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DNA-Mediated Self-Organization of Polymeric Nanocompartments Leads to Interconnected Artificial Organelles

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Department of Chemistry, University of Basel, Klingelbergstrasse 80, Basel 4056, Switzerland
BioEM lab, Biozentrum, University of Basel, Mattenstrasse 26, 4058 Basel, Switzerland
*E-mail: [email protected] (C.G.P.).
Cite this: Nano Lett. 2016, 16, 11, 7128–7136
Publication Date (Web):October 11, 2016
https://doi.org/10.1021/acs.nanolett.6b03430
Copyright © 2016 American Chemical Society

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    Abstract

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    Self-organization of nanocomponents was mainly focused on solid nanoparticles, quantum dots, or liposomes to generate complex architectures with specific properties, but intrinsically limited or not developed enough, to mimic sophisticated structures with biological functions in cells. Here, we present a biomimetic strategy to self-organize synthetic nanocompartments (polymersomes) into clusters with controlled properties and topology by exploiting DNA hybridization to interconnect polymersomes. Molecular and external factors affecting the self-organization served to design clusters mimicking the connection of natural organelles: fine-tune of the distance between tethered polymersomes, different topologies, no fusion of clustered polymersomes, and no aggregation. Unexpected, extended DNA bridges that result from migration of the DNA strands inside the thick polymer membrane (about 12 nm) represent a key stability and control factor, not yet exploited for other synthetic nano-object networks. The replacement of the empty polymersomes with artificial organelles, already reported for single polymersome architecture, will provide an excellent platform for the development of artificial systems mimicking natural organelles or cells and represents a fundamental step in the engineering of molecular factories.

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    3. Andrea Belluati, Ioana Craciun, Cornelia G. Palivan. Bioactive Catalytic Nanocompartments Integrated into Cell Physiology and Their Amplification of a Native Signaling Cascade. ACS Nano 2020, 14 (9) , 12101-12112. https://doi.org/10.1021/acsnano.0c05574
    4. Anand Lopez, Juewen Liu. DNA Oligonucleotide-Functionalized Liposomes: Bioconjugate Chemistry, Biointerfaces, and Applications. Langmuir 2018, 34 (49) , 15000-15013. https://doi.org/10.1021/acs.langmuir.8b01368
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    7. Voichita Mihali, Michal Skowicki, Daniel Messmer, Cornelia G. Palivan. Clusters of polymersomes and Janus nanoparticles hierarchically self-organized and controlled by DNA hybridization. Nano Today 2023, 48 , 101741. https://doi.org/10.1016/j.nantod.2022.101741
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    9. Shuang Liu, Chunjuan Zhang, Fan Yang, Zhenzhen Guo, Qiaoling Liu. Construction of Artificial Cells Utilizing DNA Nanotechnology. Current Chinese Science 2022, 2 (3) , 213-223. https://doi.org/10.2174/2210298102666220302095040
    10. Hedi Karoui, Pankaj Singh Patwal, B. V. V. S. Pavan Kumar, Nicolas Martin. Chemical Communication in Artificial Cells: Basic Concepts, Design and Challenges. Frontiers in Molecular Biosciences 2022, 9 https://doi.org/10.3389/fmolb.2022.880525
    11. Lukas Heuberger, Maria Korpidou, Olivia M. Eggenberger, Myrto Kyropoulou, Cornelia G. Palivan. Current Perspectives on Synthetic Compartments for Biomedical Applications. International Journal of Molecular Sciences 2022, 23 (10) , 5718. https://doi.org/10.3390/ijms23105718
    12. Hao Yu, Zhihong Liang, Longjiao Zhu, Changhui Zhao, Xiaoyun He, Keren Chen, Wentao Xu. Nucleic Acid‐Modified Liposome: Construction Methods and Biological Applications. Advanced Materials Interfaces 2022, 9 (3) https://doi.org/10.1002/admi.202101246
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    27. Shinji Sugihara. Polymerization‐Induced Self‐assembly of Block Copolymer Nano‐objects via Green RAFT Polymerization. 2019, 1-29. https://doi.org/10.1002/9783527823987.vol4_c1
    28. Chin Ken Wong, Martina H. Stenzel, Pall Thordarson. Non-spherical polymersomes: formation and characterization. Chemical Society Reviews 2019, 48 (15) , 4019-4035. https://doi.org/10.1039/C8CS00856F
    29. Martina Garni, Riccardo Wehr, Saziye Yorulmaz Avsar, Christoph John, Cornelia Palivan, Wolfgang Meier. Polymer membranes as templates for bio-applications ranging from artificial cells to active surfaces. European Polymer Journal 2019, 112 , 346-364. https://doi.org/10.1016/j.eurpolymj.2018.12.047
    30. Christine R. Laramy, Matthew N. O’Brien, Chad A. Mirkin. Crystal engineering with DNA. Nature Reviews Materials 2019, 4 (3) , 201-224. https://doi.org/10.1038/s41578-019-0087-2
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    32. Chin Ken Wong, Alexander F. Mason, Martina H. Stenzel, Pall Thordarson. Formation of non-spherical polymersomes driven by hydrophobic directional aromatic perylene interactions. Nature Communications 2017, 8 (1) https://doi.org/10.1038/s41467-017-01372-z
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