Complex coacervate-based materials for biomedicine

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 9, Issue 4, 2017, Pages

  Blocher, Whitney C ^a   Perry, Sarah L ^a  

^a University of Massachusetts   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; COMPLEXATION; NUCLEIC ACIDS; POLYELECTROLYTES; SCAFFOLDS (BIOLOGY); SELF ASSEMBLY; TISSUE CULTURE;

BIOLOGICAL ENVIRONMENTS; CHARGED MACROIONS; COACERVATE; COMPLEX COACERVATES; ELECTROSTATIC COMPLEXATION; INTELLIGENT DESIGNS; PERSONAL CARE PRODUCTS; SMALL MOLECULES;

BIOMATERIALS;

ADHESIVE AGENT; BIOMATERIAL; POLYELECTROLYTE; ELECTROLYTE; POLYMER; PROTEIN;

BIOMEDICINE; BIOREACTOR; CELL ORGANELLE; CHIRALITY; COACERVATION; DEVICE MATERIAL; ENCAPSULATION; PH; PRECIPITATION; PRIORITY JOURNAL; REVIEW; STOICHIOMETRY; TEMPERATURE; THERMODYNAMICS;

BIOCOMPATIBLE MATERIALS; ELECTROLYTES; POLYMERS; PROTEINS;

EID: 84996835532     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1442     Document Type: Review

References (262)

1. Perry S, Li Y, Priftis D, Leon L, Tirrell M. The effect of salt on the complex coacervation of vinyl polyelectrolytes. Polymers 2014, 6:1756–1772. doi:10.3390/polym6061756.
2. Priftis D, Leon L, Song Z, Perry SL, Margossian KO, Tropnikova A, Cheng J, Tirrell M. Self-assembly of α-helical polypeptides driven by complex coacervation. Angew Chem 2015, 127:11280–11284. doi:10.1002/ange.201504861.
3. Water JJ, Schack MM, Velazquez-Campoy A, Maltesen MJ, van de Weert M, Jorgensen L. Complex coacervates of hyaluronic acid and lysozyme: effect on protein structure and physical stability. Eur J Pharm Biopharm 2014, 88:325–331. doi:10.1016/j.ejpb.2014.09.001.
4. Black KA, Priftis D, Perry SL, Yip J, Byun WY, Tirrell M. Protein encapsulation via polypeptide complex coacervation. ACS Macro Lett 2014, 3:1088–1091. doi:10.1021/mz500529v.
5. Kim S, Huang J, Lee Y, Dutta S, Yoo HY, Jung YM, Jho Y, Zeng H, Hwang DS. Complexation and coacervation of like-charged polyelectrolytes inspired by mussels. Proc Natl Acad Sci USA 2016, 113:E847–E853. doi:10.1073/pnas.1521521113.
6. Wang Q, Schlenoff JB. The polyelectrolyte complex/coacervate continuum. Macromolecules 2014, 47:3108–3116. doi:10.1021/ma500500q.
7. 2+, nucleotides, and RNA. Langmuir 2016, 32:2041–2049. doi:10.1021/acs.langmuir.5b04462.
8. Tang TYD, Antognozzi M, Vicary JA, Perriman AW, Mann S. Small-molecule uptake in membrane-free peptide/nucleotide protocells. Soft Matter 2013, 9:7647–7656. doi:10.1039/c3sm50726b.
9. Hwang DS, Waite JH, Tirrell M. Promotion of osteoblast proliferation on complex coacervation-based hyaluronic acid–recombinant mussel adhesive protein coatings on titanium. Biomaterials 2010, 31:1080–1084. doi:10.1016/j.biomaterials.2009.10.041.
10. Kizilay E, Kayitmazer AB, Dubin PL. Complexation and coacervation of polyelectrolytes with oppositely charged colloids. Adv Colloid Interface Sci 2011, 167:24–37. doi:10.1016/j.cis.2011.06.006.
11. Dubin PL, Li Y, Jaeger W. Mesophase separation in polyelectrolyte-mixed micelle coacervates. Langmuir 2008, 24:4544–4549. doi:10.1021/la702405d.
12. Ifeduba EA, Akoh CC. Microencapsulation of stearidonic acid soybean oil in Maillard reaction-modified complex coacervates. Food Chem 2016, 199(C):524–532. doi:10.1016/j.foodchem.2015.12.011.
13. Hoffmann KQ, Perry SL, Leon L, Priftis D, Tirrell M, de Pablo JJ. A molecular view of the role of chirality in charge-driven polypeptide complexation. Soft Matter 2015, 11:1525–1538. doi:10.1039/C4SM02336F.
14. Perry SL, Leon L, Hoffmann KQ, Kade MJ, Priftis D, Black KA, Wong D, Klein RA, Pierce CF, Margossian KO, et al. Chirality-selected phase behaviour in ionic polypeptide complexes. Nat Commun 2015, 6:6052. doi:10.1038/ncomms7052.
15. Obermeyer AC, Mills CE, Dong X-H, Flores RJ, Olsen BD. Complex coacervation of supercharged proteins with polyelectrolytes. Soft Matter 2016, 12:3570–3581. doi:10.1039/C6SM00002A.
16. Pippa N, Karayianni M, Pispas S, Demetzos C. Complexation of cationic-neutral block polyelectrolyte with insulin and in vitro release studies. Int J Pharm 2015, 491:136–143. doi:10.1016/j.ijpharm.2015.06.013.
17. Pippa N, Kalinova R, Dimitrov I, Pispas S, Demetzos C. Insulin/poly(ethylene glycol)-block-poly(l-lysine) complexes: physicochemical properties and protein encapsulation. J Phys Chem B 2015, 119:6813–6819. doi:10.1021/acs.jpcb.5b01664.
18. Nolles A, Westphal AH, de Hoop JA, Fokkink RG, Kleijn JM, van Berkel WJH, Borst JW, Westphal AH. Encapsulation of GFP in complex coacervate core micelles. Biomacromolecules 2015, 16:1542–1549. doi:10.1021/acs.biomac.5b00092.
19. Chen WCW, Lee BG, Park DW, Kim K, Chu H, Kim K, Huard J, Wang Y. Controlled dual delivery of fibroblast growth factor-2 and Interleukin-10 by heparin-based coacervate synergistically enhances ischemic heart repair. Biomaterials 2015, 72:138–151. doi:10.1016/j.biomaterials.2015.08.050.
20. Bungenberg de Jong H, Kruyt HR. Koazervation. Kolloid-Z 1930, 50:39–48.
21. Turgeon SL, Schmitt C, Sanchez C. Protein–polysaccharide complexes and coacervates. Curr Opin Colloid Interface Sci 2007, 12:166–178. doi:10.1016/j.cocis.2007.07.007.
22. Schmitt C, Turgeon SL. Protein/polysaccharide complexes and coacervates in food systems. Adv Colloid Interface Sci 2011, 167:63–70. doi:10.1016/j.cis.2010.10.001.
23. Yeo Y, Bellas E, Firestone W, Langer R, Kohane DS. Complex coacervates for thermally sensitive controlled release of flavor compounds. J Agric Food Chem 2005, 53:7518–7525. doi:10.1021/jf0507947.
24. Matalanis A, Jones OG, McClements DJ. Structured biopolymer-based delivery systems for encapsulation, protection, and release of lipophilic compounds. Food Hydrocoll 2011, 25:1865–1880. doi:10.1016/j.foodhyd.2011.04.014.
25. Jourdain L, Leser ME, Schmitt C, Michel M, Dickinson E. Stability of emulsions containing sodium caseinate and dextran sulfate: relationship to complexation in solution. Food Hydrocoll 2008, 22:647–659. doi:10.1016/j.foodhyd.2007.01.007.
26. Weinbreck F, de Vries R, Schrooyen P, de Kruif CG. Complex coacervation of whey proteins and gum arabic. Biomacromolecules 2003, 4:293–303. doi:10.1021/bm025667n.
27. Knaapila M, Costa T, Garamus VM, Kraft M, Drechsler M, Scherf U, Burrows HD. Polyelectrolyte complexes of a cationic all conjugated fluorene–thiophene diblock copolymer with aqueous DNA. J Phys Chem B 2015, 119:3231–3241. doi:10.1021/jp5110032.
28. Arfin N, Aswal VK, Bohidar HB. Overcharging, thermal, viscoelastic and hydration properties of DNA–gelatin complex coacervates: pharmaceutical and food industries. RSC Adv 2014, 4:11705–11709. doi:10.1039/c3ra46618c.
29. Williams DS, Koga S, Hak CRC, Majrekar A, Patil AJ, Perriman AW, Mann S. Polymer/nucleotide droplets as bio-inspired functional micro-compartments. Soft Matter 2012, 8:6004–6011. doi:10.1039/c2sm25184a.
30. Koga S, Williams DS, Perriman AW, Mann S. Peptide-nucleotide microdroplets as a step towards a membrane-free protocell model. Nat Chem 2011, 3:720–724. doi:10.1038/nchem.1110.
31. Kawamura A, Harada A, Kono K, Kataoka K. Self-assembled nano-bioreactor from block ionomers with elevated and stabilized enzymatic function. Bioconjugate Chem 2007, 18:1555–1559. doi:10.1021/bc070029t.
32. Jaturanpinyo M, Harada A, Yuan X, Kataoka K. Preparation of bionanoreactor based on core−shell structured polyion complex micelles entrapping trypsin in the core cross-linked with glutaraldehyde. Bioconjugate Chem 2004, 15:344–348. doi:10.1021/bc034149m.
33. Kataoka K, Harada A. Pronounced activity of enzymes through the incorporation into the core of polyion complex micelles made from charged block copolymers. J Controlled Release 2001, 72:85–91.
34. Kataoka K, Harada A, Nagasaki Y. Block copolymer micelles for drug delivery: design, characterization and biological significance. Adv Drug Delivery Rev 2001, 47:113–131.
35. Harada A, Kataoka K. Novel polyion complex micelles entrapping enzyme molecules in the core. 2. Characterization of the micelles prepared at nonstoichiometric mixing ratios. Langmuir 1999, 15:4208–4212. doi:10.1021/la981087t.
36. Harada A, Kataoka K. Novel polyion complex micelles entrapping enzyme molecules in the core: preparation of narrowly-distributed micelles from lysozyme and poly(ethylene glycol)-poly(aspartic acid) block copolymer in aqueous medium. Macromolecules 1998, 31:288–294.
37. Harada A, Kataoka K. Formation of polyion complex micelles in an aqueous milieu from a pair of oppositely-charged block copolymers with poly(ethylene glycol) segments. Macromolecules 1995, 28:5294–5299.
38. Voets IK, de Keizer A, Cohen Stuart MA. Complex coacervate core micelles. Adv Colloid Interface Sci 2009, 147–148:300–318. doi:10.1016/j.cis.2008.09.012.
39. Kayitmazer AB, Seyrek E, Dubin PL, Staggemeier BA. Influence of chain stiffness on the interaction of polyelectrolytes with oppositely charged micelles and proteins. J Phys Chem B 2003, 107:8158–8165. doi:10.1021/jp034065a.
40. Kalantar TH, Tucker CJ, Zalusky AS, Boomgaard TA, Wilson BE, Ladika M, Jordan SL, Li WK, Zhang X, Goh CG. High throughput workflow for coacervate formation and characterization in shampoo systems. J Cosmet Sci 2007, 58:375–383.
41. Hu D, Chou KC. Re-evaluating the surface tension analysis of polyelectrolyte-surfactant mixtures using phase-sensitive sum frequency generation spectroscopy. J Am Chem Soc 2014, 136:15114–15117. doi:10.1021/ja5049175.
42. Nejati MM, Khaledi MG. Perfluoro-alcohol-induced complex coacervates of polyelectrolyte–surfactant mixtures: phase behavior and analysis. Langmuir 2015, 31:5580–5589. doi:10.1021/acs.langmuir.5b00444.
43. Szczepanowicz K, Bazylińska U, Pietkiewicz J, Szyk-Warszyńska L, Wilk KA, Warszyński P. Biocompatible long-sustained release oil-core polyelectrolyte nanocarriers: from controlling physical state and stability to biological impact. Adv Colloid Interface Sci 2015, 222:678–691. doi:10.1016/j.cis.2014.10.005.
44. Wang Y, Kimura K, Huang Q, Dubin PL, Jaeger W. Effects of salt on polyelectrolyte−micelle coacervation. Macromolecules 1999, 32:7128–7134. doi:10.1021/ma990972v.
45. Wang W, Mauroy H, Zhu K, Knudsen KD, Kjøniksen A-L, Nyström B, Sande SA. Complex coacervate micelles formed by a C18-capped cationic triblock thermoresponsive copolymer interacting with SDS. Soft Matter 2012, 8:11514–11525. doi:10.1039/c2sm26567b.
46. Karimi F, Qazvini NT, Namivandi-Zangeneh R. Fish gelatin/laponite biohybrid elastic coacervates: a complexation kinetics–structure relationship study. Int J Biol Macromol 2013, 61:102–113. doi:10.1016/j.ijbiomac.2013.06.054.
47. Pawar N, Bohidar HB. Anisotropic domain growth and complex coacervation in nanoclay-polyelectrolyte solutions. Adv Colloid Interface Sci 2011, 167:12–23. doi:10.1016/j.cis.2011.06.007.
48. Krogstad DV, Lynd NA, Choi S-H, Spruell JM, Hawker CJ, Kramer EJ, Tirrell MV. Effects of polymer and salt concentration on the structure and properties of triblock copolymer coacervate hydrogels. Macromolecules 2013, 46:1512–1518. doi:10.1021/ma302299r.
49. Krogstad DV, Choi S-H, Lynd NA, Audus DJ, Perry SL, Gopez JD, Hawker CJ, Kramer EJ, Tirrell MV. Small angle neutron scattering study of complex coacervate micelles and hydrogels formed from ionic diblock and triblock copolymers. J Phys Chem B 2014, 118:13011–13018. doi:10.1021/jp509175a.
50. Krogstad DV, Lynd NA, Miyajima D, Gopez J, Hawker CJ, Kramer EJ, Tirrell MV. Structural evolution of polyelectrolyte complex core micelles and ordered-phase bulk materials. Macromolecules 2014, 47:8026–8032. doi:10.1021/ma5017852.
51. Hunt JN, Feldman KE, Lynd NA, Deek J, Campos LM, Spruell JM, Hernandez BM, Kramer EJ, Hawker CJ. Tunable, high modulus hydrogels driven by ionic coacervation. Adv Mater 2011, 23:2327–2331. doi:10.1002/adma.201004230.
52. Stewart-Sloan CR, Olsen BD. Protonation-induced microphase separation in thin films of a polyelectrolyte-hydrophilic diblock copolymer. ACS Macro Lett 2014, 3:410–414. doi:10.1021/mz400650q.
53. Kim B, Lam CN, Olsen BD. Nanopatterned protein films directed by ionic complexation with water-soluble diblock copolymers. Macromolecules 2012, 45:4572–4580. doi:10.1021/ma2024914.
54. Wu F-G, Jiang Y-W, Chen Z, Yu Z-W. Folding behaviors of protein (lysozyme) confined in polyelectrolyte complex micelle. Langmuir 2016, 32:3655–3664. doi:10.1021/acs.langmuir.6b00235.
55. Ishii S, Kaneko J, Nagasaki Y. Development of a long-acting, protein-loaded, redox-active, injectable gel formed by a polyion complex for local protein therapeutics. Biomaterials 2016, 84:210–218. doi:10.1016/j.biomaterials.2016.01.029.
56. Wang W, Xu Y, Li A, Li T, Liu M, von Klitzing R, Ober CK, Kayitmazer AB, Li L, Guo X. Zinc induced polyelectrolyte coacervate bioadhesive and its transition to a self-healing hydrogel. RSC Adv 2015, 5:66871–66878. doi:10.1039/C5RA11915D.
57. Winslow BD, Shao H, Stewart RJ, Tresco PA. Biocompatibility of adhesive complex coacervates modeled after the sandcastle glue of Phragmatopoma californica for craniofacial reconstruction. Biomaterials 2010, 31:9373–9381. doi:10.1016/j.biomaterials.2010.07.078.
58. Favi PM, Yi S, Lenaghan SC, Xia L, Zhang M. Inspiration from the natural world: from bio-adhesives to bio-inspired adhesives. J Adhes Sci Technol 2013, 28:290–319. doi:10.1080/01694243.2012.691809.
59. Mann LK, Papanna R, Moise KJ Jr, Byrd RH, Popek EJ, Kaur S, Tseng SCG, Stewart RJ. Fetal membrane patch and biomimetic adhesive coacervates as a sealant for fetoscopic defects. Acta Biomater 2012, 8:2160–2165. doi:10.1016/j.actbio.2012.02.014.
60. Lim S, Choi YS, Kang DG, Song YH, Cha HJ. The adhesive properties of coacervated recombinant hybrid mussel adhesive proteins. Biomaterials 2010, 31:3715–3722. doi:10.1016/j.biomaterials.2010.01.063.
61. Hwang DS, Zeng H, Srivastava A, Krogstad DV, Tirrell M, Israelachvili JN, Waite JH. Viscosity and interfacial properties in a mussel-inspired adhesive coacervate. Soft Matter 2010, 6:3232–3235. doi:10.1039/c002632h.
62. Hwang DS, Zeng H, Lu Q, Israelachvili J, Waite JH. Adhesion mechanism in a DOPA-deficient foot protein from green mussels. Soft Matter 2012, 8:5640–5649. doi:10.1039/c2sm25173f.
63. Kaur S, Weerasekare GM, Stewart RJ. Multiphase adhesive coacervates inspired by the sandcastle worm. ACS Appl Mater Interfaces 2011, 3:941–944. doi:10.1021/am200082v.
64. Ahn BK, Das S, Linstadt R, Kaufman Y, Martinez-Rodriguez NR, Mirshafian R, Kesselman E, Talmon Y, Lipshutz BH, Israelachvili JN, et al. High-performance mussel-inspired adhesives of reduced complexity. Nat Commun 2015, 6:8663. doi:10.1038/ncomms9663.
65. Stewart RJ, Wang CS, Shao H. Complex coacervates as a foundation for synthetic underwater adhesives. Adv Colloid Interface Sci 2011, 167:85–93. doi:10.1016/j.cis.2010.10.009.
66. Choi YS, Kang DG, Lim S, Yang YJ, Kim CS, Cha HJ. Recombinant mussel adhesive protein fp-5 (MAP fp-5) as a bulk bioadhesive and surface coating material. Biofouling 2011, 27:729–737. doi:10.1080/08927014.2011.600830.
67. Shao H, Bachus KN, Stewart RJ. A water-borne adhesive modeled after the sandcastle glue of P. californica. Macromol Biosci 2009, 9:464–471. doi:10.1002/mabi.200800252.
68. Lim S, Moon D, Kim HJ, Seo JH, Kang IS, Cha HJ. Interfacial tension of complex coacervated mussel adhesive protein according to the Hofmeister series. Langmuir 2014, 30:1108–1115. doi:10.1021/la403680z.
69. Shao H, Weerasekare GM, Stewart RJ. Controlled curing of adhesive complex coacervates with reversible periodate carbohydrate complexes. J Biomed Mater Res A 2011, 97:46–51. doi:10.1002/jbm.a.33026.
70. Farrar DF. Bone adhesives for trauma surgery a review of challenges and developments. Int J Adhes Adhes 2012, 33:89–97. doi:10.1016/j.ijadhadh.2011.11.009.
71. Lindhoud S, de Vries R, Norde W, Cohen Stuart MA. Structure and stability of complex coacervate core micelles with lysozyme. Biomacromolecules 2007, 8:2219–2227. doi:10.1021/bm0700688.
72. Lindhoud S, Claessens MMAE. Accumulation of small protein molecules in a macroscopic complex coacervate. Soft Matter 2015, 12:408–413. doi:10.1039/C5SM02386F.
73. Kishimura A, Koide A, Osada K, Yamasaki Y, Kataoka K. Encapsulation of myoglobin in PEGylated polyion complex vesicles made from a pair of oppositely charged block ionomers: a physiologically available oxygen carrier. Angew Chem Int Ed 2007, 46:6085–6088. doi:10.1002/anie.200701776.
74. Lindhoud S, de Vries R, Schweins R, Cohen Stuart MA, Norde W. Salt-induced release of lipase from polyelectrolyte complex micelles. Soft Matter 2009, 5:242–250. doi:10.1039/B811640G.
75. Lindhoud S, Norde W, Cohen Stuart MA. Reversibility and relaxation behavior of polyelectrolyte complex micelle formation. J Phys Chem B 2009, 113:5431–5439. doi:10.1021/jp809489f.
76. Chu H, Gao J, Chen C-W, Huard J, Wang Y. Injectable fibroblast growth factor-2 coacervate for persistent angiogenesis. Proc Natl Acad Sci USA 2011, 108:13444–13449. doi:10.1073/pnas.1110121108.
77. Johnson NR, Ambe T, Wang Y. Lysine-based polycation:heparin coacervate for controlled protein delivery. Acta Biomater 2014, 10:40–46. doi:10.1016/j.actbio.2013.09.012.
78. Chu H, Chen C-W, Huard J, Wang Y. The effect of a heparin-based coacervate of fibroblast growth factor-2 on scarring in the infarcted myocardium. Biomaterials 2013, 34:1747–1756. doi:10.1016/j.biomaterials.2012.11.019.
79. Yen J, Ying H, Wang H, Yin L, Uckun F, Cheng J. CD44 mediated nonviral gene delivery into human embryonic stem cells via hyaluronic-acid-coated nanoparticles. ACS Biomater Sci Eng 2016, 2:326–335. doi:10.1021/acsbiomaterials.5b00393.
80. Perry SL, Neumann SG, Neumann T, Cheng K, Ni J, Weinstein JR, Schaffer DV, Tirrell M. Challenges in nucleic acid-lipid films for transfection. AIChE J 2013, 59:3203–3213. doi:10.1002/aic.14198.
81. Kuo C-H, Leon L, Chung EJ, Huang R-T, Sontag TJ, Reardon CA, Getz GS, Tirrell M, Fang Y. Inhibition of atherosclerosis-promoting microRNAs via targeted polyelectrolyte complex micelles. J Mater Chem B 2014, 2:8142–8153. doi:10.1039/C4TB00977K.
82. Aumiller WM Jr, Keating CD. Phosphorylation-mediated RNA/peptide complex coacervation as a model for intracellular liquid organelles. Nat Chem 2015, 8:129–137. doi:10.1038/nchem.2414.
83. Jin K-M, Kim Y-H. Injectable, thermo-reversible and complex coacervate combination gels for protein drug delivery. J Controlled Release 2008, 127:249–256. doi:10.1016/j.jconrel.2008.01.015.
84. Kinoh H, Miura Y, Chida T, Liu X, Mizuno K, Fukushima S, Morodomi Y, Nishiyama N, Cabral H, Kataoka K. Nanomedicines eradicating cancer stem-like cells in vivo by pH-triggered intracellular cooperative action of loaded drugs. ACS Nano 2016, 10:5643–5655. doi:10.1021/acsnano.6b00900.
85. Anraku Y, Kishimura A, Kamiya M, Tanaka S, Nomoto T, Toh K, Matsumoto Y, Fukushima S, Sueyoshi D, Kano MR, et al. Systemically injectable enzyme-loaded polyion complex vesicles as in vivo nanoreactors functioning in tumors. Angew Chem 2015, 128:570–575. doi:10.1002/ange.201508339.
86. Schoonen L, van Hest JCM. Compartmentalization approaches in soft matter science: from nanoreactor development to organelle mimics. Adv Mater 2015, 28:1109–1128. doi:10.1002/adma.201502389.
87. Lv K, Perriman AW, Mann S. Photocatalytic multiphase micro-droplet reactors based on complex coacervation. Chem Commun 2015, 51:8600–8602. doi:10.1039/C5CC01914A.
88. Hyman AA, Simons K. Beyond oil and water--phase transitions in cells. Science 2012, 337:1047–1049. doi:10.1126/science.1223728.
89. Hyman AA, Brangwynne CP. Beyond stereospecificity: liquids and mesoscale organization of cytoplasm. Dev Cell 2011, 21:14–16. doi:10.1016/j.devcel.2011.06.013.
90. Weber SC, Brangwynne CP. Getting RNA and protein in phase. Cell 2012, 149:1188–1191. doi:10.1016/j.cell.2012.05.022.
91. Elbaum-Garfinkle S, Kim Y, Szczepaniak K, Chen CC-H, Eckmann CR, Myong S, Brangwynne CP. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc Natl Acad Sci USA 2015, 112:7189–7194. doi:10.1073/pnas.1504822112.
92. Kato M, Han TW, Xie S, Shi K, Du X, Wu LC, Mirzaei H, Goldsmith EJ, Longgood J, Pei J, et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 2012, 149:753–767. doi:10.1016/j.cell.2012.04.017.
93. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007, 8:9–22. doi:10.1038/nrm2080.
94. Han TW, Kato M, Xie S, Wu LC, Mirzaei H, Pei J, Chen M, Xie Y, Allen J, Xiao G, et al. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 2012, 149:768–779. doi:10.1016/j.cell.2012.04.016.
95. Jia TZ, Hentrich C, Szostak JW. Rapid RNA exchange in aqueous two-phase system and coacervate droplets. Origins Life Evol Biospheres 2014, 44:1–12. doi:10.1007/s11084-014-9355-8.
96. Li P, Banjade S, Cheng H-C, Kim S, Chen B, Guo L, Llaguno M, Hollingsworth JV, King DS, Banani SF, et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 2012, 483:336–340. doi:10.1038/nature10879.
97. Walter H. Consequences of phase separation in cytoplasm. Int Rev Cytol 1999, 192:331–343.
98. Brangwynne CP, Mitchison TJ, Hyman AA. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc Natl Acad Sci USA 2011, 108:4334–4339. doi:10.1073/pnas.1017150108.
99. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Julicher F, Hyman AA. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 2009, 324:1729–1732. doi:10.1126/science.1172046.
100. Brangwynne CP. Phase transitions and size scaling of membrane-less organelles. J Cell Biol 2013, 203:875–881. doi:10.1083/jcb.201308087.
101. Zhang H, Elbaum-Garfinkle S, Langdon EM, Taylor N, Occhipinti P, Bridges AA, Brangwynne CP, Gladfelter AS. RNA controls PolyQ protein phase transitions. Mol Cell 2015, 60:220–230. doi:10.1016/j.molcel.2015.09.017.
102. Lin Y, Protter DSW, Rosen MK, Parker R. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol Cell 2015, 60:208–219. doi:10.1016/j.molcel.2015.08.018.
103. Fromm SA, Kamenz J, Nöldeke ER, Neu A, Zocher G, Sprangers R. In vitro reconstitution of a cellular phase-transition process that Involves the mRNA decapping machinery. Angew Chem Int Ed 2014, 53:7354–7359. doi:10.1002/anie.201402885.
104. Patel A, Lee HO, Jawerth L, Maharana S, Jahnel M, Hein MY, Stoynov S, Mahamid J, Saha S, Franzmann TM, et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 2015, 162:1066–1077. doi:10.1016/j.cell.2015.07.047.
105. Burke KA, Janke AM, Rhine CL, Fawzi NL. Residue-by-residue view of in vitro FUS granules that bind the C-terminal domain of RNA polymerase II. Mol Cell 2015, 60:231–241. doi:10.1016/j.molcel.2015.09.006.
106. Vehlow D, Schmidt R, Gebert A, Siebert M, Lips K, Müller M. Polyelectrolyte complex based interfacial drug delivery system with controlled loading and improved release performance for bone therapeutics. Nanomaterials 2016, 6:53. doi:10.3390/nano6030053.
107. Rauck BM, Novosat TL, Oudega M, Wang Y. Biocompatibility of a coacervate-based controlled release system for protein delivery to the injured spinal cord. Acta Biomater 2015, 11(C):204–211. doi:10.1016/j.actbio.2014.09.037.
108. Lee K-W, Johnson NR, Gao J, Wang Y. Human progenitor cell recruitment via SDF-1α coacervate-laden PGS vascular grafts. Biomaterials 2013, 34:9877–9885. doi:10.1016/j.biomaterials.2013.08.082.
109. Priftis D, Farina R, Tirrell M. Interfacial energy of polypeptide complex coacervates measured via capillary adhesion. Langmuir 2012, 28:8721–8729. doi:10.1021/la300769d.
110. Chu H, Johnson NR, Mason NS, Wang Y. A [polycation:heparin] complex releases growth factors with enhanced bioactivity. J Controlled Release 2011, 150:157–163. doi:10.1016/j.jconrel.2010.11.025.
111. Filatova LY, Donovan DM, Becker SC, Lebedev DN, Priyma AD, Koudriachova HV, Kabanov AV, Klyachko NL. Physicochemical characterization of the staphylolytic LysK enzyme in complexes with polycationic polymers as a potent antimicrobial. Biochimie 2013, 95:1689–1696. doi:10.1016/j.biochi.2013.04.013.
112. Insua I, Liamas E, Zhang Z, Peacock A, Krachler AM, Fernandez-Trillo F. Enzyme-responsive polyion complex (PIC) nanoparticles for the targeted delivery of antimicrobial polymers. Polym Chem 2016, 7:2684–2690. doi:10.1039/C6PY00146G.
113. Wang B, Jin T, Xu Q, Liu H, Ye Z, Chen H. Direct loading and tunable release of antibiotics from polyelectrolyte multilayers to reduce bacterial adhesion and biofilm formation. Bioconjugate Chem 2016, 27:1305–1313. doi:10.1021/acs.bioconjchem.6b00118.
114. Fan Y, Tang S, Thomas EL, Olsen BD. Responsive block copolymer photonics triggered by protein–polyelectrolyte coacervation. ACS Nano 2014, 8:11467–11473. doi:10.1021/nn504565r.
115. Wang J, Velders AH, Gianolio E, Aime S, Vergeldt FJ, Van As H, Yan Y, Drechsler M, de Keizer A, Cohen Stuart MA, et al. Controlled mixing of lanthanide(iii) ions in coacervate core micelles. Chem Commun 2013, 49:3736–3738. doi:10.1039/c3cc39148e.
116. Miura Y, Tsuji AB, Sugyo A, Sudo H, Aoki I, Inubushi M, Yashiro M, Hirakawa K, Cabral H, Nishiyama N, et al. Polymeric micelle platform for multimodal tomographic imaging to detect scirrhous gastric cancer. ACS Biomater Sci Eng 2015, 1:1067–1076. doi:10.1021/acsbiomaterials.5b00142.
117. Gao G, Yan Y, Pispas S, Yao P. Sustained and extended release with structural and activity recovery of lysozyme from complexes with sodium (sulfamate carboxylate) isoprene/ethylene oxide block copolymer. Macromol Biosci 2010, 10:139–146. doi:10.1002/mabi.200900186.
118. Priftis D, Xia X, Margossian KO, Perry SL, Leon L, Qin J, de Pablo JJ, Tirrell M. Ternary, tunable polyelectrolyte complex fluids driven by complex coacervation. Macromolecules 2014, 47:3076–3085. doi:10.1021/ma500245j.
119. Priftis D, Megley K, Laugel N, Tirrell M. Complex coacervation of poly(ethylene-imine)/polypeptide aqueous solutions: thermodynamic and rheological characterization. J Colloid Interface Sci 2013, 398(C):39–50. doi:10.1016/j.jcis.2013.01.055.
120. Chollakup R, Smitthipong W, Eisenbach CD, Tirrell M. Phase behavior and coacervation of aqueous poly(acrylic acid)−poly(allylamine) solutions. Macromolecules 2010, 43:2518–2528. doi:10.1021/ma902144k.
121. Chollakup R, Beck JB, Dirnberger K, Tirrell M, Eisenbach CD. Polyelectrolyte molecular weight and salt effects on the phase behavior and coacervation of aqueous solutions of poly(acrylic acid) sodium salt and poly(allylamine) hydrochloride. Macromolecules 2013, 46:2376–2390. doi:10.1021/ma202172q.
122. Priftis D, Tirrell M. Phase behaviour and complex coacervation of aqueous polypeptide solutions. Soft Matter 2012, 8:9396–9405. doi:10.1039/C2SM25604E.
123. Priftis D, Laugel N, Tirrell M. Thermodynamic characterization of polypeptide complex coacervation. Langmuir 2012, 28:15947–15957. doi:10.1021/la302729r.
124. Kayitmazer AB, Koksal AF, Iyilik EK. Complex coacervation of hyaluronic acid and chitosan: effects of pH, ionic strength, charge density, chain length and the charge ratio. Soft Matter 2015, 11:8605–8612. doi:10.1039/C5SM01829C.
125. Du X, Dubin PL, Hoagland DA, Sun L. Protein-selective coacervation with hyaluronic acid. Biomacromolecules 2014, 15:726–734. doi:10.1021/bm500041a.
126. Sing CE. Development of the modern theory of polymeric complex coacervation. Adv Colloid Interface Sci. In press. doi:10.1016/j.cis.2016.04.004.
127. Pak CW, Kosno M, Holehouse AS, Padrick SB, Mittal A, Ali R, Yunus AA, Liu DR, Pappu RV, Rosen MK. Sequence determinants of intracellular phase separation by complex coacervation of a disordered protein. Mol Cell 2016, 63:72–85. doi:10.1016/j.molcel.2016.05.042.
128. Flanagan SE, Malanowski AJ, Kizilay E, Seeman D, Dubin PL, Donato-Capel L, Bovetto L, Schmitt C. Complex equilibria, speciation, and heteroprotein coacervation of lactoferrin and β-lactoglobulin. Langmuir 2015, 31:1776–1783. doi:10.1021/la504020e.
129. van der Gucht J, Spruijt E, Lemmers M, Cohen Stuart MA. Polyelectrolyte complexes: bulk phases and colloidal systems. J Colloid Interface Sci 2011, 361:407–422. doi:10.1016/j.jcis.2011.05.080.
130. de Kruif CG, Weinbreck F, de Vries R. Complex coacervation of proteins and anionic polysaccharides. Curr Opin Colloid Interface Sci 2004, 9:340–349. doi:10.1016/j.cocis.2004.09.006.
131. Kayitmazer AB, Seeman D, Minsky BB, Dubin PL, Xu Y. Protein–polyelectrolyte interactions. Soft Matter 2013, 9:2553–2583. doi:10.1039/c2sm27002a.
132. Harada A, Kataoka K. Chain length recognition: core-shell supramolecular assembly from oppositely charged block copolymers. Science 1999, 283:65–67. doi:10.1126/science.283.5398.65.
133. Spruijt E, Westphal AH, Borst JW, Cohen Stuart MA, van der Gucht J. Binodal compositions of polyelectrolyte complexes. Macromolecules 2010, 43:6476–6484. doi:10.1021/ma101031t.
134. Spruijt E, Cohen Stuart MA, van der Gucht J. Linear viscoelasticity of polyelectrolyte complex coacervates. Macromolecules 2013, 46:1633–1641. doi:10.1021/ma301730n.
135. Spruijt E, Leermakers FAM, Fokkink R, Schweins R, van Well AA, Cohen Stuart MA, van der Gucht J. Structure and dynamics of polyelectrolyte complex coacervates studied by scattering of neutrons, X-rays, and light. Macromolecules 2013, 46:4596–4605. doi:10.1021/ma400132s.
136. Anema SG, de Kruif CGK. Coacervates of lysozyme and β-casein. J Colloid Interface Sci 2013, 398(C):255–261. doi:10.1016/j.jcis.2013.02.013.
137. Anema SG, Kees de Kruif CG. Co-acervates of lactoferrin and caseins. Soft Matter 2012, 8:4471–4478. doi:10.1039/c2sm00015f.
138. Anema SG, de Kruif CGK. Complex coacervates of lactotransferrin and β-lactoglobulin. J Colloid Interface Sci 2014, 430(C):214–220. doi:10.1016/j.jcis.2014.05.036.
139. de Kruif CGK, Pedersen J, Huppertz T, Anema SG. Coacervates of lactotransferrin and β- or κ-casein: structure determined using SAXS. Langmuir 2013, 29:10483–10490. doi:10.1021/la402236f.
140. Yan Y, Kizilay E, Seeman D, Flanagan S, Dubin PL, Bovetto L, Donato L, Schmitt C. Heteroprotein complex coacervation: bovine β-lactoglobulin and lactoferrin. Langmuir 2013, 29:15614–15623. doi:10.1021/la4027464.
141. Kayitmazer AB, Strand SP, Tribet C, Jaeger W, Dubin PL. Effect of polyelectrolyte structure on protein−polyelectrolyte coacervates: coacervates of bovine serum albumin with poly(diallyldimethylammonium chloride) versus chitosan. Biomacromolecules 2007, 8:3568–3577. doi:10.1021/bm700645t.
142. Xia J, Mattison K, Romano V, Dubin PL, Muhoberac BB. Complexation of trypsin and alcohol dehydrogenase with poly(diallyldimethylammonium chloride). Biopolymers 1997, 41:359–365. doi:10.1002/(SICI)1097-0282(19970405)41:4<359::AID-BIP1>3.0.CO;2-L.
143. Cooper CL, Goulding A, Kayitmazer AB, Ulrich S, Stoll S, Turksen S, Yusa S-I, Kumar A, Dubin PL. Effects of polyelectrolyte chain stiffness, charge mobility, and charge sequences on binding to proteins and micelles. Biomacromolecules 2006, 7:1025–1035. doi:10.1021/bm050592j.
144. Bohidar H, Dubin PL, Majhi PR, Tribet C, Jaeger W. Effects of protein−polyelectrolyte affinity and polyelectrolyte molecular weight on dynamic properties of bovine serum albumin−poly(diallyldimethylammonium chloride) coacervates. Biomacromolecules 2005, 6:1573–1585. doi:10.1021/bm049174p.
145. Cooper CL, Dubin PL, Kayitmazer AB, Turksen S. Polyelectrolyte–protein complexes. Curr Opin Colloid Interface Sci 2005, 10:52–78. doi:10.1016/j.cocis.2005.05.007.
146. Kizilay E, Seeman D, Yan Y, Du X, Dubin PL, Donato-Capel L, Bovetto L, Schmitt C. Structure of bovine β-lactoglobulin–lactoferrin coacervates. Soft Matter 2014, 10:7262–7268. doi:10.1039/C4SM01333F.
147. Lindhoud S, Voorhaar L, de Vries R, Schweins R, Cohen Stuart MA, Norde W. Salt-induced disintegration of lysozyme-containing polyelectrolyte complex micelles. Langmuir 2009, 25:11425–11430. doi:10.1021/la901591p.
148. Cohen Stuart MA, Besseling NAM, Fokkink RG. Formation of micelles with complex coacervate cores. Langmuir 1998, 14:6846–6849. doi:10.1021/la980778m.
149. Tekaat M, Bütergerds D, Schönhoff M, Fery A, Cramer C. Scaling properties of the shear modulus of polyelectrolyte complex coacervates: a time-pH superposition principle. Phys Chem Chem Phys 2015, 17:22552–22556. doi:10.1039/C5CP02940F.
150. Rawat K, Bohidar HB. Coacervation in biopolymers. J Phys Chem Biophys 2014, 4:1000165. doi:10.4172/2161-0398.1000165.
151. van der Kooij HM, Spruijt E, Voets IK, Fokkink R, Cohen Stuart MA, van der Gucht J. On the stability and morphology of complex coacervate core micelles: from spherical to wormlike micelles. Langmuir 2012, 28:14180–14191. doi:10.1021/la303211b.
152. Spruijt E, Sprakel J, Cohen Stuart MA, van der Gucht J. Interfacial tension between a complex coacervate phase and its coexisting aqueous phase. Soft Matter 2010, 6:172–178. doi:10.1039/B911541B.
153. Spruijt E, Sprakel J, Lemmers M, Cohen Stuart MA, van der Gucht J. Relaxation dynamics at different time scales in electrostatic complexes: time-salt superposition. Phys Rev Lett 2010, 105:208301–208304. doi:10.1103/PhysRevLett.105.208301.
154. Dubin PL, Gao J, Mattison K. Protein purification by selective phase separation with polyelectrolytes. Sep Purif Rev 1994, 23:1–16. doi:10.1080/03602549408001288.
155. Xu Y, Mazzawi M, Chen K, Sun L, Dubin PL. Protein purification by polyelectrolyte coacervation: influence of protein charge anisotropy on selectivity. Biomacromolecules 2011, 12:1512–1522. doi:10.1021/bm101465y.
156. Kayitmazer AB, Bohidar HB, Mattison KW, Bose A, Sarkar J, Hashidzume A, Russo PS, Jaeger W, Dubin PL. Mesophase separation and probe dynamics in protein–polyelectrolyte coacervates. Soft Matter 2007, 3:1064–1076. doi:10.1039/B701334E.
157. Kayitmazer AB, Quinn B, Kimura K, Ryan GL, Tate AJ, Pink DA, Dubin PL. Protein specificity of charged sequences in polyanions and heparins. Biomacromolecules 2010, 11:3325–3331. doi:10.1021/bm1008074.
158. Comert F, Malanowski AJ, Azarikia F, Dubin PL. Coacervation and precipitation in polysaccharide-protein systems. Soft Matter 2016, 12:4154–4161. doi:10.1039/C6SM00044D.
159. Antonov M, Mazzawi M, Dubin PL. Entering and exiting the protein−polyelectrolyte coacervate phase via nonmonotonic salt dependence of critical conditions. Biomacromolecules 2010, 11:51–59. doi:10.1021/bm900886k.
160. Hattori T, Kimura K, Seyrek E, Dubin PL. Binding of bovine serum albumin to heparin determined by turbidimetric titration and frontal analysis continuous capillary electrophoresis. Anal Biochem 2001, 295:158–167. doi:10.1006/abio.2001.5129.
161. Kaibara K, Okazaki T, Bohidar HB, Dubin PL. pH-Induced coacervation in complexes of bovine serum albumin and cationic polyelectrolytes. Biomacromolecules 2000, 1:100–107. doi:10.1021/bm990006k.
162. Qin J, Priftis D, Farina R, Perry SL, Leon L, Whitmer J, Hoffmann K, Tirrell M, de Pablo JJ. Interfacial tension of polyelectrolyte complex coacervate phases. ACS Macro Lett 2014, 3:565–568. doi:10.1021/mz500190w.
163. Fu J, Schlenoff JB. Driving forces for oppositely charged polyion association in aqueous solutions: enthalpic, entropic, but not electrostatic. J Am Chem Soc 2016, 138:980–990. doi:10.1021/jacs.5b11878.
164. Lawrence PG, Lapitsky Y. Ionically cross-linked poly(allylamine) as a stimulus-responsive underwater adhesive: ionic strength and pH effects. Langmuir 2015, 31:1564–1574. doi:10.1021/la504611x.
165. Laaser JE, Jiang Y, Sprouse D, Reineke TM, Lodge TP. pH- and ionic-strength-induced contraction of polybasic micelles in buffered aqueous solutions. Macromolecules 2015, 48:2677–2685. doi:10.1021/acs.macromol.5b00360.
166. Bae Y, Fukushima S, Harada A, Kataoka K. Design of environment-sensitive supramolecular assemblies for intracellular drug delivery: polymeric micelles that are responsive to intracellular pH change. Angew Chem Int Ed 2003, 42:4640–4643. doi:10.1002/anie.200250653.
167. Nigen M, Croguennec T, Bouhallab S. Formation and stability of α-lactalbumin–lysozyme spherical particles: involvement of electrostatic forces. Food Hydrocoll 2009, 23:510–518. doi:10.1016/j.foodhyd.2008.02.005.
168. Kunz W, Lo Nostro P, Ninham BW. The present state of affairs with Hofmeister effects. Curr Opin Colloid Interface Sci 2004, 9:1–18. doi:10.1016/j.cocis.2004.05.004.
169. Zhang Y, Cremer PS. Interactions between macromolecules and ions: the Hofmeister series. Curr Opin Chem Biol 2006, 10:658–663. doi:10.1016/j.cbpa.2006.09.020.
170. Pearson RG. Hard and soft acids and bases. J Am Chem Soc 1963, 85:3533–3539. doi:10.1021/ja00905a001.
171. Pearson RG. Hard and soft acids and bases, HSAB, part 1: fundamental principles. J Chem Educ 1968, 45:581–587. doi:10.1021/ed045p581.
172. Collins KD. Ion hydration: implications for cellular function, polyelectrolytes, and protein crystallization. Biophys Chem 2006, 119:271–281. doi:10.1016/j.bpc.2005.08.010.
173. Collins KD. Charge density-dependent strength of hydration and biological structure. Biophys J 1997, 72:65–76. doi:10.1016/S0006-3495(97)78647-8.
174. Collins KD. Ions from the Hofmeister series and osmolytes: effects on proteins in solution and in the crystallization process. Methods 2004, 34:300–311. doi:10.1016/j.ymeth.2004.03.021.
175. Rawat K, Aswal VK, Bohidar HB. DNA–gelatin complex coacervation, UCST and first-order phase transition of coacervate to anisotropic ion gel in 1-methyl-3-octylimidazolium chloride ionic liquid solutions. J Phys Chem B 2012, 116:14805–14816. doi:10.1021/jp3102089.
176. Biesheuvel PM, Lindhoud S, de Vries R, Cohen Stuart MA. Phase behavior of mixtures of oppositely charged nanoparticles: heterogeneous Poisson−Boltzmann cell model applied to lysozyme and succinylated lysozyme. Langmuir 2006, 22:1291–1300. doi:10.1021/la052334d.
177. Koga T, Tanaka F, Motokawa R, Koizumi S, Winnik FM. Theoretical modeling of associated structures in aqueous solutions of hydrophobically modified telechelic PNIPAM based on a neutron scattering study. Macromolecules 2008, 41:9413–9422. doi:10.1021/ma800957z.
178. Liberatore MW, Wyatt NB, Henry M, Dubin PL, Foun E. Shear-induced phase separation in polyelectrolyte/mixed micelle coacervates. Langmuir 2009, 25:13376–13383. doi:10.1021/la903260r.
179. Perry SL, Sing CE. PRISM-based theory of complex coacervation: excluded volume versus chain correlation. Macromolecules 2015, 48:5040–5053. doi:10.1021/acs.macromol.5b01027.
180. Turovsky T, Khalfin R, Kababya S, Schmidt A, Barenholz Y, Danino D. Celecoxib encapsulation in β-casein micelles: structure, interactions, and conformation. Langmuir 2015, 31:7183–7192. doi:10.1021/acs.langmuir.5b01397.
181. Rasente RY, Imperiale JC, Lázaro-Martínez JM, Gualco L, Oberkersch R, Sosnik A, Calabrese GC. Dermatan sulfate/chitosan polyelectrolyte complex with potential application in the treatment and diagnosis of vascular disease. Carbohydr Polym 2016, 144:362–370. doi:10.1016/j.carbpol.2016.02.046.
182. Wang L, Cao Y, Zhang K, Fang Y, Nishinari K, Phillips GO. Hydrogen bonding enhances the electrostatic complex coacervation between κ-carrageenan and gelatin. Colloids Surf A 2015, 482:604–610. doi:10.1016/j.colsurfa.2015.07.011.
183. Chai C, Lee J, Huang Q. The effect of ionic strength on the rheology of pH-induced bovine serum albumin κ-carrageenan coacervates. LWT-Food Sci Technol 2014, 59:356–360. doi:10.1016/j.lwt.2014.05.024.
184. Chremos A, Douglas JF. Counter-ion distribution around flexible polyelectrolytes having different molecular architecture. Soft Matter 2016, 12:2932–2941. doi:10.1039/C5SM02873F.
185. Laaser JE, Jiang Y, Petersen SR, Reineke TM, Lodge TP. Interpolyelectrolyte complexes of polycationic micelles and linear polyanions: structural stability and temporal evolution. J Phys Chem B 2015, 119:15919–15928. doi:10.1021/acs.jpcb.5b09010.
186. Chuanoi S, Anraku Y, Hori M, Kishimura A, Kataoka K. Fabrication of polyion complex vesicles with enhanced salt and temperature resistance and their potential applications as enzymatic nanoreactors. Biomacromolecules 2014, 15:2389–2397. doi:10.1021/bm500127g.
187. Lemmers M, Sprakel J, Voets IK, van der Gucht J, Cohen Stuart MA. Multiresponsive reversible gels based on charge-driven assembly. Angew Chem 2009, 122:720–723. doi:10.1002/ange.200905515.
188. Krogstad DV. Investigating the structure–property relationships of aqueous self-assembled materials. PhD Dissertation, University of California, Santa Barbara, 2012, 1–262.
189. Anraku Y, Kishimura A, Yamasaki Y, Kataoka K. Living unimodal growth of polyion complex vesicles via two-dimensional supramolecular polymerization. J Am Chem Soc 2013, 135:1423–1429. doi:10.1021/ja3096587.
190. Anraku Y, Kishimura A, Oba M, Yamasaki Y, Kataoka K. Spontaneous formation of nanosized unilamellar polyion complex vesicles with tunable size and properties. J Am Chem Soc 2010, 132:1631–1636. doi:10.1021/ja908350e.
191. Mao Z, Cartier R, Hohl A, Farinacci M, Dorhoi A, Nguyen T-L, Mulvaney P, Ralston J, Kaufmann SHE, Möhwald H, et al. Cells as factories for humanized encapsulation. Nano Lett 2011, 11:2152–2156. doi:10.1021/nl200801n.
192. Bourouina N, Cohen Stuart MA, Kleijn JM. Complex coacervate core micelles as diffusional nanoprobes. Soft Matter 2014, 10:320–331. doi:10.1039/C3SM52245H.
193. Bourouina N, de Kort DW, Hoeben FJM, Janssen HM, Van As H, Hohlbein J, van Duynhoven JPM, Kleijn JM. Complex coacervate core micelles with spectroscopic labels for diffusometric probing of biopolymer networks. Langmuir 2015, 31:12635–12643. doi:10.1021/acs.langmuir.5b03496.
194. Wu B-C, Degner B, McClements DJ. Soft matter strategies for controlling food texture: formation of hydrogel particles by biopolymer complex coacervation. J Phys Condens Matter 2014, 26:464104–464112. doi:10.1088/0953-8984/26/46/464104.
195. Madene A, Jacquot M, Scher J, Desobry S. Flavour encapsulation and controlled release—a review. Int J Food Sci Technol 2006, 41:1–21. doi:10.1111/j.1365-2621.2005.00980.x.
196. Augustin MA, Hemar Y. Nano- and micro-structured assemblies for encapsulation of food ingredients. Chem Soc Rev 2009, 38:902–912. doi:10.1039/B801739P.
197. Johnson NR, Wang Y. Controlled delivery of heparin-binding EGF-like growth factor yields fast and comprehensive wound healing. J Controlled Release 2013, 166:124–129. doi:10.1016/j.jconrel.2012.11.004.
198. McClements DJ, Decker EA, Park Y, Weiss J. Structural design principles for delivery of bioactive components in nutraceuticals and functional foods. Crit Rev Food Sci Nutr 2009, 49:577–606. doi:10.1080/10408390902841529.
199. McClements DJ, Li Y. Structured emulsion-based delivery systems: controlling the digestion and release of lipophilic food components. Adv Colloid Interface Sci 2010, 159:213–228. doi:10.1016/j.cis.2010.06.010.
200. Truong-Le VL, August JT, Leong KW. Controlled gene delivery by DNA-gelatin nanospheres. Hum Gene Ther 1998, 9:1707–1717.
201. Truong-Le VL, Walsh SM, Schweibert E, Mao H-Q, Guggino WB, August JT, Leong KW. Gene transfer by DNA–gelatin nanospheres. Arch Biochem Biophys 1999, 361:47–56. doi:10.1006/abbi.1998.0975.
202. Leong KW, Mao HQ, Truong-Le VL, Roy K, Walsh SM, August JT. DNA-polycation nanospheres as non-viral gene delivery vehicles. J Controlled Release 1998, 53:183–193. doi:10.1016/S0168-3659(97)00252-6.
203. Ozbas-Turan S, Aral C, Kabasakal L, Keyer-Uysal M, Akbuga J. Co-encapsulation of two plasmids in chitosan microspheres as a non-viral gene delivery vehicle. J Pharm Pharm Sci 2003, 6:27–32.
204. Thomasin C, Nam-Tran H, Merkle HP, Gander B. Drug microencapsulation by PLA/PLGA coacervation in the light of thermodynamics. 1. Overview and theoretical considerations. J Pharm Sci 1998, 87:259–268. doi:10.1021/js970047r.
205. Martin N, Li M, Mann S. Selective uptake and refolding of globular proteins in coacervate microdroplets. Langmuir 2016, 32:5881–5889. doi:10.1021/acs.langmuir.6b01271.
206. Galan A, Ballester P. Stabilization of reactive species by supramolecular encapsulation. Chem Soc Rev 2016, 45:1720–1737. doi:10.1039/C5CS00861A.
207. Sedlák E, Fedunová D, Veselá V, Sedláková D, Antalík M. Polyanion Hydrophobicity and protein basicity affect protein stability in protein−polyanion complexes. Biomacromolecules 2009, 10:2533–2538. doi:10.1021/bm900480t.
208. Khondee S, Olsen CM, Zeng Y, Middaugh CR, Berkland C. Noncovalent PEGylation by polyanion complexation as a means to stabilize keratinocyte growth factor-2 (KGF-2). Biomacromolecules 2011, 12:3880–3894. doi:10.1021/bm2007967.
209. Tiwari A, Bindal S, Bohidar HB. Kinetics of protein−protein complex coacervation and biphasic release of salbutamol sulfate from coacervate matrix. Biomacromolecules 2009, 10:184–189. doi:10.1021/bm801160s.
210. Nishiyama N, Kataoka K. Current state, achievements, and future prospects of polymeric micelles as nanocarriers for drug and gene delivery. Pharmacol Ther 2006, 112:630–648. doi:10.1016/j.pharmthera.2006.05.006.
211. Johnson NR, Wang Y. Coacervate delivery systems for proteins and small molecule drugs. Expert Opin Drug Delivery 2014, 11:1829–1832. doi:10.1517/17425247.2014.941355.
212. Plummer R, Wilson RH, Calvert H, Boddy AV, Griffin M, Sludden J, Tilby MJ, Eatock M, Pearson DG, Ottley CJ, et al. A phase I clinical study of cisplatin-incorporated polymeric micelles (NC-6004) in patients with solid tumours. Br J Cancer 2011, 104:593–598. doi:10.1038/bjc.2011.6.
213. Alsharabasy AM, Moghannem SA, El-Mazny WN. Physical preparation of alginate/chitosan polyelectrolyte complexes for biomedical applications. J Biomater Appl 2016, 30:1071–1079. doi:10.1177/0885328215613886.
214. Li H, Johnson NR, Usas A, Lu A, Poddar M, Wang Y, Huard J. Sustained release of bone morphogenetic protein 2 via coacervate improves the osteogenic potential of muscle-derived stem cells. Stem Cells Transl Med 2013, 2:667–677. doi:10.5966/sctm.2013-0027.
215. Moore KW, de Waal Malefyt R, Coffman RL, OGarra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683–765. doi:10.1146/annurev.immunol.19.1.683.
216. Ghobadi AF, Letteri R, Parelkar SS, Zhao Y, Chan-Seng D, Emrick T, Jayaraman A. Dispersing zwitterions into comb polymers for nonviral transfection: experiments and molecular simulation. Biomacromolecules 2016, 17:546–557. doi:10.1021/acs.biomac.5b01462.
217. Li S, Huang L. Nonviral gene therapy: promises and challenges. Gene Ther 2000, 7:31–34. doi:10.1038/sj.gt.3301110.
218. Chesnoy S, Huang L. Structure and function of lipid-DNA complexes for gene delivery. Annu Rev Biophys Biomol Struct 2000, 29:27–47.
219. Martin B, Sainlos M, Aissaoui A, Oudrhiri N, Hauchecorne M, Vigneron J, Lehn J, Lehn P. The design of cationic lipids for gene delivery. Curr Pharm Des 2005, 11:375–394. doi:10.2174/1381612053382133.
220. Katayose S, Kataoka K. Remarkable increase in nuclease resistance of plasmid DNA through supramolecular assembly with poly(ethylene glycol). J Pharm Sci 1998, 87:160–163. doi:10.1021/js970304s.
221. Katayose S, Kataoka K. Water-soluble polyion complex associates of DNA and aoly(ethylene glycol)−aoly(L-lysine) block copolymer. Bioconjugate Chem 1997, 8:702–707. doi:10.1021/bc9701306.
222. Ainalem M-L, Nylander T. DNA condensation using cationic dendrimers—morphology and supramolecular structure of formed aggregates. Soft Matter 2011, 7:4577–4594. doi:10.1039/c0sm01171a.
223. Cai J, Yue Y, Rui D, Zhang Y, Liu S, Wu C. Effect of chain length on cytotoxicity and endocytosis of cationic polymers. Macromolecules 2011, 44:2050–2057. doi:10.1021/ma102498g.
224. Peng HT, Shek PN. Novel wound sealants: biomaterials and applications. Expert Rev Med Devices 2014, 7:639–659. doi:10.1586/erd.10.40.
225. Wolfert MA, Schacht EH, Toncheva V, Ulbrich K, Nazarova O, Seymour LW. Characterization of vectors for gene therapy formed by self-assembly of DNA with synthetic block co-polymers. Hum Gene Ther 1996, 7:2123–2133. doi:10.1089/hum.1996.7.17-2123.
226. Tangsangasaksri M, Takemoto H, Naito M, Maeda Y, Sueyoshi D, Kim HJ, Miura Y, Ahn J, Azuma R, Nishiyama N, et al. siRNA-loaded polyion complex micelle decorated with charge-conversional polymer tuned to undergo stepwise response to intra-tumoral and intra-endosomal pHs for exerting enhanced RNAi efficacy. Biomacromolecules 2016, 17:246–255. doi:10.1021/acs.biomac.5b01334.
227. Stewart RJ. Protein-based underwater adhesives and the prospects for their biotechnological production. Appl Microbiol Biotechnol 2010, 89:27–33. doi:10.1007/s00253-010-2913-8.
228. Shao H, Stewart RJ. Biomimetic underwater adhesives with environmentally triggered setting mechanisms. Adv Mater 2010, 22:729–733. doi:10.1002/adma.200902380.
229. Wei W, Tan Y, Rodriguez NRM, Yu J, Israelachvili JN, Waite JH. A mussel-derived one component adhesive coacervate. Acta Biomater 2014, 10:1663–1670. doi:10.1016/j.actbio.2013.09.007.
230. Zhang L, Lipik V, Miserez A. Complex coacervates of oppositely charged co-polypeptides inspired by the sandcastle worm glue. J Mater Chem B 2016, 4:1544–1556. doi:10.1039/C5TB02298C.
231. Maier GP, Rapp MV, Waite JH, Israelachvili JN, Butler A. Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Chem Eng News 2015, 349:628–632. doi:10.1126/science.aab0556.
232. Lam J, Clark EC, Fong ELS, Lee EJ, Lu S, Tabata Y, Mikos AG. Evaluation of cell-laden polyelectrolyte hydrogels incorporating poly(l-Lysine) for applications in cartilage tissue engineering. Biomaterials 2016, 83(c):332–346. doi:10.1016/j.biomaterials.2016.01.020.
233. Wang D-A, Varghese S, Sharma B, Strehin I, Fermanian S, Gorham J, Fairbrother DH, Cascio B, Elisseeff JH. Multifunctional chondroitin sulphate for cartilage tissue–biomaterial integration. Nat Mater 2007, 6:385–392. doi:10.1038/nmat1890.
234. Jones JP, Sima M, O'Hara RG, Stewart RJ. Water-borne endovascular embolics inspired by the undersea adhesive of marine sandcastle worms. Adv Healthcare Mater 2016, 5:795–801. doi:10.1002/adhm.201500825.
235. Kim HJ, Hwang BH, Lim S, Choi B-H, Kang SH, Cha HJ. Mussel adhesion-employed water-immiscible fluid bioadhesive for urinary fistula sealing. Biomaterials 2015, 72:104–111. doi:10.1016/j.biomaterials.2015.08.055.
236. Papanna R, Mann LK, Tseng SCG, Stewart RJ, Kaur SS, Swindle MM, Kyriakides TR, Tatevian N, Moise KJ Jr. Cryopreserved human amniotic membrane and a bioinspired underwater adhesive to seal and promote healing of iatrogenic fetal membrane defect sites. Placenta 2015, 36:888–894. doi:10.1016/j.placenta.2015.05.015.
237. Papanna R, Moise KJ Jr, Mann LK, Fletcher S, Schniederjan R, Bhattacharjee MB, Stewart RJ, Kaur S, Prabhu SP, Tseng SCG. Cryopreserved human umbilical cord patch for in-utero spina bifida repair. Ultrasound Obstet Gynecol 2016, 47:168–176. doi:10.1002/uog.15790.
238. Williams DS, Patil AJ, Mann S. Spontaneous structuration in coacervate-based protocells by polyoxometalate-mediated membrane assembly. Small 2014, 10:1830–1840. doi:10.1002/smll.201303654.
239. Yin Y, Niu L, Zhu X, Zhao M, Zhang Z, Mann S, Liang D. Non-equilibrium behaviour in coacervate-based protocells under electric-field-induced excitation. Nat Commun 2016, 7:10658. doi:10.1038/ncomms10658.
240. Monnard P-A, Walde P. Current ideas about prebiological compartmentalization. Life 2015, 5:1239–1263. doi:10.3390/life5021239.
241. Mann S. The origins of life: old problems, new chemistries. Angew Chem Int Ed 2012, 52:155–162. doi:10.1002/anie.201204968.
242. Keating CD. Aqueous phase separation as a possible route to compartmentalization of biological molecules. Acc Chem Res 2012, 45:2114–2124. doi:10.1021/ar200294y.
243. Dominak LM, Gundermann EL, Keating CD. Microcompartmentation in artificial cells: pH-induced conformational changes alter protein localization. Langmuir 2010, 26:5697–5705. doi:10.1021/la903800e.
244. Long MS, Jones CD, Helfrich MR, Mangeney-Slavin LK, Keating CD. Dynamic microcompartmentation in synthetic cells. Proc Natl Acad Sci USA 2005, 102:5920–5925. doi:10.1073/pnas.0409333102.
245. Kolb VM, Swanson M, Menger FM. Coacervates as prebiotic chemical reactors. In: Hoover RB, Levin GV, Rozanov AY, eds. SPIE, vol. 8521. 2012, 85210E.
246. Oparin AI. The origin of primary colloidal systems. In: The Origin of Life. New York: Stratford Press, Inc.; 1953, 137–162.
247. Menger FM, Sykes BM. Anatomy of a coacervate. Langmuir 1998, 14:4131–4137. doi:10.1021/la980208m.
248. Devi N, Sarmah M, Khatun B, Maji TK. Encapsulation of active ingredients in polysaccharide-protein complex coacervates. Adv Colloid Interface Sci. In press. doi:10.1016/j.cis.2016.05.009.
249. Szostak JW, Bartel DP, Luisi PL. Synthesizing life. Nature 2001, 409:387–390. doi:10.1038/35053176.
250. Aumiller WM Jr, Keating CD. Experimental models for dynamic compartmentalization of biomolecules in liquid organelles: reversible formation and partitioning in aqueous biphasic systems. Adv Colloid Interface Sci. In press. doi:10.1016/j.cis.2016.06.011.
251. Narayanaswamy R, Levy M, Tsechansky M, Stovall GM, O'Connell JD, Mirrielees J, Ellington AD, Marcotte EM. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc Natl Acad Sci USA 2009, 106:10147–10152. doi:10.1073/pnas.0812771106.
252. Feric M, Vaidya N, Harmon TS, Mitrea DM, Zhu L, Richardson TM, Kriwacki RW, Pappu RV, Brangwynne CP. Coexisting liquid phases underlie nucleolar subcompartments. Cell 2016, 165:1686–1697. doi:10.1016/j.cell.2016.04.047.
253. Nott TJ, Petsalaki E, Farber P, Jervis D, Fussner E, Plochowietz A, Craggs TD, Bazett-Jones DP, Pawson T, Forman-Kay JD, et al. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol Cell 2015, 57:936–947. doi:10.1016/j.molcel.2015.01.013.
254. Stoeger T, Battich N, Pelkmans L. Passive noise filtering by cellular compartmentalization. Cell 2016, 164:1151–1161. doi:10.1016/j.cell.2016.02.005.
255. Decher G. Fuzzy nanoassemblies: toward layered polymeric multicomposites. Science 1997, 277:1232–1237. doi:10.1126/science.277.5330.1232.
256. Jewell C, Lynn D. Surface-mediated delivery of DNA: cationic polymers take charge. Curr Opin Colloid Interface Sci 2008, 13:395–402. doi:10.1016/j.cocis.2008.03.005.
257. Jewell CM, Lynn DM. Multilayered polyelectrolyte assemblies as platforms for the delivery of DNA and other nucleic acid-based therapeutics. Adv Drug Delivery Rev 2008, 60:979–999. doi:10.1016/j.addr.2008.02.010.
258. Jewell CM, Zhang J, Fredin NJ, Wolff MR, Hacker TA, Lynn DM. Release of plasmid DNA from intravascular stents coated with ultrathin multilayered polyelectrolyte films. Biomacromolecules 2006, 7:2483–2491. doi:10.1021/bm0604808.
259. Jewell CM, Zhang J, Fredin NJ, Lynn DM. Multilayered polyelectrolyte films promote the direct and localized delivery of DNA to cells. J Controlled Release 2005, 106:214–223. doi:10.1016/j.jconrel.2005.04.014.
260. Schaaf P, Schlenoff JB. Saloplastics: processing compact polyelectrolyte complexes. Adv Mater 2015, 27:2420–2432. doi:10.1002/adma.201500176.
261. Hariri HH, Schlenoff JB. Saloplastic macroporous polyelectrolyte complexes: cartilage mimics. Macromolecules 2010, 43:8656–8663. doi:10.1021/ma1012978.
262. Porcel CH, Schlenoff JB. Compact polyelectrolyte complexes: “saloplastic” candidates for biomaterials. Biomacromolecules 2009, 10:2968–2975. doi:10.1021/bm900373c.