Self-assembly of protein superstructures by physical interactions under cytoplasm-like conditions
The structure-driven assembly of multimeric protein complexes and the formation of intracellular phase-like protein condensates have been the subject of intense research. However, the assembly of larger superstructures comprising cellular components, such as protein nanoparticles driven by general p...
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| Published in | Biophysical journal Vol. 120; no. 13; pp. 2701 - 2709 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier Inc
06.07.2021
The Biophysical Society |
| Online Access | Get full text |
| ISSN | 0006-3495 1542-0086 1542-0086 |
| DOI | 10.1016/j.bpj.2021.05.007 |
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| Abstract | The structure-driven assembly of multimeric protein complexes and the formation of intracellular phase-like protein condensates have been the subject of intense research. However, the assembly of larger superstructures comprising cellular components, such as protein nanoparticles driven by general physical rather than specific biochemical interactions, remains relatively uncharacterized. Here, we use gas vesicles (GVs)—genetically encoded protein nanoparticles that form ordered intracellular clusters—as a model system to study the forces driving multiparticle assembly under cytoplasm-like conditions. Our calculations and experimental results show that the ordered assembly of GVs can be achieved by screening their mutual electrostatic repulsion with electrolytes and creating a crowding force with dissolved macromolecules. The precise balance of these forces results in different packing configurations. Biomacromolecules such as polylysine and DNA are capable of driving GV clustering. These results provide basic insights into how physically driven interactions affect the formation of protein superstructures, offer guidance for manipulating nanoparticle assembly in cellular environments through synthetic biology methods, and inform research on the biotechnology applications of GVs. |
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| AbstractList | The structure-driven assembly of multimeric protein complexes and the formation of intracellular phase-like protein condensates have been the subject of intense research. However, the assembly of larger superstructures comprising cellular components, such as protein nanoparticles driven by general physical rather than specific biochemical interactions, remains relatively uncharacterized. Here, we use gas vesicles (GVs)-genetically encoded protein nanoparticles that form ordered intracellular clusters-as a model system to study the forces driving multiparticle assembly under cytoplasm-like conditions. Our calculations and experimental results show that the ordered assembly of GVs can be achieved by screening their mutual electrostatic repulsion with electrolytes and creating a crowding force with dissolved macromolecules. The precise balance of these forces results in different packing configurations. Biomacromolecules such as polylysine and DNA are capable of driving GV clustering. These results provide basic insights into how physically driven interactions affect the formation of protein superstructures, offer guidance for manipulating nanoparticle assembly in cellular environments through synthetic biology methods, and inform research on the biotechnology applications of GVs.The structure-driven assembly of multimeric protein complexes and the formation of intracellular phase-like protein condensates have been the subject of intense research. However, the assembly of larger superstructures comprising cellular components, such as protein nanoparticles driven by general physical rather than specific biochemical interactions, remains relatively uncharacterized. Here, we use gas vesicles (GVs)-genetically encoded protein nanoparticles that form ordered intracellular clusters-as a model system to study the forces driving multiparticle assembly under cytoplasm-like conditions. Our calculations and experimental results show that the ordered assembly of GVs can be achieved by screening their mutual electrostatic repulsion with electrolytes and creating a crowding force with dissolved macromolecules. The precise balance of these forces results in different packing configurations. Biomacromolecules such as polylysine and DNA are capable of driving GV clustering. These results provide basic insights into how physically driven interactions affect the formation of protein superstructures, offer guidance for manipulating nanoparticle assembly in cellular environments through synthetic biology methods, and inform research on the biotechnology applications of GVs. The structure-driven assembly of multimeric protein complexes and the formation of intracellular phase-like protein condensates have been the subject of intense research. However, the assembly of larger superstructures comprising cellular components, such as protein nanoparticles driven by general physical rather than specific biochemical interactions, remains relatively uncharacterized. Here, we use gas vesicles (GVs)—genetically encoded protein nanoparticles that form ordered intracellular clusters—as a model system to study the forces driving multiparticle assembly under cytoplasm-like conditions. Our calculations and experimental results show that the ordered assembly of GVs can be achieved by screening their mutual electrostatic repulsion with electrolytes and creating a crowding force with dissolved macromolecules. The precise balance of these forces results in different packing configurations. Biomacromolecules such as polylysine and DNA are capable of driving GV clustering. These results provide basic insights into how physically driven interactions affect the formation of protein superstructures, offer guidance for manipulating nanoparticle assembly in cellular environments through synthetic biology methods, and inform research on the biotechnology applications of GVs. |
| Author | Malounda, Dina Ling, Bill Yao, Yuxing Shapiro, Mikhail G. Jin, Zhiyang |
| Author_xml | – sequence: 1 givenname: Yuxing orcidid: 0000-0003-0337-6372 surname: Yao fullname: Yao, Yuxing organization: Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California – sequence: 2 givenname: Zhiyang surname: Jin fullname: Jin, Zhiyang organization: Division of Engineering and Applied Science, California Institute of Technology, Pasadena, California – sequence: 3 givenname: Bill orcidid: 0000-0002-1276-7204 surname: Ling fullname: Ling, Bill organization: Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California – sequence: 4 givenname: Dina surname: Malounda fullname: Malounda, Dina organization: Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California – sequence: 5 givenname: Mikhail G. orcidid: 0000-0002-0291-4215 surname: Shapiro fullname: Shapiro, Mikhail G. email: mikhailshapiro@gmail.com organization: Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California |
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