Effects of Forest Environments in Attenuating D-Galactose-Induced Immunosenescence: Insights from a Murine Model
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Materials
2.2. Study Sites
2.3. Procedure
2.4. Environmental Monitoring
2.5. Lymphocyte Cells Analysis
2.6. Immune Organ Index Measurement
2.7. Immune Factor Analysis
2.8. Data Analysis
3. Results
3.1. Microclimate
3.2. Weight
3.3. Immune Organ Index
3.4. T-Lymphocyte Subpopulations
3.5. NK and NKT Cells
3.6. Immune Factors
4. Discussion
4.1. Key Findings
4.2. Potential Mechanisms of Forest Environment on Immunosenescence
4.3. Implications for Human Health and Urban Planning
4.4. Limitations and Future Directions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Song, F.; Bao, J.; Li, T.; Yu, T.; Yuan, Y.; Huang, X.; Bao, A.; De Maeyer, P. Contrasting Inequality of Green Spaces and Buildings between Cities in China. Build. Environ. 2024, 254, 111384. [Google Scholar] [CrossRef]
- Sun, L.; Chen, J.; Li, Q.; Huang, D. Dramatic Uneven Urbanization of Large Cities throughout the World in Recent Decades. Nat. Commun. 2020, 11, 5366. [Google Scholar] [CrossRef] [PubMed]
- Montecino-Rodriguez, E.; Berent-Maoz, B.; Dorshkind, K. Causes, Consequences, and Reversal of Immune System Aging. J. Clin. Investig. 2013, 123, 958–965. [Google Scholar] [CrossRef]
- Liu, S.; Li, C.; Chu, M.; Zhang, W.; Wang, W.; Wang, Y.; Guo, X.; Deng, F. Associations of Forest Negative Air Ions Exposure with Cardiac Autonomic Nervous Function and the Related Metabolic Linkages: A Repeated-Measure Panel Study. Sci. Total Environ. 2022, 850, 158019. [Google Scholar] [CrossRef] [PubMed]
- Peterfalvi, A.; Meggyes, M.; Makszin, L.; Farkas, N.; Miko, E.; Miseta, A.; Szereday, L. Forest Bathing Always Makes Sense: Blood Pressure-Lowering and Immune System-Balancing Effects in Late Spring and Winter in Central Europe. Int. J. Environ. Res. Public Health 2021, 18, 2067. [Google Scholar] [CrossRef] [PubMed]
- Tsao, T.-M.; Tsai, M.-J.; Hwang, J.-S.; Cheng, W.-F.; Wu, C.-F.; Chou, C.-C.K.; Su, T.-C. Health Effects of a Forest Environment on Natural Killer Cells in Humans: An Observational Pilot Study. Oncotarget 2018, 9, 16501–16511. [Google Scholar] [CrossRef]
- Chae, Y.; Lee, S.; Jo, Y.; Kang, S.; Park, S.; Kang, H. The Effects of Forest Therapy on Immune Function. Int. J. Environ. Res. Public Health 2021, 18, 8440. [Google Scholar] [CrossRef]
- Sun, Y.; Li, F.; He, T.; Meng, Y.; Yin, J.; Yim, I.S.; Xu, L.; Wu, J. Physiological and Affective Responses to Green Space Virtual Reality among Pregnant Women. Environ. Res. 2023, 216 Pt 1, 114499. [Google Scholar] [CrossRef]
- Li, Q.; Morimoto, K.; Kobayashi, M.; Inagaki, H.; Katsumata, M.; Hirata, Y.; Hirata, K.; Suzuki, H.; Li, Y.J.; Wakayama, Y.; et al. Visiting a Forest, but Not a City, Increases Human Natural Killer Activity and Expression of Anti-Cancer Proteins. Int. J. Immunopathol. Pharmacol. 2008, 21, 117–127. [Google Scholar] [CrossRef]
- Chen, H.; Meng, X.; Yu, Y.; Sun, J.; Niu, Z.; Wei, J.; Zhang, L.; Lu, C.; Yu, W.; Wang, T.; et al. Greenness and Its Composition and Configuration in Association with Allergic Rhinitis in Preschool Children. Environ. Res. 2024, 251 Pt 2, 118627. [Google Scholar] [CrossRef]
- Li, Y.; Li, X. Living in Urban Forests Strengthens Radical Scavenging Activity to Delay Aging: A Pilot Animal Study. Eur. J. For. Res. 2024, 143, 1563–1573. [Google Scholar] [CrossRef]
- Xie, D.; Jiang, L.; Lin, Y.; Liu, Z. Antioxidant Activity of Selenium-Enriched Chrysomyia Megacephala (Fabricius) Larvae Powder and Its Impact on Intestinal Microflora in D-Galactose Induced Aging Mice. BMC Complement. Med. Ther. 2020, 20, 264. [Google Scholar] [CrossRef] [PubMed]
- Starzomska, A.; Struzewska, J. A Six-Year Measurement-Based Analysis of Traffic-Related Particulate Matter Pollution in Urban Areas: The Case of Warsaw, Poland (2016–2021). Arch. Environ. Prot. 2024, 50, 75–84. [Google Scholar] [CrossRef]
- Azman, K.F.; Zakaria, R. D-Galactose-Induced Accelerated Aging Model: An Overview. Biogerontology 2019, 20, 763–782. [Google Scholar] [CrossRef]
- Sonar, S.A.; Watanabe, M.; Nikolich, J.Ž. Disorganization of Secondary Lymphoid Organs and Dyscoordination of Chemokine Secretion as Key Contributors to Immune Aging. Semin. Immunol. 2023, 70, 101835. [Google Scholar] [CrossRef]
- Ferrando-Martínez, S.; Ruiz-Mateos, E.; Hernández, A.; Gutiérrez, E.; Rodríguez-Méndez, M. del M.; Ordoñez, A.; Leal, M. Age-Related Deregulation of Naive T Cell Homeostasis in Elderly Humans. Age 2011, 33, 197–207. [Google Scholar] [CrossRef]
- Min, H.; Montecino-Rodriguez, E.; Dorshkind, K. Reduction in the Developmental Potential of Intrathymic T Cell Progenitors with Age. J. Immunol. Baltim. Md 1950 2004, 173, 245–250. [Google Scholar] [CrossRef]
- Pickering, H.; Schaenman, J.; Rossetti, M.; Ahn, R.; Sunga, G.; Liang, E.C.; Bunnapradist, S.; Reed, E.F. T Cell Senescence and Impaired CMV-Specific Response Are Associated with Infection Risk in Kidney Transplant Recipients. Hum. Immunol. 2022, 83, 273–280. [Google Scholar] [CrossRef]
- Franceschi, C.; Garagnani, P.; Parini, P.; Giuliani, C.; Santoro, A. Inflammaging: A New Immune-Metabolic Viewpoint for Age-Related Diseases. Nat. Rev. Endocrinol. 2018, 14, 576–590. [Google Scholar] [CrossRef]
- Condotta, S.A.; Richer, M.J. The Immune Battlefield: The Impact of Inflammatory Cytokines on CD8+ T-Cell Immunity. PLoS Pathog. 2017, 13, e1006618. [Google Scholar] [CrossRef]
- Ventura, M.T.; Casciaro, M.; Gangemi, S.; Buquicchio, R. Immunosenescence in Aging: Between Immune Cells Depletion and Cytokines up-Regulation. Clin. Mol. Allergy CMA 2017, 15, 21. [Google Scholar] [CrossRef]
- Yu, W.; Yu, Y.; Sun, S.; Lu, C.; Zhai, J.; Lei, Y.; Bai, F.; Wang, R.; Chen, J. Immune Alterations with Aging: Mechanisms and Intervention Strategies. Nutrients 2024, 16, 3830. [Google Scholar] [CrossRef]
- Silva, R.C.M.C. The Dichotomic Role of Cytokines in Aging. Biogerontology 2024, 26, 17. [Google Scholar] [CrossRef]
- Vermeesch, A.L.; Ellsworth-Kopkowski, A.; Prather, J.G.; Passel, C.; Rogers, H.H.; Hansen, M.M. Shinrin-Yoku 森林浴 (Forest Bathing): A Scoping Review of the Global Research on the Effects of Spending Time in Nature. Glob. Adv. Integr. Med. Health 2024, 13, 27536130241231258. [Google Scholar] [CrossRef]
- Ross, A.M.; Jones, R.J.F. Simulated Forest Immersion Therapy: Methods Development. Int. J. Environ. Res. Public Health 2022, 19, 5373. [Google Scholar] [CrossRef] [PubMed]
- Cheng, Y.-H.; Li, H.-K.; Yao, C.-A.; Huang, J.-Y.; Sung, Y.-T.; Chung, S.-D.; Chien, C.-T. Negative Air Ions through the Action of Antioxidation, Anti-Inflammation, Anti-Apoptosis and Angiogenesis Ameliorate Lipopolysaccharide Induced Acute Lung Injury and Promote Diabetic Wound Healing in Rat. PLoS ONE 2022, 17, e0275748. [Google Scholar] [CrossRef]
- Annerstedt, M.; Jönsson, P.; Wallergård, M.; Johansson, G.; Karlson, B.; Grahn, P.; Hansen, Å.M.; Währborg, P. Inducing Physiological Stress Recovery with Sounds of Nature in a Virtual Reality Forest—Results from a Pilot Study. Physiol. Behav. 2013, 118, 240–250. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.; Dai, F.; Yang, B.; Zhu, S. Effects of Neighborhood Green Space on PM2.5 Mitigation: Evidence from Five Megacities in China. Build. Environ. 2019, 156, 33–45. [Google Scholar] [CrossRef]
- Mestas, J.; Hughes, C.C.W. Of Mice and Not Men: Differences between Mouse and Human Immunology. J. Immunol. Baltim. Md 1950 2004, 172, 2731–2738. [Google Scholar] [CrossRef]
- Liu, B.-P.; Huxley, R.R.; Schikowski, T.; Hu, K.-J.; Zhao, Q.; Jia, C.-X. Exposure to Residential Green and Blue Space and the Natural Environment Is Associated with a Lower Incidence of Psychiatric Disorders in Middle-Aged and Older Adults: Findings from the UK Biobank. BMC Med. 2024, 22, 15. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Liu, Y.; Yang, L.; Ge, J.; Chang, X.; Zhang, X. The Impact of Urban Green Space on the Health of Middle-Aged and Older Adults. Front. Public Health 2023, 11, 1244477. [Google Scholar] [CrossRef]
- Xu, J.; Yuan, X.; Ni, W.; Sun, Y.; Zhang, H.; Zhang, Y.; Ke, P.; Xu, M.; Zhao, Z. Associations between Residential Greenness and Blood Lipids in Chinese Elderly Population. J. Endocrinol. Investig. 2022, 45, 2329–2339. [Google Scholar] [CrossRef]
- Zhang, W.; Peng, W.; Cai, J.; Jiang, Y.; Zhou, C.; Zha, Z.; Mi, J. Residential Surrounding Greenness Is Associated with Improved Lung Function in Adults: A Cross-Sectional Study in Eastern China. BMC Public Health 2023, 23, 632. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Navakatikyan, M.A.; Toms, R.; Astell-Burt, T. Leafier Communities, Healthier Hearts: An Australian Cohort Study of 104,725 Adults Tracking Cardiovascular Events and Mortality Across 10 Years of Linked Health Data. Heart Lung Circ. 2023, 32, 105–113. [Google Scholar] [CrossRef] [PubMed]
- Przewoźna, P.; Inglot, A.; Mielewczyk, M.; Maczka, K.; Matczak, P. Accessibility to Urban Green Spaces: A Critical Review of WHO Recommendations in the Light of Tree-Covered Areas Assessment. Ecol. Indic. 2024, 166, 112548. [Google Scholar] [CrossRef]
- Talen, E.; Allen, E.; Bosse, A.; Ahmann, J.; Anselin, L. LEED-ND as an Urban Metric. Landsc. Urban Plan. 2013, 119, 20–34. [Google Scholar] [CrossRef]
- Blat, A.; Stepanenko, T.; Bulat, K.; Wajda, A.; Dybas, J.; Mohaissen, T.; Alcicek, F.C.; Szczesny-Malysiak, E.; Malek, K.; Fedorowicz, A.; et al. Spectroscopic Signature of Red Blood Cells in a D-Galactose-Induced Accelerated Aging Model. Int. J. Mol. Sci. 2021, 22, 2660. [Google Scholar] [CrossRef]
Name | Catalog Number/Model | Manufacturer |
---|---|---|
Rat Anti-Mouse CD8α-PE/CY7 (53-6.7) | 1550-17 | SouthernBiotech, Birmingham, AL, USA |
APC-Cy™7 Hamster Anti-Mouse CD3e | 557, 596 | BD Pharmingen™, Franklin Lakes, NJ, USA |
FITC anti-mouse CD4 Antibody | 100, 406 | Biolegend, San Diego, CA, USA |
APC Anti-Mouse CD49b Antibody [DX5] | E-AB-F1116E | Elabscience, Wuhan, China |
Lysing Buffer | 555, 899 | BD Pharmingen™, Franklin Lakes, NJ, USA |
10× ACK Lysis Buffer | E-CK-A105 | Elabscience, Wuhan, China |
Mouse interleukin 2 (IL-2) ELISA kit | MM-0701M1 | Meimian, Yancheng, China |
Mouse interleukin 6 (IL-6) ELISA kit | MM-0163M2 | Meimian, Yancheng, China |
Mouse tumor necrosis factor α (TNF-α) ELISA kit | MM-0132M2 | Meimian, Yancheng, China |
Mouse interferon gamma (IFN-γ) ELISA kit | MM-0182M1 | Meimian, Yancheng, China |
Flow cytometer | CytoFlex | Beckman, Brea, CA, USA |
Refrigerated centrifuge | Microfuge 20R | Beckman, Brea, CA USA |
Microplate Reader | SH-1000Lab | Hitachi High, Tokyo, Japan |
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Li, Y.; Li, X. Effects of Forest Environments in Attenuating D-Galactose-Induced Immunosenescence: Insights from a Murine Model. Biology 2025, 14, 998. https://doi.org/10.3390/biology14080998
Li Y, Li X. Effects of Forest Environments in Attenuating D-Galactose-Induced Immunosenescence: Insights from a Murine Model. Biology. 2025; 14(8):998. https://doi.org/10.3390/biology14080998
Chicago/Turabian StyleLi, Yanling, and Xiaocong Li. 2025. "Effects of Forest Environments in Attenuating D-Galactose-Induced Immunosenescence: Insights from a Murine Model" Biology 14, no. 8: 998. https://doi.org/10.3390/biology14080998
APA StyleLi, Y., & Li, X. (2025). Effects of Forest Environments in Attenuating D-Galactose-Induced Immunosenescence: Insights from a Murine Model. Biology, 14(8), 998. https://doi.org/10.3390/biology14080998