IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-44256-1.html
   My bibliography  Save this article

Customizing cellular signal processing by synthetic multi-level regulatory circuits

Author

Listed:
  • Yuanli Gao

    (Zhejiang University
    University of Edinburgh)

  • Lei Wang

    (Westlake University)

  • Baojun Wang

    (Zhejiang University
    Research Center for Biological Computation, Zhejiang Lab)

Abstract

As synthetic biology permeates society, the signal processing circuits in engineered living systems must be customized to meet practical demands. Towards this mission, novel regulatory mechanisms and genetic circuits with unprecedented complexity have been implemented over the past decade. These regulatory mechanisms, such as transcription and translation control, could be integrated into hybrid circuits termed “multi-level circuits”. The multi-level circuit design will tremendously benefit the current genetic circuit design paradigm, from modifying basic circuit dynamics to facilitating real-world applications, unleashing our capabilities to customize cellular signal processing and address global challenges through synthetic biology.

Suggested Citation

  • Yuanli Gao & Lei Wang & Baojun Wang, 2023. "Customizing cellular signal processing by synthetic multi-level regulatory circuits," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44256-1
    DOI: 10.1038/s41467-023-44256-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44256-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44256-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Amir Pandi & Christoph Diehl & Ali Yazdizadeh Kharrazi & Scott A. Scholz & Elizaveta Bobkova & Léon Faure & Maren Nattermann & David Adam & Nils Chapin & Yeganeh Foroughijabbari & Charles Moritz & Nic, 2022. "A versatile active learning workflow for optimization of genetic and metabolic networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Javier Santos-Moreno & Eve Tasiudi & Joerg Stelling & Yolanda Schaerli, 2020. "Multistable and dynamic CRISPRi-based synthetic circuits," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    3. Hsin-Ho Huang & Yili Qian & Domitilla Del Vecchio, 2018. "A quasi-integral controller for adaptation of genetic modules to variable ribosome demand," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Ronald E. Rondon & Thomas M. Groseclose & Andrew E. Short & Corey J. Wilson, 2019. "Transcriptional programming using engineered systems of transcription factors and genetic architectures," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    5. Yeqing Zong & Haoqian M. Zhang & Cheng Lyu & Xiangyu Ji & Junran Hou & Xian Guo & Qi Ouyang & Chunbo Lou, 2017. "Insulated transcriptional elements enable precise design of genetic circuits," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    6. Conor J. McClune & Aurora Alvarez-Buylla & Christopher A. Voigt & Michael T. Laub, 2019. "Engineering orthogonal signalling pathways reveals the sparse occupancy of sequence space," Nature, Nature, vol. 574(7780), pages 702-706, October.
    7. Baojun Wang & Richard I Kitney & Nicolas Joly & Martin Buck, 2011. "Engineering modular and orthogonal genetic logic gates for robust digital-like synthetic biology," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
    8. Chelsea Y. Hu & Richard M. Murray, 2022. "Layered feedback control overcomes performance trade-off in synthetic biomolecular networks," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Jacob R. Rubens & Gianluca Selvaggio & Timothy K. Lu, 2016. "Synthetic mixed-signal computation in living cells," Nature Communications, Nature, vol. 7(1), pages 1-10, September.
    10. Lewis Grozinger & Martyn Amos & Thomas E. Gorochowski & Pablo Carbonell & Diego A. Oyarzún & Ruud Stoof & Harold Fellermann & Paolo Zuliani & Huseyin Tas & Angel Goñi-Moreno, 2019. "Pathways to cellular supremacy in biocomputing," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    11. Ross D. Jones & Yili Qian & Velia Siciliano & Breanna DiAndreth & Jin Huh & Ron Weiss & Domitilla Del Vecchio, 2020. "An endoribonuclease-based feedforward controller for decoupling resource-limited genetic modules in mammalian cells," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    12. Shivang Hina-Nilesh Joshi & Chentao Yong & Andras Gyorgy, 2022. "Inducible plasmid copy number control for synthetic biology in commonly used E. coli strains," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    13. Lauren Gambill & August Staubus & Kim Wai Mo & Andrea Ameruoso & James Chappell, 2023. "A split ribozyme that links detection of a native RNA to orthogonal protein outputs," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    14. Alexander A. Green & Jongmin Kim & Duo Ma & Pamela A. Silver & James J. Collins & Peng Yin, 2017. "Complex cellular logic computation using ribocomputing devices," Nature, Nature, vol. 548(7665), pages 117-121, August.
    15. Michele Felletti & Julia Stifel & Lena A. Wurmthaler & Sophie Geiger & Jörg S. Hartig, 2016. "Twister ribozymes as highly versatile expression platforms for artificial riboswitches," Nature Communications, Nature, vol. 7(1), pages 1-8, November.
    16. Miles W. Gander & Justin D. Vrana & William E. Voje & James M. Carothers & Eric Klavins, 2017. "Digital logic circuits in yeast with CRISPR-dCas9 NOR gates," Nature Communications, Nature, vol. 8(1), pages 1-11, August.
    17. Amir Pandi & Mathilde Koch & Peter L. Voyvodic & Paul Soudier & Jerome Bonnet & Manish Kushwaha & Jean-Loup Faulon, 2019. "Metabolic perceptrons for neural computing in biological systems," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    18. Filipe Pinto & Ella Lucille Thornton & Baojun Wang, 2020. "An expanded library of orthogonal split inteins enables modular multi-peptide assemblies," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    19. Ramiz Daniel & Jacob R. Rubens & Rahul Sarpeshkar & Timothy K. Lu, 2013. "Synthetic analog computation in living cells," Nature, Nature, vol. 497(7451), pages 619-623, May.
    20. Raphaël V. Gayet & Katherine Ilia & Shiva Razavi & Nathaniel D. Tippens & Makoto A. Lalwani & Kehan Zhang & Jack X. Chen & Jonathan C. Chen & Jose Vargas-Asencio & James J. Collins, 2023. "Autocatalytic base editing for RNA-responsive translational control," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    21. Timothy Frei & Federica Cella & Fabiana Tedeschi & Joaquín Gutiérrez & Guy-Bart Stan & Mustafa Khammash & Velia Siciliano, 2020. "Characterization and mitigation of gene expression burden in mammalian cells," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    22. Brian J. Caliando & Christopher A. Voigt, 2015. "Targeted DNA degradation using a CRISPR device stably carried in the host genome," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    23. Breanna DiAndreth & Noreen Wauford & Eileen Hu & Sebastian Palacios & Ron Weiss, 2022. "PERSIST platform provides programmable RNA regulation using CRISPR endoRNases," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    24. Andrew H. Ng & Taylor H. Nguyen & Mariana Gómez-Schiavon & Galen Dods & Robert A. Langan & Scott E. Boyken & Jennifer A. Samson & Lucas M. Waldburger & John E. Dueber & David Baker & Hana El-Samad, 2019. "Modular and tunable biological feedback control using a de novo protein switch," Nature, Nature, vol. 572(7768), pages 265-269, August.
    25. F. Veronica Greco & Amir Pandi & Tobias J. Erb & Claire S. Grierson & Thomas E. Gorochowski, 2021. "Harnessing the central dogma for stringent multi-level control of gene expression," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    26. Stanislav Anastassov & Maurice Filo & Ching-Hsiang Chang & Mustafa Khammash, 2023. "A cybergenetic framework for engineering intein-mediated integral feedback control systems," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    27. Nathaniel Jillette & Menghan Du & Jacqueline Jufen Zhu & Peter Cardoz & Albert Wu Cheng, 2019. "Split selectable markers," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    28. James Chappell & Alexandra Westbrook & Matthew Verosloff & Julius B. Lucks, 2017. "Computational design of small transcription activating RNAs for versatile and dynamic gene regulation," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    29. Tae Seok Moon & Chunbo Lou & Alvin Tamsir & Brynne C. Stanton & Christopher A. Voigt, 2012. "Genetic programs constructed from layered logic gates in single cells," Nature, Nature, vol. 491(7423), pages 249-253, November.
    30. Shunsuke Kawasaki & Hiroki Ono & Moe Hirosawa & Takeru Kuwabara & Shunsuke Sumi & Suji Lee & Knut Woltjen & Hirohide Saito, 2023. "Programmable mammalian translational modulators by CRISPR-associated proteins," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    31. Tackhoon Kim & Benjamin Weinberg & Wilson Wong & Timothy K. Lu, 2021. "Scalable recombinase-based gene expression cascades," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    32. Miles V. Rouches & Yasu Xu & Louis Brian Georges Cortes & Guillaume Lambert, 2022. "A plasmid system with tunable copy number," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    33. Xinyi Wan & Filipe Pinto & Luyang Yu & Baojun Wang, 2020. "Synthetic protein-binding DNA sponge as a tool to tune gene expression and mitigate protein toxicity," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    34. Luna Rizik & Loai Danial & Mouna Habib & Ron Weiss & Ramez Daniel, 2022. "Synthetic neuromorphic computing in living cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    35. Ross D. Jones & Yili Qian & Katherine Ilia & Benjamin Wang & Michael T. Laub & Domitilla Del Vecchio & Ron Weiss, 2022. "Robust and tunable signal processing in mammalian cells via engineered covalent modification cycles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    36. Benjamin H. Weinberg & Jang Hwan Cho & Yash Agarwal & N. T. Hang Pham & Leidy D. Caraballo & Maciej Walkosz & Charina Ortega & Micaela Trexler & Nathan Tague & Billy Law & William K. J. Benman & Justi, 2019. "High-performance chemical- and light-inducible recombinases in mammalian cells and mice," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    37. Sergi Regot & Javier Macia & Núria Conde & Kentaro Furukawa & Jimmy Kjellén & Tom Peeters & Stefan Hohmann & Eulàlia de Nadal & Francesc Posas & Ricard Solé, 2011. "Distributed biological computation with multicellular engineered networks," Nature, Nature, vol. 469(7329), pages 207-211, January.
    38. Rory L. Williams & Richard M. Murray, 2022. "Integrase-mediated differentiation circuits improve evolutionary stability of burdensome and toxic functions in E. coli," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    39. Federica Cella & Liliana Wroblewska & Ron Weiss & Velia Siciliano, 2018. "Engineering protein-protein devices for multilayered regulation of mRNA translation using orthogonal proteases in mammalian cells," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    40. Cong Gao & Jianshen Hou & Peng Xu & Liang Guo & Xiulai Chen & Guipeng Hu & Chao Ye & Harley Edwards & Jian Chen & Wei Chen & Liming Liu, 2019. "Programmable biomolecular switches for rewiring flux in Escherichia coli," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    41. Leo Scheller & Marc Schmollack & Adrian Bertschi & Maysam Mansouri & Pratik Saxena & Martin Fussenegger, 2020. "Phosphoregulated orthogonal signal transduction in mammalian cells," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    42. Arthur Prindle & Jangir Selimkhanov & Howard Li & Ivan Razinkov & Lev S. Tsimring & Jeff Hasty, 2014. "Rapid and tunable post-translational coupling of genetic circuits," Nature, Nature, vol. 508(7496), pages 387-391, April.
    43. Robert A. Langan & Scott E. Boyken & Andrew H. Ng & Jennifer A. Samson & Galen Dods & Alexandra M. Westbrook & Taylor H. Nguyen & Marc J. Lajoie & Zibo Chen & Stephanie Berger & Vikram Khipple Mulliga, 2019. "De novo design of bioactive protein switches," Nature, Nature, vol. 572(7768), pages 205-210, August.
    44. Patrick S. Donahue & Joseph W. Draut & Joseph J. Muldoon & Hailey I. Edelstein & Neda Bagheri & Joshua N. Leonard, 2020. "The COMET toolkit for composing customizable genetic programs in mammalian cells," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    45. Sarah Guiziou & Pauline Mayonove & Jerome Bonnet, 2019. "Hierarchical composition of reliable recombinase logic devices," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    46. Yang Liu & Xinyi Wan & Baojun Wang, 2019. "Engineered CRISPRa enables programmable eukaryote-like gene activation in bacteria," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Luna Rizik & Loai Danial & Mouna Habib & Ron Weiss & Ramez Daniel, 2022. "Synthetic neuromorphic computing in living cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Ross D. Jones & Yili Qian & Katherine Ilia & Benjamin Wang & Michael T. Laub & Domitilla Del Vecchio & Ron Weiss, 2022. "Robust and tunable signal processing in mammalian cells via engineered covalent modification cycles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Stanislav Anastassov & Maurice Filo & Ching-Hsiang Chang & Mustafa Khammash, 2023. "A cybergenetic framework for engineering intein-mediated integral feedback control systems," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Alex J. H. Fedorec & Neythen J. Treloar & Ke Yan Wen & Linda Dekker & Qing Hsuan Ong & Gabija Jurkeviciute & Enbo Lyu & Jack W. Rutter & Kathleen J. Y. Zhang & Luca Rosa & Alexey Zaikin & Chris P. Bar, 2024. "Emergent digital bio-computation through spatial diffusion and engineered bacteria," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. Baiyang Liu & Christian Cuba Samaniego & Matthew R. Bennett & Elisa Franco & James Chappell, 2023. "A portable regulatory RNA array design enables tunable and complex regulation across diverse bacteria," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    6. Shunsuke Kawasaki & Hiroki Ono & Moe Hirosawa & Takeru Kuwabara & Shunsuke Sumi & Suji Lee & Knut Woltjen & Hirohide Saito, 2023. "Programmable mammalian translational modulators by CRISPR-associated proteins," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Shivang Hina-Nilesh Joshi & Chentao Yong & Andras Gyorgy, 2022. "Inducible plasmid copy number control for synthetic biology in commonly used E. coli strains," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Brian D. Huang & Dowan Kim & Yongjoon Yu & Corey J. Wilson, 2024. "Engineering intelligent chassis cells via recombinase-based MEMORY circuits," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Kanakov, Oleg & Chen, Shangbin & Zaikin, Alexey, 2024. "Learning by selective plasmid loss for intracellular synthetic classifiers," Chaos, Solitons & Fractals, Elsevier, vol. 179(C).
    10. John P. Marken & Richard M. Murray, 2023. "Addressable and adaptable intercellular communication via DNA messaging," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    11. Yang Gao & Yuchen Zhou & Xudong Ji & Austin J. Graham & Christopher M. Dundas & Ismar E. Miniel Mahfoud & Bailey M. Tibbett & Benjamin Tan & Gina Partipilo & Ananth Dodabalapur & Jonathan Rivnay & Ben, 2024. "A hybrid transistor with transcriptionally controlled computation and plasticity," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Carlos Barajas & Hsin-Ho Huang & Jesse Gibson & Luis Sandoval & Domitilla Vecchio, 2022. "Feedforward growth rate control mitigates gene activation burden," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    13. Roberto Di Blasi & Mara Pisani & Fabiana Tedeschi & Masue M. Marbiah & Karen Polizzi & Simone Furini & Velia Siciliano & Francesca Ceroni, 2023. "Resource-aware construct design in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    14. Chenrui Qin & Yanhui Xiang & Jie Liu & Ruilin Zhang & Ziming Liu & Tingting Li & Zhi Sun & Xiaoyi Ouyang & Yeqing Zong & Haoqian M. Zhang & Qi Ouyang & Long Qian & Chunbo Lou, 2023. "Precise programming of multigene expression stoichiometry in mammalian cells by a modular and programmable transcriptional system," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    15. Judee A. Sharon & Chelsea Dasrath & Aiden Fujiwara & Alessandro Snyder & Mace Blank & Sam O’Brien & Lauren M. Aufdembrink & Aaron E. Engelhart & Katarzyna P. Adamala, 2023. "Trumpet is an operating system for simple and robust cell-free biocomputing," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Andras Gyorgy, 2023. "Competition and evolutionary selection among core regulatory motifs in gene expression control," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Amir Pandi & Christoph Diehl & Ali Yazdizadeh Kharrazi & Scott A. Scholz & Elizaveta Bobkova & Léon Faure & Maren Nattermann & David Adam & Nils Chapin & Yeganeh Foroughijabbari & Charles Moritz & Nic, 2022. "A versatile active learning workflow for optimization of genetic and metabolic networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Weiyue Ji & Handuo Shi & Haoqian Zhang & Rui Sun & Jingyi Xi & Dingqiao Wen & Jingchen Feng & Yiwei Chen & Xiao Qin & Yanrong Ma & Wenhan Luo & Linna Deng & Hanchi Lin & Ruofan Yu & Qi Ouyang, 2013. "A Formalized Design Process for Bacterial Consortia That Perform Logic Computing," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-9, February.
    19. Nicole M. Wong & Elizabeth Frias & Frederic D. Sigoillot & Justin H. Letendre & Marc Hild & Wilson W. Wong, 2021. "Engineering digitizer circuits for chemical and genetic screens in human cells," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    20. Michael B. Sheets & Nathan Tague & Mary J. Dunlop, 2023. "An optogenetic toolkit for light-inducible antibiotic resistance," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44256-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.