Synthesis of lipid membranes for artificial cells.
Journal
Nature reviews. Chemistry
ISSN: 2397-3358
Titre abrégé: Nat Rev Chem
Pays: England
ID NLM: 101703631
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
accepted:
09
06
2021
medline:
1
10
2021
pubmed:
1
10
2021
entrez:
28
4
2023
Statut:
ppublish
Résumé
A major goal of synthetic biology is to understand the transition between non-living matter and life. The bottom-up development of an artificial cell would provide a minimal system with which to study the border between chemistry and biology. So far, a fully synthetic cell has remained elusive, but chemists are progressing towards this goal by reconstructing cellular subsystems. Cell boundaries, likely in the form of lipid membranes, were necessary for the emergence of life. In addition to providing a protective barrier between cellular cargo and the external environment, lipid compartments maintain homeostasis with other subsystems to regulate cellular processes. In this Review, we examine different chemical approaches to making cell-mimetic compartments. Synthetic strategies to drive membrane formation and function, including bioorthogonal ligations, dissipative self-assembly and reconstitution of biochemical pathways, are discussed. Chemical strategies aim to recreate the interactions between lipid membranes, the external environment and internal biomolecules, and will clarify our understanding of life at the interface of chemistry and biology.
Identifiants
pubmed: 37118179
doi: 10.1038/s41570-021-00303-3
pii: 10.1038/s41570-021-00303-3
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
676-694Informations de copyright
© 2021. Springer Nature Limited.
Références
Arndt, N. T. & Nisbet, E. G. Processes on the young Earth and the habitats of early life. Annu. Rev. Earth Planet. Sci. 40, 521–549 (2012).
doi: 10.1146/annurev-earth-042711-105316
Darwin, C. The Correspondence of Charles Darwin Vol. 19 (eds Burkhardt, F. & Smith, S.) (Cambridge Univ. Press, 2012).
Luisi, P. L. The Emergence of Life: From Chemical Origins to Synthetic Biology 7–10 (Cambridge Univ. Press, 2016).
Lai, Y.-C. & Chen, I. A. Protocells. Curr. Biol. 30, R482–R485 (2020).
pubmed: 32428486
doi: 10.1016/j.cub.2020.03.038
Szostak, J. W., Bartel, D. P. & Luisi, P. L. Synthesizing life. Nature 409, 387–390 (2001).
pubmed: 11201752
doi: 10.1038/35053176
Pross, A. What is Life? How Chemistry Becomes Biology viii–xiv (Oxford Univ. Press, 2016).
Roberts, M. A. J., Cranenburgh, R. M., Stevens, M. P. & Oyston, P. C. F. Synthetic biology: biology by design. Microbiology 159, 1219–1220 (2013).
pubmed: 23744901
pmcid: 3749723
doi: 10.1099/mic.0.069724-0
Göpfrich, K., Platzman, I. & Spatz, J. P. Mastering complexity: towards bottom-up construction of multifunctional eukaryotic synthetic cells. Trends Biotechnol. 36, 938–951 (2018).
pubmed: 29685820
pmcid: 6100601
doi: 10.1016/j.tibtech.2018.03.008
Chyba, C. & Sagan, C. Endogenous production, exogenous delivery and impact-shock synthesis of organic molecules: an inventory for the origins of life. Nature 355, 125–132 (1992).
pubmed: 11538392
doi: 10.1038/355125a0
Bada, J. L. Prebiotic soup–revisiting the Miller experiment. Science 300, 745–746 (2003).
pubmed: 12730584
doi: 10.1126/science.1085145
Deamer, D. W. Assembling Life: How Can Life Begin on Earth and Other Habitable Planets? 1–10 (Oxford Univ. Press, 2019).
Trainer, M. G. Atmospheric prebiotic chemistry and organic hazes. Curr. Org. Chem. 17, 1710–1723 (2013).
pubmed: 24143126
pmcid: 3796891
doi: 10.2174/13852728113179990078
Ritson, D. J., Mojzsis, S. J. & Sutherland, J. D. Supply of phosphate to early Earth by photogeochemistry after meteoritic weathering. Nat. Geosci. 13, 344–348 (2020).
pubmed: 32395178
pmcid: 7213494
doi: 10.1038/s41561-020-0556-7
Saladino, R., Di Mauro, E. & García-Ruiz, J. M. A universal geochemical scenario for formamide condensation and prebiotic chemistry. Chem. Eur. J. 25, 3181–3189 (2019).
pubmed: 30230056
doi: 10.1002/chem.201803889
Damer, B. & Deamer, D. Coupled phases and combinatorial selection in fluctuating hydrothermal pools: a scenario to guide experimental approaches to the origin of cellular life. Life 5, 872–887 (2015).
pubmed: 25780958
pmcid: 4390883
doi: 10.3390/life5010872
Rimmer, P. B. & Shorttle, O. Origin of life’s building blocks in carbon- and nitrogen-rich surface hydrothermal vents. Life 9, 12 (2019).
pmcid: 6463091
doi: 10.3390/life9010012
Miller, S. L. A production of amino acids under possible primitive earth conditions. Science 117, 528–529 (1953).
pubmed: 13056598
doi: 10.1126/science.117.3046.528
Oró, J. & Kimball, A. P. Synthesis of purines under possible primitive earth conditions. I. Adenine from hydrogen cyanide. Arch. Biochem. Biophys. 94, 217–227 (1961).
pubmed: 13731263
doi: 10.1016/0003-9861(61)90033-9
Saladino, R., Crestini, C., Pino, S., Costanzo, G. & Di Mauro, E. Formamide and the origin of life. Phys. Life Rev. 9, 84–104 (2012).
pubmed: 22196896
doi: 10.1016/j.plrev.2011.12.002
Butlerow, A. Bildung einer zuckerartigen Substanz durch Synthese. Justus Liebigs Ann. Chem. 120, 295–298 (1861).
doi: 10.1002/jlac.18611200308
Pinto, J. P., Gladstone, G. R. & Yung, Y. L. Photochemical production of formaldehyde in Earth’s primitive atmosphere. Science 210, 183–185 (1980).
pubmed: 17741284
doi: 10.1126/science.210.4466.183
Mariani, A., Russell, D. A., Javelle, T. & Sutherland, J. D. A light-releasable potentially prebiotic nucleotide activating agent. J. Am. Chem. Soc. 140, 8657–8661 (2018).
pubmed: 29965757
pmcid: 6152610
doi: 10.1021/jacs.8b05189
Zhang, S. J., Duzdevich, D. & Szostak, J. W. Potentially prebiotic activation chemistry compatible with nonenzymatic RNA copying. J. Am. Chem. Soc. 142, 14810–14813 (2020).
pubmed: 32794700
doi: 10.1021/jacs.0c05300
Foden, C. S. et al. Prebiotic synthesis of cysteine peptides that catalyze peptide ligation in neutral water. Science 370, 865–869 (2020).
pubmed: 33184216
doi: 10.1126/science.abd5680
Liu, Z. et al. Harnessing chemical energy for the activation and joining of prebiotic building blocks. Nat. Chem. 12, 1023–1028 (2020).
pubmed: 33093680
pmcid: 7610406
doi: 10.1038/s41557-020-00564-3
Islam, S., Bučar, D.-K. & Powner, M. W. Prebiotic selection and assembly of proteinogenic amino acids and natural nucleotides from complex mixtures. Nat. Chem. 9, 584–589 (2017).
doi: 10.1038/nchem.2703
Xu, J. et al. Selective prebiotic formation of RNA pyrimidine and DNA purine nucleosides. Nature 582, 60–66 (2020).
pubmed: 32494078
pmcid: 7116818
doi: 10.1038/s41586-020-2330-9
Patel, B. H., Percivalle, C., Ritson, D. J., Duffy, C. D. & Sutherland, J. D. Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat. Chem. 7, 301–307 (2015).
pubmed: 25803468
pmcid: 4568310
doi: 10.1038/nchem.2202
Anderson, R. B., Friedel, R. A. & Storch, H. H. Fischer-Tropsch reaction mechanism involving stepwise growth of carbon chain. J. Chem. Phys. 19, 313–319 (1951).
doi: 10.1063/1.1748201
Nooner, D. W. & Oró, J. in Hydrocarbon Synthesis from Carbon Monoxide and Hydrogen Vol. 178, 159–171 (American Chemical Society, 1979).
Rushdi, A. I. & Simoneit, B. R. T. Lipid formation by aqueous Fischer-Tropsch-type synthesis over a temperature range of 100 to 400 °C. Orig. Life Evol. Biosph. 31, 103–118 (2001).
pubmed: 11296515
doi: 10.1023/A:1006702503954
McCollom, T. M., Ritter, G. & Simoneit, B. R. T. Lipid synthesis under hydrothermal conditions by Fischer-Tropsch-type reactions. Orig. Life Evol. Biosph. 29, 153–166 (1999).
pubmed: 10227201
doi: 10.1023/A:1006592502746
Scheidler, C., Sobotta, J., Eisenreich, W., Wächtershäuser, G. & Huber, C. Unsaturated C
pubmed: 27283227
pmcid: 4901337
doi: 10.1038/srep27595
Langworthy, T. A., Smith, P. F. & Mayberry, W. R. Lipids of Thermoplasma acidophilum. J. Bacteriol. 112, 1193–1200 (1972).
pubmed: 4344918
pmcid: 251548
doi: 10.1128/jb.112.3.1193-1200.1972
Woese, C. R., Magrum, L. J. & Fox, G. E. Archaebacteria. J. Mol. Evol. 11, 245–252 (1978).
pubmed: 691075
doi: 10.1007/BF01734485
Kates, M., Yengoyan, L. S. & Sastry, P. S. A diether analog of phosphatidyl glycerophosphate in Halobacterium cutirubrum. Biochim. Biophys. Acta 98, 252–268 (1965).
pubmed: 14320220
doi: 10.1016/0005-2760(65)90119-0
Lombard, J., López-García, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10, 507–515 (2012).
pubmed: 22683881
doi: 10.1038/nrmicro2815
Nooner, D. W., Sherwood, E., More, M. A. & Oró, J. Cyanamide mediated syntheses under plausible primitive earth conditions. III. Synthesis of peptides. J. Mol. Evol. 10, 211–220 (1977).
pubmed: 599571
doi: 10.1007/BF01764596
Sherwood, E., Joshi, A. & Orb, J. Cyanamide mediated syntheses under plausible primitive earth conditions. II. The polymerization of deoxythymidine 5′-triphosphate. J. Mol. Evol. 10, 193–209 (1977).
pubmed: 599570
doi: 10.1007/BF01764595
Eichberg, J., Sherwood, E., Epps, D. E. & Oró, J. Cyanamide mediated syntheses under plausible primitive earth conditions. IV. The synthesis of acylglycerols. J. Mol. Evol. 10, 221–230 (1977).
pubmed: 599572
doi: 10.1007/BF01764597
Simoneit, B. R. T., Rushdi, A. I. & Deamer, D. W. Abiotic formation of acylglycerols under simulated hydrothermal conditions and self-assembly properties of such lipid products. Adv. Space Res. 40, 1649–1656 (2007).
doi: 10.1016/j.asr.2007.07.034
Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).
pubmed: 19444213
doi: 10.1038/nature08013
Ritson, D. J. & Sutherland, J. D. Synthesis of aldehydic ribonucleotide and amino acid precursors by photoredox chemistry. Angew. Chem. Int. Ed. 52, 5845–5847 (2013).
doi: 10.1002/anie.201300321
Tsanakopoulou, M. & Sutherland, J. D. Cyanamide as a prebiotic phosphate activating agent – catalysis by simple 2-oxoacid salts. Chem. Commun. 53, 11893–11896 (2017).
doi: 10.1039/C7CC07517K
Xu, J. et al. Photochemical reductive homologation of hydrogen cyanide using sulfite and ferrocyanide. Chem. Commun. 54, 5566–5569 (2018).
doi: 10.1039/C8CC01499J
Hargreaves, W. R., Mulvihill, S. J. & Deamer, D. W. Synthesis of phospholipids and membranes in prebiotic conditions. Nature 266, 78–80 (1977).
pubmed: 840303
doi: 10.1038/266078a0
Epps, D. E., Sherwood, E., Eichberg, J. & Oró, J. Cyanamide mediated syntheses under plausible primitive earth conditions. V. The synthesis of phosphatidic acids. J. Mol. Evol. 11, 279–292 (1978).
pubmed: 722805
doi: 10.1007/BF01733838
Rao, M., Eichberg, J. & Oró, J. Synthesis of phosphatidylcholine under possible primitive Earth conditions. J. Mol. Evol. 18, 196–202 (1982).
pubmed: 7097779
doi: 10.1007/BF01733046
Fayolle, D. et al. Crude phosphorylation mixtures containing racemic lipid amphiphiles self-assemble to give stable primitive compartments. Sci. Rep. 7, 18106 (2017).
pubmed: 29273739
pmcid: 5741756
doi: 10.1038/s41598-017-18053-y
Gibard, C., Bhowmik, S., Karki, M., Kim, E.-K. & Krishnamurthy, R. Phosphorylation, oligomerization and self-assembly in water under potential prebiotic conditions. Nat. Chem. 10, 212–217 (2018).
pubmed: 29359747
doi: 10.1038/nchem.2878
Joshi, M. P., Samanta, A., Tripathy, G. R. & Rajamani, S. Formation and stability of prebiotically relevant vesicular systems in terrestrial geothermal environments. Life 7, 51 (2017).
pmcid: 5745564
doi: 10.3390/life7040051
Maurer, S. The impact of salts on single chain amphiphile membranes and implications for the location of the origin of life. Life 7, 44 (2017).
pmcid: 5745557
doi: 10.3390/life7040044
Maurer, S. E. & Nguyen, G. Prebiotic vesicle formation and the necessity of salts. Orig. Life Evol. Biosph. 46, 215–222 (2016).
pubmed: 26590931
doi: 10.1007/s11084-015-9476-8
Monnard, P.-A., Apel, C. L., Kanavarioti, A. & Deamer, D. W. Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. Astrobiology 2, 139–152 (2002).
pubmed: 12469365
doi: 10.1089/15311070260192237
Milshteyn, D., Damer, B., Havig, J. & Deamer, D. Amphiphilic compounds assemble into membranous vesicles in hydrothermal hot spring water but not in seawater. Life 8, 11 (2018).
pmcid: 6027054
doi: 10.3390/life8020011
Jordan, S. F. et al. Promotion of protocell self-assembly from mixed amphiphiles at the origin of life. Nat. Ecol. Evol. 3, 1705–1714 (2019).
pubmed: 31686020
doi: 10.1038/s41559-019-1015-y
Toparlak, Ö. D., Karki, M., Ortuno, V. E., Krishnamurthy, R. & Mansy, S. S. Cyclophospholipids increase protocellular stability to metal ions. Small 16, 1903381 (2020).
doi: 10.1002/smll.201903381
Jung, H. T., Coldren, B., Zasadzinski, J. A., Iampietro, D. J. & Kaler, E. W. The origins of stability of spontaneous vesicles. Proc. Natl Acad. Sci. USA 98, 1353–1357 (2001).
pubmed: 11171954
pmcid: 29260
doi: 10.1073/pnas.98.4.1353
Kindt, J. T., Szostak, J. W. & Wang, A. Bulk self-assembly of giant, unilamellar vesicles. ACS Nano 14, 14627–14634 (2020).
pubmed: 32602696
doi: 10.1021/acsnano.0c03125
pmcid: 8172239
Hanczyc, M. M., Mansy, S. S. & Szostak, J. W. Mineral surface directed membrane assembly. Orig. Life Evol. Biosph. 37, 67–82 (2007).
pubmed: 16909329
doi: 10.1007/s11084-006-9018-5
Hanczyc, M. M., Fujikawa, S. M. & Szostak, J. W. Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302, 618–622 (2003).
pubmed: 14576428
pmcid: 4484575
doi: 10.1126/science.1089904
Xu, J., Stevens, M. J., Oleson, T. A., Last, J. A. & Sahai, N. Role of oxide surface chemistry and phospholipid phase on adsorption and self-assembly: isotherms and atomic force microscopy. J. Phys. Chem. 113, 2187–2196 (2009).
Oleson, T. A., Sahai, N. & Pedersen, J. A. Electrostatic effects on deposition of multiple phospholipid bilayers at oxide surfaces. J. Colloid Interface Sci. 352, 327–336 (2010).
pubmed: 20869065
doi: 10.1016/j.jcis.2010.08.057
Oleson, T. A. & Sahai, N. Interaction energies between oxide surfaces and multiple phosphatidylcholine bilayers from extended-DLVO theory. J. Colloid Interface Sci. 352, 316–326 (2010).
pubmed: 20869066
doi: 10.1016/j.jcis.2010.08.056
Oleson, T. A. et al. Neutron reflectivity study of substrate surface chemistry effects on supported phospholipid bilayer formation on (11[Formula: see text]0) sapphire. J. Colloid Interface Sci. 370, 192–200 (2012).
pubmed: 22244865
doi: 10.1016/j.jcis.2011.12.031
Sahai, N. et al. Mineral surface chemistry and nanoparticle-aggregation control membrane self-assembly. Sci. Rep. 7, 43418 (2017).
pubmed: 28266537
pmcid: 5339912
doi: 10.1038/srep43418
Fiore, M., Maniti, O., Girard-Egrot, A., Monnard, P.-A. & Strazewski, P. Glass microsphere-supported giant vesicles for the observation of self-reproduction of lipid boundaries. Angew. Chem. 130, 288–292 (2018).
doi: 10.1002/ange.201710708
Dalai, P. & Sahai, N. Mineral–lipid interactions in the origins of life. Trends Biochem. Sci. 44, 331–341 (2019).
pubmed: 30583961
doi: 10.1016/j.tibs.2018.11.009
Walde, P., Wick, R., Fresta, M., Mangone, A. & Luisi, P. L. Autopoietic self-reproduction of fatty acid vesicles. J. Am. Chem. Soc. 116, 11649–11654 (1994).
doi: 10.1021/ja00105a004
Wick, R., Walde, P. & Luisi, P. L. Light microscopic investigations of the autocatalytic self-reproduction of giant vesicles. J. Am. Chem. Soc. 117, 1435–1436 (1995).
doi: 10.1021/ja00109a031
Budin, I., Debnath, A. & Szostak, J. W. Concentration-driven growth of model protocell membranes. J. Am. Chem. Soc. 134, 20812–20819 (2012).
pubmed: 23198690
pmcid: 3530389
doi: 10.1021/ja310382d
Zhu, T. F. & Szostak, J. W. Coupled growth and division of model protocell membranes. J. Am. Chem. Soc. 131, 5705–5713 (2009).
pubmed: 19323552
pmcid: 2669828
doi: 10.1021/ja900919c
Toparlak, Ö. D., Wang, A. & Mansy, S. S. Population-level membrane diversity triggers growth and division of protocells. JACS Au 1, 560–568 (2021).
pubmed: 34467319
pmcid: 8395648
doi: 10.1021/jacsau.0c00079
Bonfio, C. et al. Length-selective synthesis of acylglycerol-phosphates through energy-dissipative cycling. J. Am. Chem. Soc. 141, 3934–3939 (2019).
pubmed: 30767518
pmcid: 6506141
doi: 10.1021/jacs.8b12331
Budin, I., Prywes, N., Zhang, N. & Szostak, J. W. Chain-length heterogeneity allows for the assembly of fatty acid vesicles in dilute solutions. Biophys. J. 107, 1582–1590 (2014).
pubmed: 25296310
pmcid: 4190651
doi: 10.1016/j.bpj.2014.07.067
Jin, L., Kamat, N. P., Jena, S. & Szostak, J. W. Fatty acid/phospholipid blended membranes: a potential intermediate state in protocellular evolution. Small 14, 1704077 (2018).
doi: 10.1002/smll.201704077
Dalai, P., Ustriyana, P. & Sahai, N. Aqueous magnesium as an environmental selection pressure in the evolution of phospholipid membranes on early earth. Geochim. Cosmochim. Acta 223, 216–228 (2018).
doi: 10.1016/j.gca.2017.11.034
Budin, I. & Szostak, J. W. Physical effects underlying the transition from primitive to modern cell membranes. Proc. Natl Acad. Sci. USA 108, 5249–5254 (2011).
pubmed: 21402937
pmcid: 3069173
doi: 10.1073/pnas.1100498108
Gompertz, D. Phospholipids and their metabolism. J. Clin. Pathol. 26 (Suppl. 1), 11–16 (1973).
doi: 10.1136/jcp.s1-5.1.11
Devaraj, N. K. In situ synthesis of phospholipid membranes. J. Org. Chem. 82, 5997–6005 (2017).
pubmed: 28467841
doi: 10.1021/acs.joc.7b00604
Budin, I. & Devaraj, N. K. Membrane assembly driven by a biomimetic coupling reaction. J. Am. Chem. Soc. 134, 751–753 (2012).
pubmed: 22239722
doi: 10.1021/ja2076873
Hardy, M. D., Konetski, D., Bowman, C. N. & Devaraj, N. K. Ruthenium photoredox-triggered phospholipid membrane formation. Org. Biomol. Chem. 14, 5555–5558 (2016).
pubmed: 26924258
doi: 10.1039/C6OB00290K
Enomoto, T., Brea, R. J., Bhattacharya, A. & Devaraj, N. K. In situ lipid membrane formation triggered by intramolecular photoinduced electron transfer. Langmuir 34, 750–755 (2018).
pubmed: 28982007
doi: 10.1021/acs.langmuir.7b02783
Konetski, D., Gong, T. & Bowman, C. N. Photoinduced vesicle formation via the copper-catalyzed azide–alkyne cycloaddition reaction. Langmuir 32, 8195–8201 (2016).
pubmed: 27443396
doi: 10.1021/acs.langmuir.6b02043
Dawson, P. E., Muir, T. W., Clark-Lewis, I. & Kent, S. B. Synthesis of proteins by native chemical ligation. Science 266, 776–779 (1994).
pubmed: 7973629
doi: 10.1126/science.7973629
Brea, R. J., Cole, C. M. & Devaraj, N. K. In situ vesicle formation by native chemical ligation. Angew. Chem. Int. Ed. 53, 14102–14105 (2014).
doi: 10.1002/anie.201408538
Brea, R., Bhattacharya, A. & Devaraj, N. Spontaneous phospholipid membrane formation by histidine ligation. Synlett 28, 108–112 (2016).
doi: 10.1055/s-0036-1588634
Ruff, Y., Garavini, V. & Giuseppone, N. Reversible native chemical ligation: a facile access to dynamic covalent peptides. J. Am. Chem. Soc. 136, 6333–6339 (2014).
pubmed: 24717128
doi: 10.1021/ja4129845
Brea, R. J., Rudd, A. K. & Devaraj, N. K. Nonenzymatic biomimetic remodeling of phospholipids in synthetic liposomes. Proc. Natl Acad. Sci. USA 113, 8589–8594 (2016).
pubmed: 27439858
pmcid: 4978229
doi: 10.1073/pnas.1605541113
Seoane, A., Brea, R. J., Fuertes, A., Podolsky, K. A. & Devaraj, N. K. Biomimetic generation and remodeling of phospholipid membranes by dynamic imine chemistry. J. Am. Chem. Soc. 140, 8388–8391 (2018).
pubmed: 29886740
pmcid: 6251970
doi: 10.1021/jacs.8b04557
Konetski, D., Mavila, S., Wang, C., Worrell, B. & Bowman, C. N. Production of dynamic lipid bilayers using the reversible thiol–thioester exchange reaction. Chem. Commun. 54, 8108–8111 (2018).
doi: 10.1039/C8CC03471K
Huynh, H. et al. Control of vesicle fusion by a tyrosine phosphatase. Nat. Cell Biol. 6, 831–839 (2004).
pubmed: 15322554
doi: 10.1038/ncb1164
Marsden, H. R., Korobko, A. V., Zheng, T., Voskuhl, J. & Kros, A. Controlled liposome fusion mediated by SNARE protein mimics. Biomater. Sci. 1, 1046–1054 (2013).
doi: 10.1039/c3bm60040h
Xu, W., Wang, J., Rothman, J. E. & Pincet, F. Accelerating SNARE-mediated membrane fusion by DNA–lipid tethers. Angew. Chem. Int. Ed. 54, 14388–14392 (2015).
doi: 10.1002/anie.201506844
Kong, L., Askes, S. H. C., Bonnet, S., Kros, A. & Campbell, F. Temporal control of membrane fusion through photolabile PEGylation of liposome membranes. Angew. Chem. 128, 1418–1422 (2016).
doi: 10.1002/ange.201509673
Löffler, P. M. G. et al. A DNA-programmed liposome fusion cascade. Angew. Chem. Int. Ed. 56, 13228–13231 (2017).
doi: 10.1002/anie.201703243
Ries, O., Löffler, P. M. G., Rabe, A., Malavan, J. J. & Vogel, S. Efficient liposome fusion mediated by lipid–nucleic acid conjugates. Org. Biomol. Chem. 15, 8936–8945 (2017).
pubmed: 29043358
doi: 10.1039/C7OB01939D
Deshpande, S., Spoelstra, W. K., van Doorn, M., Kerssemakers, J. & Dekker, C. Mechanical division of cell-sized liposomes. ACS Nano 12, 2560–2568 (2018).
pubmed: 29455527
pmcid: 5876618
doi: 10.1021/acsnano.7b08411
Caspi, Y. & Dekker, C. Divided we stand: splitting synthetic cells for their proliferation. Syst. Synth. Biol. 8, 249–269 (2014).
pubmed: 25136387
pmcid: 4127174
doi: 10.1007/s11693-014-9145-7
van den Bogaart, G. et al. Membrane protein sequestering by ionic protein–lipid interactions. Nature 479, 552–555 (2011).
pubmed: 22020284
pmcid: 3409895
doi: 10.1038/nature10545
Konetski, D., Baranek, A., Mavila, S., Zhang, X. & Bowman, C. N. Formation of lipid vesicles in situ utilizing the thiol-Michael reaction. Soft Matter 14, 7645–7652 (2018).
pubmed: 30175341
doi: 10.1039/C8SM01329B
Xiong, F. et al. A bioinspired and biocompatible ortho-sulfiliminyl phenol synthesis. Nat. Commun. 8, 15912 (2017).
pubmed: 28627513
pmcid: 5481830
doi: 10.1038/ncomms15912
Liu, L. et al. Enzyme-free synthesis of natural phospholipids in water. Nat. Chem. 12, 1029–1034 (2020).
pubmed: 33046841
doi: 10.1038/s41557-020-00559-0
pmcid: 8849033
Bachmann, P. A., Walde, P., Luisi, P. L. & Lang, J. Self-replicating reverse micelles and chemical autopoiesis. J. Am. Chem. Soc. 112, 8200–8201 (1990).
doi: 10.1021/ja00178a073
Bachmann, P. A., Luisi, P. L. & Lang, J. Autocatalytic self-replicating micelles as models for prebiotic structures. Nature 357, 57–59 (1992).
doi: 10.1038/357057a0
Bachmann, P. A., Walde, P., Luisi, P. L. & Lang, J. Self-replicating micelles: aqueous micelles and enzymatically driven reactions in reverse micelles. J. Am. Chem. Soc. 113, 8204–8209 (1991).
doi: 10.1021/ja00022a002
Schmidli, P. K., Schurtenberger, P. & Luisi, P. L. Liposome-mediated enzymatic synthesis of phosphatidylcholine as an approach to self-replicating liposomes. J. Am. Chem. Soc. 113, 8127–8130 (1991).
doi: 10.1021/ja00021a043
Takahashi, H. et al. Autocatalytic membrane-amplification on a pre-existing vesicular surface. Chem. Commun. 46, 8791–8793 (2010).
doi: 10.1039/c0cc02758h
Matsuo, M. et al. A sustainable self-reproducing liposome consisting of a synthetic phospholipid. Chem. Phys. Lipids 222, 1–7 (2019).
pubmed: 31002782
doi: 10.1016/j.chemphyslip.2019.04.007
Hardy, M. D. et al. Self-reproducing catalyst drives repeated phospholipid synthesis and membrane growth. Proc. Natl Acad. Sci. USA 112, 8187–8192 (2015).
pubmed: 26100914
pmcid: 4500204
doi: 10.1073/pnas.1506704112
Post, E. A. J., J. Bissette, A. & Fletcher, S. P. Self-reproducing micelles coupled to a secondary catalyst. Chem. Commun. 54, 8777–8780 (2018).
doi: 10.1039/C8CC02136H
Post, E. A. J. & Fletcher, S. P. Controlling the kinetics of self-reproducing micelles by catalyst compartmentalization in a biphasic system. J. Org. Chem. 84, 2741–2755 (2019).
pubmed: 30698970
pmcid: 6459585
doi: 10.1021/acs.joc.8b03149
Bissette, A. J., Odell, B. & Fletcher, S. P. Physical autocatalysis driven by a bond-forming thiol–ene reaction. Nat. Commun. 5, 4607 (2014).
pubmed: 25178358
doi: 10.1038/ncomms5607
Ortega-Arroyo, J., Bissette, A. J., Kukura, P. & Fletcher, S. P. Visualization of the spontaneous emergence of a complex, dynamic, and autocatalytic system. Proc. Natl Acad. Sci. USA 113, 11122–11126 (2016).
pubmed: 27638200
pmcid: 5056079
doi: 10.1073/pnas.1602363113
Colomer, I., Morrow, S. M. & Fletcher, S. P. A transient self-assembling self-replicator. Nat. Commun. 9, 2239 (2018).
pubmed: 29884880
pmcid: 5993787
doi: 10.1038/s41467-018-04670-2
Colomer, I., Borissov, A. & Fletcher, S. P. Selection from a pool of self-assembling lipid replicators. Nat. Commun. 11, 176 (2020).
pubmed: 31924788
pmcid: 6954257
doi: 10.1038/s41467-019-13903-x
Schrödinger, E. What is Life? (Cambridge Univ. Press, 1992).
Rieß, B., Grötsch, R. K. & Boekhoven, J. The design of dissipative molecular assemblies driven by chemical reaction cycles. Chem 6, 552–578 (2020).
doi: 10.1016/j.chempr.2019.11.008
Morrow, S. M., Colomer, I. & Fletcher, S. P. A chemically fuelled self-replicator. Nat. Commun. 10, 1011 (2019).
pubmed: 30824804
pmcid: 6397266
doi: 10.1038/s41467-019-08885-9
Engwerda, A. H. J. et al. Coupled metabolic cycles allow out-of-equilibrium autopoietic vesicle replication. Angew. Chem. Int. Ed. 59, 20361–20366 (2020).
doi: 10.1002/anie.202007302
Post, E. A. J. & Fletcher, S. P. Dissipative self-assembly, competition and inhibition in a self-reproducing protocell model. Chem. Sci. 11, 9434–9442 (2020).
pubmed: 34094210
pmcid: 8162124
doi: 10.1039/D0SC02768E
Tena-Solsona, M. et al. Non-equilibrium dissipative supramolecular materials with a tunable lifetime. Nat. Commun. 8, 15895 (2017).
pubmed: 28719591
pmcid: 5520059
doi: 10.1038/ncomms15895
Tena-Solsona, M., Wanzke, C., Riess, B., Bausch, A. R. & Boekhoven, J. Self-selection of dissipative assemblies driven by primitive chemical reaction networks. Nat. Commun. 9, 2044 (2018).
pubmed: 29795292
pmcid: 5966463
doi: 10.1038/s41467-018-04488-y
Wanzke, C. et al. Dynamic vesicles formed by dissipative self-assembly. ChemSystemsChem 2, e1900044 (2020).
doi: 10.1002/syst.201900044
Singh, N., Formon, G. J. M., Piccoli, S. D. & Hermans, T. M. Devising synthetic reaction cycles for dissipative nonequilibrium self-assembly. Adv. Mater. 32, 1906834 (2020).
doi: 10.1002/adma.201906834
Lange, N. de, Leermakers, F. A. M. & Kleijn, J. M. Self-limiting aggregation of phospholipid vesicles. Soft Matter 16, 2379–2389 (2020).
pubmed: 32064491
doi: 10.1039/C9SM01692A
Alcinesio, A. et al. Controlled packing and single-droplet resolution of 3D-printed functional synthetic tissues. Nat. Commun. 11, 2105 (2020).
pubmed: 32355158
pmcid: 7192927
doi: 10.1038/s41467-020-15953-y
Ai, Y., Xie, R., Xiong, J. & Liang, Q. Microfluidics for biosynthesizing: from droplets and vesicles to artificial cells. Small 16, 1903940 (2020).
doi: 10.1002/smll.201903940
Robinson, T. Microfluidic handling and analysis of giant vesicles for use as artificial cells: a review. Adv. Biosyst. 3, 1800318 (2019).
doi: 10.1002/adbi.201800318
Ugrinic, M., deMello, A. & Tang, T.-Y. D. Microfluidic tools for bottom-up synthetic cellularity. Chem 5, 1727–1742 (2019).
doi: 10.1016/j.chempr.2019.03.012
Deng, N.-N., Yelleswarapu, M. & Huck, W. T. S. Monodisperse uni- and multicompartment liposomes. J. Am. Chem. Soc. 138, 7584–7591 (2016).
pubmed: 27243596
doi: 10.1021/jacs.6b02107
Lange, N., de, Leermakers, F. & Mieke Kleijn, J. Step-wise linking of vesicles by combining reversible and irreversible linkers–towards total control on vesicle aggregate sizes. Soft Matter 16, 6773–6783 (2020).
pubmed: 32633317
doi: 10.1039/D0SM00995D
Haller, B. et al. Charge-controlled microfluidic formation of lipid-based single- and multicompartment systems. Lab. Chip 18, 2665–2674 (2018).
pubmed: 30070293
doi: 10.1039/C8LC00582F
Weiss, M. et al. Sequential bottom-up assembly of mechanically stabilized synthetic cells by microfluidics. Nat. Mater. 17, 89–96 (2018).
pubmed: 29035355
doi: 10.1038/nmat5005
Wang, L. et al. Single-step fabrication of multi-compartmentalized biphasic proteinosomes. Chem. Commun. 53, 8537–8540 (2017).
doi: 10.1039/C7CC04180B
Göpfrich, K. et al. One-pot assembly of complex giant unilamellar vesicle-based synthetic cells. ACS Synth. Biol. 8, 937–947 (2019).
pubmed: 31042361
pmcid: 6528161
doi: 10.1021/acssynbio.9b00034
Saha, R. & Chen, I. A. Origin of life: protocells red in tooth and claw. Curr. Biol. 25, R1175–R1177 (2015).
pubmed: 26702654
doi: 10.1016/j.cub.2015.11.007
Chen, I. A., Roberts, R. W. & Szostak, J. W. The emergence of competition between model protocells. Science 305, 1474–1476 (2004).
pubmed: 15353806
pmcid: 4484590
doi: 10.1126/science.1100757
Chakrabarti, A. C., Breaker, R. R., Joyce, G. F. & Deamer, D. W. Production of RNA by a polymerase protein encapsulated within phospholipid vesicles. J. Mol. Evol. 39, 555–559 (1994).
pubmed: 7528810
doi: 10.1007/BF00160400
Deamer, D. W. & Barchfeld, G. L. Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions. J. Mol. Evol. 18, 203–206 (1982).
pubmed: 7097780
doi: 10.1007/BF01733047
Rajamani, S. et al. Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig. Life Evol. Biosph. 38, 57–74 (2008).
pubmed: 18008180
doi: 10.1007/s11084-007-9113-2
O’Flaherty, D. K. et al. Copying of mixed-sequence RNA templates inside model protocells. J. Am. Chem. Soc. 140, 5171–5178 (2018).
pubmed: 29608310
pmcid: 7547884
doi: 10.1021/jacs.8b00639
Chen, I. A., Salehi-Ashtiani, K. & Szostak, J. W. RNA catalysis in model protocell vesicles. J. Am. Chem. Soc. 127, 13213–13219 (2005).
pubmed: 16173749
pmcid: 5072289
doi: 10.1021/ja051784p
Tsuji, G., Fujii, S., Sunami, T. & Yomo, T. Sustainable proliferation of liposomes compatible with inner RNA replication. Proc. Natl Acad. Sci. USA 113, 590–595 (2016).
pubmed: 26711996
doi: 10.1073/pnas.1516893113
Kurihara, K. et al. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat. Chem. 3, 775–781 (2011).
pubmed: 21941249
doi: 10.1038/nchem.1127
Kurihara, K. et al. A recursive vesicle-based model protocell with a primitive model cell cycle. Nat. Commun. 6, 8352 (2015).
pubmed: 26418735
doi: 10.1038/ncomms9352
Matsuo, M. et al. DNA length-dependent division of a giant vesicle-based model protocell. Sci. Rep. 9, 6916 (2019).
pubmed: 31061467
pmcid: 6502804
doi: 10.1038/s41598-019-43367-4
Matsuo, M. et al. Environment-sensitive intelligent self-reproducing artificial cell with a modification-active lipo-deoxyribozyme. Micromachines 11, 606 (2020).
pmcid: 7344958
doi: 10.3390/mi11060606
Saha, R., Verbanic, S. & Chen, I. A. Lipid vesicles chaperone an encapsulated RNA aptamer. Nat. Commun. 9, 2313 (2018).
pubmed: 29899431
pmcid: 5998061
doi: 10.1038/s41467-018-04783-8
Engelhart, A. E., Adamala, K. P. & Szostak, J. W. A simple physical mechanism enables homeostasis in primitive cells. Nat. Chem. 8, 448–453 (2016).
pubmed: 27102678
pmcid: 4929987
doi: 10.1038/nchem.2475
van Nies, P. et al. Self-replication of DNA by its encoded proteins in liposome-based synthetic cells. Nat. Commun. 9, 1583 (2018).
pubmed: 29679002
pmcid: 5910420
doi: 10.1038/s41467-018-03926-1
Caschera, F., Woo Lee, J., Kenneth, K. Y. H., Liu, A. P. & Michael, C. J. Cell-free compartmentalized protein synthesis inside double emulsion templated liposomes with in vitro synthesized and assembled ribosomes. Chem. Commun. 52, 5467–5469 (2016).
doi: 10.1039/C6CC00223D
Godino, E. et al. De novo synthesized Min proteins drive oscillatory liposome deformation and regulate FtsA-FtsZ cytoskeletal patterns. Nat. Commun. 10, 4969 (2019).
pubmed: 31672986
pmcid: 6823393
doi: 10.1038/s41467-019-12932-w
Godino, E. et al. Cell-free biogenesis of bacterial division proto-rings that can constrict liposomes. Commun. Biol. 3, 539 (2020).
pubmed: 32999429
pmcid: 7527988
doi: 10.1038/s42003-020-01258-9
Garenne, D., Libchaber, A. & Noireaux, V. Membrane molecular crowding enhances MreB polymerization to shape synthetic cells from spheres to rods. Proc. Natl Acad. Sci. USA 117, 1902–1909 (2020).
pubmed: 31932440
pmcid: 6994999
doi: 10.1073/pnas.1914656117
Garenne, D. & Noireaux, V. Analysis of cytoplasmic and membrane molecular crowding in genetically programmed synthetic cells. Biomacromolecules 21, 2808–2817 (2020).
pubmed: 32441931
doi: 10.1021/acs.biomac.0c00513
Vibhute, M. A. et al. Transcription and translation in cytomimetic protocells perform most efficiently at distinct macromolecular crowding conditions. ACS Synth. Biol. 9, 2797–2807 (2020).
pubmed: 32976714
pmcid: 7573978
doi: 10.1021/acssynbio.0c00330
Exterkate, M., Caforio, A., Stuart, M. C. A. & Driessen, A. J. M. Growing membranes in vitro by continuous phospholipid biosynthesis from free fatty acids. ACS Synth. Biol. 7, 153–165 (2018).
pubmed: 28922922
doi: 10.1021/acssynbio.7b00265
Stano, P., Wehrli, E. & Luisi, P. L. Insights into the self-reproduction of oleate vesicles. J. Phys. Condens. Matter 18, S2231–S2238 (2006).
doi: 10.1088/0953-8984/18/33/S37
Bhattacharya, A., Brea, R. J., Niederholtmeyer, H. & Devaraj, N. K. A minimal biochemical route towards de novo formation of synthetic phospholipid membranes. Nat. Commun. 10, 300 (2019).
pubmed: 30655537
pmcid: 6336818
doi: 10.1038/s41467-018-08174-x
Scott, A. et al. Cell-free phospholipid biosynthesis by gene-encoded enzymes reconstituted in liposomes. PLoS ONE 11, e0163058 (2016).
pubmed: 27711229
pmcid: 5053487
doi: 10.1371/journal.pone.0163058
Blanken, D., Foschepoth, D., Serrão, A. C. & Danelon, C. Genetically controlled membrane synthesis in liposomes. Nat. Commun. 11, 4317 (2020).
pubmed: 32859896
pmcid: 7455746
doi: 10.1038/s41467-020-17863-5
Ikari, K. et al. Dynamics of fatty acid vesicles in response to pH stimuli. Soft Matter 11, 6327–6334 (2015).
pubmed: 26166464
doi: 10.1039/C5SM01248A
Miele, Y. et al. Self-division of giant vesicles driven by an internal enzymatic reaction. Chem. Sci. 11, 3228–3235 (2020).
pubmed: 34122829
pmcid: 8157745
doi: 10.1039/C9SC05195C
Kurisu, M. et al. Reproduction of vesicles coupled with a vesicle surface-confined enzymatic polymerisation. Commun. Chem. 2, 117 (2019).
doi: 10.1038/s42004-019-0218-0
Allolio, C. et al. Arginine-rich cell-penetrating peptides induce membrane multilamellarity and subsequently enter via formation of a fusion pore. Proc. Natl Acad. Sci. USA 115, 11923–11928 (2018).
pubmed: 30397112
pmcid: 6255155
doi: 10.1073/pnas.1811520115
Banerjee, P., Pal, S., Kundu, N., Mondal, D. & Sarkar, N. A cell-penetrating peptide induces the self-reproduction of phospholipid vesicles: understanding the role of the bilayer rigidity. Chem. Commun. 54, 11451–11454 (2018).
doi: 10.1039/C8CC07176D
Schwille, P. Division in synthetic cells. Emerg. Top. Life Sci. 3, 551–558 (2019).
pubmed: 33523162
doi: 10.1042/ETLS20190023
Kretschmer, S., Ganzinger, K. A., Franquelim, H. G. & Schwille, P. Synthetic cell division via membrane-transforming molecular assemblies. BMC Biol. 17, 43 (2019).
pubmed: 31126285
pmcid: 6533746
doi: 10.1186/s12915-019-0665-1
Hürtgen, D., Härtel, T., Murray, S. M., Sourjik, V. & Schwille, P. Functional modules of minimal cell division for synthetic biology. Adv. Biosyst. 3, 1800315 (2019).
doi: 10.1002/adbi.201800315
Gaut, N. J. & Adamala, K. P. Reconstituting natural cell elements in synthetic cells. Adv. Biol. 5, 2000188 (2021).
doi: 10.1002/adbi.202000188
Elani, Y., V. Law, R. & Ces, O. Protein synthesis in artificial cells: using compartmentalisation for spatial organisation in vesicle bioreactors. Phys. Chem. Chem. Phys. 17, 15534–15537 (2015).
pubmed: 25932977
doi: 10.1039/C4CP05933F
Chakraborty, T., Bartelt, S. M., Steinkühler, J., Dimova, R. & Wegner, S. V. Light controlled cell-to-cell adhesion and chemical communication in minimal synthetic cells. Chem. Commun. 55, 9448–9451 (2019).
doi: 10.1039/C9CC04768A
Elani, Y., Law, R. V. & Ces, O. Vesicle-based artificial cells as chemical microreactors with spatially segregated reaction pathways. Nat. Commun. 5, 5305 (2014).
pubmed: 25351716
doi: 10.1038/ncomms6305
Li, S., Wang, X., Mu, W. & Han, X. Chemical signal communication between two protoorganelles in a lipid-based artificial cell. Anal. Chem. 91, 6859–6864 (2019).
pubmed: 31020837
doi: 10.1021/acs.analchem.9b01128
Hindley, J. W. et al. Building a synthetic mechanosensitive signaling pathway in compartmentalized artificial cells. Proc. Natl Acad. Sci. USA 116, 16711–16716 (2019).
pubmed: 31371493
pmcid: 6708380
doi: 10.1073/pnas.1903500116
Lee, K. Y. et al. Photosynthetic artificial organelles sustain and control ATP-dependent reactions in a protocellular system. Nat. Biotechnol. 36, 530–535 (2018).
pubmed: 29806849
doi: 10.1038/nbt.4140
Lentini, R., Yeh Martín, N. & Mansy, S. S. Communicating artificial cells. Curr. Opin. Chem. Biol. 34, 53–61 (2016).
pubmed: 27352299
doi: 10.1016/j.cbpa.2016.06.013
Yeh Martín, N., Valer, L. & Mansy, S. S. Toward long-lasting artificial cells that better mimic natural living cells. Emerg. Top. Life Sci. 3, 597–607 (2019).
pubmed: 33523164
pmcid: 7288992
doi: 10.1042/ETLS20190026
Aufinger, L. & Simmel, F. C. Establishing communication between artificial cells. Chem. Eur. J. 25, 12659–12670 (2019).
pubmed: 31241792
doi: 10.1002/chem.201901726
Tang, T.-Y. D. et al. Gene-mediated chemical communication in synthetic protocell communities. ACS Synth. Biol. 7, 339–346 (2018).
pubmed: 29091420
doi: 10.1021/acssynbio.7b00306
Niederholtmeyer, H., Chaggan, C. & Devaraj, N. K. Communication and quorum sensing in non-living mimics of eukaryotic cells. Nat. Commun. 9, 5027 (2018).
pubmed: 30487584
pmcid: 6261949
doi: 10.1038/s41467-018-07473-7
Buddingh’, B. C., Elzinga, J. & van Hest, J. C. M. Intercellular communication between artificial cells by allosteric amplification of a molecular signal. Nat. Commun. 11, 1652 (2020).
pubmed: 32246068
pmcid: 7125153
doi: 10.1038/s41467-020-15482-8
Tian, L., Li, M., Patil, A. J., Drinkwater, B. W. & Mann, S. Artificial morphogen-mediated differentiation in synthetic protocells. Nat. Commun. 10, 3321 (2019).
pubmed: 31346180
pmcid: 6658542
doi: 10.1038/s41467-019-11316-4