In vitro anti-melanoma activity of imiquimod in ultradeformable nanovesicles

References

• Leonardi GC, Candido S, Falzone L, et al. Cutaneous melanoma and the immunotherapy revolution. Int J Oncol. 2020;57(3):609–618.
   PubMed Web of Science ®Google Scholar
• Miller KD, Goding Sauer A, Ortiz AP, et al. Cancer statistics for Hispanics/Latinos. CA Cancer J Clin. 2018;68(6):425–445.
   PubMed Web of Science ®Google Scholar
• Domingues B, Lopes JM, Soares P, et al. Melanoma treatment in review. Immunotargets Ther. 2018;7:35–49.
   PubMed Web of Science ®Google Scholar
• Davis LE, Shalin SC, Tackett AJ. Current state of melanoma diagnosis and treatment. Cancer Biol Ther. 2019;20(11):1366–1379.
   PubMed Web of Science ®Google Scholar
• Radny P, Caroli U, Bauer J, et al. Phase II trial of intralesional therapy with interleukin-2 in soft-tissue melanoma metastases. Br J Cancer. 2003;89(9):1620–1626.
   PubMed Web of Science ®Google Scholar
• Fujimura T, Okuyama R, Ohtani T, et al. Perilesional treatment of metastatic melanoma with interferon‐β. Clin Exp Dermatol. 2009;34(7):793–799.
   PubMed Web of Science ®Google Scholar
• Heppt MV, Goldscheider I, Tietze JK, et al. Intralesional interleukin-2 for unresectable mucosal melanoma refractory to nivolumab. Cancer Immunol Immunother. 2017;66(10):1377–1378.
   PubMed Web of Science ®Google Scholar
• Schön MP, Schön M. Imiquimod: mode of action. Br J Dermatol. 2007;157(8):8–13.
   PubMedGoogle Scholar
• Stanley M. Imiquimod and the imidazoquinolones: mechanism of action and therapeutic potential. Clin Exp Dermatol. 2002;27(7):571–577.
   PubMed Web of Science ®Google Scholar
• Vidal D, Alomar A. Mode of action and clinical use of imiquimod. Exp Rev Dermatol. 2008;3(2):151–159.
   Google Scholar
• Scarfì F, Patrizi A, Veronesi G, et al. The role of topical imiquimod in melanoma cutaneous metastases: a critical review of the literature. Dermatol Ther. 2020;33(6):e14165.
   Web of Science ®Google Scholar
• Hyde M, Hadley M, Tristani-Firouzi P, et al. Trial of the off-label use of imiquimod, 5%, cream with vs without tazarotene, 0.1%, and gel for the treatment of lentigo maligna, followed by conservative staged excisions. Arch Dermatol. 2012;148(5):592–596.
   PubMedGoogle Scholar
• Drobits B, Holcmann M, Amberg N, et al. Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells. J Clin Invest. 2012;122(2):575–585.
   PubMed Web of Science ®Google Scholar
• Schön MP, Wienrich B, Drewniok C, et al. Death receptor-independent apoptosis in malignant melanoma induced by the small-molecule immune response modifier imiquimod. J Inv Dermatol. 2004;122(5):1266–1276.
   PubMed Web of Science ®Google Scholar
• Aspord C, Tramcourt L, Leloup C, et al. Imiquimod inhibits melanoma development by promoting pDC cytotoxic functions and impeding tumor vascularization. J Inv Dermatol. 2014;134(10):2551–2561.
   PubMed Web of Science ®Google Scholar
• Rehman K, Zulfakar MH. Novel fish oil-based bigel system for controlled drug delivery and its influence on immunomodulatory activity of imiquimod against skin cancer. Pharm Res. 2017;34(1):36–48.
   PubMed Web of Science ®Google Scholar
• Smits EL, Ponsaerts P, Berneman ZN, et al. The use of TLR7 and TLR8 ligands for the enhancement of cancer immunotherapy. Oncologist. 2008;13(8):859–875.
   PubMed Web of Science ®Google Scholar
• Karve S, Feldman S, Yentzer B, et al. Imiquimod: a review of basal cell carcinoma treatments. J Drugs Dermatol. 2008;7(11):1044–1051.
   PubMedGoogle Scholar
• Chollet J, Jozwiakowski MJ, Phares K, et al. Development of a topically active imiquimod formulation. Pharm Develop Technol. 1999;4(1):35–43.
   PubMed Web of Science ®Google Scholar
• Pinho JO, Matias M, Gaspar M. Emergent nanotechnological strategies for systemic chemotherapy against melanoma. Nanomaterials. 2019;9(10):1455.
   Web of Science ®Google Scholar
• Pandey M, Choudhury H, Gorain B, et al. Site-specific vesicular drug delivery system for skin cancer: a novel approach for targeting. Gels. 2021;7(4):218.
   PubMed Web of Science ®Google Scholar
• Saindane D, Bhattacharya S, Shah R, et al. The recent development of topical nanoparticles for annihilating skin cancer. All Life. 2022;15(1):843–869.
   Web of Science ®Google Scholar
• Venturini C, Bruinsmann F, Contri R, et al. Co-encapsulation of imiquimod and copaiba oil in novel nanostructured systems: promising formulations against skin carcinoma. Eur J Pharm Sci. 2015;79:36–43.
   PubMed Web of Science ®Google Scholar
• França Dias M, Pinheiro de Figueiredo BC, Teixeira-Neto J, et al. In vivo evaluation of antitumoral and antiangiogenic effect of imiquimod-loaded polymeric nanoparticles. Biomed Pharmacother. 2018;103:1107–1114.
   PubMed Web of Science ®Google Scholar
• Lapteva M, Mignot M, Mondon K, et al. Self-assembled mPEG-hexPLA polymeric nanocarriers for the targeted cutaneous delivery of imiquimod. Eur J Pharm Biopharm. 2019;142:553–562.
   PubMed Web of Science ®Google Scholar
• Ghezzi M, Pescina S, Delledonne A, et al. Improvement of imiquimod solubilization and skin retention via TPGS micelles: exploiting the co-solubilizing effect of oleic acid. Pharmaceutics. 2021;13(9):1476.
   PubMed Web of Science ®Google Scholar
• Tampucci S, Guazzelli L, Burgalassi S, et al. pH-Responsive nanostructures based on surface active fatty acid-protic ionic liquids for imiquimod delivery in skin cancer topical therapy. Pharmaceutics. 2020;12(11):1078.
   PubMed Web of Science ®Google Scholar
• Cevc G, Blume G. Lipid vesicles penetrate into intact skin owing to the transdermal osmotic gradients and hydration force. Biochim Biophys Acta. 1992;1104(1):226–232.
   PubMed Web of Science ®Google Scholar
• Higa L, Arnal L, Vermeulen M, et al. Ultradeformable archaeosomes for needle free nanovaccination with Leishmania braziliensis antigens. PLoS One. 2016;11(3):e0150185.
   PubMed Web of Science ®Google Scholar
• Cevc G, Vierl U. Nanotechnology and the transdermal route: a state of the art review and critical appraisal. J Control Release. 2010;141(3):277–299.
   PubMed Web of Science ®Google Scholar
• Khan MA, Pandit J, Sultana Y, et al. Novel carbopol-based transfersomal gel of 5-fluorouracil for skin cancer treatment: in vitro characterization and in vivo study. Drug Deliv. 2015;22(6):795–802.
   PubMed Web of Science ®Google Scholar
• Raahulan S, Sanapalli BKR, Karri VVSR. Paclitaxel loaded transfersomal vesicular drug delivery for the treatment of melanoma skin cancers. Int J Res Pharm Sci. 2019;10:2891–2897.
   Google Scholar
• Kassab K, El Fadeel DA, Fadel M. Topical photodynamic therapy using transfersomal aluminum phthalocyanine tetrasulfonate: in vitro and in vivo study. Lasers Med Sci. 2013;28(5):1353–1361.
   PubMed Web of Science ®Google Scholar
• Caimi AT, Altube MJ, de Farias MA, et al. Novel imiquimod nanovesicles for topical vaccination. Colloids Surf B Biointerf. 2019;174:536–543.
   PubMed Web of Science ®Google Scholar
• Gonzalez R, Higa LH, Cutrullis R, et al. Archaeosomes made of Halorubrum tebenquichense total polar lipids: a new source of adjuvancy. BMC Biotechnol. 2009;9(1):71–83.
   PubMedGoogle Scholar
• Kates M, Kushwaha SC. Isoprenoids and polar lipids of extreme halophiles. In: Das Sarma F, editor. Archaea: a laboratory manual, Halophiles. New York: Cold Spring Harbor; 1995; p. 35–54.
   Google Scholar
• Böttcher CJF, Van Gent CM, Pries C. A rapid and sensitive sub-micro phosphorus determination. Anal Chim Acta. 1961;24:203–204.
   Web of Science ®Google Scholar
• Higa LH, Schilrreff P, Perez AP, et al. Ultradeformable archaeosomes as new topical adjuvants. Nanomedicine. 2012;8(8):1319–1328.
   PubMed Web of Science ®Google Scholar
• Parra F, Caimi A, Altube MJ, et al. Make It simple: (SR-A1 + TLR7) macrophage targeted NANOarchaeosomes. Front Bioeng Biotechnol. 2018;6(163):163–167.
   PubMedGoogle Scholar
• Algahtani MS, Ahmad MZ, Nourein IH, et al. Co-delivery of imiquimod and curcumin by nanoemugel for improved topical delivery and reduced psoriasis-like skin lesions. Biomolecules. 2020;10(7):968.
   PubMed Web of Science ®Google Scholar
• Khashan KS, Abdulameer FA, Jabir MS, et al. Anticancer activity and toxicity of carbon nanoparticles produced by pulsed laser ablation of graphite in water. Adv Nat Sci Nanosci Nanotechnol. 2020;11(3):035010.
   Google Scholar
• Jerez HE, Altube MJ, Gandola YB, et al. Macrophage apoptosis using alendronate in targeted nanoarchaeosomes. Eur J Pharm Biopharm. 2021;160:42–54.
   PubMed Web of Science ®Google Scholar
• Al Salman HNK, Ali ET, Jabir M, et al. 2 Benzhydrylsulfinyl N hydroxyacetamide Na extracted from fig as a novel cytotoxic and apoptosis inducer in SKOV 3 and AMJ 13 cell lines via P53 and caspase 8 pathway. Eur Food Res Tech. 2020;246(8):1–18.
   Web of Science ®Google Scholar
• Al-Ziaydi AG, Al-Shammari AM, Hamzah MI, et al. Newcastle disease virus suppress glycolysis pathway and induce breast cancer cells death. Virusdisease. 2020;31(3):341–348.
   PubMedGoogle Scholar
• Fisher D, Appenheimer M, Evans S. The two faces of IL-6 in the tumor microenvironment. Sem Immunol. 2014;26(1):38–47.
   PubMed Web of Science ®Google Scholar
• Younus A, Al-Ahmer S, Jabir M. Evaluation of some immunological markers in children with bacterial meningitis caused by Streptococcus pneumoniae. Res J Biotech. 2019;14:131–133.
   Google Scholar
• Telò I, Pescina S, Padula C, et al. Mechanisms of imiquimod skin penetration. Int J Pharm. 2016;511(1):516–523.
   PubMedGoogle Scholar
• Patel GB, Sprott GD. Archaeobacterial ether lipid liposomes (archaeosomes) as novel vaccine and drug delivery systems. Crit Rev Biotechnol. 1999;19(4):317–357.
   PubMed Web of Science ®Google Scholar
• Altube MJ, Selzer S, de Farias MA, et al. Surviving nebulization-induced stress: dexamethasone in pH-sensitive archaeosomes. Nanomedicine. 2016;11(16):2103–2117.
   PubMed Web of Science ®Google Scholar
• Schilrreff P, Simioni YR, Jerez HE, et al. Superoxide dismutase in nano-archaeosomes for targeted delivery to inflammatory macrophages. Colloids Surf B Biointerfaces. 2019;179:479–487.
   PubMed Web of Science ®Google Scholar
• Caimi AT, Parra F, de Farias MA, et al. Topical vaccination with super-stable ready to use nanovesicles. Colloids Surf B Biointerfaces. 2017;152:114–123.
   PubMed Web of Science ®Google Scholar
• Charó N, Jerez H, Tatti S, et al. The anti-inflammatory effect of nanoarchaeosomes on human endothelial cells. Pharmaceutics. 2022;14(4):736.
   PubMed Web of Science ®Google Scholar
• Higa L, Schilrreff P, Briski AM, et al. Bacterioruberin from haloarchaea plus dexamethasone in ultra-small macrophage-targeted nanoparticles as potential intestinal repairing agent. Colloids Surf B. 2020;191:110961.
   PubMed Web of Science ®Google Scholar
• Leclerc E. Chapter 8 - the role of the receptor for advanced glycation end products in malignant melanoma. In: Hayat MA, editor. Brain metastases from primary tumors, volume 3. Epidemiology, biology, and therapy of melanoma and other cancers. Cambridge (MA): Academic Press; 2016. p. 119–132.
   Google Scholar
• Jung J, Kim H, Roh M, et al. The effect of imiquimod on matrix metalloproteinases and tissue inhibitors of metalloproteinases in malignant melanoma cell invasion. Ann Dermatol. 2014;26(3):363–373.
   PubMed Web of Science ®Google Scholar
• Bong A, Bonnekoh B, Franke I, et al. Imiquimod, a topical immune response modifier, in the treatment of cutaneous metastases of malignant melanoma. Dermatol. 2002;205(2):135–138.
   PubMed Web of Science ®Google Scholar
• Broussard L, Howland A, Ryu S, et al. Melanoma cell death mechanisms. Chonnam Med J. 2018;54(3):135.
   PubMedGoogle Scholar
• de Sousa Andrade L, De Lima T, Curi R, et al. Toxicity of fatty acids on murine and human melanoma cell lines. Toxicol In Vitro. 2005;19(4):553–560.
   PubMed Web of Science ®Google Scholar
• Finstad H, Myhrstad M, Heimli H, et al. Multiplication and death-type of leukemia cell lines exposed to very long-chain polyunsaturated fatty acids. Leukemia. 1998;12(6):921–929.
   PubMed Web of Science ®Google Scholar
• Cho J, Lee HJ, Ko HJ, et al. The TLR7 agonist imiquimod induces anti-cancer effects via autophagic cell death and enhances anti-tumoral and systemic immunity during radiotherapy for melanoma. Oncotarget. 2017;8(15):24932–24948.
   PubMedGoogle Scholar
• McLaughlin PJ, Rogosnitzky M, Zagon IS. Inhibition of DNA synthesis in mouse epidermis by topical imiquimod is dependent on opioid receptors. Exp Biol Med. 2010;235(11):1292–1299.
   Web of Science ®Google Scholar
• van Horssen R, Ten Hagen T, Eggermont A. TNF‐α in cancer treatment: molecular insights, antitumor effects, and clinical utility. Oncologist. 2006;11(4):397–408.
   PubMed Web of Science ®Google Scholar
• Weber R, Riester Z, Hüser L, et al. IL-6 regulates CCR5 expression and immunosuppressive capacity of MDSC in murine melanoma. J Immunother Cancer. 2020;8(2):e000949.
   PubMed Web of Science ®Google Scholar
• Kumari N, Dwarakanath B, Das A, et al. Role of interleukin-6 in cancer progression and therapeutic resistance. Tumor Biol. 2016;37(9):11553–11572.
   PubMedGoogle Scholar