Articles

Development of a Biomimetic Peptide-Based Nanoformulation Against the Breast Cancer

Abstract

Nanotechnology has enabled the preparation of various materials for overcoming the rapid clearance of drugs, nonspecific uptake or actions, and poor tumor penetration. Based on the significance of using biomimetic substances, silk fibroin nanoparticles (SF-NPs) have been increasingly prepared for the delivery of therapeutics. Meanwhile, aggregation and low stability in the biological medium may negatively affect their efficiency. This prompted us to coat SF-NPs with polydopamine (PDA), and for efficient accumulation and increasing therapeutic efficiency against breast cancer, paclitaxel (PTX)-loaded PDA-coated SF-NPs were conjugated with targeting peptide, iRGD (iRGD-PDA-PTX-SF-NPs). The peptide impacts on the cellular uptake, cytotoxicity, tumor penetrability of NPs, and their antitumor effects were evaluated. iRGD-PDA-PTX-SF-NPs with suitable physicochemical characteristics and drug loading released PTX in a controlled manner, and efficient cellular uptake was observed. Improved pharmacological profile of PTX was revealed by increased anticancer effects in vitro and in tumor-bearing Balb/c mice, including the delayed growth of the tumor and enhanced rate of survival. The prepared NPs showed no toxic effects against the healthy tissues indicating the histocompatibility and safety of these biomimetic and long-circulating nanoplatforms. The peptide-based SF-NPs could be considered as promising biomimetic nanoformulation against breast cancer.

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin 2019;69:7-34.
2. Kassam F, Enright K, Dent R, Dranitsaris G, Myers J, Flynn C, et al. Survival outcomes for patients with metastatic triple-negative breast cancer: implications for clinical practice and trial design. Clin Breast Cancer 2009;9:29-33.
3. Anders CK, Carey LA. Biology, metastatic patterns, and treatment of patients with triple-negative breast cancer. Clin Breast Cancer 2009;9:S73-81.
4. Goldfarb Y, Ben-Eliyahu S. Surgery as a risk factor for breast cancer recurrence and metastasis: Mediating mechanisms and clinical prophylactic approaches. Breast Dis 2007;26:99-114.
5. McCubrey JA, Abrams SL, Fitzgerald TL, Cocco L, Martelli AM, Montalto G, et al. Roles of signaling pathways in drug resistance, cancer initiating cells and cancer progression and metastasis. Adv Biol Regul 2015;57:75-101.
6. Housman G, Byler S, Heerboth S, Lapinska K, Longacre M, Snyder N, et al. Drug Resistance in Cancer: An Overview. Cancers (Basel) 2014;6:1769-92.
7. Maribeth Maher. Current and Emerging Treatment Regimens for HER2-Positive Breast Cancer. P T 2014;39:206-12.
8. Shojaei S, Gardaneh M, Rahimi Shamabadi A. Target points in trastuzumab resistance. Int J Breast Cancer 2012;2012:761917.
9. Valabrega G, Montemurro F, Aglietta M. Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Ann Oncol 2007;18:977-84.
10. Reff ME, Hariharan K, Braslawsky G. Future of monoclonal antibodies in the treatment of hematologic malignancies. Cancer Control 2002;9:152-66.
11. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007;2:751-60.
12. Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer 2005;5:161-71.
13. Toy R, Bauer L, Hoimes C, Ghaghada KB, Karathanasis E. Targeted nanotechnology for cancer imaging. Adv Drug Deliv Rev 2014; 76:79-97.
14. Shi J, Kantoff PW, Wooster R, Farokhzad OC. Cancer nanomedicine: progress, challenges and opportunities. Nat Rev Cancer 2017;17:20-37.
15. Cho K, Wang X, Nie S, Shin DM. Therapeutic Nanoparticles for Drug Delivery in Cancer. Clin. Cancer Res 2008;14:1310-6.
16. Patil YB, Toti US, Khdair A, Ma L, Panyam J. Single-Step Surface Functionalization of Polymeric Nanoparticles for Targeted Drug Delivery. Biomaterials 2009;30:859-66.
17. Leal‐Egaña A, Scheibel T. Silk‐based materials for biomedical applications. Biotechnol Appl Biochem 2010;55:155‐67.
18. Wang Y, Blasioli DJ, Kim HJ, Kim HS, Kaplan DL. Cartilage tissue engineering with silk scaffolds and human articular chondrocytes. Biomaterials 2006;27:4434‐42.
19. Omenetto FG, Kaplan DL. New opportunities for an ancient material. Science 2010;329:528-31.
20. Heim M, Keerl D, Scheibel T. Spider silk: from soluble proteinto extraordinary fiber. Angew Chem Int Ed Engl 2009;48:3584-96.
21. Zheng Z, Li Y, Xie MB. Silk Fibroin-Based Nanoparticles for Drug Delivery. Int J Mol Sci 2015;16:4880-903.
22. Kundu J, Chung YI, Kim YH, Tae G, Kundu SC. Silk fibroin nanoparticles for cellular uptake and control release. Int J Pharm 2010;388:242-50.
23. Yucel T, Lovett ML, Giangregorio R, Coonahan E, Kaplan DL. Silk fibroin rods for sustained delivery of breast cancer therapeutics. Biomaterials 2014;35:8613-20.
24. Wu P, Liu Q, Li R, Wang J, Zhen X, Yue G, et al. Facile preparation of paclitaxel loaded silk fibroin nanoparticles for enhanced antitumor efficacy by loco-regional drug delivery. ACS Appl Mater Interfaces 2013;5:12638-45.
25. Seib FP, Jones GT, Rnjak-Kovacina J, Lin Y, Kaplan DL. pH-dependent anticancer drug release from silk nanoparticles. Adv Healthc Mater 2013;2:1606-11.
26. Subia B, Kundu SC. Drug loading and release on tumor cells using silk fibroin-albumin nanoparticles as carriers. Nanotechnology 2013;24:035103.
27. Hassanzadeh P, Arbabi E, Rostami F. Lipid-based nanocarriers provide prolonged anticancer activity for palbociclib: In vitro and in vivo evaluations. Acta Med Iran 2021;59:87-93.
28. Lin Z, Gao W, Hu H, Ma K, He B, Dai W, et al. Novel thermo-sensitive hydrogel system with paclitaxel nanocrystals: High drug-loading, sustained drug release and extended local retention guaranteeing better efficacy and lower toxicity. J Control Release 2014;174:161-70.
29. Zhang L, He Y, Ma G, Song C, Sun H. Paclitaxel-loaded polymeric micelles based on poly(ɛ-caprolactone)-poly(ethylene glycol)-poly(ɛ-caprolactone) triblock copolymers: in vitro and in vivo evaluation. Nanomedicine 2012;8:925-34.
30. Vepari C, Kaplan DL. Silk as a biomaterial. Prog Polym Sci 2007;32:991-1007.
31. Murphy AR, Kaplan DL. Biomedical applications of chemically‐modified silk fibroin. J Mater Chem 2009;19:6443‐50.
32. Ishihara T, Maeda T, Sakamoto H, Takasaki N, Shigyo M, Ishida T, et al. Evasion of the accelerated blood clearance phenomenon by coating of nanoparticles with various hydrophilic polymers. Biomacromolecules 2010;11:2700-6.
33. Wang X, Ishida T, Kiwada H. Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposomes. J Control Release 2007;119:236-44.
34. Hoang B, Lee H, Reilly RM, Allen C. Noninvasive monitoring of the fate of 111In-labeled block copolymer micelles by high resolution and high sensitivity MicroSPECT/CT imaging. Mol Pharm 2009;6:581-92.
35. Xu H, Wang KQ, Deng YH, Chen DW. Effects of cleavable PEG-cholesterol derivatives on the accelerated blood clearance of PEGylated liposomes. Biomaterials 2010;31:4757-63.
36. Yan P, Wang J, Wang L, Liu B, Lei Z, Yang S. The in vitro Biomineralization and Cytocompatibility of Polydopamine Coated Carbon Nanotubes. Appl Surf Sci 2011;257:4849-55.
37. Zheng QS, Lin T, Wu H, Guo L, Ye P, Hao Y, et al. Mussel-inspired polydopamine coated mesoporous silica nanoparticles as pH-sensitive nanocarriers for controlled release. Int J Pharm 2014;463:22-6.
38. Liu Y, Ai K, Lu L. Polydopamine and its derivative materials: synthesis and promising applications in energy, environmental, and biomedical fields. Chem Rev 2014;114:5057-115.
39. Ho CC, Ding SJ. Structure, properties and applications of mussel-inspired polydopamine. J Biomed Nanotechnol 2014;10:3063-84.
40. Hassanzadeh P, Arbabi E, Rostami F. Development of a novel nanoformulation against the colorectal cancer. Life Sci 2021;281:119772.
41. Sun H, Dong Y, Feijen J, Zhong Z. Peptide-decorated polymeric nanomedicines for precision cancer therapy. J Control Release 2018;290:11-27.
42. Wanjale MV, Kumar GSV. Peptides as a therapeutic avenue for nanocarrier-aided targeting of glioma. Expert Opin Drug Deliv Expert Opin Drug Deliv 2017;14:811-24.
43. Komin A, Russell LM, Hristova KA, Searson PC. Peptide-based strategies for enhanced cell uptake, transcellular transport, and circulation: mechanisms and challenges. Adv Drug Deliv Rev 2017;110-111:52-64.
44. Peng M, Qin S, Jia H, Zheng D, Rong L, Zhang X. Self delivery of a Peptide-Based Prodrug for Tumor-Targeting Therapy. Nano Res 2016;9:663-73.
45. Sugahara KN, Teesalu T, Karmali PP, Kotamraju VR, Agemy L, Greenwald DR, et al. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 2010;328:1031-5.
46. Ruoslahti E. Tumor penetrating peptides for improved drug delivery. Adv Drug Deliv Rev 2017;110-1:3-12.
47. Ruoslahti E. Access granted: iRGD helps silicasome-encased drugs breach the tumor barrier. J Clin Invest 2017;127:1622-4.
48. Rockwood DN, Preda RC, Yucel T, Wang X, Lovett ML, Kaplan DL. Materials Fabrication From Bombyx Mori Silk Fibroin. Nat Protoc 2011;6:1612-31.
49. Yu Zhang, Yixin Zhong, Man Ye, Jie Xu, Jia Liu, Jun Zhou, et al. Polydopamine-modified dual-ligand nanoparticles as highly effective and targeted magnetic resonance/photoacoustic dual-modality thrombus imaging agents. Int J Nanomedicine 2019:14;7155-71.
50. Cho HJ, Lee SJ, Park SJ, Paik CH, Leed SM, Kim S, et al. Activatable iRGD-based peptide monolith: targeting, internalization, and fluorescence activation for precise tumor imaging. J Control Release 2016;237:177-84.
51. Kotamraju VR, Sharma S, Kolhar P, Agemy L, Pavlovich J, Ruoslahti E. Increasing Tumor Accessibility with Conjugatable Disulfide-Bridged Tumor-Penetrating Peptides for Cancer Diagnosis and Treatment. Breast Cancer (Auckl) 2016;9:79-87.
52. Pan G, Sun S, Zhang W, Zhao R, Cui W, He F, et al. Biomimetic Design of Mussel-Derived Bioactive Peptides for Dual-Functionalization of Titanium-Based Biomaterials. J Am Chem Soc 2016;138:15078-86.
53. Karmali PP, Kotamraju VR, Kastantin M, Black M, Missirlis D, Tirrell M, et al. Targeting of albumin-embedded paclitaxel nanoparticles to tumors. Nanomedicine 2009;5:73-82.
54. Zhu S, Qian L, Hong M, Zhang L, Pei Y, Jiang Y. RGD-modified PEG-PAMAMDOX conjugate: in vitro and in vivo targeting to both tumor neovascular endothelial cells and tumor cells. Adv Mater 2011;23:H84e9.
55. Danhier F, Lecouturier N, Vroman B, Jérôme C, Marchand-Brynaert J, Feron O, et al. Paclitaxel-loaded PEGylated PLGA-based nanoparticles: In vitro and in vivo evaluation. J Control Release 2009;133:11-7.
56. Qifan W, Fen N, Ying X, Xinwei F, Jun D, Ge Z. iRGD-targeted delivery of a pro-apoptotic peptide activated by cathepsin B inhibits tumor growth and metastasis in mice. Tumour Biol 2016;37:10643-52.
57. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 1987;47:936-41.
58. Lammel A, Xiao H, Park SH, Kaplan DL, Scheibel TR. Controlling silk fibroin particle features for drug delivery. Biomaterials 2010;31:4583-91.
59. Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci U S A 2009;106:16157-62.
60. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010;10:9-22.
61. Jain RK. Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastasis Rev 1990;9:253-66.
62. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer 2004;4:806-13.
63. Zuo H. iRGD: A Promising Peptide for Cancer Imaging and a Potential Therapeutic Agent for Various Cancers. J Oncol 2019;2019:9367845.
64. Xiangsheng Liu, Andre E. Nel, Huan Meng. Tumor-penetrating peptide enhances transcytosis of silicasome-based chemotherapy for pancreatic cancer. J Clin Invest 2017;127:1622-4.
65. Prud'homme GJ, Glinka Y. Neuropilins are multifunctional coreceptors involved in tumor initiation, growth, metastasis and immunity. Oncotarget 2012;3:921-39.
66. Chen R, Braun GB, Luo X, Sugahara KN, Teesalu T, Ruoslahti E. application of a proapoptotic peptide to intratumorally spreading cancer therapy. Cancer Res 2013;73:1352-61.
Files
IssueVol 59, No 7 (2021) QRcode
SectionArticles
DOI https://doi.org/10.18502/acta.v59i7.7023
Keywords
Breast cancer Silk fibroin Polydopamine Internalizing arginine-glycine-aspartic acid (iRGD) Paclitaxel Balb/c mice

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Hassanzadeh P, Arbabi E, Rostami F. Development of a Biomimetic Peptide-Based Nanoformulation Against the Breast Cancer. Acta Med Iran. 2021;59(7):430-441.