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Design and function of smart biomembrane nanohybrids for biomedical applications: review

Abstract

Biological membranes that tailor their morphology to environmental stimuli are nature’s ultimate smart molecular systems. This focused review describes the design and function of smart biomembrane nanohybrids. Specifically, liposomes and exosomes can be functionalized with inorganic substances and polymers to afford hybridized artificial cell membranes. These membranes have a tailorable morphology and can incorporate functional integral membrane proteins.

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References

  1. Sasaki Y, Matsui K, Aoyama Y, Kikuchi J. Cerasome as an infusible and cell-friendly gene carrier: synthesis of cerasome-forming lipids and transfection using cerasome. Nat Protoc. 2006;1:1227–34.

    Article  CAS  Google Scholar 

  2. Vargas K, Shon Y. Hybrid lipid–nanoparticle complexes for biomedical applications. J Mater Chem B. 2019;7:695–708.

    Article  CAS  Google Scholar 

  3. Mohammadi M, Taghavi S, Abnos K, Taghdisi SM, Ramezani M, Alibolandi M. Hybrid vesicular drug delivery systems for cancer therapeutics. Adv Funct Mater. 2018;28:1802136.

    Article  Google Scholar 

  4. Sasaki Y, Akiyoshi K. Nanogel engineering for new nanobiomaterials: from chaperoning engineering to biomedical applications. Chem Rec. 2010;10:366–76.

    CAS  PubMed  Google Scholar 

  5. Sasaki Y, Akiyoshi K. Self-assembled nanogel engineering for advanced biomedical technology. Chem Lett. 2012;41:202–8.

    Article  CAS  Google Scholar 

  6. Sekine Y, Moritani Y, Ikeda-Fukazawa T, Sasaki Y, Akiyoshi K. A hybrid hydrogel biomaterial by nanogel engineering: bottom-up design with nanogel and liposome building blocks to develop a multidrug delivery system. Adv Healthc Mater. 2012;1:722–8.

    Article  CAS  Google Scholar 

  7. Ternullo S, Werning L, Holsater A, Basnet N. Curcumin-in-deformable liposomes-in-chitosan-hydrogel as a novel wound dressing. Pharmaceutics. 2020;12:8.

    Article  CAS  Google Scholar 

  8. Xu S, An X. Preparation, microstructure and function for injectable liposome-hydrogels. Colloids Surf A Physicochem Eng Asp. 2019;560:20–5.

    Article  CAS  Google Scholar 

  9. Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367. https://doi.org/10.1126/science.aau6977.

  10. Sato K, Umezaki K, Sawada S, Mukai S, Sasaki Y, Harada N, et al. Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep. 2016;6:21933.

    Article  CAS  Google Scholar 

  11. Akbari A, Jabbari N, Sharifi R, Ahmadi M, Vahhabi A, Seyedzadeh SJ, et al. Free and hydrogel encapsulated exosome-based therapies in regenerative medicine. Life Sci. 2020;249:117447.

    Article  CAS  Google Scholar 

  12. Kawasaki R, Sasaki Y, Katagiri K, Mukai SA, Sawada S, Akiyoshi K. Magnetically guided protein transduction by hybrid nanogel chaperones with iron oxide nanoparticles. Angew Chem Int Ed. 2016;55:11377–81.

    Article  CAS  Google Scholar 

  13. Ueda T, Lee SJ, Nakatani Y, Ourisson G, Sunamoto J. Coating of POPC giant liposomes with hydrophobized polysaccharide. Chem Lett. 1998;5:417–8.

    Article  Google Scholar 

  14. Mizuta R, Sasaki Y, Kawasaki R, Katagiri K, Sawada S, Mukai SA, et al. Magnetically navigated intracellular delivery of extracellular vesicles using amphiphilic nanogels. Bioconj Chem. 2019;30:2150–5.

    Article  CAS  Google Scholar 

  15. Sancho-Albero M, Encabo-Berzosa MDM, Beltrán-Visiedo M, Fernández-Messina L, Sebastián V, Sánchez-Madrid F, et al. Efficient encapsulation of theranostic nanoparticles in cell-derived exosomes: leveraging the exosomal biogenesis pathway to obtain hollow gold nanoparticle-hybrids. Nanoscale. 2019;11:18825–36.

    Article  CAS  Google Scholar 

  16. Cao Y, Wu T, Zhang K, Meng X, Dai W, Wang D, et al. Engineered exosome-mediated near-infrared-II region V2C quantum dot delivery for nucleus-target low-temperature photothermal therapy. ACS Nano. 2019;13:1499–510.

    CAS  PubMed  Google Scholar 

  17. Ando M, Akiyama M, Okuno D, Hirano M, Ide T, Sawada S, et al. Liposome chaperon in cell-free membrane protein synthesis: one-step preparation of KcsA-integrated liposomes and electrophysiological analysis by the planar bilayer method. Biomater Sci. 2015;4:258–64.

    Article  Google Scholar 

  18. Lasitza‐Male T, Bartels K, Jungwirth J, Wiggers F, Rosenblum G, Hofmann H, Löw C. Membrane chemistry tunes the structure of a peptide transporter. Angew Chem Int Ed Eng. 2020;591:19121–28.

    Article  Google Scholar 

  19. Niwa T, Sasaki Y, Uemura E, Nakamura S, Akiyama M, Ando M, et al. Comprehensive study of liposome-assisted synthesis of membrane proteins using a reconstituted cell-free translation system. Sci Rep. 2015;5:18025.

    Article  CAS  Google Scholar 

  20. Jacobs M, Boyd MA, Kamat NP. Diblock copolymers enhance folding of a mechanosensitive membrane protein during cell-free expression. Proc Natl Acad Sci. 2019;116:4031–6.

    Article  CAS  Google Scholar 

  21. Nallani M, Andreasson-Ochsner M, Tan CWD, Sinner E, Wisantoso Y, Geifman-Shochat S, et al. Proteopolymersomes: in vitro production of a membrane protein in polymersome membranes. Biointerphases. 2011;6:153–7.

    Article  CAS  Google Scholar 

  22. Isaksson S, Watkins EB, Browning KL, Lind TK, Cárdenas M, Hedfalk K, et al. Protein-containing lipid bilayers intercalated with size-matched mesoporous silica thin films. Nano Lett. 2017;17:746–85.

    Article  Google Scholar 

  23. Hurtig J, Chiu DT, Onfelt B. Intercellular nanotubes: insights from imaging studies and beyond. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2010;2:260–76.

    Article  CAS  Google Scholar 

  24. Jorsh IK, Daste F, Gallop JL. Membrane curvature in cell biology: an integration of molecular mechanisms. J Cell Biol. 2016;214:375–87.

    Article  Google Scholar 

  25. Nomura F, Honda M, Takeda S, Inaba T, Takiguchi K, Itoh TJ, et al. Morphological and topological transformation of membrane vesicles. J Biol Phys. 2002;28:225–35.

    Article  CAS  Google Scholar 

  26. Dimova R, Lipowsky R. Giant vesicles exposed to aqueous two-phase systems: membrane wetting, budding processes, and spontaneous tubulation. Adv Mater Interfaces. 2017;4:16600451.

    Google Scholar 

  27. Karlsson A, Karlsson R, Karlsson M, Cans AS, Strömberg A, Ryttsén F, et al. Networks of nanotubes and containers. Nature. 2001;490:150–2.

    Article  Google Scholar 

  28. Gerbrand K, Martijn V, Bas H, Marileen D. Membrane tube formation from giant vesicles by dynamic association of motor proteins. Proc Natl Acad Sci. 2003;100:15583–8.

    Article  Google Scholar 

  29. Hayashi M, Nishiyama M, Kazayama Y, Toyota T, Harada Y, Takiguchi K. Reversible morphological control of tubulin-encapsulating giant liposomes by hydrostatic pressure. Langmuir. 2016;32:3794–802.

    Article  Google Scholar 

  30. Brazhnik KP, Vreeland WN, Hutchison JB, Kishore R, Wells J, Helmerson K, et al. Directed growth of pure phosphatidylcholine nanotubes in microfluidic channels. Langmuir. 2005;21:10814–7.

    Article  CAS  Google Scholar 

  31. Fu M, Li Q, Sun B, Yang Y, Dai L, Nylander T, et al. Disassembly of dipeptide single crystals can transform the lipid membrane into a network. ACS Nano. 2017;11:7349–54.

    Article  CAS  Google Scholar 

  32. Koksal ES, Liese S, Kantarci I, Olsson R, Carlson A, Gozen I. Nanotube-mediated path to protocell formation. ACS Nano. 2019;13:6867–78.

    Article  CAS  Google Scholar 

  33. Castillo JA, Narciso DM, Hayes MA. Bionanotubule formation from surface-attached liposomes using electric field. Langmuir. 2009;25:391–6.

    Article  CAS  Google Scholar 

  34. Sekine Y, Abe K, Shimizu Z, Sasaki Y, Sawada S, Akiyoshi K. Shear flow-induced nanotubulation of surface-immobilized liposomes. RSC Adv. 2012;2:2682–4.

    Article  CAS  Google Scholar 

  35. Sasaki Y, Akiyoshi K. PCT Int. Appl. JP 2011;06933:PCT/JP2011/069337.

  36. Schulz M, Olubummo A, Binder WH. Beyond the lipid-bilayer: interaction of polymers and nanoparticles with membranes. Soft Matter. 2012;8:4849–64.

    Article  CAS  Google Scholar 

  37. Stachowiak JC, Hayden CC, Sasaki DY. Steric confinement of proteins on lipid membranes can drive curvature and tubulation. Proc Natl Acad Sci. 2010;107:7781–6.

    Article  CAS  Google Scholar 

  38. Safinya CR, Raviv U, Needleman DJ, Zidovska A, Choi MC, Ojeda-Lopez MA, et al. Nanoscale assembly in biological systems: from neuronal cytoskeletal proteins to curvature stabilizing lipids. Adv Mater. 2011;23:2260–70.

    Article  CAS  Google Scholar 

  39. Zuraw-Weston S, Wood DA, Torres IK, Li YW, Wang LS, Jiang Z, et al. Nanoparticles binding to lipid membranes: from vesicle-based gels to vesicle tubulation and destruction. Nanoscale. 2019;11:18464–74.

    Article  CAS  Google Scholar 

  40. Shimada N, Kinoshita H, Umegae T, Azumai S, Kume N, Ochiai T, et al. Cationic copolymer-chaperoned 2D–3D reversible conversion of lipid membranes. Adv Mater. 2019;31:1904032.

    Article  CAS  Google Scholar 

  41. Doosti BA, Pezeshkian W, Btuhn DS, Ipsen JH, Khandelia H, Jeffries GD, et al. Membrane tubulation in lipid vesicles triggered by the local application of calcium ions. Langmuir. 2017;33:11010–7.

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by a Grant-in Aid from the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number JP16H03842 (YS). We thank KA for kind support and Dr. Shinichi Sawada and Dr. Sada-atsu Mukai for their contributions. We thank Michael Scott Long from the Edanz Group (https://en-author-services.edanzgroup.com/ac) for editing a draft of this manuscript.

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Correspondence to Yoshihiro Sasaki.

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Sasaki, Y., Akiyoshi, K. Design and function of smart biomembrane nanohybrids for biomedical applications: review. Polym J 53, 587–592 (2021). https://doi.org/10.1038/s41428-020-00453-z

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