Predicting Protein–Polymer Block Copolymer Self-Assembly from Protein Properties

Huang, Aaron; Paloni, Justin M.; Wang, Amy; Obermeyer, Allie C.; Sureka, Hursh V.; Yao, Helen; Olsen, Bradley D.

doi:10.1021/acs.biomac.9b00768

Title: Predicting Protein–Polymer Block Copolymer Self-Assembly from Protein Properties

Journal Article · Tue Sep 10 00:00:00 EDT 2019 · Biomacromolecules

DOI:https://doi.org/10.1021/acs.biomac.9b00768· OSTI ID:1570580

Huang, Aaron ^[1]; Paloni, Justin M. ^[1]; Wang, Amy ^[1];

^[1]; Sureka, Hursh V. ^[1];

^[1];

^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Protein–polymer bioconjugate self-assembly has attracted a great deal of attention as a method to fabricate protein nanomaterials in solution and the solid state. To identify protein properties that affect phase behavior in protein–polymer block copolymers, a library of 15 unique protein-b-poly(N-isopropylacrylamide) (PNIPAM) copolymers comprising 11 different proteins was compiled and analyzed. Many attributes of phase behavior are found to be similar among all studied bioconjugates regardless of protein properties, such as formation of micellar phases at high temperature and low concentration, lamellar ordering with increasing temperature, and disordering at high concentration, but several key protein-dependent trends are also observed. In particular, hexagonal phases are only observed for proteins within the molar mass range 20–36 kDa, where ordering quality is also significantly enhanced. While ordering is generally found to improve with increasing molecular weight outside of this range, most large bioconjugates exhibited weaker than predicted assembly, which is attributed to chain entanglement with increasing polymer molecular weight. Additionally, order–disorder transition boundaries are found to be largely uncorrelated to protein size and quality of ordering. However, the primary finding is that bioconjugate ordering can be accurately predicted using only protein molecular weight and percentage of residues contained within β sheets. This model provides a basis for designing protein–PNIPAM bioconjugates that exhibit well-defined self-assembly and a modeling framework that can generalize to other bioconjugate chemistries.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0007106

OSTI ID:: 1570580

Journal Information:: Biomacromolecules, Vol. 20, Issue 10; ISSN 1525-7797

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 16 works

Citation information provided by
Web of Science

References (78)

Crystal Structures of Myoglobin-Ligand Complexes at Near-Atomic Resolution Vojtěchovský, Jaroslav; Chu, Kelvin; Berendzen, Joel Biophysical Journal, Vol. 77, Issue 4 https://doi.org/10.1016/s0006-3495(99)77056-6	journal	October 1999
The Nature of Protein Interactions Governing Globular Protein–Polymer Block Copolymer Self-Assembly Lam, Christopher N.; Kim, Minkyu; Thomas, Carla S. Biomacromolecules, Vol. 15, Issue 4 https://doi.org/10.1021/bm401817p	journal	March 2014
Refined Structure of an Intact IgG2a Monoclonal Antibody^, Harris, Lisa J.; Larson, Steven B.; Hasel, Karl W. Biochemistry, Vol. 36, Issue 7 https://doi.org/10.1021/bi962514+	journal	February 1997
Tungstate as a Transition State Analog for Catalysis by Alkaline Phosphatase Peck, Ariana; Sunden, Fanny; Andrews, Logan D. Journal of Molecular Biology, Vol. 428, Issue 13 https://doi.org/10.1016/j.jmb.2016.05.007	journal	July 2016
Structural and immunologic characterization of bovine, horse, and rabbit serum albumins Majorek, Karolina A.; Porebski, Przemyslaw J.; Dayal, Arjun Molecular Immunology, Vol. 52, Issue 3-4 https://doi.org/10.1016/j.molimm.2012.05.011	journal	October 2012
Nanopatterned Protein Films Directed by Ionic Complexation with Water-Soluble Diblock Copolymers Kim, Bokyung; Lam, Christopher N.; Olsen, Bradley D. Macromolecules, Vol. 45, Issue 11 https://doi.org/10.1021/ma2024914	journal	May 2012
Phase transitions in concentrated solution self-assembly of globular protein–polymer block copolymers Lam, Christopher N.; Olsen, Bradley D. Soft Matter, Vol. 9, Issue 8 https://doi.org/10.1039/c2sm27459k	journal	January 2013
X-ray Crystallographic Studies of Alanine-65 Variants of Carbonic Anhydrase II Reveal the Structural Basis of Compromised Proton Transfer in Catalysis Scolnick, Laura R.; Christianson, David W. Biochemistry, Vol. 35, Issue 51 https://doi.org/10.1021/bi9617872	journal	January 1996
Self-assembly of rod–coil block copolymers Olsen, B.; Segalman, R. Materials Science and Engineering: R: Reports, Vol. 62, Issue 2 https://doi.org/10.1016/j.mser.2008.04.001	journal	July 2008
Steric Crowding Effects on Target Detection in an Affinity Biosensor Bonanno, Lisa M.; DeLouise, Lisa A. Langmuir, Vol. 23, Issue 10 https://doi.org/10.1021/la063659c	journal	April 2007
The Effect of Protein Electrostatic Interactions on Globular Protein–Polymer Block Copolymer Self-Assembly Lam, Christopher N.; Yao, Helen; Olsen, Bradley D. Biomacromolecules, Vol. 17, Issue 9 https://doi.org/10.1021/acs.biomac.6b00522	journal	August 2016
Progress in enzyme immobilization in ordered mesoporous materials and related applications Zhou, Zhou; Hartmann, Martin Chemical Society Reviews, Vol. 42, Issue 9 https://doi.org/10.1039/c3cs60059a	journal	January 2013
Microscale Enzymatic Optical Biosensors Using Mass Transport Limiting Nanofilms. 1. Fabrication and Characterization Using Glucose as a Model Analyte Stein, Erich W.; Grant, Patrick S.; Zhu, Huiguang Analytical Chemistry, Vol. 79, Issue 4 https://doi.org/10.1021/ac061414z	journal	January 2007
Biocatalysis in non-conventional media—ionic liquids, supercritical fluids and the gas phase Cantone, Sara; Hanefeld, Ulf; Basso, Alessandra Green Chemistry, Vol. 9, Issue 9 https://doi.org/10.1039/b618893a	journal	January 2007
Temperature-Regulated Activity of Responsive Polymer−Protein Conjugates Prepared by Grafting-from via RAFT Polymerization De, Priyadarsi; Li, Ming; Gondi, Sudershan R. Journal of the American Chemical Society, Vol. 130, Issue 34 https://doi.org/10.1021/ja804495v	journal	August 2008
Crystal Structures of Human Cytochrome P450 3A4 Bound to Metyrapone and Progesterone Williams, P. A. Science, Vol. 305, Issue 5684 https://doi.org/10.1126/science.1099736	journal	July 2004
Hopping Diffusion of Nanoparticles in Polymer Matrices Li-Heng, Cai,; Michael, Rubinstein,; Sergey, Panyukov, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/mn3f-j015	text	January 2015
Three-Dimensional Ordered Antibody Arrays Through Self-Assembly of Antibody-Polymer Conjugates Dong, Xue-Hui; Obermeyer, Allie C.; Olsen, Bradley D. Angewandte Chemie International Edition, Vol. 56, Issue 5 https://doi.org/10.1002/anie.201607085	journal	December 2016
Binding of a Designed Substrate Analogue to Diisopropyl Fluorophosphatase: Implications for the Phosphotriesterase Mechanism Blum, Marc-Michael; Löhr, Frank; Richardt, Andre Journal of the American Chemical Society, Vol. 128, Issue 39 https://doi.org/10.1021/ja061887n	journal	October 2006
Predictive Self-Assembly of Polyhedra into Complex Structures Damasceno, P. F.; Engel, M.; Glotzer, S. C. Science, Vol. 337, Issue 6093 https://doi.org/10.1126/science.1220869	journal	July 2012
Polymer-Polymer Phase Behavior Bates, Frank S. Science, Vol. 251, Issue 4996, p. 898-905 https://doi.org/10.1126/science.251.4996.898	journal	February 1991
Bioactive Protein Nanoarrays on Nickel Oxide Surfaces Formed by Dip-Pen Nanolithography Nam, Jwa-Min; Han, Sang Woo; Lee, Ki-Bum Angewandte Chemie, Vol. 116, Issue 10 https://doi.org/10.1002/ange.200353203	journal	February 2004
3V: cavity, channel and cleft volume calculator and extractor Voss, N. R.; Gerstein, M. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq395	journal	May 2010
Tutorial review. Oriented immobilization of antibodies and its applications in immunoassays and immunosensors Lu, Bin; Smyth, Malcolm R.; O'Kennedy, Richard The Analyst, Vol. 121, Issue 3 https://doi.org/10.1039/an996210029r	journal	January 1996
Creating Nanopatterns of His-Tagged Proteins on Surfaces by Nanoimprint Lithography Using Specific NiNTA-Histidine Interactions Maury, Pascale; Escalante, Maryana; Péter, Mária Small, Vol. 3, Issue 9 https://doi.org/10.1002/smll.200700046	journal	September 2007
Aggregation Behavior of Giant Amphiphiles Prepared by Cofactor Reconstitution Boerakker, Mark J.; Botterhuis, Nicole E.; Bomans, Paul H. H. Chemistry - A European Journal, Vol. 12, Issue 23 https://doi.org/10.1002/chem.200600089	journal	August 2006
Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus Baumann, Herbert; Knapp, Stefan; Lundbäck, Thomas Nature Structural Biology, Vol. 1, Issue 11 https://doi.org/10.1038/nsb1194-808	journal	November 1994
Structure of the triosephosphate isomerase-phosphoglycolohydroxamate complex: an analog of the intermediate on the reaction pathway Davenport, Robert C.; Bash, Paul A.; Seaton, Barbara A. Biochemistry, Vol. 30, Issue 24 https://doi.org/10.1021/bi00238a002	journal	June 1991
Theory of Microphase Separation in Block Copolymers Leibler, Ludwik Macromolecules, Vol. 13, Issue 6 https://doi.org/10.1021/ma60078a047	journal	November 1980
Enzyme-based biofuel cells Minteer, Shelley D.; Liaw, Bor Yann; Cooney, Michael J. Current Opinion in Biotechnology, Vol. 18, Issue 3 https://doi.org/10.1016/j.copbio.2007.03.007	journal	June 2007
Large-Scale Fabrication of Protein Nanoarrays Based on Nanosphere Lithography Cai, Yuguang; Ocko, Benjamin M. Langmuir, Vol. 21, Issue 20 https://doi.org/10.1021/la051656e	journal	September 2005
Effect of Temperature on the Adsorption of Poly(N-isopropylacrylamide) at the Air−Solution Interface Lee, L. T.; Jean, B.; Menelle, A. Langmuir, Vol. 15, Issue 9 https://doi.org/10.1021/la981531s	journal	April 1999
Improved Ordering in Low Molecular Weight Protein–Polymer Conjugates Through Oligomerization of the Protein Block Paloni, Justin M.; Miller, Eric A.; Sikes, Hadley D. Biomacromolecules, Vol. 19, Issue 9 https://doi.org/10.1021/acs.biomac.8b00928	journal	August 2018
On the Direct Electron Transfer, Sensing, and Enzyme Activity in the Glucose Oxidase/Carbon Nanotubes System Wooten, Marilyn; Karra, Sushma; Zhang, Maogen Analytical Chemistry, Vol. 86, Issue 1 https://doi.org/10.1021/ac403250w	journal	December 2013
Stabilizing role of glutamic acid 222 in the structure of Enhanced Green Fluorescent Protein Royant, Antoine; Noirclerc-Savoye, Marjolaine Journal of Structural Biology, Vol. 174, Issue 2 https://doi.org/10.1016/j.jsb.2011.02.004	journal	May 2011
Nanoscale Protein Patterning Using Self-Assembled Diblock Copolymers Kumar, Nitin; Hahm, Jong-in Langmuir, Vol. 21, Issue 15 https://doi.org/10.1021/la050331v	journal	July 2005
Solid-State Nanostructured Materials from Self-Assembly of a Globular Protein–Polymer Diblock Copolymer Thomas, Carla S.; Glassman, Matthew J.; Olsen, Bradley D. ACS Nano, Vol. 5, Issue 7 https://doi.org/10.1021/nn2013673	journal	June 2011
Synthesis of Uniform Protein−Polymer Conjugates Lele, Bhalchandra S.; Murata, Hironobu; Matyjaszewski, Krzysztof Biomacromolecules, Vol. 6, Issue 6 https://doi.org/10.1021/bm050428w	journal	November 2005
Topological Effects on Globular Protein-ELP Fusion Block Copolymer Self-Assembly Qin, Guokui; Glassman, Matthew J.; Lam, Christopher N. Advanced Functional Materials, Vol. 25, Issue 5 https://doi.org/10.1002/adfm.201403453	journal	December 2014
Inhibition of triosephosphate isomerase by phosphoenolpyruvate in the feedback-regulation of glycolysis. Grüning, Nana-Maria; Du, Dijun; Keller, Markus A. The Royal Society https://doi.org/10.17863/cam.69963	journalarticle	January 2014
Immobilization as a Strategy for Improving Enzyme Properties-Application to Oxidoreductases Guzik, Urszula; Hupert-Kocurek, Katarzyna; Wojcieszyńska, Danuta Molecules, Vol. 19, Issue 7 https://doi.org/10.3390/molecules19078995	journal	June 2014
Block Copolymers—Designer Soft Materials Bates, Frank S.; Fredrickson, Glenn H. Physics Today, Vol. 52, Issue 2 https://doi.org/10.1063/1.882522	journal	February 1999
The potential of optofluidic biolasers Fan, Xudong; Yun, Seok-Hyun Nature Methods, Vol. 11, Issue 2 https://doi.org/10.1038/nmeth.2805	journal	January 2014
Direct electron transfer of glucose oxidase on carbon nanotubes Guiseppi-Elie, Anthony; Lei, Chenghong; Baughman, Ray H. Nanotechnology, Vol. 13, Issue 5 https://doi.org/10.1088/0957-4484/13/5/303	journal	August 2002
Evidence from Liposome Encapsulation for Transport-Limited Microbial Metabolism of Solid Alkanes Miller, R. M.; Bartha, R. Applied and Environmental Microbiology, Vol. 55, Issue 2 https://doi.org/10.1128/aem.55.2.269-274.1989	journal	February 1989
Novel Chromophores and Buried Charges Control Color in mFruits ^† ^, ^‡ Shu, Xiaokun; Shaner, Nathan C.; Yarbrough, Corinne A. Biochemistry, Vol. 45, Issue 32 https://doi.org/10.1021/bi060773l	journal	August 2006
Stabilization of multimeric enzymes: Strategies to prevent subunit dissociation Fernandez-Lafuente, Roberto Enzyme and Microbial Technology, Vol. 45, Issue 6-7 https://doi.org/10.1016/j.enzmictec.2009.08.009	journal	December 2009
Well-Defined Protein−Polymer Conjugates via in Situ RAFT Polymerization Boyer, Cyrille; Bulmus, Volga; Liu, Jingquan Journal of the American Chemical Society, Vol. 129, Issue 22 https://doi.org/10.1021/ja070956a	journal	May 2007
Industrial enzyme applications Kirk, Ole; Borchert, Torben Vedel; Fuglsang, Claus Crone Current Opinion in Biotechnology, Vol. 13, Issue 4 https://doi.org/10.1016/S0958-1669(02)00328-2	journal	August 2002
Enzymes as Working or Inspirational Electrocatalysts for Fuel Cells and Electrolysis Cracknell, James A.; Vincent, Kylie A.; Armstrong, Fraser A. Chemical Reviews, Vol. 108, Issue 7 https://doi.org/10.1021/cr0680639	journal	July 2008
The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes Cogdell, Richard J.; Gall, Andrew; Köhler, Jürgen Quarterly Reviews of Biophysics, Vol. 39, Issue 3 https://doi.org/10.1017/S0033583506004434	journal	August 2006
Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review Durán, Nelson; Esposito, Elisa Applied Catalysis B: Environmental, Vol. 28, Issue 2 https://doi.org/10.1016/S0926-3373(00)00168-5	journal	November 2000
Potential Applications of Enzymes in Waste Treatment Karam, Jean; Nicell, James A. Journal of Chemical Technology & Biotechnology, Vol. 69, Issue 2 https://doi.org/10.1002/(SICI)1097-4660(199706)69:2<141::AID-JCTB694>3.0.CO;2-U	journal	June 1997
The detection and identification of metal and organic pollutants in potable water using enzyme assays suitable for sensor development Cowell, D. Biosensors and Bioelectronics, Vol. 10, Issue 6-7 https://doi.org/10.1016/0956-5663(95)96926-P	journal	January 1995
Biomaterials for Mediation of Chemical and Biological Warfare Agents Russell, Alan J.; Berberich, Jason A.; Drevon, Géraldine F. Annual Review of Biomedical Engineering, Vol. 5, Issue 1 https://doi.org/10.1146/annurev.bioeng.5.121202.125602	journal	August 2003
Two-Dimensionally Self-Arranged Protein Nanoarrays on Diblock Copolymer Templates Kumar, Nitin; Parajuli, Omkar; Hahm, Jong-in The Journal of Physical Chemistry B, Vol. 111, Issue 17 https://doi.org/10.1021/jp068509p	journal	April 2007
Microsphere Solid-State Biolasers Ta, Van Duong; Caixeiro, Soraya; Fernandes, Francisco M. Advanced Optical Materials, Vol. 5, Issue 8 https://doi.org/10.1002/adom.201601022	journal	March 2017
Immobilized enzymes — learning from past successes and failures Katchalski-Katzir, Ephraim Trends in Biotechnology, Vol. 11, Issue 11 https://doi.org/10.1016/0167-7799(93)90080-S	journal	November 1993
Improvement of enzyme activity, stability and selectivity via immobilization techniques Mateo, Cesar; Palomo, Jose M.; Fernandez-Lorente, Gloria Enzyme and Microbial Technology, Vol. 40, Issue 6 https://doi.org/10.1016/j.enzmictec.2007.01.018	journal	May 2007
Structural and functional stabilization of protein entities: state-of-the-art Balcão, Victor M.; Vila, Marta M. D. C. Advanced Drug Delivery Reviews, Vol. 93 https://doi.org/10.1016/j.addr.2014.10.005	journal	October 2015
Enzyme immobilization: an overview on techniques and support materials Datta, Sumitra; Christena, L. Rene; Rajaram, Yamuna Rani Sriramulu 3 Biotech, Vol. 3, Issue 1 https://doi.org/10.1007/s13205-012-0071-7	journal	June 2012
Modifying enzyme activity and selectivity by immobilization Rodrigues, Rafael C.; Ortiz, Claudia; Berenguer-Murcia, Ángel Chem. Soc. Rev., Vol. 42, Issue 15 https://doi.org/10.1039/C2CS35231A	journal	January 2013
Control of protein immobilization: Coupling immobilization and site-directed mutagenesis to improve biocatalyst or biosensor performance Hernandez, Karel; Fernandez-Lafuente, Roberto Enzyme and Microbial Technology, Vol. 48, Issue 2 https://doi.org/10.1016/j.enzmictec.2010.10.003	journal	February 2011
Bioactive Protein Nanoarrays on Nickel Oxide Surfaces Formed by Dip-Pen Nanolithography Nam, Jwa-Min; Han, Sang Woo; Lee, Ki-Bum Angewandte Chemie International Edition, Vol. 43, Issue 10 https://doi.org/10.1002/anie.200353203	journal	February 2004
Kinetic Effects on Self-Assembly and Function of Protein-Polymer Bioconjugates in Thin Films Prepared by Flow Coating Chang, Dongsook; Huang, Aaron; Olsen, Bradley D. Macromolecular Rapid Communications, Vol. 38, Issue 1 https://doi.org/10.1002/marc.201600449	journal	November 2016
Thermoresponsive giant biohybrid amphiphiles Lavigueur, Christine; García, Jordi González; Hendriks, Linda Polym. Chem., Vol. 2, Issue 2 https://doi.org/10.1039/C0PY00229A	journal	January 2011
Highly Active Biocatalytic Coatings from Protein–Polymer Diblock Copolymers Huang, Aaron; Qin, Guokui; Olsen, Bradley D. ACS Applied Materials & Interfaces, Vol. 7, Issue 27 https://doi.org/10.1021/acsami.5b01884	journal	July 2015
Self-assembly of anisotropic tethered nanoparticle shape amphiphiles Glotzer, Sharon C.; Horsch, Mark A.; Iacovella, Christopher R. Current Opinion in Colloid & Interface Science, Vol. 10, Issue 5-6 https://doi.org/10.1016/j.cocis.2005.09.011	journal	December 2005
Effect of polymer chemistry on globular protein–polymer block copolymer self-assembly Chang, Dongsook; Lam, Christopher N.; Tang, Shengchang Polym. Chem., Vol. 5, Issue 17 https://doi.org/10.1039/C4PY00448E	journal	January 2014
Self-assembly of protein-zwitterionic polymer bioconjugates into nanostructured materials Chang, Dongsook; Olsen, Bradley D. Polymer Chemistry, Vol. 7, Issue 13 https://doi.org/10.1039/C5PY01894C	journal	January 2016
Self-Assembly of Differently Shaped Protein-Polymer Conjugates through Modification of the Bioconjugation Site Huang, Aaron; Olsen, Bradley D. Macromolecular Rapid Communications, Vol. 37, Issue 15 https://doi.org/10.1002/marc.201500744	journal	June 2016
Inhibition of triosephosphate isomerase by phosphoenolpyruvate in the feedback-regulation of glycolysis Grüning, Nana-Maria; Du, Dijun; Keller, Markus A. Open Biology, Vol. 4, Issue 3 https://doi.org/10.1098/rsob.130232	journal	March 2014
Water‐Restructuring Mutations Can Reverse the Thermodynamic Signature of Ligand Binding to Human Carbonic Anhydrase Fox, Jerome M.; Kang, Kyungtae; Sastry, Madhavi Angewandte Chemie International Edition, Vol. 56, Issue 14 https://doi.org/10.1002/anie.201609409	journal	March 2017
Hydrogen atoms in protein structures: high-resolution X-ray diffraction structure of the DFPase Elias, Mikael; Liebschner, Dorothee; Koepke, Jurgen BMC Research Notes, Vol. 6, Issue 1 https://doi.org/10.1186/1756-0500-6-308	journal	January 2013
VADAR: a web server for quantitative evaluation of protein structure quality Willard, L. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg565	journal	July 2003
Stable and unstable phases of a diblock copolymer melt Matsen, M. W.; Schick, M. Physical Review Letters, Vol. 72, Issue 16 https://doi.org/10.1103/PhysRevLett.72.2660	journal	April 1994
Hopping Diffusion of Nanoparticles in Polymer Matrices Cai, Li-Heng; Panyukov, Sergey; Rubinstein, Michael Macromolecules, Vol. 48, Issue 3 https://doi.org/10.1021/ma501608x	journal	January 2015
Coil fraction-dependent phase behaviour of a model globular protein–polymer diblock copolymer Thomas, Carla S.; Olsen, Bradley D. Soft Matter, Vol. 10, Issue 17 https://doi.org/10.1039/C3SM52531G	journal	January 2014