Influence of ageing on Langerhans cell migration in mice: identification of a putative deficiency of epidermal interleukin‐1β
Abstract
Summary: Previous studies in mice have reported a decrease in epidermal Langerhans cell (LC) density in aged skin, however, the impact of this reduction on LC function and cutaneous immune responses is unclear. In the present series of experiments, the frequency of major histocompatibility complex class II+ LC in the epidermis of older (6‐month‐old) mice was found to be reduced significantly compared with that observed for young (6–8‐week‐old) mice. LC mobilization and the subsequent accumulation of dendritic cells (DC) in regional lymph nodes in response to topical challenge with a chemical allergen were found to be less vigorous in older mice. Flow cytometric analyses of DC derived from the draining lymph nodes of fluorescein isothiocyanate (FITC)‐sensitized mice revealed that the frequency of FITC+‐DC arriving in draining lymph nodes was also reduced in older mice but that the fluorescence intensity was comparable. Control and allergen‐treated‐older mice also displayed decreased total lymph node cellularity. Contact hypersensitivity responses were found not to be compromised in older mice. However, the cytokine regulation of LC migration in the two age groups of mice did differ. LC migration provoked by intradermal injection of tumour necrosis factor‐α (TNF‐α) was reduced in older animals, whereas, the percentage of LC that migrated in response to exogenous interleukin‐1β (IL‐1β) was comparable for both young and aged mice. Since both allergen‐ and TNF‐α‐induced LC responses are known to require receipt by LC of a signal from IL‐1β for effective migration, the suggestion is that impaired LC migration in older mice may be due to a reduced availability of epidermal IL‐1β.
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Many immune cell subsets become hyporesponsive to acute challenges with age.
“Thus, many immune cell subsets become hyporesponsive to acute challenges as we age17,19-25.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [20]
Cites
The aging immune system: primer and prospectus
Miller, R. A. (1996) · Science · doi:10.1126/science.273.5271.70 · Cited by 1,165 · see citing works
Age Influence on the Immune System
Makinodan, T., & Kay, M. M. B. (1980) · Advances in Immunology · doi:10.1016/s0065-2776(08)60047-4 · Cited by 699 · see citing works
Macatonia, S. E., Knight, S. C., Edwards, A. J., Griffiths, S., & Fryer, P. R. (1987) · The Journal of Experimental Medicine · doi:10.1084/jem.166.6.1654 · Cited by 585 · see citing works
Miller, R. A. (1991) · International review of cytology · doi:10.1016/s0074-7696(08)61527-2 · Cited by 353 · see citing works
Langerhans cells require signals from both tumour necrosis factor‐α and interleukin‐1β for migration
Cumberbatch, M., Dearman, R. J., & Kimber, I. (1997) · Immunology · doi:10.1046/j.1365-2567.1997.00360.x · Cited by 335 · see citing works
Self-citationMehta, V. B., Hart, J., & Wewers, M. D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006814200 · Cited by 255 · see citing works
Cumberbatch, M., & Kimber, I. (1995) · PubMed Central · Cited by 245 · see citing works
Self-citationInterleukin-1β Secretion Is Impaired by Inhibitors of the Atp Binding Cassette Transporter, ABC1
Hamon, Y., Luciani, M., Becq, F., Verrier, B., Rubartelli, A., & Chimini, G. (1997) · Blood · doi:10.1182/blood.v90.8.2911 · Cited by 224 · see citing works
Flow cytometric measurement of intracellular cytokines
Pala, P., Hussell, T., & Openshaw, P. (2000) · Journal of Immunological Methods · doi:10.1016/s0022-1759(00)00230-1 · Cited by 222 · see citing works
Kimber, I., Cumberbatch, M., Dearman, R. J., et al. (2000) · British Journal of Dermatology · doi:10.1046/j.1365-2133.2000.03349.x · Cited by 201 · see citing works
Self-citationImmunological responses of healthy elderly population.
Goodwin, J. S., Searles, R., & Tung, K. S. K. (1982) · PubMed Central · Cited by 180 · see citing works
Schumann, R. R., Belka, C., Reuter, D., Lamping, N., Kirschning, C. J., Weber, J. R., & Pfeil, D. (1998) · Blood · doi:10.1182/blood.v91.2.577 · Cited by 165 · see citing works
Enhanced Epidermal Langerhans Cell Migration in IL-10 Knockout Mice
Wang, B., Zhuang, L., Fujisawa, H., Shinder, G. A., Feliciani, C., Shivji, G. M., Suzuki, H., Amerio, P., Toto, P., & Sauder, D. N. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.1.277 · Cited by 149 · see citing works
The role of dendritic cells in the initiation of immune responses to contact sensitizers
Knight, S. C., Krejčí, J., Malkovský, M., et al. (1985) · Cellular Immunology · doi:10.1016/0008-8749(85)90266-7 · Cited by 146 · see citing works
Dendritic Cells: Biology and Clinical Applications
Ploegh, H. L. (1999) · Nature Medicine · doi:10.1038/12406 · Cited by 140 · see citing works
Three populations of mouse lymph node dendritic cells with different origins and dynamics
Salomon, B. L. (1997) · Immunology Letters · doi:10.1016/s0165-2478(97)87647-x · Cited by 126 · see citing works
Modulation of epidermal Langerhans' cell frequency by tumour necrosis factor-alpha.
Cumberbatch, M., Fielding, I., & Kimber, I. (1994) · PubMed · Cited by 124 · see citing works
Self-citationCumberbatch, M., Dearman, R. J., & Kimber, I. (1997) · Archives of Dermatological Research · doi:10.1007/s004030050193 · Cited by 115 · see citing works
Self-citationWANG, B., Kondo, S., Shivji, G. M., Fujisawa, H., Mak, T. W., & Sauder, D. N. (1996) · Immunology · doi:10.1111/j.1365-2567.1996.tb00016.x · Cited by 102 · see citing works
Three Populations of Mouse Lymph Node Dendritic Cells with Different Origins and Dynamics
Salomon, B. L., Cohen, J. L., Masurier, C., & Klatzmann, D. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.2.708 · Cited by 100 · see citing works
Tumour necrosis factor-α induces Langerhans cell migration in humans
Cumberbatch, Griffiths, C. E. M., Tucker, Dearman, & Kimber (1999) · British Journal of Dermatology · doi:10.1046/j.1365-2133.1999.02964.x · Cited by 98 · see citing works
Effect of Aging on Epidermal Dendritic Cell Populations in C57BL/6J Mice
Sprecher, E., Becker, Y., Kraal, G., Hall, E. J., Harrison, D. G., & Shultz, L. D. (1990) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12874586 · Cited by 91 · see citing works
Pulmonary tuberculosis in elderly men
Álvarez, S., Shell, C. G., & Berk, S. L. (1987) · The American Journal of Medicine · doi:10.1016/0002-9343(87)90106-9 · Cited by 86 · see citing works
Cumberbatch, M., & Kimber, I. (1990) · PubMed · Cited by 84 · see citing works
Self-citationAge-Related Changes in Cell-Mediated Immunity in BALB/C Mice
Walters, C. S., & Claman, H. N. (1975) · The Journal of Immunology · doi:10.4049/jimmunol.115.5.1438 · Cited by 83 · see citing works
Skin Lesions of the Aged and Their Association With Internal Changes
Tindall, J. P., & Smith, J. R. (1963) · JAMA · doi:10.1001/jama.1963.03710120021004 · Cited by 66 · see citing works
The Decline of Cell-mediated Immunity in Aging Mice
Menon, M., Jaroslow, B. N., & Koesterer, R. (1974) · Journal of Gerontology · doi:10.1093/geronj/29.5.499 · Cited by 62 · see citing works
Skin ageing and immune competence
Thivolet, J., & Nicolas, J. (1990) · British Journal of Dermatology · doi:10.1111/j.1365-2133.1990.tb16129.x · Cited by 53 · see citing works
Epidermal langerhans cell density and contact sensitivity in young and aged BALB/c mice
Choi, K. L., & Sauder, D. N. (1987) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(87)90087-x · Cited by 51 · see citing works
Belsito, D. V., Epstein, S., Schultz, J. M., et al. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.143.5.1530 · Cited by 46 · see citing works
Buchanan, J., Peters, C., Rasmussen, C. J., & Rothstein, G. (1996) · Experimental Gerontology · doi:10.1016/0531-5565(95)02016-0 · Cited by 36 · see citing works
Langerhans cell migration in mice requires intact type I interleukin 1 receptor (IL-1RI) function
Cumberbatch, M., Dearman, R. J., & Kimber, I. (1999) · Archives of Dermatological Research · doi:10.1007/s004030050422 · Cited by 35 · see citing works
Self-citationAge-associated changes in Langerhans cells of murine oral epithelium and epidermis
Rittman, B. R. J., Hill, M. W., Rittman, G. A., & Mackenzie, I. C. (1987) · Archives of Oral Biology · doi:10.1016/0003-9969(87)90102-6 · Cited by 30 · see citing works
Effect of Age on Epidermal Immune Function
Sander, D. N. (1986) · Dermatologic Clinics · doi:10.1016/s0733-8635(18)30807-6 · Cited by 29 · see citing works
Mechanisms Underlying the Increased Susceptibility of Aged Mice to Tuberculosis
Orme, I. M. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1995.tb01514.x · Cited by 28 · see citing works
Effect of age on cutaneous interleukin 1 expression
Sauder, D. N., Ponnappan, U., & Cinader, B. (1989) · Immunology Letters · doi:10.1016/0165-2478(89)90094-1 · Cited by 22 · see citing works
The effect of aging on the density and distribution of oral mucosal langerhans cells
SCHWARTZ, J. L., Weichselbaum, R., & Frim, S. R. (1983) · Experimental Gerontology · doi:10.1016/0531-5565(83)90052-9 · Cited by 21 · see citing works
Ford, P. M. (1986) · Clinics in Rheumatic Diseases · doi:10.1016/s0307-742x(21)00617-2 · Cited by 21 · see citing works
Effect of Age on Epidermal Immune Function
Sauder, D. N. (1989) · Clinics in Geriatric Medicine · doi:10.1016/s0749-0690(18)30701-8 · Cited by 19 · see citing works
Nagami, P., & Yoshikawa, T. T. (2009) · Gerontology · doi:10.1159/000212650 · Cited by 18 · see citing works
Meyer, K. B., & Ireland, J. (1998) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199805)28:05 · Cited by 17 · see citing works
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Sorted by citations
The twilight of immunity: emerging concepts in aging of the immune system
Nikolich-Žugich, J. (2018) · Nature Immunology · doi:10.1038/s41590-017-0006-x · Cited by 1,240 · see citing works
Agrawal, A., Agrawal, S., Cao, J.-N., Su, H., Osann, K., & Gupta, S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.6912 · Cited by 435 · see citing works
SARS-CoV-2, COVID-19 and the aging immune system
Bartleson, J. M., Radenkovic, D., Covarrubias, A. J., Furman, D., Winer, D. A., & Verdin, E. (2021) · Nature Aging · doi:10.1038/s43587-021-00114-7 · Cited by 359 · see citing works
Inflammaging as a prodrome to Alzheimer's disease
Giunta, B., Fernandez, F., Nikolic, W. V., Obregon, D., Rrapo, E., Town, T., & Tan, J. (2008) · Journal of Neuroinflammation · doi:10.1186/1742-2094-5-51 · Cited by 327 · see citing works
Contribution of Aging, Obesity, and Microbiota on Tumor Immunotherapy Efficacy and Toxicity
Baiden-Amissah, R. E. M., & Tuyaerts, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20143586 · Cited by 30 · see citing works
- Authors
- Cumberbatch, M., Dearman, R. J., & Kimber, I.
- Affiliations
- Syngenta (United Kingdom) (GB)
- Corresponding author
- Cumberbatch, Marie
- ORCID
- Kimber, Ian
- Venue
- Immunology
- Publisher
- Wiley
- Published
- 2002-04
- Volume
- 105
- Issue
- 4
- Pages
- 466-477
- ISSN
- 0019-2805 (ISSN-L)
- 1365-2567
- OpenAlex
- W2001018816
- Cited by
- 78
- References
- 41
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 5 · 2023: 3 · 2022: 3 · 2021: 7 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 2 · 2016: 2 · 2014: 1 · 2013: 3 · 2012: 2
- FWCI
- 1.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Immunology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Dermatology › Contact Dermatitis and Allergies
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- Langerhans cells, aging, Langerhans cell migration, dendritic cells, skin immune response, contact hypersensitivity, TNF-α, draining lymph nodes, MHC class II
- MeSH terms
- Aging, Allergens, Animals, Histocompatibility Antigens Class II, Cell Count, Cell Movement, Cells, Cultured, Dendritic Cells, Dermatitis, Contact, Epidermis, Flow Cytometry, Fluorescent Dyes, Interleukin-1, Langerhans Cells, Lymph Nodes, Mice, Inbred BALB C, Oxazolone, Tumor Necrosis Factor-alpha, Fluorescein-5-isothiocyanate, Mice
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