Progress in Hydrogels Based on Regenerated Silk Fibroin†

doi:10.7503/cjcu20170635

Abstract

Abstract:

Regenerated silk fibroin(RSF) is a fibrillar protein obtained from Bombyx mori silkworm silk. Recently, RSF-based hydrogels have attracted extensive research interest, which has yielded an improved understanding in the gelling mechanisms, physical and mechanical properties as well as the applications in regenerative medicine and tissue engineering. Mechanistically, RSF hydrogel networks can be formed via two pathways, chemical cross-linking including enzymatic cross-linking, and physical cross-linking through conformational transition, during which thermodynamically more stable β-sheet structures are induced. An advantage of RSF hydrogels is that the physical and mechanical properties of hydrogels can be further controlled by the β-sheet content in the conformation on top of concentration and cross-linking density. RSF can be mixed with other polymers and/or inorganic components to prepare composite hydrogels for a wider spectrum of mechanical properties. Furthermore, we summarize most recent applications of RSF hydrogels in biomaterials, including controlled drug release, muscle, tendon and bone tissue engineering.

Key words: Biopolymer, Protein, Scaffold, Conformation, Regenerative medicine, Tissue engineering, Regenerated silk fibroin hydrogel

CLC Number:

O631

TrendMD:

LONG Xingtong, GUAN Juan, CHEN Xin, SHAO Zhengzhong. Progress in Hydrogels Based on Regenerated Silk Fibroin^†[J]. Chem. J. Chinese Universities, 2018, 39(1): 1.

Figures/Tables 4

Fig.1 Morphology and network structure of silk-based hydrogels

Fig.2 Ethanol induced RSF hydrogel fibrillar network formation process showing by TEM images at 1 min(A), 10 min(B), 23 min(C) and AFM height images at 10 min(D), 15 min(E) and 23 min(F)Reprinted with permission from Ref.[36], copyright 2010 Royal Society of Chemistry.

Table 1 Mechanical properties of silk hydrogels and silk-based composite hydrogels

Solid content of RSF(%)	Component polymer	Gelation condition	Storage modulus,G'/kPa	Ref.
0.8		pH=2, 50 ℃	3	[28]
3		Sonication	0.01	[45]
4—5		0.5% Ethanol	0.1	[36]
		1% Ethanol	1	[36]
5.4		12% Genipin	46.1	[48]
	80%Gelatin	12% Genipin	1.1	[48]
3	30%PAM	37 ℃	20	[30]
3—4	Collagen	0.05%EDC	3	[49]
	Collagen	0.15%EDC	10	[49]
10	30%HPC	37 ℃	1	[50]
2.4	~40%PEG300	PEG	20	[51]
4.8	~40%PEG300	PEG	54	[51]
5.5	~40%PEG300	PEG	70	[51]
15	~45%PEG300	PEG	70	[51]
15	~42.5%PEG400	PEG	200	[51]

Fig.3 Silk-based hydrogels and their potential applications in tissue engineering

References 92

[1]	Omenetto F. G., Kaplan D. L., Science, 2010, 329(5991), 528—531
[2]	Vollrath F., Porter D., Holland C., MRS Bulletin, 2013, 38(1), 73—80
[3]	Wray L. S., Hu X., Gallego J., Georgakoudi I., Omenetto F. G., Schmidt D., Kaplan D. L., Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2011, 99(1), 89—101
[4]	Mo C., Holland C., Porter D., Shao Z. Z., Vollrath F., Biomacromolecules, 2009, 10(10), 2724—2728
[5]	Wang Q., Chen Q., Yang Y. H., Shao Z. Z., Biomacromolecules, 2013, 14(1), 285—289
[6]	Phillips D. M., Drummy L. F., Conrady D. G., Fox D. M., Naik R. R., Stone M. O., Trulove P. C., Long H. C. D., Mantz R. A., Journal of the American Chemical Society, 2004, 126(44), 14350—14351
[7]	Zhang C., Chen X., Shao Z. Z., ACS Biomaterials Science & Engineering, 2016, 2(1), 12—18
[8]	Silva S. S., Santos T. C., Cerqueira M. T., Marques A. P., Reys L. L., Silva T. H., Caridade S. G., Mano J. F., Rui L. R., Green Chemistry, 2012, 14(5), 1463—1470
[9]	Schroeder W. A., Kay L. M., Lewis B., Munger N., Journal of the American Chemical Society, 1955, 77(14), 3908—3913
[10]	Elliott W. H., Bonani W., Maniglio D., Motta A., Tan W., Migliaresi C., ACS Applied Materials & Interfaces, 2015, 7(22), 12099—12108
[11]	Taddei P., Chiono V., Anghileri A., Vozzi G., Freddi G., Ciardelli G., Macromol. Biosci., 2013, 13(11), 1492—1510
[12]	Partlow B. P., Applegate M. B., Omenetto F. G., Kaplan D. L., ACS Biomaterials Science & Engineering, 2016, 2(12), 2108—2121
[13]	Hiromu S., Mamoru T., Takashi I., Journal of Polymer Science Part B: Polymer Physics, 1988, 26(8), 1761—1768
[14]	Ayub Z. H., Arai M., Hirabayashi K., Bioscience Biotechnology & Biochemistry, 2014, 57(11), 1910—1912
[15]	Matsumoto A., Chen J., Collette A. L., Kim U. J., Altman G. H., Cebe P., Kaplan D. L., Journal of Physical Chemistry B, 2006, 110(43), 21630—21638
[16]	Nagarkar S., Patil A., Lele A., Bhat S., Bellare J., Mashelkar R. A., Industrial & Engineering Chemistry Research, 2009, 48(17), 8014—8023
[17]	Kapoor S., Kundu S. C., Acta Biomaterialia, 2016, 31, 17—32
[18]	Bai S., Zhang X., Lu Q., Sheng W., Liu L., Dong B., Kaplan D. L., Zhu H., Biomacromolecules, 2014, 15(8), 3044—3051
[19]	Mallepally R. R., Marin M. A., Mchugh M. A., Acta Biomater., 2014, 10(10), 4419—4424
[20]	Kundu J., Poole-Warren L. A., Martens P., Kundu S. C., Acta Biomater., 2012, 8(5), 1720—1729
[21]	Wang X., Kluge J. A., Leisk G. G., Kaplan D. L., Biomaterials, 2008, 29(8), 1054—1064
[22]	Kim U. J., Park J. Y., Li C. M., Jin H. J., Valluzzi R., Kaplan D. L., Biomacromolecules, 2004, 5(3), 786—792
[23]	Chen D. Q., Yin Z. P., Wu F., Fu H., Kundu S. C., Lu S. Z., Journal of Applied Polymer Science, 2017, 134(32), 45050
[24]	Numata K., Ifuku N., Masunaga H., Hikima T., Sakai T., Biomacromolecules, 2017, 18(6), 1937—1946
[25]	Dickerson M. B., Dennis P. B., Tondiglia V. P., Nadeau L. J., Singh K. M., Drummy L. F., Partlow B. P., Brown D. P., Omenetto F. G., Kaplan D. L., Naik R. R., ACS Biomaterials Science & Engineering, 2017, 3(9), 2064—2075
[26]	Inoue S., Tanaka K., Arisaka F., Kimura S., Ohtomo K., Mizuno S., Journal of Biological Chemistry, 2000, 275(51), 40517—40528
[27]	Yin Z. P., Wu F., Zheng Z. Z., Kaplan D. L., Kundu S. C., Lu S. Z., ACS Biomaterials Science & Engineering, 2017, 3(10), 2617—2627
[28]	Nagarkar S., Nicolai T., Chassenieux C., Lele A., Phys. Chem. Chem. Phys., 2010, 12(15), 3834—3844
[29]	Lu Q., Bai S. M., Ding Z. Z., Guo H., Shao Z. Z., Zhu H. S., Kaplan D. L., Advanced Materials Interfaces, 2016, 3(8), 1500687
[30]	Mandal B. B., Kapoor S., Kundu S. C., Biomaterials, 2009, 30(14), 2826—2836
[31]	Gil E. S., Hudson S. M., Biomacromolecules, 2007, 8(1), 258—264
[32]	Numata K., Yamazaki S., Katashima T., Chuah J. A., Naga N., Sakai T., Macromol. Biosci., 2014, 14(6), 799—806
[33]	Foo C. W. P., Bini E., Hensman J., Knight D. P., Lewis R. V., Kaplan D. L., Applied Physics A, 2006, 82(2), 223—233
[34]	Matsumoto A., Chen J. S., Collette A. L., Kim U. J., Altman G. H., Cebe P., Kaplan D. L., Journal of Physical Chemistry B, 2006, 110(43), 21630—21638
[35]	Floren M. L., Spilimbergo S., Motta A., Migliaresi C., Biomacromolecules, 2012, 13(7), 2060—2072
[36]	Gong Z. G., Yang Y. H., Ren Q. G., Chen X., Shao Z. Z., Soft Matter, 2010, 6(6), 1217—1223
[37]	Altman G. H., Diaz F., Jakuba C., Calabro T., Horan R. L., Chen J., Lu H., Richmond J., Kaplan D. L., Biomaterials, 2003, 24(3), 401—416
[38]	Yang Y., Chen X., Ding F., Zhang P., Liu J., Gu X., Biomaterials, 2007, 28(9), 1643—1652
[39]	Luo K. Y., Yang Y. H., Shao Z. Z., Advanced Functional Materials, 2016, 26(6), 872—880
[40]	Numata K., Katashima T., Sakai T., Biomacromolecules, 2011, 12(6), 2137—2144
[41]	Numata K., Cebe P., Kaplan D. L., Biomaterials, 2010, 31(10), 2926—2933
[42]	Horan R. L., Antle K., Collette A. L., Wang Y., Huang J., Moreau J. E., Volloch V., Kaplan D. L., Altman G. H., Biomaterials, 2005, 26(17), 3385—3393
[43]	Kim M. H., Park W. H., International Journal of Nanomedicine, 2016, 11, 2967—2978
[44]	Qian J. F., Cai L. H., Qi W. D., Zhao X., Chen X., Chinese Journal of Biomedical Engineering, 2016, 35(4), 507—511
	(千建峰, 蔡丽慧, 亓卫东, 赵霞, 陈新.中国生物医学工程学报, 2016, 35(4), 507—511)
[45]	Kim H. H., Song D. W., Kim M. J., Ryu S. J., Um I. C., Ki C. S., Park Y. H., Polymer, 2016, 90, 26—33
[46]	Luo K. Y., Yang Y. H., Shao Z. Z., Advanced Functional Materials, 2016, 26(6), 872—880
[47]	Li Z., Zheng Z. K., Yang Y. H., Fang G. Q., Yao J. R., Shao Z. Z., Chen X., ACS Sustainable Chemistry & Engineering, 2016, 4(3), 1500—1506
[48]	Sun W., Incitti T., Migliaresi C., Quattrone A., Casarosa S., Motta A., J. Tissue Eng. Regen. Med., 2014, 10, 876—887
[49]	Lv Q., Hu K., Feng Q., Cui F., J. Biomed. Mater. Res. A, 2008, 84(1), 198—207
[50]	Gong Z. G., Yang Y. H., Ren Q. G., Chen X., Shao Z. Z., Soft Matter, 2012, 8(10), 2875—2883
[51]	Wang X., Partlow B., Liu J., Zheng Z., Su B., Wang Y., Kaplan D. L., Acta Biomater., 2015, 12, 51—61
[52]	Numata K., Yamazaki S., Naga N., Biomacromolecules, 2012, 13(5), 1383—1389
[53]	Singh S. K., Bhunia B. K., Bhardwaj N., Gilotra S., Mandal B. B., Mol. Pharm., 2016, 13(12), 4066—4081
[54]	Pritchard E. M., Kaplan D. L., Expert. Opin. Drug Deliv., 2011, 8(6), 797—811
[55]	Fang J. Y., Chen J. P., Leu Y. L., Wang H. Y., Chemical & Pharmaceutical Bulletin, 2006, 54(2), 156—162
[56]	Amsden B., Macromolecules, 1998, 31(23), 8382—8395
[57]	Canal T., Peppas N. A., Journal of Biomedical Materials Research Part A, 1989, 23(10), 1183—1193
[58]	Mason M. N., Metters A. T., Bowman C. N., Anseth K. S., Macromolecules, 2001, 34(13), 4630—4635
[59]	Hamidi M., Azadi A., Rafiei P., Advanced Drug Delivery Reviews, 2008, 60(15), 1638—1649
[60]	Marin M. A., Mallepally R. R., Mchugh M. A., Journal of Supercritical Fluids, 2014, 91(7), 84—89
[61]	Cao H., Yang Y. H., Shao Z. Z., Journal of Controlled Release, 2015, 213, e39
[62]	Zhong T. Y., Jiang Z. J., Wang P., Bie S. Y., Zhang F., Zuo B. Q., International Journal of Pharmaceutics, 2015, 494(1), 264—270
[63]	Floren M., Bonani W., Dharmarajan A., Motta A., Migliaresi C., Tan W., Acta Biomater., 2016, 31, 156—166
[64]	Das S., Pati F., Choi Y. J., Rijal G., Shim J. H., Kim S. W., Ray A. R., Cho D. W., Ghosh S., Acta Biomaterialia, 2015, 11(1), 233
[65]	Ziv K., Nuhn H., Ben-Haim Y., Sasportas L. S., Kempen P. J., Niedringhaus T. P., Hrynyk M., Sinclair R., Barron A. E., Gambhir S. S., Biomaterials, 2014, 35(12), 3736—3743
[66]	Chen X., Li W. J., Zhong W., Lu Y. H., Yu T. Y., Journal of Applied Polymer Science, 1997, 65(11), 2257—2262
[67]	Chen G. Q., Acta Polymerica Sinica, 2002, 18(3), 379—384
[68]	Chao P. H. G., Yodmuang S., Wang X., Sun L., Kaplan D. L., Vunjak-Novakovic G., Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2010, 95(1), 84—90
[69]	Singh Y. P., Bhardwaj N., Mandal B. B., ACS Applied Materials & Interfaces, 2016, 8(33), 21236—21249
[70]	Mirahmadi F., Tafazzoli-Shadpour M., Shokrgozar M. A., Bonakdar S., Mater. Sci. Eng. C: Mater. Biol. Appl., 2013, 33(8), 4786—4794
[71]	Yodmuang S., Mcnamara S. L., Nover A. B., Mandal B. B., Agarwal M., Kelly T. A., Chao P. H., Hung C., Kaplan D. L., Vunjak-Novakovic G., Acta Biomaterialia, 2015, 11(1), 27—36
[72]	Singh Y. P., Adhikary M., Bhardwaj N., Bhunia B. K., Mandal B. B., Biomed. Mater., 2017, 12(4), 045012
[73]	Jin Y. S., Kundu B., Cai Y. R., Kundu S. C., Yao J. M., Colloids and Surfaces B-Biointerfaces, 2015, 134, 339—345
[74]	Ming J. F., Bie S. Y., Jiang Z. J., Wang P., Zuo B. Q., Materials Letters, 2014, 126, 169—173
[75]	Ming J. F., Jiang Z. J., Wang P., Bie S. Y., Zuo B. Q., Materials Science & Engineering C: Materials for Biological Applications, 2015, 51, 287—293
[76]	Chen L., Hu J. X., Ran J. B., Shen X. Y., Tong H., International Journal of Biological Macromolecules, 2014, 65, 1—7
[77]	Ding Z. Z., Han H. Y., Fan Z. H., Lu H. J., Sang Y. H., Yao Y. L., Cheng Q. Q., Lu Q., Kaplan D. L., ACS Appl. Mater. Interfaces, 2017, 9(20), 16913—16921
[78]	Mitropoulos A. N., Marelli B., Ghezzi C. E., Applegate M. B., Partlow B. P., Kaplan D. L., Omenetto F. G., ACS Biomaterials Science & Engineering, 2015, 1(10), 964—970
[79]	Applegate M. B., Partlow B. P., Coburn J., Marelli B., Pirie C., Pineda R., Kaplan D. L., Omenetto F. G., Adv. Mater., 2016, 28(12), 2417—2420
[80]	Sun W., Incitti T., Migliaresi C., Quattrone A., Casarosa S., Motta A., J. Tissue Eng. Regen. Med., 2017, 11(5), 1532—1541
[81]	Sun W., Motta A., Shi Y., Seekamp A., Schmidt H., Gorb S. N., Migliaresi C., Fuchs S., Biomed. Mater., 2016, 11(3), 035009
[82]	Yu L., Ding J. D., Cheminform, 2008, 37(8), 1473—1481
[83]	Hu J. G., Chen B., Guo F., Du J. Y., Gu P. C., Lin X. J., Yang W. P., Zhang H. L., Lu M., Huang Y. P., Xu G. W., J. Mater. Sci. Mater. Med., 2012, 23(3), 711—722
[84]	Liu Y. X., Ling S. J., Wang S. H., Chen X., Shao Z. Z., Biomaterials Science, 2014, 2(10), 1338—1342
[85]	Su D., Jiang L., Xin C., Jian D., Shao Z., ACS Applied Materials & Interfaces, 2016, 8(15), 9619
[86]	Mieszawska A. J., Llamas J. G., Vaiana C. A., Kadakia M. P., Naik R. R., Kaplan D. L., Acta Biomaterialia, 2011, 7(8), 3036—3041
[87]	Ribeiro M., Moraes M. a. D., Beppu M. M., Garcia M. P., Fernandes M. H., Monteiro F. J., Ferraz M. P., European Polymer Journal, 2015, 67, 66—77
[88]	Yucel T., Cebe P., Kaplan D. L., Biophysical Journal, 2009, 97(7), 2044—2050
[89]	Zhang W. J., Wang X. L., Wang S. Y., Zhao J., Xu L. Y., Zhu C., Zeng D. L., Chen J., Zhang Z. Y., Kaplan D. L., Jiang X. Q., Biomaterials, 2011, 32(35), 9415—9424
[90]	Yu D. H., Sun C. L., Zheng Z. Z., Wang X. L., Chen D. Y., Wu H., Wang X. Q., Shi F. X., Int. J. Pharm., 2016, 503(1/2), 229—237
[91]	Wu H., Liu S., Xiao L., Dong X., Lu Q., Kaplan D. L., ACS Appl. Mater. Interfaces, 2016, 8(27), 17118—17126
[92]	Kojic N., Pritchard E. M., Tao H., Brenckle M. A., Mondia J. P., Panilaitis B., Omenetto F., Kaplan D. L., Advanced Functional Materials, 2012, 22(18), 3793—3798