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Research Article

Dual-functional microneedle with programmatic regulation of macrophage for autoimmune psoriasis treatment

Ze Qiang Zhao1,2, Bo Zhi Chen1,2 ( ), Jia Li Gan1,2, Yun Hao Feng1,2, Ling Liang1,2, Lingyun Yu1,2, Zi Yi Wang3,4, Samin Abbaszadeh5, Mohammad-Ali Shahbazi5,6,7( ), Ruixing Yu4( ), Xin Dong Guo1,2 ( )
State Key Laboratory of Organic-Inorganic Composites, Beijing University of Chemical Technology, Beijing 100029, China
Beijing Laboratory of Biomedical Materials, College of Materials Science and Engineering, Beijing University of Chemical Technology, Beijing 100029, China
China-Japan Friendship Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing 100029, China
Department of Dermatology, China-Japan Friendship Hospital, Beijing 100029, China
Department of Pharmaceutical Biomaterials, School of Pharmacy, Zanjan University of Medical Sciences, Zanjan 45139-56184, Iran
Department of Biomaterials and Biomedical Technology, University Medical Center Groningen, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands
W.J. Kolff Institute for Biomedical Engineering and Materials Science, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands
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Graphical Abstract

A dual-functional microneedle array system composed of two distinct components induce M2 macrophage polarization simultaneously, rapidly, and for a prolonged period of time via dual subcutaneous lysis. This innovative system holds the potential to induce a robust anti-inflammatory response, effectively suppressing immune disorders and providing a promising therapeutic avenue for psoriasis treatment.

Abstract

Modulating the immune microenvironment to establish sustained positive feedback within immune pathways represents a promising avenue for the treatment of autoimmunity. However, the precise and efficient delivery of therapeutic systems to the subcutaneous basal layer to modulate immune disorders is a major challenge in the treatment of autoimmune psoriasis. In this project, we introduce a dual-functional microneedle (DF-MN) designed to combine MNs with multiple release kinetics and immunotherapy, the programmed treatment is achieved through segmented design of the MN structure, realizing the unification of rapid and long-lasting treatment of autoimmune psoriasis. In vivo imaging results showed that GelMA@M-CSF showed fluorescent signals after 5 days of delivery to subcutaneous tissues, whereas HA@IL-13 showed minimal fluorescent signals after 2 days. The multistage release behavior of MNs and the diffusion mechanism of drugs were explained at the molecular level, in combination with coarse-grained molecular dynamics. Additionally, DF-MN can successfully induce macrophage reprogramming in vitro and ameliorate overall symptoms in a psoriasis mice model, suggesting that it has the potential to be an effective strategy for the treatment of psoriasis and portends to be a transformative platform for the treatment of other autoimmune diseases.

Keywords

microneedlepsoriasisM2 macrophageimmunoregulation

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References

[1]

Armstrong, A. W.; Read, C. Pathophysiology, clinical presentation, and treatment of psoriasis: A review. JAMA 2020, 323, 1945–1960.
Crossref Google Scholar
[2]

Ogawa, E.; Sato, Y.; Minagawa, A.; Okuyama, R. Pathogenesis of psoriasis and development of treatment. J. Dermatol. 2018, 45, 264–272.
Crossref Google Scholar
[3]

Rendon, A.; Schäkel, K. Psoriasis pathogenesis and treatment. Int. J. Mol. Sci. 2019, 20, 1475.
Crossref Google Scholar
[4]

Nestle, F. O.; Kaplan, D. H.; Barker, J. Psoriasis. N. Engl. J. Med. 2009, 361, 496–509.
Crossref Google Scholar
[5]

Perera, G. K.; Di Meglio, P.; Nestle, F. O. Psoriasis. Annu. Rev. Pathol. Mech. Dis. 2012, 7, 385–422.
Crossref Google Scholar
[6]

Harden, J. L.; Krueger, J. G.; Bowcock, A. M. The immunogenetics of psoriasis: A comprehensive review. J. Autoimmun. 2015, 64, 66–73.
Crossref Google Scholar
[7]

Kamata, M.; Tada, Y. Dendritic cells and macrophages in the pathogenesis of psoriasis. Front. Immunol. 2022, 13, 941071.
Crossref Google Scholar
[8]

Stratis, A.; Pasparakis, M.; Rupec, R. A.; Markur, D.; Hartmann, K.; Scharffetter-Kochanek, K.; Peters, T.; Van Rooijen, N.; Krieg, T.; Haase, I. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J. Clin. Invest. 2006, 116, 2094–2104.
Crossref Google Scholar
[9]

Wang, H. L.; Peters, T.; Kess, D.; Sindrilaru, A.; Oreshkova, T.; Van Rooijen, N.; Stratis, A.; Renkl, A. C.; Sunderkötter, C.; Wlaschek, M. et al. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J. Clin. Invest. 2006, 116, 2105–2114.
Crossref Google Scholar
[10]

Clark, R. A.; Kupper, T. S. Misbehaving macrophages in the pathogenesis of psoriasis. J. Clin. Invest. 2006, 116, 2084–2087.
Crossref Google Scholar
[11]

Van De Loosdrecht, A. A.; Nennie, E.; Ossenkoppele, G. J.; Beelen, R. H. J.; Langenhuijsen, M. M. A. C. Cell mediated cytotoxicity against U 937 cells by human monocytes and macrophages in a modified colorimetric MTT assay: A methodological study. J. Immunol. Methods 1991, 141, 15–22.
Crossref Google Scholar
[12]

Gordon, S. The macrophage: Past, present and future. Eur. J. Immunol. 2007, 37, S9–S17.
Crossref Google Scholar
[13]

Murray, P. J. Macrophage polarization. Annu. Rev. Physiol. 2017, 79, 541–566.
Crossref Google Scholar
[14]

Wynn, T. A.; Chawla, A.; Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496, 445–455.
Crossref Google Scholar
[15]

Li, L.; Zhang, H. Y.; Zhong, X. Q.; Lu, Y.; Wei, J. N.; Li, L.; Chen, H. M.; Lu, C. J.; Han, L. PSORI-CM02 formula alleviates imiquimod-induced psoriasis via affecting macrophage infiltration and polarization. Life Sci. 2020, 243, 117231.
Crossref Google Scholar
[16]

Huang, J. H.; Lin, Y. L.; Wang, L. C.; Chiang, B. L. M2-like macrophages polarized by foxp3- Treg-of-B cells ameliorate imiquimod-induced psoriasis. J. Cell. Mol. Med. 2023, 27, 1477–1492.
Crossref Google Scholar
[17]

Sun, H. F.; Zhao, Y. P.; Zhang, P. F.; Zhai, S. M.; Li, W. W.; Cui, J. W. Transcutaneous delivery of mung bean-derived nanoparticles for amelioration of psoriasis-like skin inflammation. Nanoscale 2022, 14, 3040–3048.
Crossref Google Scholar
[18]

Rostam, H. M.; Singh, S.; Salazar, F.; Magennis, P.; Hook, A.; Singh, T.; Vrana, N. E.; Alexander, M. R.; Ghaemmaghami, A. M. The impact of surface chemistry modification on macrophage polarisation. Immunobiology 2016, 221, 1237–1246.
Crossref Google Scholar
[19]

Davenport Huyer, L.; Mandla, S.; Wang, Y. F.; Campbell, S. B.; Yee, B.; Euler, C.; Lai, B. F.; Bannerman, A. D.; Lin, D. S. Y.; Montgomery, M. et al. Macrophage immunomodulation through new polymers that recapitulate functional effects of itaconate as a power house of innate immunity. Adv. Funct. Mater. 2021, 31, 2003341.
Crossref Google Scholar
[20]

Nuttelman, C. R.; Tripodi, M. C.; Anseth, K. S. Synthetic hydrogel niches that promote hMSC viability. Matrix Biol. 2005, 24, 208–218.
Crossref Google Scholar
[21]

Cha, B. H.; Shin, S. R.; Leijten, J.; Li, Y. C.; Singh, S.; Liu, J. C.; Annabi, N.; Abdi, R.; Dokmeci, M. R.; Vrana, N. E. et al. Integrin-mediated interactions control macrophage polarization in 3D hydrogels. Adv. Healthc. Mater. 2017, 6, 1700289.
Crossref Google Scholar
[22]

Yuan, Y.; Fan, D. D.; Shen, S. H.; Ma, X. X. An M2 macrophage-polarized anti-inflammatory hydrogel combined with mild heat stimulation for regulating chronic inflammation and impaired angiogenesis of diabetic wounds. Chem. Eng. J. 2022, 433, 133859.
Crossref Google Scholar
[23]

Chen, B. Z.; He, Y. T.; Zhao, Z. Q.; Feng, Y. H.; Liang, L.; Peng, J.; Yang, C. Y.; Uyama, H.; Shahbazi, M. A.; Guo, X. D. Strategies to develop polymeric microneedles for controlled drug release. Adv. Drug Deliv. Rev. 2023, 203, 115109.
Crossref Google Scholar
[24]

Wang, C. Y.; He, G. Q.; Zhao, H. H.; Lu, Y.; Jiang, P.; Li, W. Enhancing deep-seated melanoma therapy through wearable self-powered microneedle patch. Adv. Mater. 2024, 36, 2311246.
Crossref Google Scholar
[25]
Prausnitz, M. R.; Mikszta, J. A.; Cormier, M.; Andrianov, A. K. Microneedle-based vaccines. In Vaccines for Pandemic Influenza. Compans, R. W.; Orenstein, W. A., Eds.; Springer; Berlin, Heidelberg, 2009; pp 369–393.
Crossref
[26]

Chen, B. Z.; Zhang, L. Q.; Xia, Y. Y.; Zhang, X. P.; Guo, X. D. A basal-bolus insulin regimen integrated microneedle patch for intraday postprandial glucose control. Sci. Adv. 2020, 6, eaba7260.
Crossref Google Scholar
[27]

Yang, Y.; Xu, L. L.; Jiang, D. J.; Chen, B. Z.; Luo, R. Z.; Liu, Z.; Qu, X. C.; Wang, C.; Shan, Y. Z.; Cui, Y. et al. Self-powered controllable transdermal drug delivery system. Adv. Funct. Mater. 2021, 31, 2104092.
Crossref Google Scholar
[28]

Chen, B. Z.; Zhao, Z. Q.; Shahbazi, M. A.; Guo, X. D. Microneedle-based technology for cell therapy: Current status and future directions. Nanoscale Horiz. 2022, 7, 715–728.
Crossref Google Scholar
[29]

Liu, T. Q.; Sun, Y. F.; Zhang, W. J.; Wang, R.; Lv, X. Y.; Nie, L.; Shavandi, A.; Yunusov, K. E.; Jiang, G. H. Hollow-adjustable polymer microneedles for prolonged hypoglycemic effect on diabetic rats. Chem. Eng. J. 2024, 481, 148670.
Crossref Google Scholar
[30]

Jiang, X.; Zhang, W.; Terry, R.; Li, W. The progress of fabrication designs of polymeric microneedles and related biomedical applications. BMEMat 2023, 1, e12044.
Crossref Google Scholar
[31]

Jiang, X.; Zeng, Y. N.; Zhang, W.; Wang, C. Y.; Li, W. Advances in microneedle patches for long-acting contraception. Acta Mater. Med. 2023, 2, 1–8.
Crossref Google Scholar
[32]

Bi, D. H.; Qu, F.; Xiao, W. Y.; Wu, J. X.; Liu, P.; Du, H. Y.; Xie, Y. W.; Liu, H. M.; Zhang, L. B.; Tao, J. et al. Reactive oxygen species-responsive gel-based microneedle patches for prolonged and intelligent psoriasis management. ACS Nano 2023, 17, 4346–4357.
Crossref Google Scholar
[33]

Wu, D.; Shou, X.; Yu, Y. R.; Wang, X. C.; Chen, G. P.; Zhao, Y. J.; Sun, L. Y. Biologics-loaded photothermally dissolvable hyaluronic acid microneedle patch for psoriasis treatment. Adv. Funct. Mater. 2022, 32, 2205847.
Crossref Google Scholar
[34]

Zhou, Y.; Yang, L.; Lyu, Y.; Wu, D.; Zhu, Y.; Li, J. J.; Jiang, D. B.; Xin, X. F.; Yin, L. F. Topical delivery of ROS-responsive methotrexate prodrug nanoassemblies by a dissolvable microneedle patch for psoriasis therapy. Int. J. Nanomed. 2023, 18, 899–915.
Crossref Google Scholar
[35]

Tekko, I. A.; Permana, A. D.; Vora, L.; Hatahet, T.; McCarthy, H. O.; Donnelly, R. F. Localised and sustained intradermal delivery of methotrexate using nanocrystal-loaded microneedle arrays: Potential for enhanced treatment of psoriasis. Eur. J. Pharm. Sci. 2020, 152, 105469.
Crossref Google Scholar
[36]

Chen, B. Z.; He, M. C.; Zhang, X. P.; Fei, W. M.; Cui, Y.; Guo, X. D. A novel method for fabrication of coated microneedles with homogeneous and controllable drug dosage for transdermal drug delivery. Drug Deliv. Transl. Res. 2022, 12, 2730–2739.
Crossref Google Scholar
[37]

Yang, Y.; Chen, B. Z.; Zhang, X. P.; Zheng, H.; Li, Z.; Zhang, C. Y.; Guo, X. D. Conductive microneedle patch with electricity-triggered drug release performance for atopic dermatitis treatment. ACS Appl. Mater. Interfaces 2022, 14, 31645–31654.
Crossref Google Scholar
[38]

Qian, L. L.; Jin, F.; Wei, Z. D.; Li, T.; Sun, Z. Y.; Lai, C. T.; Ma, J.; Xiong, R. Y.; Ma, X. Y.; Wang, F. Y. et al. Wearable, self-powered, drug-loaded electronic microneedles for accelerated tissue repair of inflammatory skin disorders. Adv. Funct. Mater. 2023, 33, 2209407.
Crossref Google Scholar
[39]

He, H.; Zhang, S. Z.; Tighe, S.; Son, J.; Tseng, S. C. G. Immobilized heavy chain-hyaluronic acid polarizes lipopolysaccharide-activated macrophages toward M2 phenotype. J. Biol. Chem. 2013, 288, 25792–25803.
Crossref Google Scholar
[40]

Bauer, C.; Niculescu-Morzsa, E.; Jeyakumar, V.; Kern, D.; Späth, S. S.; Nehrer, S. Chondroprotective effect of high-molecular-weight hyaluronic acid on osteoarthritic chondrocytes in a co-cultivation inflammation model with m1 macrophages. J. Inflamm. 2016, 13, 31.
Crossref Google Scholar
[41]

Maharjan, A. S.; Pilling, D.; Gomer, R. H. High and low molecular weight hyaluronic acid differentially regulate human fibrocyte differentiation. PLoS One 2011, 6, e26078.
Crossref Google Scholar
[42]

Brochériou, I.; Maouche, S.; Durand, H.; Braunersreuther, V.; Le Naour, G.; Gratchev, A.; Koskas, F.; Mach, F.; Kzhyshkowska, J.; Ninio, E. Antagonistic regulation of macrophage phenotype by M-CSF and GM-CSF: Implication in atherosclerosis. Atherosclerosis 2011, 214, 316–324.
Crossref Google Scholar
[43]

Jaguin, M.; Houlbert, N.; Fardel, O.; Lecureur, V. Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell. Immunol. 2013, 281, 51–61.
Crossref Google Scholar
[44]

Zhao, Z. Q.; Zhang, B. L.; Chu, H. Q.; Liang, L.; Chen, B. Z.; Zheng, H.; Guo, X. D. A high-dosage microneedle for programmable lidocaine delivery and enhanced local long-lasting analgesia. Biomater. Adv. 2022, 133, 112620.
Crossref Google Scholar
[45]

Zhuang, Z. M.; Zhang, Y.; Sun, S. N.; Li, Q.; Chen, K. W.; An, C. F.; Wang, L. B.; Van Den Beucken, J. J. J. P.; Wang, H. N. Control of matrix stiffness using methacrylate-gelatin hydrogels for a macrophage-mediated inflammatory response. ACS Biomater. Sci. Eng. 2020, 6, 3091–3102.
Crossref Google Scholar
[46]

Zhuang, Z. M.; Zhang, Y.; Yang, X. Y.; Yu, T. Z.; Zhang, Y.; Sun, K.; Zhang, Y. G.; Cheng, F.; Zhang, L. J.; Wang, H. N. Matrix stiffness regulates the immunomodulatory effects of mesenchymal stem cells on macrophages via AP1/TSG-6 signaling pathways. Acta Biomater. 2022, 149, 69–81.
Crossref Google Scholar
[47]

Li, J. Y.; Feng, Y. H.; He, Y. T.; Hu, L. F.; Liang, L.; Zhao, Z. Q.; Chen, B. Z.; Guo, X. D. Thermosensitive hydrogel microneedles for controlled transdermal drug delivery. Acta Biomater. 2022, 153, 308–319.
Crossref Google Scholar
[48]

Xu, Z. Y.; Gao, L. J.; Chen, P. Y.; Yan, L. T. Diffusive transport of nanoscale objects through cell membranes: A computational perspective. Soft Matter 2020, 16, 3869–3881.
Crossref Google Scholar
[49]

Burov, S.; Tabei, S. M. A.; Huynh, T.; Murrell, M. P.; Philipson, L. H.; Rice, S. A.; Gardel, M. L.; Scherer, N. F.; Dinner, A. R. Distribution of directional change as a signature of complex dynamics. Proc. Natl. Acad. Sci. USA 2013, 110, 19689–19694.
Crossref Google Scholar
[50]

Tabei, S. M. A.; Burov, S.; Kim, H. Y.; Kuznetsov, A.; Huynh, T.; Jureller, J.; Philipson, L. H.; Dinner, A. R.; Scherer, N. F. Intracellular transport of insulin granules is a subordinated random walk. Proc. Natl. Acad. Sci. USA 2013, 110, 4911–4916.
Crossref Google Scholar
Nano Research
Volume 17 Issue 8,
August 2024
Pages 7436-7448
DOI: 10.1007/s12274-024-6711-5
Cite this article:
Zhao ZQ, Chen BZ, Gan JL, et al. Dual-functional microneedle with programmatic regulation of macrophage for autoimmune psoriasis treatment. Nano Research, 2024, 17(8): 7436-7448. https://doi.org/10.1007/s12274-024-6711-5
Topics:
Controlled drug delivery

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Received: 21 March 2024
Revised: 16 April 2024
Accepted: 18 April 2024
Published: 18 May 2024
© Tsinghua University Press 2024
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