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Nano Research 2023, 16(5): 7199-7215 https://doi.org/10.1007/s12274-022-5349-4
Research Article | Issue | Published: 15 February 2023

Carvacrol combined with NIR light-responsive nano-drug delivery system with specific anti-bacteria, anti-inflammation, and immunomodulation for periodontitis

Show Author's Information Daorun Hu1,2,§,  Congkai Zhang3,§,  Chao Sun2,  Haijing Bai2,  Jialiang Xie2,4,  Yawen Gu2,  Mengyuan Li2,  Junkai Jiang2,  Aiping Le3( ),  Jiaxuan Qiu1( ),  Xiaolei Wang2,4( )
Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital of Nanchang University, Nanchang 330006, China
The National Engineering Research Center for Bioengineering Drugs and the Technologies, Institute of Translational Medicine, Nanchang University, Nanchang 330088, China
Department of Transfusion Medicine, The First Affiliated Hospital of Nanchang University; Key Laboratory of Jiangxi Province for Transfusion Medicine, The First Affiliated Hospital of Nanchang University, Nanchang 330006, China
College of Chemistry and Chemical Engineering, Nanchang University, Nanchang 330088, China

§ Daorun Hu and Congkai Zhang contributed equally to this work.

Keywords:
drug delivery, near-infrared light, anti-bacteria, periodontitis, upconversion nanoparticle
Topics:
Biomaterials Core shell nanoparticlesDrug delivery
Cite this article:
Hu D, Zhang C, Sun C, et al. Carvacrol combined with NIR light-responsive nano-drug delivery system with specific anti-bacteria, anti-inflammation, and immunomodulation for periodontitis. Nano Research, 2023, 16(5): 7199-7215. https://doi.org/10.1007/s12274-022-5349-4
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Abstract Full text Electronic supplementary material About this article

Bacterial infection, biofilm formation, and immune dysfunction are common triggers and aggravators in periodontitis, which render periodontal restoration challenging. Thus, a strategy with antibacterial, anti-inflammatory, and immunoregulatory capacities has great promise in the clinical practice of periodontitis. Herein, carvacrol (CA)-based near-infrared (NIR) light-responsive nano-drug delivery system is developed for the first time. The system consists of upconversion nanoparticles (UCNPs, which upconvert 808 nm NIR to blue light), mesoporous silica (mSiO2, the carrier channel), and hydrophobic CA (blue light response properties). Under the irradiation of 808 nm NIR, owing to the synergy of CA and upconverted blue light, the UCNPs@mSiO2-CA (UCMCs) exhibit the properties of specific anti-bacteria (including anaerobic bacteria), anti-inflammation, and immunomodulation. Notably, high-throughput sequencing results exhibit that many classic inflammatory immune-related signaling pathways, including the MAPK signaling pathway, tumor necrosis factor (TNF) signaling pathway, and IL-17 signaling pathway, are enriched to remodel the immune microenvironment. Additionally, UCMCs with NIR irradiation accelerate periodontal restoration and serve as promising non-invasive management of periodontitis. Altogether, this study verifies the feasibility of herbal monomer combined with light-responsive in situ nano-drug delivery system and provides a more effective and reliable strategy for various potential applications of deep tissue diseases.


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Electronic supplementary material
About this article

Carvacrol combined with NIR light-responsive nano-drug delivery system with specific anti-bacteria, anti-inflammation, and immunomodulation for periodontitis

Show Author's information Daorun Hu1,2,§, Congkai Zhang3,§, Chao Sun2, Haijing Bai2, Jialiang Xie2,4, Yawen Gu2, Mengyuan Li2, Junkai Jiang2, Aiping Le3( ), Jiaxuan Qiu1( ), Xiaolei Wang2,4( )
Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital of Nanchang University, Nanchang 330006, China
The National Engineering Research Center for Bioengineering Drugs and the Technologies, Institute of Translational Medicine, Nanchang University, Nanchang 330088, China
Department of Transfusion Medicine, The First Affiliated Hospital of Nanchang University; Key Laboratory of Jiangxi Province for Transfusion Medicine, The First Affiliated Hospital of Nanchang University, Nanchang 330006, China
College of Chemistry and Chemical Engineering, Nanchang University, Nanchang 330088, China

§ Daorun Hu and Congkai Zhang contributed equally to this work.

Abstract

Bacterial infection, biofilm formation, and immune dysfunction are common triggers and aggravators in periodontitis, which render periodontal restoration challenging. Thus, a strategy with antibacterial, anti-inflammatory, and immunoregulatory capacities has great promise in the clinical practice of periodontitis. Herein, carvacrol (CA)-based near-infrared (NIR) light-responsive nano-drug delivery system is developed for the first time. The system consists of upconversion nanoparticles (UCNPs, which upconvert 808 nm NIR to blue light), mesoporous silica (mSiO2, the carrier channel), and hydrophobic CA (blue light response properties). Under the irradiation of 808 nm NIR, owing to the synergy of CA and upconverted blue light, the UCNPs@mSiO2-CA (UCMCs) exhibit the properties of specific anti-bacteria (including anaerobic bacteria), anti-inflammation, and immunomodulation. Notably, high-throughput sequencing results exhibit that many classic inflammatory immune-related signaling pathways, including the MAPK signaling pathway, tumor necrosis factor (TNF) signaling pathway, and IL-17 signaling pathway, are enriched to remodel the immune microenvironment. Additionally, UCMCs with NIR irradiation accelerate periodontal restoration and serve as promising non-invasive management of periodontitis. Altogether, this study verifies the feasibility of herbal monomer combined with light-responsive in situ nano-drug delivery system and provides a more effective and reliable strategy for various potential applications of deep tissue diseases.

Keywords: drug delivery, near-infrared light, anti-bacteria, periodontitis, upconversion nanoparticle

References(63)

[1]

Peres, M. A.; Macpherson, L. M. D.; Weyant, R. J.; Daly, B.; Venturelli, R.; Mathur, M. R.; Listl, S.; Celeste, R. K.; Guarnizo-Herreño, C. C.; Kearns, C. et al. Oral diseases: A global public health challenge. Lancet 2019, 394, 249–260.
DOI Google Scholar
[2]

Kinane, D. F.; Stathopoulou, P. G.; Papapanou, P. N. Periodontal diseases. Nat. Rev. Dis. Primers 2017, 3, 17038.
DOI Google Scholar
[3]

Lamont, R. J.; Koo, H.; Hajishengallis, G. The oral microbiota: Dynamic communities and host interactions. Nat. Rev. Microbiol. 2018, 16, 745–759.
DOI Google Scholar
[4]

Belstrøm, D.; Constancias, F.; Drautz-Moses, D. I.; Schuster, S. C.; Veleba, M.; Mahe, F.; Givskov, M. Periodontitis associates with species-specific gene expression of the oral microbiota. npj Biofilms Microbiomes 2021, 7, 76.
DOI Google Scholar
[5]

Czesnikiewicz-Guzik, M.; D'Aiuto, F.; Deanfield, J. E. Understanding residual inflammatory risk sheds new light on the clinical importance of periodontitis in cardiovascular disease. Eur. Heart J. 2020, 41, 818–819.
DOI Google Scholar
[6]

Michaud, D. S.; Lu, J. Y.; Peacock-Villada, A. Y.; Barber, J. R.; Joshu, C. E.; Prizment, A. E.; Beck, J. D.; Offenbacher, S.; Platz, E. A. Periodontal disease assessed using clinical dental measurements and cancer risk in the ARIC study. J. Natl. Cancer Inst. 2018, 110, 843–854.
DOI Google Scholar
[7]

Eke, P. I.; Borgnakke, W. S.; Genco, R. J. Recent epidemiologic trends in periodontitis in the USA. Periodontol 2000 2020, 82, 257–267.
DOI Google Scholar
[8]

Vergnes, J. N.; Canceill, T.; Monsarrat, P. Intensive periodontal therapy and type 2 diabetes. Lancet Diabetes Endocrinol. 2019, 7, 174–175.
DOI Google Scholar
[9]

Kitamoto, S.; Nagao-Kitamoto, H.; Jiao, Y. Z.; Gillilland III, M. G.; Hayashi, A.; Imai, J.; Sugihara, K.; Miyoshi, M.; Brazil, J. C.; Kuffa, P. et al. The intermucosal connection between the mouth and gut in commensal pathobiont-driven colitis. Cell 2020, 182, 447–462.e14.
DOI Google Scholar
[10]

Hajishengallis, G.; Chavakis, T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat. Rev. Immunol. 2021, 21, 426–440.
DOI Google Scholar
[11]

Nakajima, M.; Tanner, E. E. L.; Nakajima, N.; Ibsen, K. N.; Mitragotri, S. Topical treatment of periodontitis using an iongel. Biomaterials 2021, 276, 121069.
DOI Google Scholar
[12]

Zhao, Z. M.; Ukidve, A.; Kim, J.; Mitragotri, S. Targeting strategies for tissue-specific drug delivery. Cell 2020, 181, 151–167.
DOI Google Scholar
[13]

Ahamad, N.; Kar, A.; Mehta, S.; Dewani, M.; Ravichandran, V.; Bhardwaj, P.; Sharma, S.; Banerjee, R. Immunomodulatory nanosystems for treating inflammatory diseases. Biomaterials 2021, 274, 120875.
DOI Google Scholar
[14]

Li, C. H.; Landis, R. F.; Makabenta, J. M.; Nabawy, A.; Tronchet, T.; Archambault, D.; Liu, Y. C.; Huang, R.; Golan, M.; Cui, W. et al. Nanotherapeutics using all-natural materials. Effective treatment of wound biofilm infections using crosslinked nanoemulsions. Mater. Horiz. 2021, 8, 1776–1782.
DOI Google Scholar
[15]

Landis, R. F.; Gupta, A.; Lee, Y. W.; Wang, L. S.; Golba, B.; Couillaud, B.; Ridolfo, R.; Das, R.; Rotello, V. M. Cross-linked polymer-stabilized nanocomposites for the treatment of bacterial biofilms. ACS Nano 2017, 11, 946–952.
DOI Google Scholar
[16]

Kachur, K.; Suntres, Z. The antibacterial properties of phenolic isomers, carvacrol and thymol. Crit. Rev. Food Sci. Nutr. 2020, 60, 3042–3053.
DOI Google Scholar
[17]

Liu, T. H.; Feng, C. Q.; Li, Z. F.; Gu, Z. B.; Ban, X. F.; Hong, Y.; Cheng, L.; Li, C. M. Efficient formation of carvacrol inclusion complexes during β-cyclodextrin glycosyltransferase-catalyzed cyclodextrin synthesis. Food Control 2021, 130, 108296.
DOI Google Scholar
[18]

Lu, M.; Wang, S.; Wang, T.; Hu, S. S.; Bhayana, B.; Ishii, M.; Kong, Y. F.; Cai, Y. C.; Dai, T. H.; Cui, W. G. et al. Bacteria-specific phototoxic reactions triggered by blue light and phytochemical carvacrol. Sci. Transl. Med. 2021, 13, eaba3571.
DOI Google Scholar
[19]

Li, Y. L.; Wu, M. X. Reversal of polymicrobial biofilm tolerance to ciprofloxacin by blue light plus carvacrol. Microorganisms 2021, 9, 2074.
DOI Google Scholar
[20]

Wang, S.; Wong, K. I.; Li, Y. L.; Ishii, M.; Li, X.; Wei, L.; Lu, M.; Wu, M. X. Blue light potentiates safety and bactericidal activity of p-toluquinone. J. Photochem. Photobiol. B 2022, 230, 112427.
DOI Google Scholar
[21]

Li, Y. L.; Wu, M. X. Visualization and elimination of polymicrobial biofilms by a combination of ALA-carvacrol-blue light. J. Photochem. Photobiol. B 2022, 234, 112525.
DOI Google Scholar
[22]

Leanse, L. G.; Dos Anjos, C.; Mushtaq, S.; Dai, T. H. Antimicrobial blue light: A ‘Magic Bullet’ for the 21st century and beyond? Adv. Drug Delivery Rev. 2022, 180, 114057.
DOI Google Scholar
[23]

Wu, J. L.; Wang, M. Y.; Yang, X. P.; Yi, C. W.; Jiang, J.; Yu, Y. H.; Ye, H. F. A non-invasive far-red light-induced split-Cre recombinase system for controllable genome engineering in mice. Nat. Commun. 2020, 11, 3708.
DOI Google Scholar
[24]

Zheng, X.; Kankala, R. K.; Liu, C. G.; Wen, Y.; Wang, S. B.; Chen, A. Z.; Zhang, Y. Tailoring lanthanide upconversion luminescence through material designs and regulation strategies. Adv. Opt. Mater. 2022, 10, 2200167.
DOI Google Scholar
[25]

Teh, D. B. L.; Bansal, A.; Chai, C.; Toh, T. B.; Tucker, R. A. J.; Gammad, G. G. L.; Yeo, Y.; Lei, Z. D.; Zheng, X.; Yang, F. Y. et al. A flexi-PEGDA upconversion implant for wireless brain photodynamic therapy. Adv. Mater. 2020, 32, 2001459.
DOI Google Scholar
[26]

Liu, S. B.; Yan, L.; Huang, J. S.; Zhang, Q. Y.; Zhou, B. Controlling upconversion in emerging multilayer core–shell nanostructures: From fundamentals to frontier applications. Chem. Soc. Rev. 2022, 51, 1729–1765.
DOI Google Scholar
[27]

Chen, S.; Weitemier, A. Z.; Zeng, X.; He, L. M.; Wang, X. Y.; Tao, Y. Q.; Huang, A. J. Y.; Hashimotodani, Y.; Kano, M.; Iwasaki, H. et al. Near-infrared deep brain stimulation via upconversion nanoparticle-mediated optogenetics. Science 2018, 359, 679–684.
DOI Google Scholar
[28]

Pearson, S.; Feng, J.; Del. Campo, A. Lighting the path: Light delivery strategies to activate photoresponsive biomaterials in vivo. Adv. Funct. Mater. 2021, 31, 2105989.
DOI Google Scholar
[29]

Ye, J.; Jiang, J. K.; Zhou, Z. R.; Weng, Z. Z.; Xu, Y. Y.; Liu, L. B.; Zhang, W.; Yang, Y. F.; Luo, J.; Wang, X. L. Near-infrared light and upconversion nanoparticle defined nitric oxide-based osteoporosis targeting therapy. ACS Nano 2021, 15, 13692–13702.
DOI Google Scholar
[30]

Liu, S. C.; Sun, Y.; Zhang, T.; Cao, L. T.; Zhong, Z. W.; Cheng, H. X.; Wang, Q. Q.; Qiu, Z.; Zhou, W. M.; Wang, X. L. Upconversion nanoparticles regulated drug & gas dual-effective nanoplatform for the targeting cooperated therapy of thrombus and anticoagulation. Bioact. Mater. 2022, 18, 91–103.
DOI Google Scholar
[31]

Yang, B. W.; Chen, Y.; Shi, J. L. Mesoporous silica/organosilica nanoparticles: Synthesis, biological effect and biomedical application. Mater. Sci. Eng. R 2019, 137, 66–105.
DOI Google Scholar
[32]

Noreen, S.; Maqbool, A.; Maqbool, I.; Shafique, A.; Khan, M. M.; Junejo, Y.; Ahmed, B.; Anwar, M.; Majeed, A.; Abbas, M. et al. Multifunctional mesoporous silica-based nanocomposites: Synthesis and biomedical applications. Mater. Chem. Phys. 2022, 285, 126132.
DOI Google Scholar
[33]

Lei, C.; Cao, Y. X.; Hosseinpour, S.; Gao, F.; Liu, J. Y.; Fu, J. Y.; Staples, R.; Ivanovski, S.; Xu, C. Hierarchical dual-porous hydroxyapatite doped dendritic mesoporous silica nanoparticles based scaffolds promote osteogenesis in vitro and in vivo. Nano Res. 2021, 14, 770–777.
DOI Google Scholar
[34]

Nguyen, H. C. B.; Adlanmerini, M.; Hauck, A. K.; Lazar, M. A. Dichotomous engagement of HDAC3 activity governs inflammatory responses. Nature 2020, 584, 286–290.
DOI Google Scholar
[35]

Rodriguez, A. E.; Ducker, G. S.; Billingham, L. K.; Martinez, C. A.; Mainolfi, N.; Suri, V.; Friedman, A.; Manfredi, M. G.; Weinberg, S. E.; Rabinowitz, J. D. et al. Serine metabolism supports macrophage IL-1β production. Cell Metab. 2019, 29, 1003–1011.e4.
DOI Google Scholar
[36]

Tang, Y.; Huang, Q. X.; Zheng, D. W.; Chen, Y.; Ma, L.; Huang, C.; Zhang, X. Z. Engineered Bdellovibrio bacteriovorus: A countermeasure for biofilm-induced periodontitis. Mater. Today 2022, 53, 71–83.
DOI Google Scholar
[37]

Guo, J. W.; Li, D. D.; Tao, H.; Li, G.; Liu, R. F.; Dou, Y.; Jin, T. T.; Li, L. L.; Huang, J.; Hu, H. Y. et al. Cyclodextrin-derived intrinsically bioactive nanoparticles for treatment of acute and chronic inflammatory diseases. Adv. Mater. 2019, 31, 1904607.
DOI Google Scholar
[38]

Luo, G. F.; Chen, W. H.; Zeng, X.; Zhang, X. Z. Cell primitive-based biomimetic functional materials for enhanced cancer therapy. Chem. Soc. Rev. 2021, 50, 945–985.
DOI Google Scholar
[39]

Reyes, L. Porphyromonas gingivalis. Trends Microbiolbiol. 2021, 29, 376–377.
DOI Google Scholar
[40]

Kuboniwa, M.; Houser, J. R.; Hendrickson, E. L.; Wang, Q.; Alghamdi, S. A.; Sakanaka, A.; Miller, D. P.; Hutcherson, J. A.; Wang, T. S.; Beck, D. A. C. et al. Metabolic crosstalk regulates Porphyromonas gingivalis colonization and virulence during oral polymicrobial infection. Nat. Microbiol. 2017, 2, 1493–1499.
DOI Google Scholar
[41]

Mehta, B.; Luo, Y. M.; Xu, J. H.; Sammaritano, L.; Salmon, J.; Lockshin, M.; Goodman, S.; Ibrahim, S. Trends in maternal and fetal outcomes among pregnant women with systemic lupus erythematosus in the United States: A cross-sectional analysis. Ann. Intern. Med. 2019, 171, 164–171.
DOI Google Scholar
[42]

Wu, X. F.; Yang, M. Y.; Kim, J. S.; Wang, R.; Kim, G.; Ha, J.; Kim, H.; Cho, Y.; Nam, K. T.; Yoon, J. Reactivity differences enable ROS for selective ablation of bacteria. Angew. Chem., Int. Ed. 2022, 61, e202200808.
DOI Google Scholar
[43]

Xie, J. Y.; Zhou, M.; Qian, Y. X.; Cong, Z. H.; Chen, S.; Zhang, W. J.; Jiang, W. N.; Dai, C. Z.; Shao, N.; Ji, Z. M. et al. Addressing MRSA infection and antibacterial resistance with peptoid polymers. Nat. Commun. 2021, 12, 5898.
DOI Google Scholar
[44]

Cheng, H. X.; Liu, H. M.; Liu, Z. Q.; Xu, Z. Y.; Liu, X. R.; Jia, S.; He, C. N.; Liu, S. C.; Zhang, J.; Wang, X. L. Yellow responsive material based modification to reduce earphone induced Infection and hearing loss. Nano Res. 2022, 15, 6297–6305.
DOI Google Scholar
[45]

Tyers, M.; Wright, G. D. Drug combinations: A strategy to extend the life of antibiotics in the 21st century. Nat. Rev. Microbiol. 2019, 17, 141–155.
DOI Google Scholar
[46]

Karygianni, L.; Ren, Z.; Koo, H.; Thurnheer, T. Biofilm matrixome: Extracellular components in structured microbial communities. Trends Microbiol. 2020, 28, 668–681.
DOI Google Scholar
[47]

Yan, J.; Bassler, B. L. Surviving as a community: Antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe 2019, 26, 15–21.
DOI Google Scholar
[48]

He, W. H.; You, M. L.; Wan, W. T.; Xu, F.; Li, F.; Li, A. Point-of-care periodontitis testing: Biomarkers, current technologies, and perspectives. Trends Biotechnol. 2018, 36, 1127–1144.
DOI Google Scholar
[49]

Cox, N.; Pokrovskii, M.; Vicario, R.; Geissmann, F. Origins, biology, and diseases of tissue macrophages. Annu. Rev. Immunol. 2021, 39, 313–344.
DOI Google Scholar
[50]

Borcherding, N.; Jia, W. T.; Giwa, R.; Field, R. L.; Moley, J. R.; Kopecky, B. J.; Chan, M. M.; Yang, B. Q.; Sabio, J. M.; Walker, E. C. et al. Dietary lipids inhibit mitochondria transfer to macrophages to divert adipocyte-derived mitochondria into the blood. Cell Metab. 2022, 34, 1499–1513.e8.
DOI Google Scholar
[51]

Shapouri-Moghaddam, A.; Mohammadian, S.; Vazini, H.; Taghadosi, M.; Esmaeili, S. A.; Mardani, F.; Seifi, B.; Mohammadi, A.; Afshari, J. T.; Sahebkar, A. Macrophage plasticity, polarization, and function in health and disease. J. Cell. Physiol. 2018, 233, 6425–6440.
DOI Google Scholar
[52]

Lee, S.; Park, J.; Kim, S.; Ok, J.; Yoo, J. I.; Kim, Y. S.; Ahn, Y.; Kim, T. I.; Ko, H. C.; Lee, J. Y. High-performance implantable bioelectrodes with immunocompatible topography for modulation of macrophage responses. ACS Nano 2022, 16, 7471–7485.
DOI Google Scholar
[53]

Russell, D. G.; Huang, L.; VanderVen, B. C. Immunometabolism at the interface between macrophages and pathogens. Nat. Rev. Immunol. 2019, 19, 291–304.
DOI Google Scholar
[54]

Liu, Y.; Hu, P.; Zheng, Z. H.; Zhong, D.; Xie, W. C.; Tang, Z. B.; Pan, B. X.; Luo, J.; Zhang, W. H.; Wang, X. L. Photoresponsive vaccine-like CAR-M system with high-efficiency central immune regulation for inflammation-related depression. Adv. Mater. 2022, 34, 2108525.
DOI Google Scholar
[55]

Kourtzelis, I.; Li, X. F.; Mitroulis, I.; Grosser, D.; Kajikawa, T.; Wang, B. M.; Grzybek, M.; Von Renesse, J.; Czogalla, A.; Troullinaki, M. et al. DEL-1 promotes macrophage efferocytosis and clearance of inflammation. Nat. Immunol. 2019, 20, 40–49.
DOI Google Scholar
[56]

Ronkina, N.; Gaestel, M. MAPK-activated protein kinases:Servant or partner? Annu. Rev. Biochem. 2022, 91, 505–540.
DOI Google Scholar
[57]

De Maeyer, R. P. H.; Van De Merwe, R. C.; Louie, R.; Bracken, O. V.; Devine, O. P.; Goldstein, D. R.; Uddin, M.; Akbar, A. N.; Gilroy, D. W. Blocking elevated p38 MAPK restores efferocytosis and inflammatory resolution in the elderly. Nat. Immunol. 2020, 21, 615–625.
DOI Google Scholar
[58]

Yuan, Z.; Wu, J. S.; Fu, Z. X.; Meng, S. Y.; Dai, L. L.; Cai, K. Y. Polydopamine-mediated interfacial functionalization of implants for accelerating infected bone repair through light-activatable antibiosis and carbon monoxide gas regulated macrophage polarization. Adv. Funct. Mater. 2022, 32, 2200374.
DOI Google Scholar
[59]

Li, J.; Song, S.; Meng, J. S.; Tan, L.; Liu, X. M.; Zheng, Y. F.; Li, Z. Y.; Yeung, K. W. K.; Cui, Z. D.; Liang, Y. Q. et al. 2D MOF periodontitis photodynamic ion therapy. J. Am. Chem. Soc. 2021, 143, 15427–15439.
DOI Google Scholar
[60]

Williams, D. W.; Greenwell-Wild, T.; Brenchley, L.; Dutzan, N.; Overmiller, A.; Sawaya, A. P.; Webb, S.; Martin, D.; NIDCD/NIDCR Genomics and Computational Biology Core; Hajishengallis, G. et al. Human oral mucosa cell atlas reveals a stromal-neutrophil axis regulating tissue immunity. Cell 2021, 184, 4090–4104.e15.
DOI Google Scholar
[61]

Plemmenos, G.; Evangeliou, E.; Polizogopoulos, N.; Chalazias, A.; Deligianni, M.; Piperi, C. Central regulatory role of cytokines in periodontitis and targeting options. Curr. Med. Chem. 2021, 28, 3032–3058.
DOI Google Scholar
[62]

Vieira, L. V.; De Sousa, L. M.; Maia, T. A. C.; Gusmão, J. N. F. M.; Goes, P.; Pereira, K. M. A.; Miyajima, F.; Gondim, D. V. Milk kefir therapy reduces inflammation and alveolar bone loss on periodontitis in rats. Biomed. Pharmacother. 2021, 139, 111677.
DOI Google Scholar
[63]

Bai, B. B.; Gu, C. Y.; Lu, X. H.; Ge, X. Y.; Yang, J. L.; Wang, C. F.; Gu, Y. C.; Deng, A. D.; Guo, Y. H.; Feng, X. M. et al. Polydopamine functionalized mesoporous silica as ROS-sensitive drug delivery vehicles for periodontitis treatment by modulating macrophage polarization. Nano Res. 2021, 14, 4577–4583.
DOI Google Scholar
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Publication history
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Acknowledgements

Publication history

Received: 17 October 2022
Revised: 17 November 2022
Accepted: 19 November 2022
Published: 15 February 2023
Issue date: May 2023

Copyright

© Tsinghua University Press 2022

Acknowledgements

Acknowledgements

This work was funded by the National Natural Science Foundation of China (Nos. 31860263, 81860477, 32071223, and 82260194), Key Youth Project of Jiangxi Province (No. 20202ACB216002), Key Research and Development Program of Jiangxi Province (Nos. 20212BBG73004, 20212BBG71005, and 20192ACB50014), the Local Science and Technology Development Fund (No. 20221ZDG020068), Key Laboratory of Jiangxi Province for Transfusion Medicine (No. 20212BCD42006), and Graduate Innovative Special Fund Projects of Jiangxi Province (Nos. YC2021-B045 and YC2021-B057).

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