Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers (original) (raw)

References

1. Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340 (2012).
   CAS Google Scholar
2. Kato, M. et al. Cell-free formation of RNA granules: Low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753–767 (2012).
   CAS Google Scholar
3. Weber, S. C. & Brangwynne, C. P. Getting RNA and protein in phase. Cell 149, 1188–1191 (2012).
   CAS Google Scholar
4. Vekilov, P. G. Phase transitions of folded proteins. Soft Matter 6, 5254–5272 (2010).
   CAS Google Scholar
5. Toretsky, J. A. & Wright, P. E. Assemblages: Functional units formed by cellular phase separation. J. Cell Biol. 206, 579–588 (2014).
   CAS Google Scholar
6. Frey, S., Richter, R. P. & Görlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314, 815–817 (2006).
   CAS Google Scholar
7. Roy, D., Brooks, W. L. & Sumerlin, B. S. New directions in thermoresponsive polymers. Chem. Soc. Rev. 42, 7214–7243 (2013).
   CAS Google Scholar
8. Stuart, M. A. C. et al. Emerging applications of stimuli-responsive polymer materials. Nature Mater. 9, 101–113 (2010).
   Google Scholar
9. McDaniel, J. R. et al. Self-assembly of thermally responsive nanoparticles of a genetically encoded peptide polymer by drug conjugation. Angew. Chem. Int. Ed. 52, 1683–1687 (2013).
   CAS Google Scholar
10. MacKay, J. A. et al. Self-assembling chimeric polypeptide–doxorubicin conjugate nanoparticles that abolish tumours after a single injection. Nature Mater. 8, 993–999 (2009).
    Google Scholar
11. Liu, W. et al. Brachytherapy using injectable seeds that are self-assembled from genetically encoded polypeptides in situ. Cancer Res. 72, 5956–5965 (2012).
    CAS Google Scholar
12. Nishida, K. et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. New Eng. J. Med. 351, 1187–1196 (2004).
    CAS Google Scholar
13. Caves, J. M. et al. Elastin-like protein matrix reinforced with collagen microfibers for soft tissue repair. Biomaterials 32, 5371–5379 (2011).
    CAS Google Scholar
14. Koria, P. et al. Self-assembling elastin-like peptides growth factor chimeric nanoparticles for the treatment of chronic wounds. Proc. Natl Acad. Sci. USA 108, 1034–1039 (2011).
    CAS Google Scholar
15. Meyer, D. E. & Chilkoti, A. Purification of recombinant proteins by fusion with thermally-responsive polypeptides. Nature Biotechnol. 17, 1112–1115 (1999).
    CAS Google Scholar
16. Bellucci, J. J., Amiram, M., Bhattacharyya, J., McCafferty, D. & Chilkoti, A. Three-in-one chromatography-free purification, tag removal, and site-specific modification of recombinant fusion proteins using sortase A and elastin-like polypeptides. Angew. Chem. Int. Ed. 52, 3703–3708 (2013).
    CAS Google Scholar
17. Stayton, P. S. et al. Control of protein–ligand recognition using a stimuli-responsive polymer. Nature 378, 472–474 (1995).
    CAS Google Scholar
18. Dill, K. A. & MacCallum, J. L. The protein-folding problem, 50 years on. Science 338, 1042–1046 (2012).
    CAS Google Scholar
19. Habchi, J., Tompa, P., Longhi, S. & Uversky, V. N. Introducing protein intrinsic disorder. Chem. Rev. 114, 6561–6588 (2014).
    CAS Google Scholar
20. Li, N. K., Quiroz, F. G., Hall, C. K., Chilkoti, A. & Yingling, Y. G. Molecular description of the LCST behaviour of an elastin-like polypeptide. Biomacromolecules 15, 3522–3530 (2014).
    CAS Google Scholar
21. Muiznieks, L. D. & Keeley, F. W. Proline periodicity modulates the self-assembly properties of elastin-like polypeptides. J. Biol. Chem. 285, 39779–39789 (2010).
    CAS Google Scholar
22. Dutta, N. K. et al. A genetically engineered protein responsive to multiple stimuli. Angew. Chem. Int. Ed. 50, 4428–4431 (2011).
    CAS Google Scholar
23. Rauscher, S., Baud, S., Miao, M., Keeley, F. W. & Pomès, R. Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. Structure 14, 1667–1676 (2006).
    CAS Google Scholar
24. De Las Heras Alarcon, C., Pennadam, S. & Alexander, C. Stimuli responsive polymers for biomedical applications. Chem. Soc. Rev. 34, 276–285 (2005).
    Google Scholar
25. Amiram, M., Quiroz, F. G., Callahan, D. J. & Chilkoti, A. A highly parallel method for synthesizing DNA repeats enables the discovery of ‘smart’ protein polymers. Nature Mater. 10, 141–148 (2011).
    CAS Google Scholar
26. Balu, R. et al. An16-resilin: An advanced multi-stimuli-responsive resilin-mimetic protein polymer. Acta Biomater. 10, 4768–4777 (2014).
    CAS Google Scholar
27. Urry, D. W. et al. Hydrophobicity scale for proteins based on inverse temperature transitions. Biopolymers 32, 1243–1250 (1992).
    CAS Google Scholar
28. Das, R. K. & Pappu, R. V. Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues. Proc. Natl Acad. Sci. USA 110, 13392–13397 (2013).
    CAS Google Scholar
29. Yokoi, H., Kinoshita, T. & Zhang, S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc. Natl Acad. Sci. USA 102, 8414–8419 (2005).
    CAS Google Scholar
30. Müller-Späth, S. et al. Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 107, 14609–14614 (2010).
    Google Scholar
31. Möglich, A., Joder, K. & Kiefhaber, T. End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation. Proc. Natl Acad. Sci. USA 103, 12394–12399 (2006).
    Google Scholar
32. Meyer, D. E. & Chilkoti, A. Genetically encoded synthesis of protein-based polymers with precisely specified molecular weight and sequence by recursive directional ligation: Examples from the elastin-like polypeptide system. Biomacromolecules 3, 357–367 (2002).
    CAS Google Scholar
33. Seuring, J. & Agarwal, S. First example of a universal and cost-effective approach: Polymers with tunable upper critical solution temperature in water and electrolyte solution. Macromolecules 45, 3910–3918 (2012).
    CAS Google Scholar
34. Shimada, N. et al. Ureido-derivatized polymers based on both poly (allylurea) and poly (L-citrulline) exhibit UCST-type phase transition behaviour under physiologically relevant conditions. Biomacromolecules 12, 3418–3422 (2011).
    CAS Google Scholar
35. Seuring, J. & Agarwal, S. Polymers with upper critical solution temperature in aqueous solution: Unexpected properties from known building blocks. ACS Macro Lett. 2, 597–600 (2013).
    CAS Google Scholar
36. Seuring, J. & Agarwal, S. Polymers with upper critical solution temperature in aqueous solution. Macromol. Rapid Commun. 33, 1898–1920 (2012).
    CAS Google Scholar
37. Azzaroni, O., Brown, A. A. & Huck, W. T. UCST wetting transitions of polyzwitterionic brushes driven by self-association. Angew. Chem. 118, 1802–1806 (2006).
    Google Scholar
38. Lowe, A. B. & McCormick, C. L. Synthesis and solution properties of zwitterionic polymers. Chem. Rev. 102, 4177–4190 (2002).
    CAS Google Scholar
39. Mason, P., Neilson, G., Dempsey, C., Barnes, A. & Cruickshank, J. The hydration structure of guanidinium and thiocyanate ions: Implications for protein stability in aqueous solution. Proc. Natl Acad. Sci. USA 100, 4557–4561 (2003).
    CAS Google Scholar
40. Mahadevi, A. S. & Sastry, G. N. Cation-π interaction: Its role and relevance in chemistry, biology, and material science. Chem. Rev. 113, 2100–2138 (2013).
    CAS Google Scholar
41. Kao, W. J., Lee, D., Schense, J. C. & Hubbell, J. A. Fibronectin modulates macrophage adhesion and FBGC formation: The role of RGD, PHSRN, and PRRARV domains. J. Biomed. Mater. Res. 55, 79–88 (2001).
    CAS Google Scholar
42. Iwamoto, Y. et al. YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 238, 1132–1134 (1987).
    CAS Google Scholar
43. Pierschbacher, M. D. & Ruoslahti, E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30–33 (1983).
    Google Scholar
44. Lee, B. W. et al. Strongly binding cell-adhesive polypeptides of programmable valencies. Angew. Chem. Int. Ed. 49, 1971–1975 (2010).
    CAS Google Scholar
45. van der Lee, R. et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114, 6589–6631 (2014).
    CAS Google Scholar
46. Brassart, B. et al. Conformational dependence of collagenase (matrix metalloproteinase-1) up-regulation by elastin peptides in cultured fibroblasts. J. Biol. Chem. 276, 5222–5227 (2001).
    CAS Google Scholar
47. Dreher, M. R. et al. Temperature triggered self-assembly of polypeptides into multivalent spherical micelles. J. Am. Chem. Soc. 130, 687–694 (2008).
    CAS Google Scholar
48. Callahan, D. J. et al. Triple stimulus-responsive polypeptide nanoparticles that enhance intratumoral spatial distribution. Nano Lett. 12, 2165–2170 (2012).
    CAS Google Scholar
49. Crick, S. L., Ruff, K. M., Garai, K., Frieden, C. & Pappu, R. V. Unmasking the roles of N-and C-terminal flanking sequences from exon 1 of huntingtin as modulators of polyglutamine aggregation. Proc. Natl Acad. Sci. USA 110, 20075–20080 (2013).
    CAS Google Scholar
50. Bates, F. S. et al. Multiblock polymers: Panacea or Pandora’s box? Science 336, 434–440 (2012).
    CAS Google Scholar
51. Hassouneh, W., Zhulina, E. B., Chilkoti, A. & Rubinstein, M. Elastin-like polypeptide diblock copolymers self-assemble into weak micelles. Macromolecules 48, 4183–4195 (2015).
    CAS Google Scholar
52. Tong, R., Chiang, H. H. & Kohane, D. S. Photoswitchable nanoparticles for in vivo cancer chemotherapy. Proc. Natl Acad. Sci. USA 110, 19048–19053 (2013).
    CAS Google Scholar
53. Wong, C. et al. Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl Acad. Sci. USA 108, 2426–2431 (2011).
    CAS Google Scholar
54. Clark, J. I. Self-assembly of protein aggregates in ageing disorders: The lens and cataract model. Phil. Trans. R. Soc. B 368, 20120104 (2013).
    Google Scholar
55. Smith, F. J. et al. Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nature Genet. 38, 337–342 (2006).
    CAS Google Scholar
56. Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132 (1982).
    CAS Google Scholar
57. McDaniel, J. R., MacKay, J. A., Quiroz, F. G. & Chilkoti, A. Recursive directional ligation by plasmid reconstruction allows rapid and seamless cloning of oligomeric genes. Biomacromolecules 11, 944–952 (2010).
    CAS Google Scholar

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