VK, Khare SD. Proteins 86 354-369 (2018)
  54. A noncommutative combinatorial protein logic circuit controls cell orientation in nanoenvironments. Chen J, Vishweshwaraiah YL, Mailman RB, Tabdanov ED, Dokholyan NV. Sci Adv 9 eadg1062 (2023)
  55. Dissecting the Determinants of Domain Insertion Tolerance and Allostery in Proteins. Mathony J, Aschenbrenner S, Becker P, Niopek D. Adv Sci (Weinh) 10 e2303496 (2023)
  56. Enhancing response of a protein conformational switch by using two disordered ligand binding domains. Sekhon H, Ha JH, Loh SN. Front Mol Biosci 10 1114756 (2023)
  57. Mapping co-regulatory interactions among ligand-binding sites in ryanodine receptor 1. Chirasani VR, Popov KI, Meissner G, Dokholyan NV. Proteins 90 385-394 (2022)
  58. Allosteric regulation of kinase activity in living cells. Godbole SS, Dokholyan NV. Elife 12 RP90574 (2023)
  59. Engineering Optogenetic Protein Analogs. Liu B, Marston DJ, Hahn KM. Methods Mol Biol 2173 113-126 (2020)
  60. Engineering memory with an extrinsically disordered kinase. Ripoli C, Dagliyan O, Renna P, Pastore F, Paciello F, Sollazzo R, Rinaudo M, Battistoni M, Martini S, Tramutola A, Sattin A, Barone E, Saneyoshi T, Fellin T, Hayashi Y, Grassi C. Sci Adv 9 eadh1110 (2023)
  61. Light-switchable transcription factors obtained by direct screening in mammalian cells. Zhu L, McNamara HM, Toettcher JE. Nat Commun 14 3185 (2023)
  62. Microbial Rhodopsin Optogenetic Tools: Application for Analyses of Synaptic Transmission and of Neuronal Network Activity in Behavior. Bergs A, Henss T, Glock C, Nagpal J, Gottschalk A. Methods Mol Biol 2468 89-115 (2022)
  63. Optogenetics: Rho GTPases Activated by Light in Living Macrophages. Hülsemann M, Verkhusha PV, Guo P, Miskolci V, Cox D, Hodgson L. Methods Mol Biol 2108 281-293 (2020)
  64. Reversible photoregulation of cell-cell adhesions with opto-E-cadherin. Nzigou Mombo B, Bijonowski BM, Raab CA, Niland S, Brockhaus K, Müller M, Eble JA, Wegner SV. Nat Commun 14 6292 (2023)


Quick links