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Proliferation-mediated asymmetric nanoencapsulation of single-cell and motility differentiation

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Abstract

The biointerface engineering of living cells by creating an abiotic shell has important implications for endowing cells with exogenous properties with improved cellular behavior, which then boosts the development of the emerging field of living cell hybrid materials. Herein, we develop a way to perform active nanoencapsulation of single cell, which then endows the encapsulated cells with motion ability that they do not inherently possess. The emerging motion characteristics of the encapsulated cells could be self-regulated in terms of both the motion velocity and orbits by different proliferation modes. Accordingly, by taking advantage of the emergence of differentiated moving abilities, we achieve the self-sorting between mother cells and daughter cells in a proliferated Saccharomyces cerevisiae cell community. Therefore, it is anticipated that our highlighted study could not only serve as a new technique in the field of single-cell biology analysis and sorting such as in studying the aging process in Saccharomyces cerevisiae, but also open up opportunities to manipulate cell functionality by creating biohybrid materials to fill the gap between biological systems and engineering abiotic materials.

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References

  1. Chen H, Wang L, Wang S, et al. Construction of hybrid bi-micro-compartments with exocytosis-inspired behavior toward fast temperature-modulated transportation of living organisms. Angew Chem Int Ed, 2021, 60: 20795–20802

    Article  Google Scholar 

  2. Li J, Xu Z, Zhu M, et al. Programmable spatial organization of liquid-phase condensations. Chem, 2022, 8: 784–800

    Article  Google Scholar 

  3. Chu J C H, Shao C, Ha S Y Y, et al. One-pot peptide cyclisation and surface modification of photosensitiser-loaded red blood cells for targeted photodynamic therapy. Biomater Sci, 2021, 9: 7832–7837

    Article  Google Scholar 

  4. Guo Z, Liu J, Li Y, et al. Biocatalytic metal-organic framework nanomotors for active water decontamination. Chem Commun, 2020, 56: 14837–14840

    Article  Google Scholar 

  5. Yao S, Jin B, Liu Z, et al. Biomineralization: From material tactics to biological strategy. Adv Mater, 2017, 29: 1605903

    Article  Google Scholar 

  6. Lei Q, Guo J, Kong F, et al. Bioinspired cell silicification: From extracellular to intracellular. J Am Chem Soc, 2021, 143: 6305–6322

    Article  Google Scholar 

  7. Zhao C, Li J, Wang S, et al. Membranization of coacervates into artificial phagocytes with predation toward bacteria. ACS Nano, 2021, 15: 10048–10057

    Article  Google Scholar 

  8. Drachuk I, Calabrese R, Harbaugh S, et al. Silk macromolecules with amino acid-poly(ethylene glycol) grafts for controlling layer-by-layer encapsulation and aggregation of recombinant bacterial cells. ACS Nano, 2015, 9: 1219–1235

    Article  Google Scholar 

  9. Park J H, Kim K, Lee J, et al. A cytoprotective and degradable metal-polyphenol nanoshell for single-cell encapsulation. Angew Chem Int Ed, 2014, 53: 12420

    Article  Google Scholar 

  10. Maciel M M, Correia T R, Gaspar V M, et al. Partial coated stem cells with bioinspired silica as new generation of cellular hybrid materials. Adv Funct Mater, 2021, 31: 2009619

    Article  Google Scholar 

  11. Jiang N, Yang X Y, Deng Z, et al. A stable, reusable, and highly active photosynthetic bioreactor by bio-interfacing an individual cyanobacterium with a mesoporous bilayer nanoshell. Small, 2015, 11: 2003–2010

    Article  Google Scholar 

  12. Liang K, Richardson J J, Doonan C J, et al. An enzyme-coated metal-organic framework shell for synthetically adaptive cell survival. Angew Chem Int Ed, 2017, 56: 8510–8515

    Article  Google Scholar 

  13. Wang W, Zhang L, Deng Q, et al. Yeast@MOF bioreactor as a tumor metabolic symbiosis disruptor for the potent inhibition of metabolically heterogeneous tumors. Nano Today, 2022, 42: 101331

    Article  Google Scholar 

  14. Liu R, Cao Z, Wang L, et al. Multimodal oncolytic bacteria by coating with tumor cell derived nanoshells. Nano Today, 2022, 45: 101537

    Article  Google Scholar 

  15. Meng L, Yang F, Pang Y, et al. Nanocapping-enabled charge reversal generates cell-enterable endosomal-escapable bacteriophages for intracellular pathogen inhibition. Sci Adv, 2022, 8: eabq2005

    Article  Google Scholar 

  16. Pan C, Li J, Hou W, et al. Polymerization-mediated multi-functionalization of living cells for enhanced cell-based therapy. Adv Mater, 2021, 33: 2007379

    Article  Google Scholar 

  17. Wang S L, Xu Z J, Lin S, et al. Polymer-chlorella cells conjugating with aggregation-induced functionality switch towards hydrogen evolution. Sci China Tech Sci, 2020, 63: 1416–1425

    Article  Google Scholar 

  18. Youn W, Ko E H, Kim M H, et al. Cytoprotective encapsulation of individual Jurkat T cells within durable TiO2 shells for T-cell therapy. Angew Chem Int Ed, 2017, 56: 10702–10706

    Article  Google Scholar 

  19. Zhao Y, Fan M, Chen Y, et al. Surface-anchored framework for generating RhD-epitope stealth red blood cells. Sci Adv, 2020, 6: eaaw9679

    Article  Google Scholar 

  20. Su D, Qi J, Liu X, et al. Enzyme-modulated anaerobic encapsulation of Chlorella cells allows switching from O2 to H2 production. Angew Chem Int Ed, 2019, 58: 3992–3995

    Article  Google Scholar 

  21. Xu Z, Wang S, Zhao C, et al. Photosynthetic hydrogen production by droplet-based microbial micro-reactors under aerobic conditions. Nat Commun, 2020, 11: 5985

    Article  Google Scholar 

  22. Youn W, Kim J Y, Park J, et al. Single-cell nanoencapsulation: From passive to active shells. Adv Mater, 2020, 32: 1907001

    Article  Google Scholar 

  23. Boquet-Pujadas A, Olivo-Marin J C, Guillen N. Bioimage analysis and cell motility. Patterns, 2021, 2: 100170

    Article  Google Scholar 

  24. Shao J, Xuan M, Zhang H, et al. Chemotaxis-guided hybrid neutrophil micromotors for targeted drug transport. Angew Chem Int Ed, 2017, 129: 13115

    Article  Google Scholar 

  25. San-Miguel A. Optogenetics gets the worm. Sci Robot, 2021, 6: eabj3937

    Article  Google Scholar 

  26. Wang B, Kostarelos K, Nelson B J, et al. Trends in micro-/nanorobotics: Materials development, actuation, localization, and system integration for biomedical applications. Adv Mater, 2021, 33: 2002047

    Article  Google Scholar 

  27. Kumar M S, Philominathan P. The physics of flagellar motion of E. Coli during chemotaxis. Biophys Rev, 2009, 2: 13–20

    Article  Google Scholar 

  28. Wakabayashi K, Misawa Y, Mochiji S, et al. Reduction-oxidation poise regulates the sign of phototaxis in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA, 2011, 108: 11280–11284

    Article  Google Scholar 

  29. Wallach E, Amelar R D, Dubin L, et al. Sperm motility. Fertility Sterility, 1980, 34: 197–215

    Article  Google Scholar 

  30. Geng W, Jiang N, Qing G Y, et al. Click reaction for reversible encapsulation of single yeast cells. ACS Nano, 2019, 13: 14459–14467

    Article  Google Scholar 

  31. Ma X, Wang X, Hahn K, et al. Motion control of urea-powered biocompatible hollow microcapsules. ACS Nano, 2016, 10: 3597–3605

    Article  Google Scholar 

  32. Wen P, Wang X, Chen H, et al. A pH self-monitoring heterogeneous multicompartmental proteinosome with spatiotemporal regulation of insulin transportation. Chin J Chem, 2021, 39: 3386–3392

    Article  Google Scholar 

  33. Liu Y, Dai Q, Jin X, et al. Negative impacts of biochars on urease activity: High pH, heavy metals, polycyclic aromatic hydrocarbons, or free radicals? Environ Sci Technol, 2018, 52: 12740–12747

    Article  Google Scholar 

  34. Xu D, Zhou C, Zhan C, et al. Enzymatic micromotors as a mobile photosensitizer platform for highly efficient on-chip targeted antibacteria photodynamic therapy. Adv Funct Mater, 2019, 29: 1807727

    Article  Google Scholar 

  35. Liu C, Zhou C, Wang W, et al. Bimetallic microswimmers speed up in confining channels. Phys Rev Lett, 2016, 117: 198001

    Article  Google Scholar 

  36. Kline T R, Iwata J, Lammert P E, et al. Catalytically driven colloidal patterning and transport. J Phys Chem B, 2006, 110: 24513–24521

    Article  Google Scholar 

  37. Chiang T Y, Velegol D. Localized electroosmosis (LEO) induced by spherical colloidal motors. Langmuir, 2014, 30: 2600–2607

    Article  Google Scholar 

  38. Meng G, Paulose J, Nelson D R, et al. Elastic instability of a crystal growing on a curved surface. Science, 2014, 343: 634–637

    Article  Google Scholar 

  39. Yang X Y, Li Z Q, Liu B, et al. “Fish-in-Net” encapsulation of enzymes in macroporous cages for stable, reusable, and active heterogeneous biocatalysts. Adv Mater, 2006, 18: 410–414

    Article  Google Scholar 

  40. Howse J R, Jones RAL, Ryan A J, et al. Self-motile colloidal particles: From directed propulsion to random walk. Phys Rev Lett, 2007, 99: 048102

    Article  Google Scholar 

  41. Pijpers I A B, Cao S, Llopis-Lorente A, et al. Hybrid biodegradable nanomotors through compartmentalized synthesis. Nano Lett, 2020, 20: 4472–4480

    Article  Google Scholar 

  42. Ji Y, Lin X, Zhang H, et al. Thermoresponsive polymer brush modulation on the direction of motion of phoretically driven janus micromotors. Angew Chem Int Ed, 2019, 58: 4184–4188

    Article  Google Scholar 

  43. Herskowitz I. Life cycle of the budding yeast saccharomyces cerevisiae. Microbiol Rev, 1988, 52: 536–553

    Article  Google Scholar 

  44. Bitterman K J, Medvedik O, Sinclair D A. Longevity regulation in Saccharomyces cerevisiae: Linking metabolism, genome stability, and heterochromatin. Microbiol Mol Biol Rev, 2003, 67: 376–399

    Article  Google Scholar 

  45. Arqué X, Andrés X, Mestre R, et al. Ionic species affect the self-propulsion of urease-powered micromotors. Research, 2020, 2020, doi: https://doi.org/10.34133/2020/2424972

  46. Atilgan E, Magidson V, Khodjakov A, et al. Morphogenesis of the fission yeast cell through cell wall expansion. Curr Biol, 2015, 25: 2150–2157

    Article  Google Scholar 

  47. Sipiczki M. Splitting of the fission yeast septum. FEMS Yeast Res, 2007, 7: 761–770

    Article  Google Scholar 

  48. Steinkraus K A, Kaeberlein M, Kennedy B K. Replicative aging in yeast: The means to the end. Annu Rev Cell Dev Biol, 2008, 24: 29–54

    Article  Google Scholar 

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Correspondence to Xin Huang.

Additional information

This work was supported by the National Natural Science Foundation of China (Grant Nos. 22171058 and 21871069), and the Fundamental Research Funds for the Central Universities (Grant No. HIT.OCEF.2021027).

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The supporting information is available online at https://tech.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

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Wang, S., Xu, Z., Chen, H. et al. Proliferation-mediated asymmetric nanoencapsulation of single-cell and motility differentiation. Sci. China Technol. Sci. 66, 2134–2146 (2023). https://doi.org/10.1007/s11431-022-2252-3

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  • DOI: https://doi.org/10.1007/s11431-022-2252-3

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