CC BY-NC-ND 4.0 · Organic Materials 2020; 02(04): 342-357
DOI: 10.1055/s-0040-1721741
Review

Biomedical Uses of Sulfobetaine-Based Zwitterionic Materials

a  Chemical & Biomolecular Engineering Department, University of Notre Dame, Notre Dame, IN 46556, United States
b  Department of Complex Tissue Regeneration, MERLN Institute for Technology Inspired Regenerative Medicine, Maastricht University, 6211 LK, Maastricht, The Netherlands
,
b  Department of Complex Tissue Regeneration, MERLN Institute for Technology Inspired Regenerative Medicine, Maastricht University, 6211 LK, Maastricht, The Netherlands
,
a  Chemical & Biomolecular Engineering Department, University of Notre Dame, Notre Dame, IN 46556, United States
› Author Affiliations
Funding Information M.J.W. acknowledges funding support through the University of Notre Dame “Advancing our Vision” initiative. M.B.B. acknowledges financial support from the Province of Limburg.


Abstract

Protein fouling can render a biomedical device dysfunctional, and also serves to nucleate the foreign body reaction to an implanted material. Hydrophilic coatings have emerged as a commonly applied route to combat interface-mediated complications and promote device longevity and limited inflammatory response. While polyethylene glycol has received a majority of the attention in this regard, coatings based on zwitterionic moieties have been more recently explored. Sulfobetaines in particular constitute one such class of zwitterions explored for use in mitigating surface fouling, and have been shown to reduce protein adsorption, limit cellular adhesion, and promote increased functional lifetimes and limited inflammatory responses when applied to implanted materials and devices. Here, we present a focused review of the literature surrounding sulfobetaine, beginning with an understanding of its chemistry and the methods by which it is applied to the surface of a biomedical device in molecular and polymeric forms, and then advancing to the many early demonstrations of function in a variety of biomedical applications. Finally, we provide some insights into the benefits and challenges presented by its use, as well as some outlook on the future prospects for using this material to improve biomedical device practice by addressing interface-mediated complications.



Publication History

Received: 27 September 2020

Accepted: 15 November 2020

Publication Date:
23 December 2020 (online)

© 2020. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Peppas NA, Langer R. Science 1994; 263: 1715
  • 2 Langer R, Tirrell DA. Nature 2004; 428: 487
  • 3 Webber MJ, Appel EA, Meijer EW, Langer R. Nat. Mater. 2016; 15: 13
  • 4 Huebsch N, Mooney DJ. Nature 2009; 462: 426
  • 5 Wagner WR, Sakiyama-Elbert SE, Zhang G, Yaszemski MJ. Biomaterials Science: An Introduction to Materials in Medicine. Academic Press; San Diego: 2020
  • 6 Anderson JM, Rodriguez A, Chang DT. Semin. Immunol. 2008; 20: 86
  • 7 Grainger DW. Nat. Biotechnol. 2013; 31: 507
  • 8 Zhou G, Groth T. Macromol. Biosci. 2018; 18: 1800112
  • 9 Wei Q, Becherer T, Angioletti-Uberti S, Dzubiella J, Wischke C, Neffe AT, Lendlein A, Ballauff M, Haag R. Angew. Chem. Int. Ed. 2014; 53: 8004
  • 10 Gorbet MB, Sefton MV. Biomaterials 2004; 25: 5681
  • 11 Anderson JM. Annu. Rev. Mater. Res. 2001; 31: 81
  • 12 Wu P, Grainger DW. Biomaterials 2006; 27: 2450
  • 13 Yu B, Wang C, Ju YM, West L, Harmon J, Moussy Y, Moussy F. Biosens. Bioelectron. 2008; 23: 1278
  • 14 Fey PD. Curr. Opin. Microbiol. 2010; 13: 610
  • 15 Donlan RM. Emerging Infect. Dis. 2001; 7: 277
  • 16 Zheng J, Li L, Tsao H.-K, Sheng Y.-J, Chen S, Jiang S. Biophys. J. 2005; 89: 158
  • 17 Chen S, Yu F, Yu Q, He Y, Jiang S. Langmuir 2006; 22: 8186
  • 18 Chen Y, Thayumanavan S. Langmuir 2009; 25: 13795
  • 19 Jeon SI, Lee JH, Andrade JD, De Gennes P. J. Colloid Interface Sci. 1991; 142: 149
  • 20 Chapman RG, Ostuni E, Takayama S, Holmlin RE, Yan L, Whitesides GM. J. Am. Chem. Soc. 2000; 122: 8303
  • 21 Holmlin RE, Chen X, Chapman RG, Takayama S, Whitesides GM. Langmuir 2001; 17: 2841
  • 22 Jevševar S, Kunstelj M, Porekar VG. Biotechnol. J.: Healthcare Nutr. Technol. 2010; 5: 113
  • 23 Kolate A, Baradia D, Patil S, Vhora I, Kore G, Misra A. J. Controlled Release 2014; 192: 67
  • 24 Zhang P, Sun F, Liu S, Jiang S. J. Controlled Release 2016; 244: 184
  • 25 Li L, Chen S, Jiang S. J. Biomater. Sci., Polym. Ed. 2007; 18: 1415
  • 26 Bindra DS, Williams TD, Stella VJ. Pharm. Res. 1994; 11: 1060
  • 27 Hildebrandt C, Joos L, Saedler R, Winter G. J. Pharm. Sci. 2015; 104: 1938
  • 28 Hubbell JA. Curr. Opin. Biotechnol. 2003; 14: 551
  • 29 Hayward JA, Chapman D. Biomaterials 1984; 5: 135
  • 30 Leng C, Huang H, Zhang K, Hung H.-C, Xu Y, Li Y, Jiang S, Chen Z. Langmuir 2018; 34: 6538
  • 31 Laschewsky A. Polymers (Basel) 2014; 6: 1544
  • 32 Hess M, Jones RG, Kahovec J, Kitayama T, Kratochvíl P, Kubisa P, Mormann W, Stepto RF. T, Tabak D, Vohlídal J. J. Macromol. Sci. Part A Pure Appl. Chem. 2006; 78: 2067
  • 33 Mihara S, Yamaguchi K, Kobayashi M. Langmuir 2019; 35: 1172
  • 34 Paschke S, Lienkamp K. ACS Appl. Polym. Mater . 2020; 2: 129
  • 35 Pradhan S, Kumar S, Mohanty S, Nayak SK. Polym.-Plast. Technol. Mater. 2019; 58: 498
  • 36 Phiri I, Bon CY, Mwemezi M, Hamenu L, Madzvamuse A, Park JH, Lee KS, Ko JM, Lu Y. Mater. Chem. Phys. 2020; 243: 122577
  • 37 Liu Q, Patel AA, Liu L. ACS Appl. Mater. Interfaces 2014; 6: 8996
  • 38 Wei T, Tang Z, Yu Q, Chen H. ACS Appl. Mater. Interfaces 2017; 9: 37511
  • 39 Singha P, Locklin J, Handa H. Acta Biomater. 2017; 50: 20
  • 40 Mi L, Jiang S. Angew. Chem. Int. Ed. Engl. 2014; 53: 1746
  • 41 Li X, Wu B, Chen H, Nan K, Jin Y, Sun L, Wang B. J. Mater. Chem. B 2018; 6: 4274
  • 42 Campoccia D, Montanaro L, Arciola CR. Biomaterials 2013; 34: 8533
  • 43 Ishihara K. Trends Polym. Sci. 1997; 12: 401
  • 44 Bain CD, Whitesides GM. J. Am. Chem. Soc. 1988; 110: 5897
  • 45 Storey R, Jones RG. W. Phytochemistry 1977; 16: 447
  • 46 Ernst R, Miller EJ. Surface-Active Betaines. In: Amphoteric Surfactants. Bluestein BR, Hilton CL. Marcel Dekker; New York: 1982: 148-154
  • 47 Lowe AB, Vamvakaki M, Wassall MA, Wong L, Billingham NC, Armes SP, Lloyd AW. J. Biomed. Mater. Res. 2000; 52: 88
  • 48 Tuzar Z, Pospisil H, Plestil J, Lowe AB, Baines FL, Billingham NC, Armes SP. Macromolecules 1997; 30: 2509
  • 49 Lee JH, Ju YM, Lee WK, Park KD, Kim YH. J. Biomed. Mater. Res. 1998; 40: 314
  • 50 Thompson AR, Harker LA. Manual of Hemostasis and Thrombosis. FA Davis Company; Philadelphia: 1983
  • 51 Yuan YL, Ai F, Zhang J, Zang XB, Shen J, Lin SC. J. Biomater. Sci., Polym. Ed. 2002; 13: 1081
  • 52 Yuan Y, Zhang J, Ai F, Yuan J, Zhou J, Shen J, Lin S. Colloids Surf., B 2003; 29: 247
  • 53 Chen S, Zheng J, Li L, Jiang S. J. Am. Chem. Soc. 2005; 127: 14473
  • 54 Zhang Z, Chao T, Chen S, Jiang S. Langmuir 2006; 22: 10072
  • 55 Li Q, Bi Q.-Y, Zhou B, Wang X.-L. Appl. Surf. Sci. 2012; 258: 4707
  • 56 Zhao W, Ye Q, Hu H, Wang X, Zhou F. J. Mater. Chem. B 2014; 2: 5352
  • 57 Zhang J, Yuan J, Yuan Y, Zang X, Shen J, Lin S. Biomaterials 2003; 24: 4223
  • 58 Kratzer D, Barner L, Friedmann C, Bräse S, Lahann J. Eur. J. Org. Chem. 2014; 2014: 8064
  • 59 Liu Q, Chiu A, Wang L, An D, Li W, Chen EY, Zhang Y, Pardo Y, McDonough SP, Liu L, Liu WF, Chen J, Ma M. Biomaterials 2020; 230: 119640
  • 60 Yuan J, Lin S, Shen J. Colloids Surf., B 2008; 66: 90
  • 61 Koc J, Schönemann E, Amuthalingam A, Clarke J, Finlay JA, Clare AS, Laschewsky A, Rosenhahn A. Langmuir 2019; 35: 1552
  • 62 Schönemann E, Koc J, Aldred N, Clare AS, Laschewsky A, Rosenhahn A, Wischerhoff E. Macromol. Rapid Commun. 2020; 41: 1900447
  • 63 Hildebrand V, Laschewsky A, Päch M, Müller-Buschbaum P, Papadakis CM. Polym. Chem. 2017; 8: 310
  • 64 Laschewsky A, Rosenhahn A. Langmuir 2019; 35: 1056
  • 65 Mo F, Ren H, Chen S, Ge Z. Mater. Lett. 2015; 145: 174
  • 66 Graiver D, Baer E, Litt M, Baney RH. J. Polym. Sci., Part A: Polym. Chem. 1979; 17: 3559
  • 67 Zhu Y, Noy J.-M, Lowe AB, Roth PJ. Polym. Chem. 2015; 6: 5705
  • 68 Fischer RF. Ind. Eng. Chem. 1964; 56: 41
  • 69 Yuan J, Zhang J, Zhu J, Shen J, Lin SC, Zhu W, Fang JL. J. Biomater. Appl. 2003; 18: 123
  • 70 Yuan J, Zhu J, Zhu CH, Shen J, Lin SC. Polym. Int. 2004; 53: 1722
  • 71 Jiang Y, Qingfeng H, Baolei L, Jian S, Sicong L. Colloids Surf., B 2004; 36: 19
  • 72 Lowe AB, Billingham NC, Armes SP. Chem. Commun. 1996; 13: 1555
  • 73 Abu-Thabit NY, Hamdy AS. Surf. Coat. Technol. 2016; 303: 406
  • 74 Roy SG, Banerjee S, De P. Cationic Polymerization of Nonpolar Vinyl Monomers for Producing High Performance Polymers. In: Reference Module in Materials Science and Materials Engineering. Elsevier; Philadelphia: 2016
  • 75 Minko S. Grafting on Solid Surfaces: “Grafting To” and “grafting From” Methods. In: Polymer surfaces and interfaces. Stamm M. Springer; Berlin: 2008: 215-234
  • 76 Li G, Xue H, Cheng G, Chen S, Zhang F, Jiang S. J. Phys. Chem. B 2008; 112: 15269
  • 77 Matyjaszewski K, Xia J. Chem. Rev. 2001; 101: 2921
  • 78 Chang Y, Chang Y, Higuchi A, Shih Y.-J, Li P.-T, Chen W.-Y, Tsai E.-M, Hsiue G.-H. Langmuir 2012; 28: 4309
  • 79 Yu B.-Y, Zheng J, Chang Y, Sin M.-C, Chang C.-H, Higuchi A, Sun Y.-M. Langmuir 2014; 30: 7502
  • 80 Ippel BD, Komil MI, Bartels PA. A, Söntjens SH. M, Boonen RJ. E. A, Smulders MM. J, Dankers PY. W. Macromolecules 2020; 53: 4454
  • 81 Yuan YL, Ai F, Zhang J, Zang XB, Shen J, Lin SC. J. Biomater. Sci., Polym. Ed. 2002; 13: 1081
  • 82 Shan B, Yan H, Shen J, Lin S. J. Appl. Polym. Sci. 2006; 101: 3697
  • 83 Chiang Y.-C, Chang Y, Higuchi A, Chen W.-Y, Ruaan R.-C. J. Membr. Sci. 2009; 339: 151
  • 84 Jun Z, Youling Y, Kehua W, Jian S, Sicong L. Colloids Surf., B 2003; 28: 1
  • 85 Yuan Y, Ai F, Zang X, Zhuang W, Shen J, Lin S. Colloids Surf., B 2004; 35: 1
  • 86 Jiang Y, Rongbing B, Ling T, Jian S, Sicong L. Colloids Surf., B 2004; 36: 27
  • 87 Yuan J, Chen L, Jiang X, Shen J, Lin S. Colloids Surf., B 2004; 39: 87
  • 88 Wikberg E, Verhage JJ, Viklund C, Irgum K. J. Sep. Sci. 2009; 32: 2008
  • 89 Du Y, Gao J, Chen T, Zhang C, Ji J, Xu Z.-K. Langmuir 2017; 33: 7298
  • 90 Hanton LR, Lee K. J. Chem. Soc., Dalton Trans. 2000; 1161
  • 91 Cho WK, Kong B, Choi IS. Langmuir 2007; 23: 5678
  • 92 Fan M, Ma Y, Mao J, Zhang Z, Tan H. Acta Biomater. 2015; 20: 60
  • 93 Chou Y.-N, Wen T.-C, Chang Y. Acta Biomater. 2016; 40: 78
  • 94 Kwon HJ, Lee Y, Phuong LT, Seon GM, Kim E, Park JC, Yoon H, Park KD. Acta Biomater. 2017; 61: 169
  • 95 Chien H.-W, Tsai C.-C, Tsai W.-B, Wang M.-J, Kuo W.-H, Wei T.-C, Huang S.-T. Colloids Surf., B 2013; 107: 152
  • 96 Lee H, Dellatore SM, Miller WM, Messersmith PB. Science 2007; 318: 426
  • 97 Dreyer DR, Miller DJ, Freeman BD, Paul DR, Bielawski CW. Langmuir 2012; 28: 6428
  • 98 Yesilyurt V, Veiseh O, Doloff JC, Li J, Bose S, Xie X, Bader AR, Chen M, Webber MJ, Vegas AJ, Langer R, Anderson DG. Adv. Healthcare Mater. 2017; 6: 1601091
  • 99 Dizon GV, Chou Y.-N, Yeh L.-C, Venault A, Huang J, Chang Y. J. Colloid Interface Sci. 2018; 529: 77
  • 100 Li G, Cheng G, Xue H, Chen S, Zhang F, Jiang S. Biomaterials 2008; 29: 4592
  • 101 Huang J, Xu W. J. Appl. Polym. Sci. 2011; 122: 1251
  • 102 Chien H.-W, Keng M.-C, Chen H.-Y, Huang S.-T, Tsai W.-B. Biomater. Biomech. Bioeng. 2016; 3: 59
  • 103 Estephan ZG, Jaber JA, Schlenoff JB. Langmuir 2010; 26: 16884
  • 104 Knowles BR, Wagner P, Maclaughlin S, Higgins MJ, Molino PJ. ACS Appl. Mater. Interfaces 2017; 9: 18584
  • 105 Hammond PT. Mater. Today 2012; 15: 196
  • 106 Kuo W.-H, Wang M.-J, Chien H.-W, Wei T.-C, Lee C, Tsai W.-B. Biomacromolecules 2011; 12: 4348
  • 107 O'Brien P. Chemical Vapor Deposition. In: Encyclopedia of Materials: Science and Technology. Buschow KH. J, Cahn RW, Flemings MC, Ilschner B, Kramer EJ, Mahajan S, Veyssière P. Elsevier; Oxford: 2001: 1173-1176
  • 108 Brown RH, Hunley MT, Allen MH, Long TE. Polymer (Guildf.) 2009; 50: 4781
  • 109 Yang W, Sundaram HS, Ella J.-R, He N, Jiang S. Acta Biomater. 2016; 40: 92
  • 110 Venault A, Chang Y, Yang H.-S, Lin P.-Y, Shih Y.-J, Higuchi A. J. Membr. Sci. 2014; 454: 253
  • 111 Chang Y, Chen S, Zhang Z, Jiang S. Langmuir 2006; 22: 2222
  • 112 Zhou Q, Lei X.-P, Li J.-H, Yan B.-F, Zhang Q.-Q. Desalination 2014; 337: 6
  • 113 Chen S.-H, Chang Y, Lee K.-R, Wei T.-C, Higuchi A, Ho F.-M, Tsou C.-C, Ho H.-T, Lai J.-Y. Langmuir 2012; 28: 17733
  • 114 Zhao J, Shi Q, Luan S, Song L, Yang H, Shi H, Jin J, Li X, Yin J, Stagnaro P. J. Membr. Sci. 2011; 369: 5
  • 115 An Y, Wang Z, Wu Z, Yang D, Zhou Q. Chem. Eng. J. 2009; 155: 709
  • 116 Jhaveri JH, Murthy ZV. P. Desalination 2016; 379: 137
  • 117 Ayyavoo J, Nguyen TP. N, Jun B.-M, Kim I.-C, Kwon Y.-N. Colloids Surf., A 2016; 506: 190
  • 118 Dizon GV, Venault A. J. Membr. Sci. 2018; 550: 45
  • 119 Zhang Y, Wang Z, Lin W, Sun H, Wu L, Chen S. J. Membr. Sci. 2013; 446: 164
  • 120 Zhou M, Liu H, Kilduff JE, Langer R, Anderson DG, Belfort G. Environ. Sci. Technol. 2009; 43: 3865
  • 121 Zhao Y.-H, Wee K.-H, Bai R. J. Membr. Sci. 2010; 362: 326
  • 122 Zhao Y.-H, Wee K.-H, Bai R. ACS Appl. Mater. Interfaces 2010; 2: 203
  • 123 Li M.-Z, Li J.-H, Shao X.-S, Miao J, Wang J.-B, Zhang Q.-Q, Xu X.-P. J. Membr. Sci. 2012; 405: 141
  • 124 Thankappan H, Bousquet G, Semsarilar M, Venault A, Chang Y, Bouyer D, Quemener D. Membranes 2019; 9: 93
  • 125 Li J.-H, Li M.-Z, Miao J, Wang J.-B, Shao X.-S, Zhang Q.-Q. Appl. Surf. Sci. 2012; 258: 6398
  • 126 Ang WS, Elimelech M. J. Membr. Sci. 2007; 296: 83
  • 127 Jarusutthirak C, Amy G, Croué J.-P. Desalination 2002; 145: 247
  • 128 Hothi DK, Geary DF. Pediatric Hemodialysis Prescription, Efficacy, and Outcome. In: Comprehensive Pediatric Nephrology. Geary DF, Schaefer F. Mosby; Philadelphia: 2008: 867-893
  • 129 Yuan J, Zhang J, Zang X, Shen J, Lin S. Colloids Surf., B 2003; 30: 147
  • 130 Liu P.-S, Chen Q, Liu X, Yuan B, Wu S.-S, Shen J, Lin S.-C. Biomacromolecules 2009; 10: 2809
  • 131 Tolwani AJ, Connor MJ, Palevsky PM. Renal Replacement Therapy for Acute Kidney Injury. In: Chronic Kidney Disease, Dialysis, and Transplantation (Fourth Edition). Himmelfarb J, Ikizler TA. Elsevier; Philadelphia: 2019: 739-753.e8
  • 132 Carpenter AW, de Lannoy C.-F, Wiesner MR. Environ. Sci. Technol. 2015; 49: 5277
  • 133 Jhong J.-F, Venault A, Hou C.-C, Chen S.-H, Wei T.-C, Zheng J, Huang J, Chang Y. ACS Appl. Mater. Interfaces 2013; 5: 6732
  • 134 Lin H.-T, Venault A, Chang Y. J. Membr. Sci. 2019; 591: 117319
  • 135 Wu J, Xiao Z, Chen A, He H, He C, Shuai X, Li X, Chen S, Zhang Y, Ren B, Zheng J, Xiao J. Acta Biomater. 2018; 71: 293
  • 136 He H, Xiao Z, Zhou Y, Chen A, Xuan X, Li Y, Guo X, Zheng J, Xiao J, Wu J. J. Mater. Chem. B 2019; 7: 1697
  • 137 Ruseva K, Ivanova K, Todorova K, Gabrashanska M, Hinojosa-Caballero D, Tzanov T, Vassileva E. Eur. Polym. J. 2019; 117: 391
  • 138 Xie J, Xu C, Kohler N, Hou Y, Sun S. Adv. Mater. 2007; 19: 3163
  • 139 Elsabahy M, Wooley KL. Chem. Soc. Rev. 2012; 41: 2545
  • 140 Wilhelm S, Tavares AJ, Dai Q, Ohta S, Audet J, Dvorak HF, Chan WC. W. Nat. Rev. Mater. 2016; 1: 1
  • 141 García KP, Zarschler K, Barbaro L, Barreto JA, O'Malley W, Spiccia L, Stephan H, Graham B. Small 2014; 10: 2516
  • 142 Jin Q, Chen Y, Wang Y, Ji J. Colloids Surf., B 2014; 124: 80
  • 143 Fam SY, Chee CF, Yong CY, Ho KL, Mariatulqabtiah AR, Tan WS. Nanomaterials 2020; 10: E787
  • 144 Rouhana LL, Jaber JA, Schlenoff JB. Langmuir 2007; 23: 12799
  • 145 Li H, Han J, Liang G. ACS Applied Nano Mater. 2020; 3: 1489
  • 146 van Andel E, de Bus I, Tijhaar EJ, Smulders MM. J, Savelkoul HF. J, Zuilhof H. ACS Appl. Mater. Interfaces 2017; 9: 38211
  • 147 Xiao Y, Du J. J. Mater. Chem. B 2020; 8: 354
  • 148 Chouly C, Pouliquen D, Lucet I, Jeune JJ, Jallet P. J. Microencapsulation 1996; 13: 245
  • 149 Meng J, Xiao B, Zhang Y, Liu J, Xue H, Lei J, Kong H, Huang Y, Jin Z, Gu N, Xu H. Sci. Rep. 2013; 3: 2655
  • 150 Estephan ZG, Hariri HH, Schlenoff JB. Langmuir 2013; 29: 2572
  • 151 Wei H, Insin N, Lee J, Han H.-S, Cordero JM, Liu W, Bawendi MG. Nano Lett. 2012; 12: 22
  • 152 Zhou Z, Wang L, Chi X, Bao J, Yang L, Zhao W, Chen Z, Wang X, Chen X, Gao J. ACS Nano 2013; 7: 3287
  • 153 Peng S, Ouyang B, Men Y, Du Y, Cao Y, Xie R, Pang Z, Shen S, Yang W. Biomaterials 2020; 231: 119680
  • 154 Schlorf T, Meincke M, Kossel E, Glüer C.-C, Jansen O, Mentlein R. Int. J. Mol. Sci. 2010; 12: 12
  • 155 Knowles BR, Yang D, Wagner P, Maclaughlin S, Higgins MJ, Molino PJ. Langmuir 2019; 35: 1335
  • 156 Knowles BR, Wagner P, Maclaughlin S, Higgins MJ, Molino PJ. Biointerphases 2020; 15: 021009
  • 157 Kairdolf BA, Smith AM, Stokes TH, Wang MD, Young AN, Nie S. Annu. Rev. Anal. Chem. 2013; 6: 143
  • 158 Sun M, Hoffman D, Sundaresan G, Yang L, Lamichhane N, Zweit J. Am. J. Nucl. Med. Mol. Imaging 2012; 2: 122
  • 159 Muro E, Fragola A, Pons T, Lequeux N, Ioannou A, Skourides P, Dubertret B. Small 2012; 8: 1029
  • 160 Muro E, Pons T, Lequeux N, Fragola A, Sanson N, Lenkei Z, Dubertret B. J. Am. Chem. Soc. 2010; 132: 4556
  • 161 Deng T, Peng Y, Zhang R, Wang J, Zhang J, Gu Y, Huang D, Deng D. ACS Appl. Mater. Interfaces 2017; 9: 11405
  • 162 Giovanelli E, Muro E, Sitbon G, Hanafi M, Pons T, Dubertret B, Lequeux N. Langmuir 2012; 28: 15177
  • 163 Zhan N, Palui G, Safi M, Ji X, Mattoussi H. J. Am. Chem. Soc. 2013; 135: 13786
  • 164 Susumu K, Oh E, Delehanty JB, Blanco-Canosa JB, Johnson BJ, Jain V, Hervey IV WJ, Algar WR, Boeneman K, Dawson PE, Medintz IL. J. Am. Chem. Soc. 2011; 133: 9480
  • 165 Park J, Nam J, Won N, Jin H, Jung S, Jung S, Cho S, Kim S. Adv. Funct. Mater. 2011; 21: 1558
  • 166 Tasso M, Giovanelli E, Zala D, Bouccara S, Fragola A, Hanafi M, Lenkei Z, Pons T, Lequeux N. ACS Nano 2015; 9: 11479
  • 167 Debayle M, Marchandier T, Xu X, Lequeux N, Pons T. ACS Appl. Mater. Interfaces 2019; 11: 25008
  • 168 Trapiella-Alfonso L, Pons T, Lequeux N, Leleu L, Grimaldi J, Tasso M, Oujagir E, Seguin J, d'Orlyé F, Girard C, Doan B.-T, Varenne A. ACS Appl. Mater. Interfaces 2018; 10: 17107
  • 169 Mangeolle T, Yakavets I, Lequeux N, Pons T, Bezdetnaya L, Marchal F. Photodiagn. Photodyn. Ther. 2019; 26: 150
  • 170 Baggerman J, Smulders MM. J, Zuilhof H. Langmuir 2019; 35: 1072
  • 171 Kitano H, Suzuki H, Matsuura K, Ohno K. Langmuir 2010; 26: 6767
  • 172 Li Y, Giesbers M, Gerth M, Zuilhof H. Langmuir 2012; 28: 12509
  • 173 Robinson KJ, Coffey JW, Muller DA, Young PR, Kendall MA. F, Thurecht KJ, Grøndahl L, Corrie SR. Biointerphases 2015; 10: 04A305
  • 174 Kim G, Yong Y, Kang HJ, Park K, Kim SI, Lee M, Huh N. Biomaterials 2014; 35: 294
  • 175 Cao J, Xiu K.-M, Zhu K, Chen Y.-W, Luo X.-L. J. Biomed. Mater. Res. Part A 2012; 100: 2079
  • 176 Cao J, Lu A, Li C, Cai M, Chen Y, Li S, Luo X. Colloids Surf., B 2013; 112: 35
  • 177 Cao J, Xie X, Lu A, He B, Chen Y, Gu Z, Luo X. Biomaterials 2014; 35: 4517
  • 178 Wu Z, Cai M, Xie X, He L, Huang L, Chen Y, Luo X. RSC Adv. 2015; 5: 106989
  • 179 Xie X, Ma Y, Huang L, Cai M, Chen Y, Luo X. Colloids Surf., A 2015; 468: 31
  • 180 Zhai S, Ma Y, Chen Y, Li D, Cao J, Liu Y, Cai M, Xie X, Chen Y, Luo X. Polym. Chem. 2014; 5: 1285
  • 181 Cai M, Leng M, Lu A, He L, Xie X, Huang L, Ma Y, Cao J, Chen Y, Luo X. Colloids Surf., B 2015; 126: 1
  • 182 Dai F, Wang P, Wang Y, Tang L, Yang J, Liu W, Li H, Wang G. Polymer (Guildf.. 2008; 49: 5322
  • 183 Shih Y, Venault A, Tayo LL, Chen S.-H, Higuchi A, Deratani A, Chinnathambi A, Alharbi SA, Quemener D, Chang Y. Langmuir 2017; 33: 1914
  • 184 Wang W, Nan W, Sun L, Liu W. React. Funct. Polym. 2013; 73: 993
  • 185 Dai F, Liu Y, Wang W, Liu W. J. Biomater. Sci., Polym. Ed. 2013; 24: 330
  • 186 Zhai X, Wang W, Wang C, Wang Q, Liu W. J. Mater. Chem. 2012; 22: 23576
  • 187 Hoffman AS. Adv. Drug Delivery Rev. 2012; 64: 18
  • 188 Mantooth SM, Munoz-Robles BG, Webber MJ. Macromol. Biosci. 2019; 19: e1800281
  • 189 Carr L, Cheng G, Xue H, Jiang S. Langmuir 2010; 26: 14793
  • 190 Zhang Z, Chao T, Jiang S. J. Phys. Chem. B 2008; 112: 5327
  • 191 Kasák P, Kroneková Z, Krupa I, Lacík I. Polymer (Guildf.. 2011; 52: 3011
  • 192 Ning J, Kubota K, Li G, Haraguchi K. React. Funct. Polym. 2013; 73: 969
  • 193 Zhang Z, Chao T, Liu L, Cheng G, Ratner BD, Jiang S. J. Biomater. Sci., Polym. Ed. 2009; 20: 1845
  • 194 Venault A, Huang C.-W, Zheng J, Chinnathambi A, Alharbi SA, Chang Y, Chang Y. Int. J. Polym. Mater. Polym. Biomater. 2016; 65: 65
  • 195 Chang Y, Yandi W, Chen W.-Y, Shih Y.-J, Yang C.-C, Chang Y, Ling Q.-D, Higuchi A. Biomacromolecules 2010; 11: 1101
  • 196 Susanto H, Ulbricht M. Langmuir 2007; 23: 7818
  • 197 Kasák P, Mosnáček J, Danko M, Krupa I, Hloušková G, Chorvát D, Koukaki M, Karamanou S, Economou A, Lacík I. RSC Adv. 2016; 6: 83890
  • 198 Ning J, Li G, Haraguchi K. Macromolecules 2013; 46: 5317
  • 199 Ning J, Li G, Haraguchi K. Macromol. Chem. Phys. 2014; 215: 235
  • 200 Haraguchi K, Ning J, Li G. Eur. Polym. J. 2015; 68: 630
  • 201 Liu Q, Chiu A, Wang L.-H, An D, Zhong M, Smink AM, de Haan BJ, de Vos P, Keane K, Vegge A, Chen EY, Song W, Liu WF, Flanders J, Rescan C, Grunnet LG, Wang X, Ma M. Nat. Commun. 2019; 10: 5262
  • 202 Yong Y, Qiao M, Chiu A, Fuchs S, Liu Q, Pardo Y, Worobo R, Liu Z, Ma M. Langmuir 2019; 35: 1927
  • 203 Ladd J, Zhang Z, Chen S, Hower JC, Jiang S. Biomacromolecules 2008; 9: 1357
  • 204 Emmenegger CR, Rodriguez Emmenegger C, Brynda E, Riedel T, Sedlakova Z, Houska M, Bologna Alles A. Langmuir 2009; 25: 6328
  • 205 Danko M, Kroneková Z, Mrlik M, Osicka J, Bin Yousaf A, Mihálová A, Tkac J, Kasak P. Langmuir 2019; 35: 1391
  • 206 Zhang Z, Chen S, Jiang S. Biomacromolecules 2006; 7: 3311
  • 207 Izumrudov VA, Zelikin AN, Zhiryakova MV, Jaeger W, Bohrisch J. J. Phys. Chem. B 2003; 107: 7982
  • 208 Wu L, Jasinski J, Krishnan S. J. Appl. Polym. Sci. 2012; 124: 2154
  • 209 Lim J, Matsuoka H, Saruwatari Y. Langmuir 2020; 36: 1727
  • 210 McPherson T, Kidane A, Szleifer I, Park K. Langmuir 1998; 14: 176
  • 211 van Andel E, Lange SC, Pujari SP, Tijhaar EJ, Smulders MM. J, Savelkoul HF. J, Zuilhof H. Langmuir 2019; 35: 1181
  • 212 Kisley L, Miller KA, Davis CM, Guin D, Murphy EA, Gruebele M, Leckband DE. Biomacromolecules 2018; 19: 3894
  • 213 Iqbal Z, Moses W, Kim S, Kim EJ, Fissell WH, Roy S. J. Biomed. Mater. Res. Part B 2018; 106: 2327
  • 214 Iqbal Z, Kim S, Moyer J, Moses W, Abada E, Wright N, Kim EJ, Park J, Fissell WH, Vartanian S, Roy S. J. Biomater. Appl. 2019; 34: 297
  • 215 Chen X, Yang D. Biomater. Sci. 2020; 8: 4906
  • 216 Lichtenberg JY, Ling Y, Kim S. Sensors 2019; 19: E2488
  • 217 Feiner R, Dvir T. Nat. Rev. Mater. 2018; 3: 17076