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Transdermal drug delivery is an appealing option except for oral and hypodermic administration. With the advancement of skin penetration strategies, various anticancer therapeutics ranging from lipophilic small-molecule drugs to hydrophilic biomacromolecules, can be administered transdermally, offering an optional regimen to treat skin cancers. In addition, the activation of the skin immune systems can also assist the treatment of distal sites. Current approaches on enhancing the transdermal delivery efficacy of anticancer drugs are summarized in this review. We also survey recent advances in micro- and nanotechnology-based transdermal formulations for cancer treatment, such as chemotherapy, gene therapy, immunotherapy, phototherapy and combination therapy. New penetration enhancers, materials, formulations and their hypothesized mechanisms for transdermal delivery are highlighted. Advantages and limitations regarding the state-of-the-art transdermal delivery technologies, as well as future perspective are also discussed.


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Progress in transdermal drug delivery systems for cancer therapy

Show Author's information Tianyue Jiang1Guo Xu1Guojun Chen2,3Yu Zheng1Bingfang He1( )Zhen Gu2,3( )
School of Pharmaceutical Sciences, Nanjing Tech University, Nanjing 211816, China
Department of Bioengineering, University of California, Los Angeles, Los Angeles, CA 90095, USA
Jonsson Comprehensive Cancer Center and California NanoSystems Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA

Abstract

Transdermal drug delivery is an appealing option except for oral and hypodermic administration. With the advancement of skin penetration strategies, various anticancer therapeutics ranging from lipophilic small-molecule drugs to hydrophilic biomacromolecules, can be administered transdermally, offering an optional regimen to treat skin cancers. In addition, the activation of the skin immune systems can also assist the treatment of distal sites. Current approaches on enhancing the transdermal delivery efficacy of anticancer drugs are summarized in this review. We also survey recent advances in micro- and nanotechnology-based transdermal formulations for cancer treatment, such as chemotherapy, gene therapy, immunotherapy, phototherapy and combination therapy. New penetration enhancers, materials, formulations and their hypothesized mechanisms for transdermal delivery are highlighted. Advantages and limitations regarding the state-of-the-art transdermal delivery technologies, as well as future perspective are also discussed.

Keywords: immunotherapy, drug delivery, cancer therapy, combination therapy, chemotherapy, transdermal delivery

References(165)

[1]
Prausnitz, M. R.; Langer, R. Transdermal drug delivery. Nat. Biotechnol. 2008, 26, 1261-1268.
[2]
Di Meglio, P.; Perera, G. K.; Nestle, F. O. The multitasking organ: Recent insights into skin immune function. Immunity 2011, 35, 857-869.
[3]
Menon, G. K.; Cleary, G. W.; Lane, M. E. The structure and function of the stratum corneum. Int. J. Pharm. 2012, 435, 3-9.
[4]
Roberts, M. S.; Mohammed, Y.; Pastore, M. N.; Namjoshi, S.; Yousef, S.; Alinaghi, A.; Haridass, I. N.; Abd, E.; Leite-Silva, V. R.; Benson, H. A. E. et al. Topical and cutaneous delivery using nanosystems. J. Control. Release 2017, 247, 86-105.
[5]
Neubert, R. H. H. Potentials of new nanocarriers for dermal and transdermal drug delivery. Eur. J. Pharm. Biopharm. 2011, 77, 1-2.
[6]
Lu, Y.; Aimetti, A. A.; Langer, R.; Gu, Z. Bioresponsive materials. Nat. Rev. Mater. 2016, 2, 16075.
[7]
Lee, J. S.; Hwang, Y.; Oh, H.; Kim, S.; Kim, J. H.; Lee, J. H.; Shin, Y. C.; Tae, G.; Choi, W. I. A novel chitosan nanocapsule for enhanced skin penetration of cyclosporin A and effective hair growth in vivo. Nano Res. 2019, 12, 3024-3030.
[8]
Williams, A. C.; Barry, B. W. Penetration enhancers. Adv. Drug Deliv. Rev. 2012, 64, 128-137.
[9]
Marwah, H.; Garg, T.; Goyal, A. K.; Rath, G. Permeation enhancer strategies in transdermal drug delivery. Drug Deliv. 2016, 23, 564-578.
[10]
Karande, P.; Jain, A.; Ergun, K.; Kispersky, V.; Mitragotri, S. Design principles of chemical penetration enhancers for transdermal drug delivery. Proc. Natl. Acad. Sci. USA 2005, 102, 4688-4693.
[11]
Ruan, R. Q.; Chen, M.; Zou, L. L.; Wei, P. F.; Liu, J. J.; Ding, W. P.; Wen, L. P. Recent advances in peptides for enhancing transdermal macromolecular drug delivery. Ther. Deliv. 2016, 7, 89-100.
[12]
Seong, J. S.; Yun, M. E.; Park, S. N. Surfactant-stable and pH-sensitive liposomes coated with N-succinyl-chitosan and chitooligosaccharide for delivery of quercetin. Carbohydr. Polym. 2018, 181, 659-667.
[13]
Rai, V. K.; Mishra, N.; Yadav, K. S.; Yadav, N. P. Nanoemulsion as pharmaceutical carrier for dermal and transdermal drug delivery: Formulation development, stability issues, basic considerations and applications. J. Control. Release 2018, 270, 203-225.
[14]
Yang, Y.; Pearson, R. M.; Lee, O.; Lee, C. W.; Chatterton, R. T. Jr.; Khan, S. A.; Hong, S. Dendron-based micelles for topical delivery of endoxifen: A potential chemo-preventive medicine for breast cancer. Adv. Funct. Mater. 2014, 24, 2442-2449.
[15]
Lee, H.; Lee, J. H.; Kim, J.; Mun, J. H.; Chung, J.; Koo, H.; Kim, C.; Yun, S. H.; Hahn, S. K. Hyaluronate-gold nanorod/DR5 antibody complex for noninvasive theranosis of skin cancer. ACS Appl. Mater. Interfaces 2016, 8, 32202-32210.
[16]
Siu, K. S.; Chen, D.; Zheng, X. F.; Zhang, X. S.; Johnston, N.; Liu, Y. L.; Yuan, K.; Koropatnick, J.; Gillies, E. R.; Min, W. P. Non-covalently functionalized single-walled carbon nanotube for topical siRNA delivery into melanoma. Biomaterials 2014, 35, 3435-3442.
[17]
Prausnitz, M. R. A practical assessment of transdermal drug delivery by skin electroporation. Adv. Drug Deliv. Rev. 1999, 35, 61-76.
[18]
Lee, H.; Choi, T. K.; Lee, Y. B.; Cho, H. R.; Ghaffari, R.; Wang, L.; Choi, H. J.; Chung, T. D.; Lu, N. S.; Hyeon, T. et al. A graphene-based electrochemical device with thermoresponsive microneedles for diabetes monitoring and therapy. Nat. Nanotechnol. 2016, 11, 566-572.
[19]
Murthy, S. N.; Sammeta, S. M.; Bowers, C. Magnetophoresis for enhancing transdermal drug delivery: Mechanistic studies and patch design. J. Control. Release 2010, 148, 197-203.
[20]
Siegel, R. L.; Miller, K. D.; Jemal, A. Cancer statistics, 2019. CA: A Cancer J. Clin. 2019, 69, 7-34.
[21]
Finger, P. T.; Milner, M. S.; McCormick, S. A. Topical chemotherapy for conjunctival melanoma. Br. J. Ophthalmol. 1993, 77, 751-753.
[22]
Kris, M. G.; Hellmann, M. D.; Chaft, J. E. Chemotherapy for lung cancers: Here to stay. Am. Soc. Clin. Oncol. Educ. Book 2014, 34, e375-e380.
[23]
Ethun, C. G.; Bilen, M. A.; Jani, A. B.; Maithel, S. K.; Ogan, K.; Master, V. A. Frailty and cancer: Implications for oncology surgery, medical oncology, and radiation oncology. CA: A Cancer J. Clin. 2017, 67, 362-377.
[24]
Citrin, D. E. Recent developments in radiotherapy. N. Engl. J. Med. 2017, 377, 1065-1075.
[25]
Buscail, L.; Bournet, B.; Vernejoul, F.; Cambois, G.; Lulka, H.; Hanoun, N.; Dufresne, M.; Meulle, A.; Vignolle-Vidoni, A.; Ligat, L. et al. First-in-man phase 1 clinical trial of gene therapy for advanced pancreatic cancer: Safety, biodistribution, and preliminary clinical findings. Mol. Ther. 2015, 23, 779-789.
[26]
Portnow, J.; Synold, T. W.; Badie, B.; Tirughana, R.; Lacey, S. F.; D’Apuzzo, M.; Metz, M. Z.; Najbauer, J.; Bedell, V.; Vo, T. et al. Neural stem cell-based anticancer gene therapy: A first-in-human study in recurrent high-grade glioma patients. Clin. Cancer Res. 2017, 23, 2951-2960.
[27]
Kirkwood, J. M.; Butterfield, L. H.; Tarhini, A. A.; Zarour, H.; Kalinski, P.; Ferrone, S. Immunotherapy of cancer in 2012. CA: A Cancer J. Clin. 2012, 62, 309-335.
[28]
Knuth, A.; Jäger, D.; Jäger, E. Cancer immunotherapy in clinical oncology. Cancer Chemother. Pharmacol. 2000, 46, S46-S51.
[29]
Wang, C.; Ye, Y. Q.; Hu, Q. Y.; Bellotti, A.; Gu, Z. Tailoring biomaterials for cancer immunotherapy: Emerging trends and future outlook. Adv. Mater. 2017, 29, 1606036.
[30]
Xu, X.; Li, T.; Shen, S. Y.; Wang, J. Q.; Abdou, P.; Gu, Z.; Mo, R. Advances in engineering cells for cancer immunotherapy. Theranostics 2019, 9, 7889-7905.
[31]
Ye, Y. Q.; Wang, C.; Zhang, X. D.; Hu, Q. Y.; Zhang, Y. Q.; Liu, Q.; Wen, D.; Milligan, J.; Bellotti, A.; Huang, L. et al. A melanin-mediated cancer immunotherapy patch. Sci. Immunol. 2017, 2, eaan5692.
[32]
Beack, S.; Kong, W. H.; Jung, H. S.; Do, I. H.; Han, S.; Kim, H.; Kim, K. S.; Yun, S. H.; Hahn, S. K. Photodynamic therapy of melanoma skin cancer using carbon dot-chlorin e6-hyaluronate conjugate. Acta Biomater. 2015, 26, 295-305.
[33]
Gu, Z.; Chen, X. Y. Towards enhancing skin drug delivery. Adv. Drug Deliv. Rev. 2018, 127, 1-2.
[34]
van der Maaden, K.; Heuts, J.; Camps, M.; Pontier, M.; Terwisscha van Scheltinga, A.; Jiskoot, W.; Ossendorp, F.; Bouwstra, J. Hollow microneedle-mediated micro-injections of a liposomal HPV E743-63 synthetic long peptide vaccine for efficient induction of cytotoxic and T-helper responses. J. Control. Release 2018, 269, 347-354.
[35]
Mathers, A. R.; Larregina, A. T. Professional antigen-presenting cells of the skin. Immunol. Res. 2006, 36, 127-136.
[36]
Zhao, Z. M.; Ukidve, A.; Dasgupta, A.; Mitragotri, S. Transdermal immunomodulation: Principles, advances and perspectives. Adv. Drug Deliv. Rev. 2018, 127, 3-19.
[37]
Walter, K.; Kurz, H. Binding of drugs to human skin: Influencing factors and the role of tissue lipids. J. Pharm. Pharmacol. 1988, 40, 689-693.
[38]
Prausnitz, M. R.; Elias, P. M.; Franz, T. J.; Schmuth, M.; Tsai, J.-C.; Menon, G. K.; Holleran, W. M.; Feingold, K. R. Skin barrier and transdermal drug delivery. Dermatology 2012, 3, 2065-2073.
[39]
McGrath, J. A.; Eady, R. A. J.; Pope, F. M. Anatomy and organization of human skin. In Rook’s Textbook of Dermatology, 7th ed.; Burns, T.; Breathnach, S.; Cox, N.; Griffiths, N., Eds.; Blackwell: Hoboken, 2004.
[40]
Christophers, E. Cellular architecture of the stratum corneum. J. Invest. Dermatol. 1971, 56, 165-169.
[41]
Behl, C. R.; Flynn, G. L.; Kurihara, T.; Harper, N.; Smith, W.; Higuchi, W. I.; Ho, N. F.; Pierson, C. L. Hydration and percutaneous absorption: I. Influence of hydration on alkanol permeation through hairless mouse skin. J. Invest. Dermatol. 1980, 75, 346-352.
[42]
Jhawat, V. C.; Saini, V.; Kamboj, S.; Maggon, N. Transdermal drug delivery systems: Approaches and advancements in drug absorption through skin. Int. J. Pharm. Sci. Rev. Res. 2013, 20, 47-56.
[43]
Allen, L. Jr.; Ansel, H. C. Ansel’s Pharmaceutical Dosage Forms and Drug Delivery Systems, 10th ed.; Lippincott Williams & Wilkins: Baltimore, MD, 2013.
[44]
Ye, Y. Q.; Wang, J. Q.; Sun, W. J.; Bomba, H. N.; Gu, Z. Topical and transdermal nanomedicines for cancer therapy. In Nanotheranostics for Cancer Applications; Rai, P.; Morris, S. A., Eds.; Springer: Cham, 2019; pp 231-251.
[45]
Lipinski, C. A.; Lombardo, F.; Dominy, B. W.; Feeney, P. J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 1997, 23, 3-25.
[46]
Swain, S.; Beg, S.; Singh, A.; Patro, C. N.; Rao, M. E. B. Advanced techniques for penetration enhancement in transdermal drug delivery system. Curr. Drug Deliv. 2011, 8, 456-473.
[47]
Benson, H. A. E. Transdermal drug delivery: Penetration enhancement techniques. Curr. Drug Deliv. 2005, 2, 23-33.
[48]
Dragicevic, N.; Maibach, H. Combined use of nanocarriers and physical methods for percutaneous penetration enhancement. Adv. Drug Deliv. Rev. 2018, 127, 58-84.
[49]
Dias, M.; Naik, A.; Guy, R. H.; Hadgraft, J.; Lane, M. E. In vivo infrared spectroscopy studies of alkanol effects on human skin. Eur. J. Pharm. Biopharm. 2008, 69, 1171-1175.
[50]
Lane, M. E. Skin penetration enhancers. Int. J. Pharm. 2013, 447, 12-21.
[51]
Barry, B. W. Mode of action of penetration enhancers in human skin. J. Control. Release 1987, 6, 85-97.
[52]
Barry, B. W. Novel mechanisms and devices to enable successful transdermal drug delivery. Eur. J. Pharm. Sci. 2001, 14, 101-114.
[53]
Haque, T.; Talukder, M. M. U. Chemical enhancer: A simplistic way to modulate barrier function of the stratum corneum. Adv. Pharm. Bull. 2018, 8, 169-179.
[54]
Trommer, H.; Neubert, R. H. H. Overcoming the stratum corneum: The modulation of skin penetration. Skin Pharmacol. Physiol. 2006, 19, 106-121.
[55]
Moghadam, S. H.; Saliaj, E.; Wettig, S. D.; Dong, C.; Ivanova, M. V.; Huzil, J. T.; Foldvari, M. Effect of chemical permeation enhancers on stratum corneum barrier lipid organizational structure and interferon alpha permeability. Mol. Pharmaceutics 2013, 10, 2248-2260.
[56]
Tupker, R. A.; Pinnagoda, J.; Nater, J. P. The transient and cumulative effect of sodium lauryl sulphate on the epidermal barrier assessed by transepidermal water loss: Inter-individual variation. Acta Derm. Venereol. 1990, 70, 1-5.
[57]
Ashtikar, M.; Nagarsekar, K.; Fahr, A. Transdermal delivery from liposomal formulations-evolution of the technology over the last three decades. J. Control. Release 2016, 242, 126-140.
[58]
Candan, G.; Michiue, H.; Ishikawa, S.; Fujimura, A.; Hayashi, K.; Uneda, A.; Mori, A.; Ohmori, I.; Nishiki, T.; Matsui, H. et al. Combining poly-arginine with the hydrophobic counter-anion 4-(1-pyrenyl)-butyric acid for protein transduction in transdermal delivery. Biomaterials 2012, 33, 6468-6475.
[59]
Kim, Y. C.; Ludovice, P. J.; Prausnitz, M. R. Transdermal delivery enhanced by magainin pore-forming peptide. J. Control. Release 2007, 122, 375-383.
[60]
Cohen-Avrahami, M.; Libster, D.; Aserin, A.; Garti, N. Sodium diclofenac and cell-penetrating peptides embedded in hii mesophases: Physical characterization and delivery. J. Phys. Chem. B 2011, 115, 10189-10197.
[61]
Kumar, S.; Sahdev, P.; Perumal, O.; Tummala, H. Identification of a novel skin penetration enhancement peptide by phage display peptide library screening. Mol. Pharmaceutics 2012, 9, 1320-1330.
[62]
Johnson, L. N.; Cashman, S. M.; Read, S. P.; Kumar-Singh, R. Cell penetrating peptide pod mediates delivery of recombinant proteins to retina, cornea and skin. Vision Res. 2010, 50, 686-697.
[63]
Chen, Y. P.; Shen, Y. Y.; Guo, X.; Zhang, C. S.; Yang, W. J.; Ma, M. L.; Liu, S.; Zhang, M. B.; Wen, L. P. Transdermal protein delivery by a coadministered peptide identified via phage display. Nat. Biotechnol. 2006, 24, 455-460.
[64]
Ruan, R. Q.; Wang, S. S.; Wang, C. L.; Zhang, L.; Zhang, Y. J.; Zhou, W.; Ding, W. P.; Jin, P. P.; Wei, P. F.; Man, N. et al. Transdermal delivery of human epidermal growth factor facilitated by a peptide chaperon. Eur. J. Med. Chem. 2013, 62, 405-409.
[65]
Carmichael, N. M. E.; Dostrovsky, J. O.; Charlton, M. P. Peptide-mediated transdermal delivery of botulinum neurotoxin type a reduces neurogenic inflammation in the skin. Pain 2010, 149, 316-324.
[66]
Chang, M. M.; Li, X. H.; Sun, Y. M.; Cheng, F.; Wang, Q.; Xie, X. H.; Zhao, W. J.; Tian, X. Effect of cationic cyclopeptides on transdermal and transmembrane delivery of insulin. Mol. Pharmaceutics 2013, 10, 951-957.
[67]
Chen, M.; Gupta, V.; Anselmo, A. C.; Muraski, J. A.; Mitragotri, S. Topical delivery of hyaluronic acid into skin using space-peptide carriers. J. Control. Release 2014, 173, 67-74.
[68]
Vij, M.; Natarajan, P.; Pattnaik, B. R.; Alam, S.; Gupta, N.; Santhiya, D.; Sharma, R.; Singh, A.; Ansari, K. M.; Gokhale, R. S. et al. Non-invasive topical delivery of plasmid DNA to the skin using a peptide carrier. J. Control. Release 2016, 222, 159-168.
[69]
Hsu, T.; Mitragotri, S. Delivery of siRNA and other macromolecules into skin and cells using a peptide enhancer. Proc. Natl. Acad. Sci. USA 2011, 108, 15816-15821.
[70]
Chen, M.; Zakrewsky, M.; Gupta, V.; Anselmo, A. C.; Slee, D. H.; Muraski, J. A.; Mitragotri, S. Topical delivery of siRNA into skin using SPACE-peptide carriers. J. Control. Release 2014, 179, 33-41.
[71]
Jiang, T. Y.; Wang, T.; Li, T.; Ma, Y. D.; Shen, S. Y.; He, B. F.; Mo, R. Enhanced transdermal drug delivery by transfersome-embedded oligopeptide hydrogel for topical chemotherapy of melanoma. ACS Nano 2018, 12, 9693-9701.
[72]
Niu, J.; Chu, Y.; Huang, Y. F.; Chong, Y. S.; Jiang, Z. H.; Mao, Z. W.; Peng, L. H.; Gao, J. Q. Transdermal gene delivery by functional peptide-conjugated cationic gold nanoparticle reverses the progression and metastasis of cutaneous melanoma. ACS Appl. Mater. Interfaces 2017, 9, 9388-9401.
[73]
Kumar, S.; Zakrewsky, M.; Chen, M.; Menegatti, S.; Muraski, J. A.; Mitragotri, S. Peptides as skin penetration enhancers: Mechanisms of action. J. Control. Release 2015, 199, 168-178.
[74]
Zhou, X. L.; Hao, Y.; Yuan, L. P.; Pradhan, S.; Shrestha, K.; Pradhan, O.; Liu, H. J.; Li, W. Nano-formulations for transdermal drug delivery: A review. Chin. Chem. Lett. 2018, 29, 1713-1724.
[75]
Zou, L. L.; Ding, W. P.; Zhang, Y. Y.; Cheng, S. H.; Li, F. F.; Ruan, R. Q.; Wei, P. F.; Qiu, B. S. Peptide-modified vemurafenib-loaded liposomes for targeted inhibition of melanoma via the skin. Biomaterials 2018, 182, 1-12.
[76]
Wu, J.; Paudel, K. S.; Strasinger, C.; Hammell, D.; Stinchcomb, A. L.; Hinds, B. J. Programmable transdermal drug delivery of nicotine using carbon nanotube membranes. Proc. Natl. Acad. Sci. USA 2010, 107, 11698-11702.
[77]
Labala, S.; Mandapalli, P. K.; Kurumaddali, A.; Venuganti, V. V. K. Layer-by-layer polymer coated gold nanoparticles for topical delivery of imatinib mesylate to treat melanoma. Mol. Pharmaceutics 2015, 12, 878-888.
[78]
Desai, P.; Patlolla, R. R.; Singh, M. Interaction of nanoparticles and cell-penetrating peptides with skin for transdermal drug delivery. Mol. Membr. Biol. 2010, 27, 247-259.
[79]
Labouta, H. I.; El-Khordagui, L. K.; Kraus, T.; Schneider, M. Mechanism and determinants of nanoparticle penetration through human skin. Nanoscale 2011, 3, 4989-4999.
[80]
Raju, G.; Katiyar, N.; Vadukumpully, S.; Shankarappa, S. A. Penetration of gold nanoparticles across the stratum corneum layer of thick-skin. J. Dermatol. Sci. 2018, 89, 146-154.
[81]
Rancan, F.; Gao, Q.; Graf, C.; Troppens, S.; Hadam, S.; Hackbarth, S.; Kembuan, C.; Blume-Peytavi, U.; Rühl, E.; Lademann, J. et al. Skin penetration and cellular uptake of amorphous silica nanoparticles with variable size, surface functionalization, and colloidal stability. ACS Nano 2012, 6, 6829-6842.
[82]
Wiraja, C.; Zhu, Y.; Lio, D. C. S.; Yeo, D. C.; Xie, M.; Fang, W. N.; Li, Q.; Zheng, M. J.; Van Steensel, M.; Wang, L. H. et al. Framework nucleic acids as programmable carrier for transdermal drug delivery. Nat. Commun. 2019, 10, 1147.
[83]
Nummelin, S.; Kommeri, J.; Kostiainen, M. A.; Linko, V. Evolution of structural DNA nanotechnology. Adv. Mater. 2018, 30, 1703721.
[84]
Seeman, N. C. Nucleic acid junctions and lattices. J. Theor. Biol. 1982, 99, 237-247.
[85]
Mathur, D.; Medintz, I. L. The growing development of DNA nanostructures for potential healthcare-related applications. Adv. Healthc. Mater. 2019, 8, 1801546.
[86]
Shah, S. M.; Ashtikar, M.; Jain, A. S.; Makhija, D. T.; Nikam, Y.; Gude, R. P.; Steiniger, F.; Jagtap, A. A.; Nagarsenker, M. S.; Fahr, A. LeciPlex, invasomes, and liposomes: A skin penetration study. Int. J. Pharm. 2015, 490, 391-403.
[87]
Dragicevic-Curic, N.; Gräfe, S.; Gitter, B.; Winter, S.; Fahr, A. Surface charged temoporfin-loaded flexible vesicles: In vitro skin penetration studies and stability. Int. J. Pharm. 2010, 384, 100-108.
[88]
Kong, M.; Hou, L.; Wang, J.; Feng, C.; Liu, Y.; Cheng, X. J.; Chen, X. G. Enhanced transdermal lymphatic drug delivery of hyaluronic acid modified transfersomes for tumor metastasis therapy. Chem. Commun. 2015, 51, 1453-1456.
[89]
Jung, H. S.; Kong, W. H.; Sung, D. K.; Lee, M. Y.; Beack, S. E.; Keum, D. H.; Kim, K. S.; Yun, S. H.; Hahn, S. K. Nanographene oxide-hyaluronic acid conjugate for photothermal ablation therapy of skin cancer. ACS Nano 2014, 8, 260-268.
[90]
Alexander, A.; Dwivedi, S.; Ajazuddin; Giri, T. K.; Saraf, S.; Saraf, S.; Tripathi, D. K. Approaches for breaking the barriers of drug permeation through transdermal drug delivery. J. Control. Release 2012, 164, 26-40.
[91]
Yang, G.; Chen, Q.; Wen, D.; Chen, Z. W.; Wang, J. Q.; Chen, G. J.; Wang, Z. J.; Zhang, X. D.; Zhang, Y. Q.; Hu, Q. Y. et al. A therapeutic microneedle patch made from hair-derived keratin for promoting hair regrowth. ACS Nano 2019, 13, 4354-4360.
[92]
Ye, Y. Q.; Yu, J. C.; Wen, D.; Kahkoska, A. R.; Gu, Z. Polymeric microneedles for transdermal protein delivery. Adv. Drug Deliv. Rev. 2018, 127, 106-118.
[93]
Tomoda, K.; Terashima, H.; Suzuki, K.; Inagi, T.; Terada, H.; Makino, K. Enhanced transdermal delivery of indomethacin using combination of PLGA nanoparticles and iontophoresis in vivo. Colloids Surf. B: Biointerfaces 2012, 92, 50-54.
[94]
Wu, C. S.; Jiang, P.; Li, W.; Guo, H. Y.; Wang, J.; Chen, J.; Prausnitz, M. R.; Wang, Z. L. Self-powered iontophoretic transdermal drug delivery system driven and regulated by biomechanical motions. Adv. Funct. Mater. 2019, 30, 1907378.
[95]
Wang, Y. P.; Thakur, R.; Fan, Q. X.; Michniak, B. Transdermal iontophoresis: Combination strategies to improve transdermal iontophoretic drug delivery. Eur. J. Pharm. Biopharm. 2005, 60, 179-191.
[96]
Denet, A. R.; Vanbever, R.; Préat, V. Skin electroporation for transdermal and topical delivery. Adv. Drug Deliv. Rev. 2004, 56, 659-674.
[97]
Wenande, E.; Tam, J.; Bhayana, B.; Schlosser, S. K.; Ishak, E.; Farinelli, W. A.; Chlopik, A.; Hoang, M. P.; Pinkhasov, O. R.; Caravan, P. et al. Laser-assisted delivery of synergistic combination chemotherapy in in vivo skin. J. Control. Release 2018, 275, 242-253.
[98]
Svenskaya, Y. I.; Genina, E. A.; Parakhonskiy, B. V.; Lengert, E. V.; Talnikova, E. E.; Terentyuk, G. S.; Utz, S. R.; Gorin, D. A.; Tuchin, V. V.; Sukhorukov, G. B. A simple non-invasive approach toward efficient transdermal drug delivery based on biodegradable particulate system. ACS Appl. Mater. Interfaces 2019, 11, 17270-17282.
[99]
Azagury, A.; Khoury, L.; Enden, G.; Kost, J. Ultrasound mediated transdermal drug delivery. Adv. Drug Deliv. Rev. 2014, 72, 127-143.
[100]
Polat, B. E.; Hart, D.; Langer, R.; Blankschtein, D. Ultrasound-mediated transdermal drug delivery: Mechanisms, scope, and emerging trends. J. Control. Release 2011, 152, 330-348.
[101]
Kim, Y. C.; Park, J. H.; Prausnitz, M. R. Microneedles for drug and vaccine delivery. Adv. Drug Deliv. Rev. 2012, 64, 1547-1568.
[102]
Prausnitz, M. R. Microneedles for transdermal drug delivery. Adv. Drug Deliv. Rev. 2004, 56, 581-587.
[103]
Yu, J. C.; Zhang, Y. Q.; Ye, Y. Q.; DiSanto, R.; Sun, W. J.; Ranson, D.; Ligler, F. S.; Buse, J. B.; Gu, Z. Microneedle-array patches loaded with hypoxia-sensitive vesicles provide fast glucose-responsive insulin delivery. Proc. Natl. Acad. Sci. USA 2015, 112, 8260-8265.
[104]
Zhang, Y. Q.; Yu, J. C.; Kahkoska, A. R.; Wang, J. Q.; Buse, J. B.; Gu, Z. Advances in transdermal insulin delivery. Adv. Drug Deliv. Revi. 2019, 139, 51-70.
[105]
Rzhevskiy, A. S.; Singh, T. R. R.; Donnelly, R. F.; Anissimov, Y. G. Microneedles as the technique of drug delivery enhancement in diverse organs and tissues. J. Control. Release 2018, 270, 184-202.
[106]
Huang, Y. Z.; Park, Y. S.; Moon, C.; David, A. E.; Chung, H. S.; Yang, V. C. Synthetic skin-permeable proteins enabling needleless immunization. Angew. Chem., Int. Ed. 2010, 49, 2724-2727.
[107]
Kalia, Y. N.; Naik, A.; Garrison, J.; Guy, R. H. Iontophoretic drug delivery. Adv. Drug Deliv. Rev. 2004, 56, 619-658.
[108]
Petrilli, R.; Eloy, J. O.; Saggioro, F. P.; Chesca, D. L.; de Souza, M. C.; Dias, M. V. S.; daSilva, L. L. P.; Lee, R. J.; Lopez, R. F. V. Skin cancer treatment effectiveness is improved by iontophoresis of EGFR-targeted liposomes containing 5-FU compared with subcutaneous injection. J. Control. Release 2018, 283, 151-162.
[109]
Prausnitz, M. R.; Bose, V. G.; Langer, R.; Weaver, J. C. Electroporation of mammalian skin: A mechanism to enhance transdermal drug delivery. Proc. Natl. Acad. Sci. 1993, 90, 10504-10508.
[110]
Ibrahim, O.; Wenande, E.; Hogan, S.; Arndt, K. A.; Haedersdal, M.; Dover, J. S. Challenges to laser-assisted drug delivery: Applying theory to clinical practice. Lasers Surg. Med. 2018, 50, 20-27.
[111]
Zhang, Y. Q.; Yu, J. C.; Bomba, H. N.; Zhu, Y.; Gu, Z. Mechanical force-triggered drug delivery. Chem. Rev. 2016, 116, 12536-12563.
[112]
Di, J.; Yu, J. C.; Wang, Q.; Yao, S. S.; Suo, D. J.; Ye, Y. Q.; Pless, M.; Zhu, Y.; Jing, Y.; Gu, Z. Ultrasound-triggered noninvasive regulation of blood glucose levels using microgels integrated with insulin nanocapsules. Nano Res. 2017, 10, 1393-1402.
[113]
Mangalathillam, S.; Rejinold, N. S.; Nair, A.; Lakshmanan, V. K.; Nair, S. V.; Jayakumar, R. Curcumin loaded chitin nanogels for skin cancer treatment via the transdermal route. Nanoscale 2012, 4, 239-250.
[114]
Lin, Y. L.; Chen, C. H.; Wu, H. Y.; Tsai, N. M.; Jian, T. Y.; Chang, Y. C.; Lin, C. H.; Wu, C. H.; Hsu, F. T.; Leung, T. K. et al. Inhibition of breast cancer with transdermal tamoxifen-encapsulated lipoplex. J. Nanobiotechnol. 2016, 14, 11.
[115]
Moses, M. A.; Brem, H.; Langer, R. Advancing the field of drug delivery: Taking aim at cancer. Cancer Cell 2003, 4, 337-341.
[116]
Jiang, T. Y.; Mo, R.; Bellotti, A.; Zhou, J. P.; Gu, Z. Gel-liposome-mediated co-delivery of anticancer membrane-associated proteins and small-molecule drugs for enhanced therapeutic efficacy. Adv. Funct. Mater. 2014, 24, 2295-2304.
[117]
Jiang, T. Y.; Zhang, Z. H.; Zhang, Y. L.; Lv, H. X.; Zhou, J. P.; Li, C. C.; Hou, L. L.; Zhang, Q. Dual-functional liposomes based on ph-responsive cell-penetrating peptide and hyaluronic acid for tumor-targeted anticancer drug delivery. Biomaterials 2012, 33, 9246-9258.
[118]
Rao, Y. F.; Chen, W.; Liang, X. G.; Huang, Y. Z.; Miao, J.; Liu, L.; Lou, Y.; Zhang, X. G.; Wang, B.; Tang, R. K. et al. Epirubicin-loaded superparamagnetic iron-oxide nanoparticles for transdermal delivery: Cancer therapy by circumventing the skin barrier. Small 2015, 11, 239-247.
[119]
Yang, H. J.; Wu, X. J.; Zhou, Z. Z.; Chen, X. G.; Kong, M. Enhanced transdermal lymphatic delivery of doxorubicin via hyaluronic acid based transfersomes/microneedle complex for tumor metastasis therapy. Int. J. Biol. Macromol. 2019, 125, 9-16.
[120]
Luo, Z. M.; Sun, W. J.; Fang, J.; Lee, K.; Li, S.; Gu, Z.; Dokmeci, M. R.; Khademhosseini, A. Biodegradable gelatin methacryloyl microneedles for transdermal drug delivery. Adv. Healthc. Mater. 2019, 8, 1801054.
[121]
Ahmed, K. S.; Shan, X. T.; Mao, J.; Qiu, L. P.; Chen, J. H. Derma roller® microneedles-mediated transdermal delivery of doxorubicin and celecoxib co-loaded liposomes for enhancing the anticancer effect. Mater. Sci. Eng. C 2019, 99, 1448-1458.
[122]
Ma, L. L.; Wang, X. Y.; Wu, J. L.; Zhang, D. D.; Zhang, L.; Song, X. R.; Hong, H. Y.; He, C. L.; Mo, X. M.; Wu, S. F. et al. Polyethylenimine and sodium cholate-modified ethosomes complex as multidrug carriers for the treatment of melanoma through transdermal delivery. Nanomedicine 2019, 14, 2395-2408.
[123]
Anirudhan, T. S.; Nair, A. S.; Bino, S. J. Nanoparticle assisted solvent selective transdermal combination therapy of curcumin and 5-flurouracil for efficient cancer treatment. Carbohydr. Polym. 2017, 173, 131-142.
[124]
Liu, J. B.; Wang, Z. G.; Zhao, S.; Ding, B. Q. Multifunctional nucleic acid nanostructures for gene therapies. Nano Res. 2018, 11, 5017-5027.
[125]
Zakrewsky, M.; Kumar, S.; Mitragotri, S. Nucleic acid delivery into skin for the treatment of skin disease: Proofs-of-concept, potential impact, and remaining challenges. J. Control. Release 2015, 219, 445-456.
[126]
Chen, X. F. Current and future technological advances in transdermal gene delivery. Adv. Drug Deliv. Rev. 2018, 127, 85-105.
[127]
Pan, J. T.; Ruan, W. Y.; Qin, M.; Long, Y. M.; Wan, T.; Yu, K. Y.; Zhai, Y. H.; Wu, C. B.; Xu, Y. H. Intradermal delivery of STAT3 siRNA to treat melanoma via dissolving microneedles. Sci. Rep. 2018, 8, 1117.
[128]
Ruan, R. Q.; Chen, M.; Sun, S. J.; Wei, P. F.; Zou, L. L.; Liu, J.; Gao, D. Y.; Wen, L. P.; Ding, W. P. Topical and targeted delivery of siRNAs to melanoma cells using a fusion peptide carrier. Sci. Rep. 2016, 6, 29159.
[129]
Li, X. F.; Xu, Q.; Zhang, P.; Zhao, X.; Wang, Y. X. Cutaneous microenvironment responsive microneedle patch for rapid gene release to treat subdermal tumor. J. Control. Release 2019, 314, 72-80.
[130]
Khalil, D. N.; Smith, E. L.; Brentjens, R. J.; Wolchok, J. D. The future of cancer treatment: Immunomodulation, CARs and combination immunotherapy. Nat. Rev. Clin. Oncol. 2016, 13, 273-290.
[131]
Bluestone, J. A.; Bour-Jordan, H. Current and future immunomodulation strategies to restore tolerance in autoimmune diseases. Cold Spring Harb. Perspect. Biol. 2012, 4, a007542.
[132]
Dunn, G. P.; Bruce, A. T.; Ikeda, H.; Old, L. J.; Schreiber, R. D. Cancer immunoediting: From immunosurveillance to tumor escape. Nat. Immunol. 2002, 3, 991-998.
[133]
Neelapu, S. S.; Tummala, S.; Kebriaei, P.; Wierda, W.; Gutierrez, C.; Locke, F. L.; Komanduri, K. V.; Lin, Y.; Jain, N.; Daver, N. et al. Chimeric antigen receptor T-cell therapy-assessment and management of toxicities. Nat. Rev. Clin. Oncol. 2018, 15, 47-62.
[134]
Hargadon, K. M.; Johnson, C. E.; Williams, C. J. Immune checkpoint blockade therapy for cancer: An overview of FDA-approved immune checkpoint inhibitors. Int. Immunopharmacol. 2018, 62, 29-39.
[135]
Jäger, E.; Jäger, D.; Knuth, A. Clinical cancer vaccine trials. Curr. Opin. Immunol. 2002, 14, 178-182.
[136]
Cheever, M. A.; Higano, C. S. Provenge (sipuleucel-t) in prostate cancer: The first FDA-approved therapeutic cancer vaccine. Clin. Cancer Res. 2011, 17, 3520-3526.
[137]
Haniffa, M.; Gunawan, M.; Jardine, L. Human skin dendritic cells in health and disease. J. Dermatol. Sci. 2015, 77, 85-92.
[138]
Riley, R. S.; June, C. H.; Langer, R.; Mitchell, M. J. Delivery technologies for cancer immunotherapy. Nat. Rev. Drug Discovery 2019, 18, 175-196.
[139]
Yu, J. C.; Zhang, Y. Q.; Kahkoska, A. R.; Gu, Z. Bioresponsive transcutaneous patches. Curr. Opin. Biotechnol. 2017, 48, 28-32.
[140]
Wang, C.; Ye, Y. Q.; Hochu, G. M.; Sadeghifar, H.; Gu, Z. Enhanced cancer immunotherapy by microneedle patch-assisted delivery of anti-PD1 antibody. Nano Lett. 2016, 16, 2334-2340.
[141]
Ye, Y. Q.; Wang, J. Q.; Hu, Q. Y.; Hochu, G. M.; Xin, H. J.; Wang, C.; Gu, Z.; Ye, Y.; Wang, J.; Hu, Q. et al. Synergistic transcutaneous immunotherapy enhances antitumor immune responses through delivery of checkpoint inhibitors. ACS Nano 2016, 10, 8956-8963.
[142]
Tan, L.; Sun, X. Recent advances in mRNA vaccine delivery. Nano Res. 2018, 11, 5338-5354.
[143]
Zhao, Y.; Guo, Y. G.; Tang, L. Engineering cancer vaccines using stimuli-responsive biomaterials. Nano Res. 2018, 11, 5355-5371.
[144]
Lee, K.; Kim, M.; Seo, Y.; Lee, H. Development of mRNA vaccines and their prophylactic and therapeutic applications. Nano Res. 2018, 11, 5173-5192.
[145]
Palena, C.; Abrams, S. I.; Schlom, J.; Hodge, J. W. Cancer vaccines: Preclinical studies and novel strategies. Adv. Cancer Res. 2006, 95, 115-145.
[146]
Wakabayashi, R.; Kono, H.; Kozaka, S.; Tahara, Y.; Kamiya, N.; Goto, M. Transcutaneous codelivery of tumor antigen and resiquimod in solid-in-oil nanodispersions promotes antitumor immunity. ACS Biomater. Sci. Eng. 2019, 5, 2297-2306.
[147]
Kim, N. W.; Kim, S. Y.; Lee, J. E.; Yin, Y.; Lee, J. H.; Lim, S. Y.; Kim, E. S.; Duong, H. T. T.; Kim, H. K.; Kim, S. et al. Enhanced cancer vaccination by in situ nanomicelle-generating dissolving microneedles. ACS Nano 2018, 12, 9702-9713.
[148]
Duong, H. T. T.; Yin, Y.; Thambi, T.; Nguyen, T. L.; Giang Phan, V. H.; Lee, M. S.; Lee, J. E.; Kim, J.; Jeong, J. H.; Lee, D. S. Smart vaccine delivery based on microneedle arrays decorated with ultra-pH-responsive copolymers for cancer immunotherapy. Biomaterials 2018, 185, 13-24.
[149]
Xu, J. J.; Xu, B. H.; Tao, J.; Yang, Y. X.; Hu, Y.; Huang, Y. Z. Microneedle-assisted, DC-targeted codelivery of pTRP-2 and adjuvant of paclitaxel for transcutaneous immunotherapy. Small 2017, 13, 1700666.
[150]
Tawde, S. A.; Chablani, L.; Akalkotkar, A.; D’Souza, M. J. Evaluation of microparticulate ovarian cancer vaccine via transdermal route of delivery. J. Control. Release 2016, 235, 147-154.
[151]
Jarvi, M. T.; Niedre, M. J.; Patterson, M. S.; Wilson, B. C. The influence of oxygen depletion and photosensitizer triplet-state dynamics during photodynamic therapy on accurate singlet oxygen luminescence monitoring and analysis of treatment dose response. Photochem. Photobiol. 2011, 87, 223-234.
[152]
Yang, J. A.; Kim, E. S.; Kwon, J. H.; Kim, H.; Shin, J. H.; Yun, S. H.; Choi, K. Y.; Hahn, S. K. Transdermal delivery of hyaluronic acid- human growth hormone conjugate. Biomaterials 2012, 33, 5947-5954.
[153]
Brown, M. B.; Jones, S. A. Hyaluronic acid: A unique topical vehicle for the localized delivery of drugs to the skin. J. Eur. Acad. Dermatol. Venereol. 2005, 19, 308-318.
[154]
Banerji, S.; Wright, A. J.; Noble, M.; Mahoney, D. J.; Campbell, I. D.; Day, A. J.; Jackson, D. G. Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction. Nat. Struct. Mol. Biol. 2007, 14, 234-239.
[155]
Jain, A. K.; Lee, C. H.; Gill, H. S. 5-aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors. J. Control. Release 2016, 239, 72-81.
[156]
Zhao, X.; Li, X. F.; Zhang, P.; Du, J. W.; Wang, Y. X. Tip-loaded fast-dissolving microneedle patches for photodynamic therapy of subcutaneous tumor. J. Control. Release 2018, 286, 201-209.
[157]
Shahbazi, M. A.; Shrestha, N.; Mäkilä, E.; Araújo, F.; Correia, A.; Ramos, T.; Sarmento, B.; Salonen, J.; Hirvonen, J.; Santos, H. A. A prospective cancer chemo-immunotherapy approach mediated by synergistic CD326 targeted porous silicon nanovectors. Nano Res. 2015, 8, 1505-1521.
[158]
Song, Y. L.; Wang, Y. D.; Wang, S. Y.; Cheng, Y.; Lu, Q. L.; Yang, L. F.; Tan, F. P.; Li, N. Immune-adjuvant loaded Bi2Se3 nanocage for photothermal-improved PD-L1 checkpoint blockade immune-tumor metastasis therapy. Nano Res. 2019, 12, 1770-1780.
[159]
Shen, S. Y.; Liu, M.; Li, T.; Lin, S. Q.; Mo, R. Recent progress in nanomedicine-based combination cancer therapy using a site-specific co-delivery strategy. Biomater. Sci. 2017, 5, 1367-1381.
[160]
Ali, O. A.; Emerich, D.; Dranoff, G.; Mooney, D. J. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci. Transl. Med. 2009, 1, 8ra19.
[161]
Kim, J.; Li, W. A.; Choi, Y.; Lewin, S. A.; Verbeke, C. S.; Dranoff, G.; Mooney, D. J. Injectable, spontaneously assembling, inorganic scaffolds modulate immune cells in vivo and increase vaccine efficacy. Nat. Biotechnol. 2015, 33, 64-72.
[162]
Stephan, S. B.; Taber, A. M.; Jileaeva, I.; Pegues, E. P.; Sentman, C. L.; Stephan, M. T. Biopolymer implants enhance the efficacy of adoptive T-cell therapy. Nat. Biotechnol. 2015, 33, 97-101.
[163]
Dong, L. Y.; Li, Y. C.; Li, Z.; Xu, N.; Liu, P.; Du, H. Y.; Zhang, Y. M.; Huang, Y. Q.; Zhu, J. J.; Ren, G. C. et al. Au nanocage-strengthened dissolving microneedles for chemo-photothermal combined therapy of superficial skin tumors. ACS Appl. Mater. Interfaces 2018, 10, 9247-9256.
[164]
Chen, M. C.; Lin, Z. W.; Ling, M. H. Near-infrared light-activatable microneedle system for treating superficial tumors by combination of chemotherapy and photothermal therapy. ACS Nano 2016, 10, 93-101.
[165]
Mitragotri, S.; Anderson, D. G.; Chen, X.; Chow, E. K.; Ho, D.; Kabanov, A. V.; Karp, J. M.; Kataoka, K.; Mirkin, C. A.; Petrosko, S. H. et al. Accelerating the translation of nanomaterials in biomedicine. ACS Nano 2015, 9, 6644-6654.
Publication history
Copyright
Acknowledgements

Publication history

Received: 13 December 2019
Revised: 16 January 2020
Accepted: 16 January 2020
Published: 06 March 2020
Issue date: July 2020

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020

Acknowledgements

This work was supported by the Natural Science Foundation of Jiangsu Province of China for Excellent Young Scholars (No. BK20190084), the Young Elite Scientists Sponsorship Program by CAST and National Students’ platform for Innovation and Entrepreneurship Training Program (No. 201910291094Z) to T. Y. J. and the UCLA start-up package to Z. G.

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