دورية أكاديمية

Transcriptional regulation of living materials via extracellular electron transfer.

التفاصيل البيبلوغرافية
العنوان: Transcriptional regulation of living materials via extracellular electron transfer.
المؤلفون: Graham AJ; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Partipilo G; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Dundas CM; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Miniel Mahfoud IE; Interdisciplinary Life Sciences Graduate Program, University of Texas at Austin, Austin, TX, USA., Halwachs KN; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Holwerda AJ; Interdisciplinary Life Sciences Graduate Program, University of Texas at Austin, Austin, TX, USA., Simmons TR; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., FitzSimons TM; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Coleman SM; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Rinehart R; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Chiu D; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Tyndall AE; Department of Chemical and Biological Engineering, Colorado School of Mines, Golden, CO, USA., Sajbel KC; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Rosales AM; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA., Keitz BK; McKetta Department of Chemical Engineering, University of Texas at Austin, Austin, TX, USA. keitz@utexas.edu.
المصدر: Nature chemical biology [Nat Chem Biol] 2024 May 23. Date of Electronic Publication: 2024 May 23.
Publication Model: Ahead of Print
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: United States NLM ID: 101231976 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1552-4469 (Electronic) Linking ISSN: 15524450 NLM ISO Abbreviation: Nat Chem Biol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: New York, NY : Nature Pub. Group, [2005]-
مستخلص: Engineered living materials combine the advantages of biological and synthetic systems by leveraging genetic and metabolic programming to control material-wide properties. Here, we demonstrate that extracellular electron transfer (EET), a microbial respiration process, can serve as a tunable bridge between live cell metabolism and synthetic material properties. In this system, EET flux from Shewanella oneidensis to a copper catalyst controls hydrogel cross-linking via two distinct chemistries to form living synthetic polymer networks. We first demonstrate that synthetic biology-inspired design rules derived from fluorescence parameterization can be applied toward EET-based regulation of polymer network mechanics. We then program transcriptional Boolean logic gates to govern EET gene expression, which enables design of computational polymer networks that mechanically respond to combinations of molecular inputs. Finally, we control fibroblast morphology using EET as a bridge for programmed material properties. Our results demonstrate how rational genetic circuit design can emulate physiological behavior in engineered living materials.
(© 2024. The Author(s), under exclusive licence to Springer Nature America, Inc.)
References: Martyn, I. & Gartner, Z. J. Expanding the boundaries of synthetic development. Dev. Biol. 474, 62–70 (2021). (PMID: 3358791310.1016/j.ydbio.2021.01.017)
Luo, N., Wang, S. & You, L. Synthetic pattern formation. Biochemistry 58, 1478–1483 (2019). (PMID: 3066686710.1021/acs.biochem.8b01242)
Sirisaengtaksin, N., Odem, M. A., Bosserman, R. E., Flores, E. M. & Krachler, A. M. The E. coli transcription factor GrlA is regulated by subcellular compartmentalization and activated in response to mechanical stimuli. Proc. Natl Acad. Sci. USA 117, 9519–9528 (2020). (PMID: 32277032719682810.1073/pnas.1917500117)
Goodwin, K. & Nelson, C. M. Mechanics of development. Dev. Cell 56, 240–250 (2021). (PMID: 3332110510.1016/j.devcel.2020.11.025)
Humphries, J. et al. Species-independent attraction to biofilms through electrical signaling. Cell 168, 200–209.e12 (2017). (PMID: 28086091549750110.1016/j.cell.2016.12.014)
Roth, J. G. et al. Advancing models of neural development with biomaterials. Nat. Rev. Neurosci. 22, 593–615 (2021). (PMID: 34376834861287310.1038/s41583-021-00496-y)
Kholodenko, B. N. Cell-signalling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 7, 165–176 (2006). (PMID: 16482094167990510.1038/nrm1838)
Fern, J. & Schulman, R. Modular DNA strand-displacement controllers for directing material expansion. Nat. Commun. 9, 3766 (2018). (PMID: 30217991613864510.1038/s41467-018-06218-w)
Rodrigo-Navarro, A., Sankaran, S., Dalby, M. J., del Campo, A. & Salmeron-Sanchez, M. Engineered living biomaterials. Nat. Rev. Mater. 6, 1175–1190 (2021). (PMID: 10.1038/s41578-021-00350-8)
Cao, Y. et al. Programmable assembly of pressure sensors using pattern-forming bacteria. Nat. Biotechnol. 35, 1087–1093 (2017). (PMID: 28991268600341910.1038/nbt.3978)
Praveschotinunt, P. et al. Engineered E. coli Nissle 1917 for the delivery of matrix-tethered therapeutic domains to the gut. Nat. Commun. 10, 5580 (2019). (PMID: 31811125689832110.1038/s41467-019-13336-6)
Duraj-Thatte, A. M. et al. Water-processable, biodegradable and coatable aquaplastic from engineered biofilms. Nat. Chem. Biol. 17, 732–738 (2021). (PMID: 33737758815986310.1038/s41589-021-00773-y)
Kang, S.-Y. et al. Engineering Bacillus subtilis for the formation of a durable living biocomposite material. Nat. Commun. 12, 7133 (2021). (PMID: 34880257865492210.1038/s41467-021-27467-2)
Smith, R. S. H. et al. Hybrid living materials: digital design and fabrication of 3D multimaterial structures with programmable biohybrid surfaces. Adv. Funct. Mater. 30, 1907401 (2020). (PMID: 10.1002/adfm.201907401)
Gilbert, C. et al. Living materials with programmable functionalities grown from engineered microbial co-cultures. Nat. Mater. 20, 691–700 (2021). (PMID: 3343214010.1038/s41563-020-00857-5)
Rivera-Tarazona, L. K., Campbell, Z. T. & Ware, T. H. Stimuli-responsive engineered living materials. Soft Matter 17, 785–809 (2021). (PMID: 3341084110.1039/D0SM01905D)
González, L. M., Mukhitov, N. & Voigt, C. A. Resilient living materials built by printing bacterial spores. Nat. Chem. Biol. 16, 126–133 (2020). (PMID: 3179244410.1038/s41589-019-0412-5)
Graham, A. J. & Keitz, B. K. in Engineered Living Materials (ed. Srubar III, W. V.) 27–49 (Springer International, 2023).
Rosales, A. M. & Anseth, K. S. The design of reversible hydrogels to capture extracellular matrix dynamics. Nat. Rev. Mater. 1, 15012 (2016). (PMID: 29214058571432710.1038/natrevmats.2015.12)
Kaspar, C., Ravoo, B. J., van der Wiel, W. G., Wegner, S. V. & Pernice, W. H. P. The rise of intelligent matter. Nature 594, 345–355 (2021). (PMID: 3413551810.1038/s41586-021-03453-y)
Zhang, X. et al. The pathway to intelligence: using stimuli-responsive materials as building blocks for constructing smart and functional systems. Adv. Mater. 31, 1804540 (2019). (PMID: 10.1002/adma.201804540)
English, M. A. et al. Programmable CRISPR-responsive smart materials. Science 365, 780–785 (2019). (PMID: 3143979110.1126/science.aaw5122)
Zhang, H., Zeng, H., Priimagi, A. & Ikkala, O. Viewpoint: Pavlovian materials—functional biomimetics inspired by classical conditioning. Adv. Mater. 32, 1906619 (2020). (PMID: 10.1002/adma.201906619)
Ikeda, M. et al. Installing logic-gate responses to a variety of biological substances in supramolecular hydrogel–enzyme hybrids. Nat. Chem. 6, 511–518 (2014). (PMID: 2484823710.1038/nchem.1937)
Badeau, B. A., Comerford, M. P., Arakawa, C. K., Shadish, J. A. & DeForest, C. A. Engineered modular biomaterial logic gates for environmentally triggered therapeutic delivery. Nat. Chem. 10, 251–258 (2018). (PMID: 29461528582273510.1038/nchem.2917)
Korevaar, P. A., Kaplan, C. N., Grinthal, A., Rust, R. M. & Aizenberg, J. Non-equilibrium signal integration in hydrogels. Nat. Commun. 11, 386 (2020). (PMID: 31959819697103510.1038/s41467-019-14114-0)
Daly, A. C., Prendergast, M. E., Hughes, A. J. & Burdick, J. A. Bioprinting for the biologist. Cell 184, 18–32 (2021). (PMID: 334178591033500310.1016/j.cell.2020.12.002)
Rivera-Tarazona, L. K., Bhat, V. D., Kim, H., Campbell, Z. T. & Ware, T. H. Shape-morphing living composites. Sci. Adv. 6, eaax8582 (2020). (PMID: 32010767696894210.1126/sciadv.aax8582)
Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016). (PMID: 2757357910.1038/nrmicro.2016.93)
Fan, G., Graham, A. J., Kolli, J., Lynd, N. A. & Keitz, B. K. Aerobic radical polymerization mediated by microbial metabolism. Nat. Chem. 12, 638–646 (2020). (PMID: 32424254732191610.1038/s41557-020-0460-1)
Graham, A. J. et al. Genetic control of radical cross-linking in a semisynthetic hydrogel. ACS Biomater. Sci. Eng. 6, 1375–1386 (2020). (PMID: 33313392772527310.1021/acsbiomaterials.9b01773)
Beliaev, A. S. et al. Gene and protein expression profiles of Shewanella oneidensis during anaerobic growth with different electron acceptors. OMICS J. Integr. Biol. 6, 39–60 (2002). (PMID: 10.1089/15362310252780834)
Coursolle, D. & Gralnick, J. A. Reconstruction of extracellular respiratory pathways for iron(III) reduction in Shewanella oneidensis strain MR-1. Front. Microbiol. 3, 56 (2012). (PMID: 22363330328294310.3389/fmicb.2012.00056)
Brophy, J. A. N. & Voigt, C. A. Principles of genetic circuit design. Nat. Methods 11, 508–520 (2014). (PMID: 24781324423027410.1038/nmeth.2926)
Dundas, C. M., Walker, D. J. F. & Keitz, B. K. Tuning extracellular electron transfer by Shewanella oneidensis using transcriptional logic gates. ACS Synth. Biol. 9, 2301–2315 (2020). (PMID: 32786362781651610.1021/acssynbio.9b00517)
Nielsen, A. A. K. et al. Genetic circuit design automation. Science 352, aac7341 (2016). (PMID: 2703437810.1126/science.aac7341)
Reis, A. C. & Salis, H. M. An automated model test system for systematic development and improvement of gene expression models. ACS Synth. Biol. 9, 3145–3156 (2020). (PMID: 3305418110.1021/acssynbio.0c00394)
Rosenfeld, N. & Alon, U. Response delays and the structure of transcription networks. J. Mol. Biol. 329, 645–654 (2003). (PMID: 1278766610.1016/S0022-2836(03)00506-0)
Xiong, Y. et al. Targeted protein degradation of outer membrane decaheme cytochrome MtrC metal reductase in Shewanella oneidensis MR-1 measured using biarsenical probe CrAsH-EDT2. Biochemistry 50, 9738–9751 (2011). (PMID: 2199951810.1021/bi200602f)
Stanton, B. C. et al. Genomic mining of prokaryotic repressors for orthogonal logic gates. Nat. Chem. Biol. 10, 99–105 (2014). (PMID: 2431673710.1038/nchembio.1411)
Tamsir, A., Tabor, J. J. & Voigt, C. A. Robust multicellular computing using genetically encoded NOR gates and chemical ‘wires’. Nature 469, 212–215 (2011). (PMID: 2115090310.1038/nature09565)
Partipilo, G., Graham, A. J., Belardi, B. & Keitz, B. K. Extracellular electron transfer enables cellular control of Cu(I)-catalyzed alkyne–azide cycloaddition. ACS Cent. Sci. https://doi.org/10.1021/acscentsci.1c01208 (2022). (PMID: 10.1021/acscentsci.1c01208352334568875427)
Gao, H., Chan, N., Oh, J. K. & Matyjaszewski, K. in In-Situ Gelling Polymers (ed. Loh, X. J.) 69–105 (Springer, 2014).
Tibbitt, M. W., Kloxin, A. M., Sawicki, L. & Anseth, K. S. Mechanical properties and degradation of chain and step polymerized photodegradable hydrogels. Macromolecules 46, 2785–2792 (2013). (PMID: 24496435365261710.1021/ma302522x)
Adzima, B. J. et al. spatial and temporal control of the alkyne–azide cycloaddition by photoinitiated Cu(II) reduction. Nat. Chem. 3, 256–259 (2011). (PMID: 2133633410.1038/nchem.980)
Hillsley, A., Santos, J. E. & Rosales, A. M. A deep learning approach to identify and segment alpha-smooth muscle actin stress fiber positive cells. Sci. Rep. 11, 21855 (2021). (PMID: 34750438857594310.1038/s41598-021-01304-4)
Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C. & Brown, R. A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349–363 (2002). (PMID: 1198876910.1038/nrm809)
Chaudhuri, O., Cooper-White, J., Janmey, P. A., Mooney, D. J. & Shenoy, V. B. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 584, 535–546 (2020). (PMID: 32848221767615210.1038/s41586-020-2612-2)
Hay, J. J. et al. Bacteria-based materials for stem cell engineering. Adv. Mater. 30, 1804310 (2018). (PMID: 10.1002/adma.201804310)
Su, L., Fukushima, T. & Ajo-Franklin, C. M. A hybrid cyt C maturation system enhances the bioelectrical performance of engineered Escherichia coli by improving the rate-limiting step. Biosens. Bioelectron. 165, 112312 (2020). (PMID: 3272947110.1016/j.bios.2020.112312)
Klumpp, S., Zhang, Z. & Hwa, T. Growth rate-dependent global effects on gene expression in bacteria. Cell 139, 1366–1375 (2009). (PMID: 20064380281899410.1016/j.cell.2009.12.001)
Zhang, H. M. et al. Measurements of gene expression at steady state improve the predictability of part assembly. ACS Synth. Biol. 5, 269–273 (2015). (PMID: 2665230710.1021/acssynbio.5b00156)
Hu, Y., Yang, Y., Katz, E. & Song, H. Programming the quorum sensing-based AND gate in shewanella oneidensis for logic gated-microbial fuel cells. Chem. Commun. Camb. Engl. 51, 4184–4187 (2015). (PMID: 10.1039/C5CC00026B)
Alon, U. An Introduction to Systems Biology: Design Principles of Biological Circuits 2nd edn (Chapman and Hall, 2019).
Groseclose, T. M., Rondon, R. E., Herde, Z. D., Aldrete, C. A. & Wilson, C. J. Engineered systems of inducible anti-repressors for the next generation of biological programming. Nat. Commun. 11, 4440 (2020). (PMID: 32895374747757310.1038/s41467-020-18302-1)
Molinari, S. et al. A de novo matrix for macroscopic living materials from bacteria. Nat. Commun. 13, 5544 (2022). (PMID: 36130968949268110.1038/s41467-022-33191-2)
Dai, Z. et al. Living fabrication of functional semi-interpenetrating polymeric materials. Nat. Commun. 12, 3422 (2021). (PMID: 34103521818737510.1038/s41467-021-23812-7)
Wang, F. et al. A biocompatible heterogeneous MOF–Cu catalyst for in vivo drug synthesis in targeted subcellular organelles. Angew. Chem. Int. Ed. 58, 6987–6992 (2019). (PMID: 10.1002/anie.201901760)
Hinz, B., Mastrangelo, D., Iselin, C. E., Chaponnier, C. & Gabbiani, G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am. J. Pathol. 159, 1009–1020 (2001). (PMID: 11549593185045510.1016/S0002-9440(10)61776-2)
Witte, K., Rodrigo-Navarro, A. & Salmeron-Sanchez, M. Bacteria-laden microgels as autonomous three-dimensional environments for stem cell engineering. Mater. Today Bio. 2, 100011 (2019). (PMID: 32159146706154810.1016/j.mtbio.2019.100011)
Petaroudi, M., Rodrigo‐Navarro, A., Dobre, O., Dalby, M. J. & Salmeron‐Sanchez, M. Living biomaterials to engineer hematopoietic stem cell niches. Adv. Healthc. Mater. 11, 2200964 (2022). (PMID: 10.1002/adhm.202200964)
Lee, K. Y. & Mooney, D. J. Hydrogels for tissue engineering. Chem. Rev. 101, 1869–1880 (2001). (PMID: 1171023310.1021/cr000108x)
Jeon, J. W., Cho, I. H., Ha, U. H., Seo, S. K. & Paek, S. H. Chemiluminometric immuno-analysis of innate immune response against repetitive bacterial stimulations for the same mammalian cells. Sci. Rep. 4, 6011 (2014). (PMID: 25109895412750210.1038/srep06011)
Schultz, G. S., Davidson, J. M., Kirsner, R. S., Bornstein, P. & Herman, I. M. Dynamic reciprocity in the wound microenvironment. Wound Repair Regen. 19, 134–148 (2011). (PMID: 21362080305135310.1111/j.1524-475X.2011.00673.x)
Freedman, B. R. et al. Enhanced tendon healing by a tough hydrogel with an adhesive side and high drug-loading capacity. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-021-00810-0 (2022). (PMID: 10.1038/s41551-021-00810-0356104849228023)
Heveran, C. M. et al. Biomineralization and successive regeneration of engineered living building materials. Matter 2, 481–494 (2020). (PMID: 10.1016/j.matt.2019.11.016)
Caro-Astorga, J., Walker, K. T., Herrera, N., Lee, K.-Y. & Ellis, T. Bacterial cellulose spheroids as building blocks for 3D and patterned living materials and for regeneration. Nat. Commun. 12, 5027 (2021). (PMID: 34413311837707310.1038/s41467-021-25350-8)
Cubillos-Ruiz, A. et al. An engineered live biotherapeutic for the prevention of antibiotic-induced dysbiosis. Nat. Biomed. Eng. 6, 910–921 (2022). (PMID: 3541111410.1038/s41551-022-00871-9)
Karbelkar, A. A., Reynolds, E. E., Ahlmark, R. & Furst, A. L. A microbial electrochemical technology to detect and degrade organophosphate pesticides. ACS Cent. Sci. 7, 1718–1727 (2021). (PMID: 34729415855484210.1021/acscentsci.1c00931)
Green, A. A. et al. Complex cellular logic computation using ribocomputing devices. Nature 548, 117–121 (2017). (PMID: 28746304607820310.1038/nature23271)
Yeh, Y.-C. et al. Mechanically dynamic PDMS substrates to investigate changing cell environments. Biomaterials 145, 23–32 (2017). (PMID: 28843064587143210.1016/j.biomaterials.2017.08.033)
معلومات مُعتمدة: FA9550-20-1-0088 United States Department of Defense | United States Air Force | AFMC | Air Force Office of Scientific Research (AF Office of Scientific Research); 1944334 National Science Foundation (NSF); DMR-1720595 National Science Foundation (NSF); ECCS-1542159 National Science Foundation (NSF); 1015895 Burroughs Wellcome Fund (BWF); F-1929 Welch Foundation; R35GM133640 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
تواريخ الأحداث: Date Created: 20240523 Latest Revision: 20240717
رمز التحديث: 20240718
DOI: 10.1038/s41589-024-01628-y
PMID: 38783133
قاعدة البيانات: MEDLINE
الوصف
تدمد:1552-4469
DOI:10.1038/s41589-024-01628-y