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Ting Zhang, James Zhenggui Tang, Xiaofan Fei, Yanping Li, Yi Song, Zhiyong Qian, Qiang Peng. Can nanoparticles and nano-protein interactions bring a bright future for insulin delivery?[J]. Acta Pharmaceutica Sinica B, 2021, 11(3): 651-667

Can nanoparticles and nano-protein interactions bring a bright future for insulin delivery?
Ting Zhanga,b, James Zhenggui Tangc, Xiaofan Feia, Yanping Lid, Yi Songa, Zhiyong Qiane, Qiang Pengb
a Department of Pharmacy, West China Hospital, Sichuan University, Chengdu 610041, China;
b State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China;
c Research Institute in Healthcare Science, Faculty of Science and Engineering, School of Pharmacy, University of Wolverhampton, Wolverhampton, WV1 1LY, UK;
d Laboratory of Clinical Pharmacy and Adverse Drug Reaction, West China Hospital of Sichuan University, Chengdu 610041, China;
e State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center, Chengdu 610041, China
Abstract:
Insulin therapy plays an essential role in the treatment of diabetes mellitus. However, frequent injections required to effectively control the glycemic levels lead to substantial inconvenience and low patient compliance. In order to improve insulin delivery, many efforts have been made, such as developing the nanoparticles (NPs)-based release systems and oral insulin. Although some improvements have been achieved, the ultimate results are still unsatisfying and none of insulin-loaded NPs systems have been approved for clinical use so far. Recently, nano-protein interactions and protein corona formation have drawn much attention due to their negative influence on the in vivo fate of NPs systems. As the other side of a coin, such interactions can also be used for constructing advanced drug delivery systems. Herein, we aim to provide an insight into the advance and flaws of various NPs-based insulin delivery systems. Particularly, an interesting discussion on nano-protein interactions and its potentials for developing novel insulin delivery systems is initiated.
Key words:    Insulin    Diabetic    Nanomaterials    Absorption    Controlled release    Protein adsorption   
Received: 2020-05-19     Revised: 2020-07-09
DOI: 10.1016/j.apsb.2020.08.016
Funds: This work was supported by the National Natural Science Foundation of China (No. 81973261 and 81700538), the Foundation of West China Hospital of Stomatology (No. RD-02-201903, China) and the Research Funding for Talents Developing, West China Hospital of Stomatology, Sichuan University (No. RCDWJS20207, China).
Corresponding author: Qiang Peng     Email:qiangpengzz@scu.edu.cn,lijm2002@163.com
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Ting Zhang
James Zhenggui Tang
Xiaofan Fei
Yanping Li
Yi Song
Zhiyong Qian
Qiang Peng

References:
1. Sharma G, Sharma AR, Nam JS, Doss GP, Lee SS, Chakraborty C. Nanoparticle based insulin delivery system: the next generation efficient therapy for type 1 diabetes. J Nanobiotechnol 2015;13:74.
2. Veiseh O, Tang BC, Whitehead KA, Anderson DG, Langer R. Managing diabetes with nanomedicine: challenges and opportunities. Nat Rev Drug Discov 2015;14:45-57.
3. Petersmann A, Nauck M, Muller-Wieland D, Kerner W, Muller UA, Landgraf R, et al. Definition, classification and diagnosis of diabetes mellitus. Exp Clin Endocrinol Diabetes 2018;126:406-10.
4. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010;87:4-14.
5. Zhang P, Zhang XZ, Brown J, Vistisen D, Sicree R, Shaw J, et al. Global healthcare expenditure on diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010;87:293-301.
6. Juntti-Berggren L, Refai E, Appelskog I, Andersson M, Imreh G, Dekki N, et al. Apolipoprotein CIII promotes Ca2+-dependent beta cell death in type 1 diabetes. Proc Natl Acad Sci U S A 2004;101: 10090-4.
7. Regnell SE, Lernmark A. Early prediction of autoimmune (type 1) diabetes. Diabetologia 2017;60:1370-81.
8. Devarshi PP, McNabney SM, Henagan TM. Skeletal muscle nucleomitochondrial crosstalk in obesity and type 2 diabetes. Int J Mol Sci 2017;18:831.
9. Tuomilehto J, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 2001;344:1343-50.
10. Wadden TA, Webb VL, Moran CH, Bailer BA. Lifestyle modification for obesity: new developments in diet, physical activity, and behavior therapy. Circulation 2012;125:1157-70.
11. American Diabetes A. Standards of medical care in diabetesd—2014. Diabetes Care 2014;37(Suppl 1):S14-80.
12. Umpierrez GE, Gonzalez A, Umpierrez D, Pimentel D. Diabetes mellitus in the Hispanic/Latino population: an increasing health care challenge in the United States. Am J Med Sci 2007;334:274-82.
13. Ismail-Beigi F. Clinical practice. Glycemic management of type 2 diabetes mellitus. N Engl J Med 2012;366:1319-27.
14. Haas LB. Optimizing insulin use in type 2 diabetes: role of basal and prandial insulin in long-term care facilities. J Am Med Dir Assoc 2007;8:502-10.
15. Bray GA. Potential health risks from beverages containing fructose found in sugar or high-fructose corn syrup. Diabetes Care 2013;36: 11-2.
16. Moroz E, Matoori S, Leroux JC. Oral delivery of macromolecular drugs: where we are after almost 100 years of attempts. Adv Drug Deliv Rev 2016;101:108-21.
17. Wong CY, Al-Salami H, Dass CR. Potential of insulin nanoparticle formulations for oral delivery and diabetes treatment. J Control Release 2017;264:247-75.
18. Wong CY, Al-Salami H, Dass CR. Microparticles, microcapsules and microspheres: a review of recent developments and prospects for oral delivery of insulin. Int J Pharm 2018;537:223-44.
19. Picone P, Sabatino MA, Ditta LA, Amato A, San Biagio PL, Mule F, et al. Nose-to-brain delivery of insulin enhanced by a nanogel carrier. J Control Release 2018;270:23-36.
20. Kim NA, Thapa R, Jeong SH, Bae HD, Maeng J, Lee K, et al. Enhanced intranasal insulin delivery by formulations and tumor protein-derived protein transduction domain as an absorption enhancer. J Control Release 2019;294:226-36.
21. Chen X, Wang L, Yu HJ, Li CJ, Feng JY, Haq F, et al. Preparation, properties and challenges of the microneedles-based insulin delivery system. J Control Release 2018;288:173-88.
22. Peng Q, Sun X, Gong T, Wu CY, Zhang T, Tan J, et al. Injectable and biodegradable thermosensitive hydrogels loaded with PHBHHx nanoparticles for the sustained and controlled release of insulin. Acta Biomater 2013;9:5063-9.
23. Sheng JY, He HN, Han LM, Qin J, Chen SH, Ru G, et al. Enhancing insulin oral absorption by using mucoadhesive nanoparticles loaded with LMWP-linked insulin conjugates. J Control Release 2016;233: 181-90.
24. Lee KC, Chen WJ, Chen YC. Using dextran-encapsulated gold nanoparticles as insulin carriers to prolong insulin activity. Nanomedicine 2017;12:1823-34.
25. Sun L, Liu Z, Tian H, Le Z, Liu L, Leong KW, et al. Scalable manufacturing of enteric encapsulation systems for site-Specific oral insulin delivery. Biomacromolecules 2018;20:528-38.
26. Liu J, Peng Q. Protein-gold nanoparticle interactions and their possible impact on biomedical applications. Acta Biomater 2017;55:13-27.
27. Charbgoo F, Nejabat M, Abnous K, Soltani F, Taghdisi SM, Alibolandi M, et al. Gold nanoparticle should understand protein corona for being a clinical nanomaterial. J Control Release 2018;272:39-53.
28. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci U S A 2008;105:14265-70.
29. Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, Laurent S. Protein-nanoparticle interactions: opportunities and challenges. Chem Rev 2011;111:5610-37.
30. Salvati A, Pitek AS, Monopoli MP, Prapainop K, Bombelli FB, Hristov DR, et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat Nanotechnol 2013;8:137-43.
31. Peng Q, Mu HL. The potential of protein-nanomaterial interaction for advanced drug delivery. J Control Release 2016;225:121-32.
32. Peng Q, Zhang S, Yang Q, Zhang T, Wei XQ, Jiang L, et al. Preformed albumin corona, a protective coating for nanoparticles based drug delivery system. Biomaterials 2013;34:8521-30.
33. Peng Q, Wei XQ, Yang Q, Zhang S, Zhang T, Shao XR, et al. Enhanced biostability of nanoparticle-based drug delivery systems by albumin corona. Nanomedicine 2015;10:205-14.
34. Chen MC, Sonaje K, Chen KJ, Sung HW. A review of the prospects for polymeric nanoparticle platforms in oral insulin delivery. Biomaterials 2011;32:9826-38.
35. Kaklotar D, Agrawal P, Abdulla A, Singh RP, Mehata AK, Singh S, et al. Transition from passive to active targeting of oral insulin nanomedicines: enhancement in bioavailability and glycemic control in diabetes. Nanomedicine 2016;11:1465-86 (London).
36. Naidu PSR, Norret M, Dunlop SA, Fitzgerald M, Clemons TD, Iyer KS. Novel hydrophilic copolymer-based nanoparticle enhances the therapeutic efficiency of doxorubicin in cultured MCF-7 cells. ACS Omega 2019;4:17083-9.
37. Daneman D. Type 1 diabetes. Lancet 2006;367:847-58.
38. Shilo M, Berenstein P, Dreifuss T, Nash Y, Goldsmith G, Kazimirsky G, et al. Insulin-coated gold nanoparticles as a new concept for personalized and adjustable glucose regulation. Nanoscale 2015;7:20489-96.
39. Qi W, Yan X, Duan L, Cui Y, Yang Y, Li J. Glucose-sensitive microcapsules from glutaraldehyde cross-linked hemoglobin and glucose oxidase. Biomacromolecules 2009;10:1212-6.
40. Tan YF, Lao LL, Xiong GM, Venkatraman S. Controlled-release nanotherapeutics: state of translation. J Control Release 2018;284: 39-48.
41. Finotelli PV, Da Silva D, Sola-Penna M, Rossi AM, Farina M, Andrade LR, et al. Microcapsules of alginate/chitosan containing magnetic nanoparticles for controlled release of insulin. Colloids Surf B Biointerfaces 2010;81:206-11.
42. Saravanan S, Malathi S, Sesh PSL, Selvasubramanianc S, Balasubramanian S, Pandiyan V. Hydrophilic poly (ethylene glycol) capped poly (lactic-co-glycolic) acid nanoparticles for subcutaneous delivery of insulin in diabetic rats. Int J Biol Macromol 2017;95: 1190-8.
43. Tomar L, Tyagi C, Kumar M, Kumar P, Singh H, Choonara YE, et al. In vivo evaluation of a conjugated poly(lactide-ethylene glycol) nanoparticle depot formulation for prolonged insulin delivery in the diabetic rabbit model. Int J Nanomed 2013;8:505-20.
44. Peng Q, Zhang ZR, Gong T, Chen GQ, Sun X. A rapid-acting, longacting insulin formulation based on a phospholipid complex loaded PHBHHx nanoparticles. Biomaterials 2012;33:1583-8.
45. Muggeo M, Zoppini G, Bonora E, Brun E, Bonadonna RC, Moghetti P, et al. Fasting plasma glucose variability predicts 10-year survival of type 2 diabetic patients: the verona diabetes study. Diabetes Care 2000;23:45-50.
46. McCoy RG, Van Houten HK, Ziegenfuss JY, Shah ND, Wermers RA, Smith SA. Increased mortality of patients with diabetes reporting severe hypoglycemia. Diabetes Care 2012;35:1897-901.
47. Bratlie KM, York RL, Invernale MA, Langer R, Anderson DG. Materials for diabetes therapeutics. Adv Healthc Mater 2012;1: 267-84.
48. VandenBerg MA, Webber MJ. Biologically inspired and chemically derived methods for glucose-responsive insulin therapy. Adv Healthc Mater 2019;8:1801466.
49. Kazuhiko Ishihara MK, Ishimaru Naoshi, Shinohara Isao. Glucose induced permeation control of insulin through a complex membrane consisting of immobilized glucose oxidase and a poly(amine). Polym J 1984;16:625-31.
50. Bankar SB, Bule MV, Singhal RS, Ananthanarayan L. Glucose oxidasedan overview. Biotechnol Adv 2009;27:489-501.
51. Farahani BV, Ghasemzaheh H, Afraz S. Intelligent semi-IPN chitosan-PEG-PAAm hydrogel for closed-loop insulin delivery and kinetic modeling. RSC Adv 2016;6:26590-8.
52. Gu Z, Aimetti A, Wang Q, Dang TT, Zhang Y, Veiseh O, et al. Injectable nano-network for glucose-mediated insulin delivery. ACS Nano 2013;7:4194-201.
53. Siegel RA, Gu Y, Lei M, Baldi A, Nuxoll EE, Ziaie B. Hard and soft micro- and nanofabrication: an integrated approach to hydrogelbased biosensing and drug delivery. J Control Release 2010;141: 303-13.
54. Yoshida K, Hasebe Y, Takahashi S, Sato K, Anzai J. Layer-by-layer deposited nano- and micro-assemblies for insulin delivery: a review. Mater Sci Eng C Mater Biol Appl 2014;34:384-92.
55. Tong ZZ, Zhou JY, Zhong JX, Tang QJ, Lei ZT, Luo HP, et al. Glucose- and H2O2-responsive polymeric vesicles integrated with microneedle patches for glucose-sensitive transcutaneous delivery of insulin in diabetic rats. ACS Appl Mater Interfaces 2018;10: 20014-24.
56. Duan Y, Ye FG, Huang YL, Qin YM, He CM, Zhao SL. One-pot synthesis of a metal-organic framework-based drug carrier for intelligent glucose-responsive insulin delivery. Chem Commun 2018; 54:5377-80.
57. Jamwal S, Ram B, Ranote S, Dharela R, Chauhan GS. New glucose oxidase-immobilized stimuli-responsive dextran nanoparticles for insulin delivery. Int J Biol Macromol 2018;123: 968-78.
58. Aznar E, Villalonga R, Gimenez C, Sancenon F, Marcos MD, Martinez-Manez R, et al. Glucose-triggered release using enzyme-gated mesoporous silica nanoparticles. Chem Commun 2013;49:6391-3.
59. Chen MJ, Huang CS, He CS, Zhu WP, Xu YF, Lu YF. A glucoseresponsive controlled release system using glucose oxidase-gated mesoporous silica nanocontainers. Chem Commun 2012;48:9522-4.
60. Diez P, Sanchez A, Gamella M, Martinez-Ruiz P, Aznar E, de la Torre C, et al. Toward the design of smart delivery systems controlled by integrated enzyme-based biocomputing ensembles. J Am Chem Soc 2014;136:9116-23.
61. Ravaine V, Ancla C, Catargi B. Chemically controlled closed-loop insulin delivery. J Control Release 2008;132:2-11.
62. Gu Z, Dang TT, Ma M, Tang BC, Cheng H, Jiang S, et al. Glucoseresponsive microgels integrated with enzyme nanocapsules for closed-loop insulin delivery. ACS Nano 2013;7:6758-66.
63. Tai W, Mo R, Di J, Subramanian V, Gu X, Buse JB, et al. Bioinspired synthetic nanovesicles for glucose-responsive release of insulin. Biomacromolecules 2014;15:3495-502.
64. Yu JC, Zhang YQ, Ye YQ, DiSanto R, Sun WJ, Ranson D, et al. Microneedle-array patches loaded with hypoxia-sensitive vesicles provide fast glucose-responsive insulin delivery. Proc Natl Acad Sci U S A 2015;112:8260-5.
65. Sharon N, Lis H. Lectins: cell-agglutinating and sugar-specific proteins. Science 1972;177:949-59.
66. Brownlee M, Cerami A. A glucose-controlled insulin-delivery system: semisynthetic insulin bound to lectin. Science 1979;206:1190-1.
67. Kim JJ, Park K. Glucose-binding property of pegylated concanavalin A. Pharm Res 2001;18:794-9.
68. Sung Wan K, Chaul Min P, Kimiko M, Seminoff LA, Holmberg DL, Gleeson JM, et al. Self-regulated glycosylated insulin delivery. J Control Release 1990;11:193-201.
69. Makino K, Mack EJ, Okano T, Sung Wan K. A microcapsule selfregulating delivery system for insulin. J Control Release 1990;12: 235-9.
70. Liu F, Song SC, Mix D, Baudys M, Kim SW. Glucose-induced release of glycosylpoly(ethylene glycol) insulin bound to a soluble conjugate of concanavalin A. Bioconjugate Chem 1997;8:664-72.
71. Taylor MJ, Tanna S, Sahota T. In vivo study of a polymeric glucosesensitive insulin delivery system using a rat model. J Pharmaceut Sci 2010;99:4215-27.
72. Kim JJ, Park K. Modulated insulin delivery from glucose-sensitive hydrogel dosage forms. J Control Release 2001;77:39-47.
73. Yin RX, Bai MR, He J, Nie J, Zhang WJ. Concanavalin A-sugar affinity based system: binding interactions, principle of glucoseresponsiveness, and modulated insulin release for diabetes care. Int J Biol Macromol 2019;124:724-32.
74. Yin RX, Han J, Zhang JF, Nie J. Glucose-responsive composite microparticles based on chitosan, concanavalin A and dextran for insulin delivery. Colloids Surf B Biointerfaces 2010;76:483-8.
75. You LC, Lu FZ, Li ZC, Zhang W, Li FM. Glucose-sensitive aggregates formed by poly(ethylene oxide) block poly(2-glucosyl-oxyethyl acrylate) with concanavalin A in dilute aqueous medium. Macromolecules 2003;36:1-4.
76. Wu SS, Huang X, Du XZ. Glucose- and pH-responsive controlled release of cargo from protein-gated carbohydrate-functionalized mesoporous silica nanocontainers. Angew Chem Int Ed Engl 2013; 52:5580-4.
77. Kataoka K, Miyazaki H, Okano T, Sakurai Y. Sensitive glucoseinduced change of the lower critical solution temperature of poly [N,N-(dimethylacrylamide)-co-3-(acrylamido)-phenylboronic acid] in physiological saline. Macromolecules 1994;27:1061-2.
78. Huang Q, Wang L, Yu HJ, Ur-Rahman K. Advances in phenylboronic acid-based closed-loop smart drug delivery system for diabetic therapy. J Control Release 2019;305:50-64.
79. Wu WT, Mitra N, Yan EC, Zhou SQ. Multifunctional hybrid nanogel for integration of optical glucose sensing and self-regulated insulin release at physiological pH. ACS Nano 2010;4:4831-9.
80. Matsumoto A, Yamamoto K, Yoshida R, Kataoka K, Aoyagi T, Miyahara Y. A totally synthetic glucose-responsive gel operating in physiological aqueous conditions. Chem Commun 2010;46:2203-5.
81. Gaballa H, Theato P. Glucose-responsive polymeric micelles via boronic acid-diol complexation for insulin delivery at neutral pH. Biomacromolecules 2019;20:871-81.
82. Wu JZ, Williams GR, Li HY, Wang DX, Li SD, Zhu LM. Insulinloaded PLGA microspheres for glucose-responsive release. Drug Deliv 2017;24:1513-25.
83. Shi DJ, Ran MS, Zhang L, Huang H, Li XJ, Chen MQ, et al. Fabrication of biobased polyelectrolyte capsules and their application for glucose-triggered insulin delivery. ACS Appl Mater Interfaces 2016;8:13688-97.
84. Yao Y, Zhao LY, Yang JJ, Yang J. Glucose-responsive vehicles containing phenylborate ester for controlled insulin release at neutral pH. Biomacromolecules 2012;13:1837-44.
85. Wang BL, Ma RJ, Liu G, Li Y, Liu XJ, An YL, et al. Glucoseresponsive micelles from self-assembly of poly(ethylene glycol)-bpoly(acrylic acid-co-acrylamidophenylboronic acid) and the controlled release of insulin. Langmuir 2009;25:12522-8.
86. Wu JZ, Williams GR, Li HY, Wang D, Wu H, Li SD, et al. Glucoseand temperature-sensitive nanoparticles for insulin delivery. Int J Nanomed 2017;12:4037-57.
87. Gao L, Wang TT, Jia KK, Wu X, Yao CH, Shao W, et al. Glucoseresponsive supramolecular vesicles based on water-soluble pillar[5] arene and pyridylboronic acid derivatives for controlled insulin delivery. Chemistry 2017;23:6605-14.
88. Zeng ZY, Qi DM, Yang L, Liu J, Tang YQ, Chen H, et al. Stimuliresponsive self-assembled dendrimers for oral protein delivery. J Control Release 2019;315:206-13.
89. Zhao Y, Trewyn BG, Slowing II, Lin VS. Mesoporous silica nanoparticle-based double drug delivery system for glucoseresponsive controlled release of insulin and cyclic AMP. J Am Chem Soc 2009;131:8398-400.
90. He HS, Lu Y, Qi JP, Zhao WL, Dong XC, Wu W. Biomimetic thiamine- and niacin-decorated liposomes for enhanced oral delivery of insulin. Acta Pharm Sin B 2018;8:97-105.
91. Kanzarkar M, Pathak PP, Vaidya M, Brumlik C, Choudhury A. Oral insulin-delivery system for diabetes mellitus. Pharm Pat Anal 2015; 4:29-36.
92. Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 1988;29:1035-41.
93. Alai MS, Lin WJ, Pingale SS. Application of polymeric nanoparticles and micelles in insulin oral delivery. J Food Drug Anal 2015;23:351-8.
94. Langguth P, Bohner V, Heizmann J, Merkle HP, Wolffram S, Amidon GL, et al. The challenge of proteolytic enzymes in intestinal peptide delivery. J Control Release 1997;46:39-57.
95. Bernkop-Schnurch A. The use of inhibitory agents to overcome the enzymatic barrier to perorally administered therapeutic peptides and proteins. J Control Release 1998;52:1-16.
96. Andrews CW, Bennett L, Yu LX. Predicting human oral bioavailability of a compound: development of a novel quantitative structurebioavailability relationship. Pharm Res 2000;17:639-44.
97. Damgé C, Michel C, Aprahamian M, Couvreur P. New approach for oral administration of insulin with polyalkylcyanoacrylate nanocapsules as drug carrier. Diabetes 1988;37:246-51.
98. Mesiha MS, Sidhom MB, Fasipe B. Oral and subcutaneous absorption of insulin poly(isobutylcyanoacrylate) nanoparticles. Int J Pharm 2005;288:289-93."
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