Ionic liquids as biocompatible stabilizers of proteins

Biophysical Reviews - Tập 10 Số 3 - Trang 781-793 - 2018
Mouhamad Reslan1, Veysel Kayser1
1Faculty of Pharmacy, The University of Sydney, Sydney, Australia

Tóm tắt

Từ khóa


Tài liệu tham khảo

Alvarez-Guerra M, Albo J, Alvarez-Guerra E, Irabien A (2015) Ionic liquids in the electrochemical valorization of CO2. Energy Environ Sci 8:2574–2599. https://doi.org/10.1039/C5EE01486G

Angell CA, Byrne N, Belieres J-P (2007) Parallel developments in aprotic and protic ionic liquids: physical chemistry and applications. Acc Chem Res 40:1228–1236. https://doi.org/10.1021/ar7001842

Angell M, Pan C-J, Rong Y, Yuan C, Lin M-C, Hwang B-J, Dai H (2017) High Coulombic efficiency aluminum-ion battery using an AlCl3-urea ionic liquid analog electrolyte. Proc Natl Acad Sci 114:834–839. https://doi.org/10.1073/pnas.1619795114

Attri P, Venkatesu P, Kumar A (2011) Activity and stability of [small alpha]-chymotrypsin in biocompatible ionic liquids: enzyme refolding by triethyl ammonium acetate. Phys Chem Chem Phys 13:2788–2796. https://doi.org/10.1039/C0CP01291B

Batchelor JD, Olteanu A, Tripathy A, Pielak GJ (2004) Impact of protein denaturants and stabilizers on water structure. J Am Chem Soc 126:1958–1961. https://doi.org/10.1021/ja039335h

Benedetto A, Ballone P (2016) Room temperature ionic liquids interacting with bio-molecules: an overview of experimental and computational studies. Philos Mag 96:870–894. https://doi.org/10.1080/14786435.2015.1119323

Bisht M, Mondal D, Pereira MM, Freire MG, Venkatesu P, Coutinho JAP (2017) Long-term protein packaging in cholinium-based ionic liquids: improved catalytic activity and enhanced stability of cytochrome c against multiple stresses. Green Chem 19:4900–4911. https://doi.org/10.1039/C7GC02011B

Bisht M, Venkatesu P (2017) Influence of cholinium-based ionic liquids on the structural stability and activity of [small alpha]-chymotrypsin. New J Chem. https://doi.org/10.1039/C7NJ03023A

Buchfink R, Tischer A, Patil G, Rudolph R, Lange C (2010) Ionic liquids as refolding additives: variation of the anion. J Biotechnol 150:64–72. https://doi.org/10.1016/j.jbiotec.2010.07.003

Byrne N, Rodoni B, Constable F, Varghese S, Davis JH (2012) Enhanced stabilization of the tobacco mosaic virus using protic ionic liquids. Phys Chem Chem Phys 14:10119–10121. https://doi.org/10.1039/C2CP41625E

Chevrot G, Fileti EE, Chaban VV (2015) Enhanced stability of the model mini-protein in amino acid ionic liquids and their aqueous solutions. J Comput Chem 36:2044–2051. https://doi.org/10.1002/jcc.24042

da Costa Lopes AM, João KG, Rubik DF, Bogel-Łukasik E, Duarte LC, Andreaus J, Bogel-Łukasik R (2013) Pre-treatment of lignocellulosic biomass using ionic liquids: wheat straw fractionation. Bioresour Technol 142:198–208. https://doi.org/10.1016/j.biortech.2013.05.032

Egorova KS, Gordeev EG, Ananikov VP (2017) Biological activity of ionic liquids and their application in pharmaceutics and medicine. Chem Rev 117:7132–7189. https://doi.org/10.1021/acs.chemrev.6b00562

Elgundi Z, Reslan M, Cruz E, Sifniotis V, Kayser V (2017) The state-of-play and future of antibody therapeutics. Adv Drug Deliv Rev 122:2–19. https://doi.org/10.1016/j.addr.2016.11.004

Fang J, Lyu M, Wang X, Wu Y, Zhao J (2015) Synthesis and performance of novel anion exchange membranes based on imidazolium ionic liquids for alkaline fuel cell applications. J Power Sources 284:517–523. https://doi.org/10.1016/j.jpowsour.2015.03.065

Fedorov MV, Kornyshev AA (2014) Ionic liquids at electrified interfaces. Chem Rev 114:2978–3036. https://doi.org/10.1021/cr400374x

Foureau DM, Vrikkis RM, Jones CP, Weaver KD, MacFarlane DR, Salo JC, McKillop IH, Elliott GD (2012) In vitro assessment of choline dihydrogen phosphate (CDHP) as a vehicle for recombinant human Interleukin-2 (rhIL-2). Cell Mol Bioeng 5:390–401. https://doi.org/10.1007/s12195-012-0243-x

Frade RFM, Afonso CAM (2010) Impact of ionic liquids in environment and humans: an overview. Human & Experimental Toxicology 29:1038–1054. https://doi.org/10.1177/0960327110371259

Fujita K, Forsyth M, MacFarlane DR, Reid RW, Elliott GD (2006) Unexpected improvement in stability and utility of cytochrome c by solution in biocompatible ionic liquids. Biotechnol Bioeng 94:1209–1213. https://doi.org/10.1002/bit.20928

Fujita K, MacFarlane DR, Forsyth M, Yoshizawa-Fujita M, Murata K, Nakamura N, Ohno H (2007) Solubility and stability of cytochrome c in hydrated ionic liquids: effect of oxo acid residues and kosmotropicity. Biomacromolecules 8:2080–2086. https://doi.org/10.1021/bm070041o

Fujita K, Nakamura N, Igarashi K, Samejima M, Ohno H (2009) Biocatalytic oxidation of cellobiose in an hydrated ionic liquid. Green Chem 11:351–354. https://doi.org/10.1039/B813529K

Gao W-W, Zhang F-X, Zhang G-X, Zhou C-H (2015) Key factors affecting the activity and stability of enzymes in ionic liquids and novel applications in biocatalysis. Biochem Eng J 99:67–84. https://doi.org/10.1016/j.bej.2015.03.005

Garcia-Lorenzo A, Tojo E, Tojo J, Teijeira M, Rodriguez-Berrocal FJ, Gonzalez MP, Martinez-Zorzano VS (2008) Cytotoxicity of selected imidazolium-derived ionic liquids in the human Caco-2 cell line. Sub-structural toxicological interpretation through a QSAR study. Green Chem 10:508–516. https://doi.org/10.1039/B718860A

Gouveia W, Jorge TF, Martins S, Meireles M, Carolino M, Cruz C, Almeida TV, Araújo MEM (2014) Toxicity of ionic liquids prepared from biomaterials. Chemosphere 104:51–56. https://doi.org/10.1016/j.chemosphere.2013.10.055

Greaves TL, Drummond CJ (2015) Protic ionic liquids: evolving structure–property relationships and expanding applications. Chem Rev 115:11379–11448. https://doi.org/10.1021/acs.chemrev.5b00158

Guncheva M, Paunova K, Ossowicz P, Rozwadowski Z, Janus E, Idakieva K, Todinova S, Raynova Y, Uzunova V, Apostolova S, Tzoneva R, Yancheva D (2015) Modification of Rapana thomasiana hemocyanin with choline amino acid salts significantly enhances its antiproliferative activity against MCF-7 human breast cancer cells. RSC Adv 5:63345–63354. https://doi.org/10.1039/C5RA12214G

Haberler M, Schroder C, Steinhauser O (2011) Solvation studies of a zinc finger protein in hydrated ionic liquids. Phys Chem Chem Phys 13:6955–6969. https://doi.org/10.1039/C0CP02487B

Hayes R, Imberti S, Warr GG, Atkin R (2012) How water dissolves in protic ionic liquids. Angew Chem Int Ed 51:7468–7471. https://doi.org/10.1002/anie.201201973

Hayes R, Warr GG, Atkin R (2015) Structure and nanostructure in ionic liquids. Chem Rev 115:6357–6426. https://doi.org/10.1021/cr500411q

Haykir NI, Bahcegul E, Bicak N, Bakir U (2013) Pretreatment of cotton stalk with ionic liquids including 2-hydroxy ethyl ammonium formate to enhance biomass digestibility. Ind Crop Prod 41:430–436. https://doi.org/10.1016/j.indcrop.2012.04.041

He Q, O'Brien JW, Kitselman KA, Tompkins LE, Curtis GCT, Kerton FM (2014) Synthesis of cyclic carbonates from CO2 and epoxides using ionic liquids and related catalysts including choline chloride-metal halide mixtures. Catal Sci Technol 4:1513–1528. https://doi.org/10.1039/C3CY00998J

Huddleston JG, Visser AE, Reichert WM, Willauer HD, Broker GA, Rogers RD (2001) Characterization and comparison of hydrophilic and hydrophobic room temperature ionic liquids incorporating the imidazolium cation. Green Chem 3:156–164. https://doi.org/10.1039/b103275p

Jha I, Attri P, Venkatesu P (2014) Unexpected effects of the alteration of structure and stability of myoglobin and hemoglobin in ammonium-based ionic liquids. Phys Chem Chem Phys 16:5514–5526. https://doi.org/10.1039/C3CP54398F

Jing B, Lan N, Qiu J, Zhu Y (2016) Interaction of ionic liquids with a lipid bilayer: a biophysical study of ionic liquid cytotoxicity. J Phys Chem B 120:2781–2789. https://doi.org/10.1021/acs.jpcb.6b00362

Jouannin C, Tourne-Peteilh C, Darcos V, Sharkawi T, Devoisselle J-M, Gaveau P, Dieudonne P, Vioux A, Viau L (2014) Drug delivery systems based on pharmaceutically active ionic liquids and biocompatible poly(lactic acid). J Mater Chem B 2:3133–3141. https://doi.org/10.1039/C4TB00264D

Kayser V, Chennamsetty N, Voynov V, Helk B, Forrer K, Trout BL (2011) Evaluation of a non-Arrhenius model for therapeutic monoclonal antibody aggregation. J Pharm Sci 100:2526–2542. https://doi.org/10.1002/jps.22493

Khan I, Kurnia KA, Mutelet F, Pinho SP, Coutinho JAP (2014) Probing the interactions between ionic liquids and water: experimental and quantum chemical approach. J Phys Chem B 118:1848–1860. https://doi.org/10.1021/jp4113552

Klahn M, Lim GS, Seduraman A, Wu P (2011) On the different roles of anions and cations in the solvation of enzymes in ionic liquids. Phys Chem Chem Phys 13:1649–1662. https://doi.org/10.1039/C0CP01509A

Kumar A, Bisht M, Venkatesu P (2017a) Biocompatibility of ionic liquids towards protein stability: a comprehensive overview on the current understanding and their implications. Int J Biol Macromol 96:611–651. https://doi.org/10.1016/j.ijbiomac.2016.12.005

Kumar PK, Jha I, Venkatesu P, Bahadur I, Ebenso EE (2017b) A comparative study of the stability of stem bromelain based on the variation of anions of imidazolium-based ionic liquids. J Mol Liq 246:178–186. https://doi.org/10.1016/j.molliq.2017.09.037

Kumar RA, Papaiconomou N, Lee J-M, Salminen J, Clark DS, Prausnitz JM (2009) In vitro cytotoxicities of ionic liquids: effect of cation rings, functional groups, and anions. Environ Toxicol 24:388–395. https://doi.org/10.1002/tox.20443

Kumar A, Venkatesu P (2014) Does the stability of proteins in ionic liquids obey the Hofmeister series? Int J Biol Macromol 63:244–253. https://doi.org/10.1016/j.ijbiomac.2013.10.031

Lange C, Patil G, Rudolph R (2005) Ionic liquids as refolding additives: N'-alkyl and N'-(omega-hydroxyalkyl) N-methylimidazolium chlorides. Protein Sci 14:2693–2701. https://doi.org/10.1110/ps.051596605

Lim GS, Zidar J, Cheong DW, Jaenicke S, Klähn M (2014) Impact of ionic liquids in aqueous solution on bacterial plasma membranes studied with molecular dynamics simulations. J Phys Chem B 118:10444–10459. https://doi.org/10.1021/jp5060952

MacFarlane DR, Forsyth M, Howlett PC, Kar M, Passerini S, Pringle JM, Ohno H, Watanabe M, Yan F, Zheng W, Zhang S, Zhang J (2016) Ionic liquids and their solid-state analogues as materials for energy generation and storage. Nat Rev Mater 1:15005. https://doi.org/10.1038/natrevmats.2015.5

MacFarlane DR, Tachikawa N, Forsyth M, Pringle JM, Howlett PC, Elliott GD, Davis JH, Watanabe M, Simon P, Angell CA (2014) Energy applications of ionic liquids. Energy Environ Sci 7:232–250. https://doi.org/10.1039/C3EE42099J

Marrucho IM, Branco LC, Rebelo LPN (2014) Ionic liquids in pharmaceutical applications. Annual Review of Chemical and Biomolecular Engineering 5:527–546. https://doi.org/10.1146/annurev-chembioeng-060713-040024

Mazid RR, Vijayaraghavan R, MacFarlane DR, Cortez-Jugo C, Cheng W (2015) Inhibited fragmentation of mAbs in buffered ionic liquids. Chem Commun 51:8089–8092. https://doi.org/10.1039/C5CC01877C

McEwen AB, Ngo HL, LeCompte K, Goldman JL (1999) Electrochemical properties of imidazolium salt electrolytes for electrochemical capacitor applications. J Electrochem Soc 146:1687–1695. https://doi.org/10.1149/1.1391827

Micaêlo NM, Soares CM (2008) Protein structure and dynamics in ionic liquids. Insights from molecular dynamics simulation studies. J Phys Chem B 112:2566–2572. https://doi.org/10.1021/jp0766050

Ngo HL, LeCompte K, Hargens L, McEwen AB (2000) Thermal properties of imidazolium ionic liquids. Thermochim Acta 357-358:97–102. https://doi.org/10.1016/S0040-6031(00)00373-7

Nony P, Girard P, Chabaud S, Hessel L, Thébault C, Boissel JP (2001) Impact of osmolality on burning sensations during and immediately after intramuscular injection of 0.5 ml of vaccine suspensions in healthy adults. Vaccine 19:3645–3651. https://doi.org/10.1016/S0264-410X(01)00098-6

Pandey A, Ekka MK, Ranjan S, Maiti S, Sachidanandan C (2017) Teratogenic, cardiotoxic and hepatotoxic properties of related ionic liquids reveal the biological importance of anionic components. RSC Adv 7:22927–22935. https://doi.org/10.1039/C7RA01520H

Patel R, Kumari M, Khan AB (2014) Recent advances in the applications of ionic liquids in protein stability and activity: a review. Appl Biochem Biotechnol 172:3701–3720. https://doi.org/10.1007/s12010-014-0813-6

Pereira MM, Pedro SN, Quental MV, Lima ÁS, Coutinho JAP, Freire MG (2015) Enhanced extraction of bovine serum albumin with aqueous biphasic systems of phosphonium- and ammonium-based ionic liquids. J Biotechnol 206:17–25. https://doi.org/10.1016/j.jbiotec.2015.03.028

Peric B, Sierra J, Martí E, Cruañas R, Garau MA, Arning J, Bottin-Weber U, Stolte S (2013) (Eco)toxicity and biodegradability of selected protic and aprotic ionic liquids. J Hazard Mater 261:99–105. https://doi.org/10.1016/j.jhazmat.2013.06.070

Persson M, Bornscheuer UT (2003) Increased stability of an esterase from Bacillus stearothermophilus in ionic liquids as compared to organic solvents. J Mol Catal B Enzym 22:21–27. https://doi.org/10.1016/S1381-1177(02)00294-1

Quental MV, Caban M, Pereira MM, Stepnowski P, Coutinho JAP, Freire MG (2015) Enhanced extraction of proteins using cholinium-based ionic liquids as phase-forming components of aqueous biphasic systems. Biotechnol J 10:1457–1466. https://doi.org/10.1002/biot.201500003

Qureshi ZS, Deshmukh KM, Bhanage BM (2014) Applications of ionic liquids in organic synthesis and catalysis. Clean Technol Environ Policy 16:1487–1513. https://doi.org/10.1007/s10098-013-0660-0

Ranke J, Müller A, Bottin-Weber U, Stock F, Stolte S, Arning J, Störmann R, Jastorff B (2007) Lipophilicity parameters for ionic liquid cations and their correlation to in vitro cytotoxicity. Ecotoxicol Environ Saf 67:430–438. https://doi.org/10.1016/j.ecoenv.2006.08.008

Rodrigues JV, Prosinecki V, Marrucho I, Rebelo LPN, Gomes CM (2011) Protein stability in an ionic liquid milieu: on the use of differential scanning fluorimetry. Phys Chem Chem Phys 13:13614–13616. https://doi.org/10.1039/C1CP21187K

Rogers RD, Seddon KR (2003) Ionic liquids—solvents of the future? Science 302:792–793. https://doi.org/10.1126/science.1090313

Sankaranarayanan K, Sathyaraj G, Nair BU, Dhathathreyan A (2012) Reversible and irreversible conformational transitions in myoglobin: role of hydrated amino acid ionic liquid. J Phys Chem B 116:4175–4180. https://doi.org/10.1021/jp300596z

Schneider CP, Shukla D, Trout BL (2011) Arginine and the Hofmeister series: the role of ion–ion interactions in protein aggregation suppression. J Phys Chem B 115:7447–7458. https://doi.org/10.1021/jp111920y

Schröder C (2017) Proteins in ionic liquids: current status of experiments and simulations. Top Curr Chem 375:25. https://doi.org/10.1007/s41061-017-0110-2

Shu Y, Liu M, Chen S, Chen X, Wang J (2011) New insight into molecular interactions of imidazolium ionic liquids with bovine serum albumin. J Phys Chem B 115:12306–12314. https://doi.org/10.1021/jp2071925

Sivapragasam M, Moniruzzaman M, Goto M (2016) Recent advances in exploiting ionic liquids for biomolecules: solubility, stability and applications. Biotechnol J 11:1000–1013. https://doi.org/10.1002/biot.201500603

Smiatek J (2017) Aqueous ionic liquids and their effects on protein structures: an overview on recent theoretical and experimental results. J Phys Condens Matter 29:233001

Smiglak M, Pringle JM, Lu X, Han L, Zhang S, Gao H, MacFarlane DR, Rogers RD (2014) Ionic liquids for energy, materials, and medicine. Chem Commun 50:9228–9250. https://doi.org/10.1039/C4CC02021A

Stasiewicz M, Mulkiewicz E, Tomczak-Wandzel R, Kumirska J, Siedlecka EM, Golebiowski M, Gajdus J, Czerwicka M, Stepnowski P (2008) Assessing toxicity and biodegradation of novel, environmentally benign ionic liquids (1-alkoxymethyl-3-hydroxypyridinium chloride, saccharinate and acesulfamates) on cellular and molecular level. Ecotoxicol Environ Saf 71:157–165. https://doi.org/10.1016/j.ecoenv.2007.08.011

Steudte S, Neumann J, Bottin-Weber U, Diedenhofen M, Arning J, Stepnowski P, Stolte S (2012) Hydrolysis study of fluoroorganic and cyano-based ionic liquid anions—consequences for operational safety and environmental stability. Green Chem 14:2474–2483. https://doi.org/10.1039/C2GC35855G

Stolte S, Arning J, Bottin-Weber U, Mueller A, Pitner W-R, Welz-Biermann U, Jastorff B, Ranke J (2007) Effects of different head groups and functionalised side chains on the cytotoxicity of ionic liquids. Green Chem 9:760–767. https://doi.org/10.1039/b615326g

Summers CA, Flowers RA (2000) Protein renaturation by the liquid organic salt ethylammonium nitrate. Protein Sci 9:2001–2008

Taha M, Almeida MR, Silva FAE, Domingues P, SPM V, JAP C, Freire MG (2015) Novel biocompatible and self-buffering ionic liquids for biopharmaceutical applications. Chem Eur J 21:4781–4788. https://doi.org/10.1002/chem.201405693

Takekiyo T, Ishikawa Y, Yoshimura Y (2017) Cryopreservation of proteins using ionic liquids: a case study of cytochrome c. J Phys Chem B 121:7614–7620. https://doi.org/10.1021/acs.jpcb.7b05158

Takekiyo T, Yamazaki K, Yamaguchi E, Abe H, Yoshimura Y (2012) High ionic liquid concentration-induced structural change of protein in aqueous solution: a case study of lysozyme. J Phys Chem B 116:11092–11097. https://doi.org/10.1021/jp3057064

Tarannum A, Rao JR, Fathima NN (2018) Choline-based amino acid ILs–collagen interaction: enunciating its role in stabilization/destabilization phenomena. J Phys Chem B 122:1145–1151. https://doi.org/10.1021/acs.jpcb.7b10645

Thuy Pham TP, Cho C-W, Yun Y-S (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–372. https://doi.org/10.1016/j.watres.2009.09.030

Torrecilla JS, García J, Rojo E, Rodríguez F (2009) Estimation of toxicity of ionic liquids in leukemia rat cell line and acetylcholinesterase enzyme by principal component analysis, neural networks and multiple lineal regressions. J Hazard Mater 164:182–194. https://doi.org/10.1016/j.jhazmat.2008.08.022

Vrikkis RM, Fraser KJ, Fujita K, MacFarlane DR, Elliott GD (2009) Biocompatible ionic liquids: a new approach for stabilizing proteins in liquid formulation. J Biomech Eng 131(074514–074514-074514). https://doi.org/10.1115/1.3156810

Wang W (2015) Tolerability of hypertonic injectables. Int J Pharm 490:308–315. https://doi.org/10.1016/j.ijpharm.2015.05.069

Wang Z, Dang L, Han Y, Jiang P, Wei H (2010) Crystallization control of thermal stability and morphology of hen egg white lysozyme crystals by ionic liquids. J Agric Food Chem 58:5444–5448. https://doi.org/10.1021/jf1000343

Wang X, Liu J, Sun L, Yu L, Jiao J, Wang R (2012) Interaction of bovine serum albumin with ester-functionalized anionic surface-active ionic liquids in aqueous solution: a detailed physicochemical and conformational study. J Phys Chem B 116:12479–12488. https://doi.org/10.1021/jp307516a

Wang X, Ohlin CA, Lu Q, Fei Z, Hu J, Dyson PJ (2007) Cytotoxicity of ionic liquids and precursor compounds towards human cell line HeLa. Green Chem 9:1191–1197. https://doi.org/10.1039/B704503D

Weaver KD, Kim HJ, Sun J, MacFarlane DR, Elliott GD (2010) Cyto-toxicity and biocompatibility of a family of choline phosphate ionic liquids designed for pharmaceutical applications. Green Chem 12:507–513. https://doi.org/10.1039/B918726J

Weaver KD, Vrikkis RM, Van Vorst MP, Trullinger J, Vijayaraghavan R, Foureau DM, McKillop IH, MacFarlane DR, Krueger JK, Elliott GD (2012) Structure and function of proteins in hydrated choline dihydrogen phosphate ionic liquid. Phys Chem Chem Phys 14:790–801. https://doi.org/10.1039/C1CP22965F

Wei W, Danielson ND (2011) Fluorescence and circular dichroism spectroscopy of cytochrome c in alkylammonium formate ionic liquids. Biomacromolecules 12:290–297. https://doi.org/10.1021/bm1008052

Weingartner H, Cabrele C, Herrmann C (2012) How ionic liquids can help to stabilize native proteins. Phys Chem Chem Phys 14:415–426. https://doi.org/10.1039/C1CP21947B

Wilkes JS, Zaworotko MJ (1992) Air and water stable 1-ethyl-3-methylimidazolium based ionic liquids. J Chem Soc Chem Commun 965–967. https://doi.org/10.1039/C39920000965

Yamaguchi S, Yamamoto E, Tsukiji S, Nagamune T (2008) Successful control of aggregation and folding rates during refolding of denatured lysozyme by adding N-methylimidazolium cations with various N'-substituents. Biotechnol Prog 24:402–408. https://doi.org/10.1021/bp070207x