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Ice-binding proteins: from antifreeze mechanism to resistant soft materials

Periodic Reporting for period 4 - PRISM (Ice-binding proteins: from antifreeze mechanism to resistant soft materials)

Reporting period: 2019-11-01 to 2021-04-30

Crystallization of water into ice is lethal to most organisms and detrimental to many soft materials. Freeze-tolerant fish living in polar seas evolved to tackle this problem with an unusual coping strategy. They produce ‘antifreeze’ proteins that block the growth of nascent ice crystals within a narrow temperature range known as the ‘thermal hysteresis gap’ enabling survival under extreme conditions. Encoding this functionality into synthetic polymers would open up new avenues in biomedicine, agrifood and materials science for e.g. cryopreservation, crop hardiness, ice-templating, dispersion stability, and advanced coatings. Progress requires a profound understanding of the mechanism of non-colligative freezing point depression at the molecular level and allows for efficient strategies for the design and preparation of powerful macromolecular antifreezes.
PRISM has advanced our understanding of the mechanism by which antifreeze proteins (AFPs) function. Design principles for the engineering of ice-binding polymers have been established which facilitate the development of freeze-resistant soft materials. Novel ice-binders have been prepared. Our work revealed that small amounts of artificial ice-binders are sufficient to realize concrete with enhanced freeze-thaw resistance.

On-line animations and lectures:
1. Prof. Voets @ the University of the Netherlands: https://www.youtube.com/watch?v=x1GLoWA6krI
2. Prof. Voets @ KNCV on ice-binding proteins: https://www.eye-openers.nl/nl/seethecast/ilja-voets/
3. Animation of ice-binding proteins: https://www.youtube.com/watch?v=uoRgpqAVsTE&ab_channel=ICMS

Selected publications in peer-reviewed journals
1. Voets, I. K. From ice-binding proteins to bio-inspired antifreeze materials, Soft matter 2017, 13 (28), 4808-4823.
2. Oude Vrielink, A. S.; Aloi, A.; Olijve, L. L.C.; Voets, I. K. Interaction of ice-binding proteins with ice, water and ions, Biointerphases 2016, 11, 018906
3. Surís-Valls, R.; Mehmedbasic, M.; Voets, I. K Marine Fish Antifreeze Proteins: The Key Towards Cryopreserving The Winter Soldier Superhero Science and Technology 2018, 1 (1), doi.org/10.24413/sst.2018.1.2105
4. Olijve, L. L.C.; Meister, K.; DeVries, A. L.; Duman, J. G.; Guo, S.; Bakker, H. J.; Voets, I. K. Blocking rapid ice crystal growth through non-basal plane adsorption of antifreeze proteins, Proceedings of the National Academy of Sciences of the United States of America 2016, 113 (14), 3740-3745.
5. Olijve, L. L. C.; Oude Vrielink, A. S.; Voets, I. K. A simple and quantitative method to evaluate ice recrystallization kinetics using the circle Hough transform algorithm, Crystal Growth & Design 2016, 16 (8), 4190–4195.
6. Brotzakis Z. F.; Gehre M.; Voets, I. K.; Bolhuis, P. G. Stability and growth mechanism of self-assembling putative anti-freeze cyclic peptides, Physical Chemistry Chemical Physics 2017, 19 (29), 19032-19042
7. Surís-Valls, R.; Voets, I.K. The Impact of Salts on the Ice Recrystallization Inhibition Activity of Antifreeze (Glyco)Proteins Biomolecules 2019, 9(8), 347.
8. Sproncken, C. C. M; Surís-Valls, R.; Cingil, H. E.; Detrembleur, C.; Voets, I. K. Complex Coacervate Core Micelles Containing Poly(vinyl alcohol) Inhibit Ice Recrystallization, Macromolecular Rapid Communications 2018, 39 (17), 1700814
9. Olijve, L. L. C.; Hendrix, M. M. R. M.; Voets, I. K. Influence of Polymer Chain Architecture of Poly(vinyl Alcohol) on the inhibition of Ice Recrystallization, Macromolecular Chemistry and Physics 2016, doi: 10.1002/macp.201500497 (COVER).
10. Brotzakis, Z. F.; Voets, I. K.; Bakker, H. J.; Bolhuis, P. G. Water structure and dynamics in the hydration layer of a type III anti-freeze protein, Physical Chemistry Chemical Physics, DOI: 10.1039/C8CP00170G
11. Qu, Z.; Guo, S.; Sproncken, C. C.M.; Surís-Valls, R.; Yu, Q.; Voets, I. K. Enhancing the Freeze-Thaw Durability of Concrete through Ice Recrystallization Inhibition by Poly(vinyl alcohol) ACS Omega 2020, 5 (22), 12825-12831
12. Qu, Z.; Guo, S.; Zheng, Y.; Giakoumatos, E.C.; Yu, Q.; Voets, I. K. A simple method to create hydrophobic mortar using bacteria grown in liquid cultures Construction and Building Materials 2021, 297, 23, 123744
13. Pujals, S.; Feiner-Gracia, N.; Delcanale, P.; Voets, I. K.; Albertazzi, L., Super-resolution microscopy as a powerful tool to study complex synthetic materials, Nature Reviews Chemistry 2019, 3 (2), 68-84
14. Aloi, A.; Voets, I. K. Soft Matter Nanoscopy, Current Opinion in Colloid and Interface Science 2018, DOI: 10.1016/j.cocis.2018.03.001
15. Oude Vrielink, A. S.; Vance, T.; De Jong, A. M.; Davies, P. L.; Voets, I. K. Unusually high mechanical stability of bacterial adhesin extender domains having calcium clamps, Plos One 2017, 12 (4), e0174682
16. Guo, S.; Langelaan, D. N.; Phippen, S. W.; Smith, S. P.; Voets, I. K.; Davies, Peter L. Conserved structural features anchor biofilm-associated RTX–adhesins to the outer membrane of bacteria, The FEBS Journal 2018, 285, DOI: 10.1111/febs.14441
17. Guo, S.; Stevens, C.; Vance, T. D. R.; Olijve, L. L. C.; Graham, L. A.; Campbell, R. L.; Yazdi, S. R.; Escobedo, C.; Bar-Dolev, M.; Vashunsky, V.; Braslavsky, I.; Langelaan, D. N.; Smith, S. P.; Allingham, J. S.; Voets, I. K.; Davies, P. L. Structure of a 1.5-MDa adhesin that binds Antarctic bacteria with diatoms to ice, Science Advances 2017, 3(8), e1701440
18. Guo, S.; Vance, Tyler D. R.; Stevens, C. A.; Voets, I. K.; Davies, P. L., RTX Adhesins are key bacterial surface megaproteins in the formation of biofilms, Trends in Microbiology 2019, 27 (5), 453-467
19. Surís-Valls, R.; Voets, I.K. Peptidic antifreeze materials: prospects and challenges, International Journal of Molecular Sciences 2019, 20 (20), 5149.
20. Tas, R. P.; Sampaio-Pinto, V.; Wennekes, T.; van Laake, L. W.; Voets, I. K. From the freezer to the clinic: Antifreeze proteins in the preservation of cells, tissues, and organs EMBO Reports 2021, 22 (3), e52162
21. Sampaio-Pinto, V.; Janssen, J.; Chirico, N.; Serra, M.; Alves, P. M.; Doevendans, P. A.; Voets, I. K.; Sluijter, J. P. G.; van Laake, L. W.; van Mil, Alain A Roadmap to Cardiac Tissue-Engineered Construct Preservation: Insights from Cells, Tissues, and Organs Advanced Materials 2021, e2008517 doi: 10.1002/adma.202008517
One of the most exciting experiments performed in PRISM are the world’s first single-molecule experiments on ice-bound antifreeze proteins. These shed light on long-standing hypotheses pertaining to the working mechanism of antifreeze proteins. The results allow us to better understand how natural ice-binding proteins work and support the rational design of synthetic ice-binders.
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