Targeting macrophages rescues age‐related immune deficiencies in C57 BL/6J geriatric mice
Open accessAbstract
Changes to innate cells, such as macrophages and myeloid-derived suppressor cells (MDSCs), during aging in healthy or tumor-bearing hosts are not well understood. We compared macrophage subpopulations and MDSCs from healthy young (6-8 weeks) C57BL/6J mice to those from healthy geriatric (24-28 months) mice. Spleens, lymph nodes, and bone marrow of geriatric hosts contained significantly more M2 macrophages and MDSCs than their younger counterparts. Peritoneal macrophages from geriatric, but not young, mice co-expressed CD40 and CX3CR1 that are usually mutually exclusively expressed by M1 or M2 macrophages. Nonetheless, macrophages from geriatric mice responded to M1 or M2 stimuli similarly to macrophages from young mice, although they secreted higher levels of TGF-β in response to IL-4. We mimicked conditions that may occur within tumors by exposing macrophages from young vs. geriatric mice to mesothelioma or lung carcinoma tumor cell-derived supernatants. While both supernatants skewed macrophages toward the M2-phenotype regardless of age, only geriatric-derived macrophages produced IL-4, suggesting a more immunosuppressive tumor microenvironment will be established in the elderly. Both geriatric- and young-derived macrophages induced allogeneic T-cell proliferation, regardless of the stimuli used, including tumor supernatant. However, only macrophages from young mice induced T-cell IFN-γ production. We examined the potential of an IL-2/agonist anti-CD40 antibody immunotherapy that eradicates large tumors in young hosts to activate macrophages from geriatric mice. IL-2-/CD40-activated macrophages rescued T-cell production of IFN-γ in geriatric mice. Therefore, targeting macrophages with IL-2/anti-CD40 antibody may improve innate and T-cell immunity in aging hosts.
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Geriatric mice aged 24-28 months have more macrophages in spleen and bone marrow than young mice.
“Geriatric mice (24-28 months old) have elevated numbers of macrophages in the spleen and bone marrow as compared to young mice (57).”
From The impact of ageing on monocytes and macrophages (2021) · cites this paper as [57]
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“Splenocytes were labeled with carboxyfluorescein diacetate succinimidyl ester (CFSE; Invitrogen) a fluorescent dye that binds permanently to cell membranes.(26,27) CFSElabeled splenocytes were incubated for 2–4 h (37x C, 5% CO2) to remove adherent macrophages and DCs and collect nonadherent cells (consisting of 40% T…”
BackgroundMethodThe senescence accelerated mouse prone 8 (SAMP8): A novel murine model for cardiac aging
Karuppagounder, V., Arumugam, S., Babu, S. S., Palaniyandi, S. S., Watanabe, K., Cooke, J. P., & Thandavarayan, R. A. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.10.006 · Cited by 56 · see citing works
Characterization of regulatory T cells in obese omental adipose tissue in humans
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The “Trojan Horse” Approach to Tumor Immunotherapy: Targeting the Tumor Microenvironment
Nelson, D. J., Fisher, S. A., & Robinson, B. W. S. (2014) · Journal of Immunology Research · doi:10.1155/2014/789069 · Cited by 52 · see citing works
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New insights into the role of cellular senescence and chronic wounds
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MDSCs, ageing and inflammageing
Pawelec, G., Picard, E., Bueno, V., Verschoor, C. P., & Ostrand‐Rosenberg, S. (2021) · Cellular Immunology · doi:10.1016/j.cellimm.2021.104297 · Cited by 49 · see citing works
Innate Immune Cells and Their Contribution to T-Cell-Based Immunotherapy
Ginefra, P., Lorusso, G., & Vannini, N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124441 · Cited by 47 · see citing works
“Congruently, old mice have a higher proportion of M2 macrophages both in the spleen and in the bone marrow [177], while neutrophils in aged patients produce more anti-inflammatory cytokines [178].”
BackgroundKovacs, E. J., Boe, D. M., Boule, L. A., & Curtis, B. J. (2017) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2017.06.002 · Cited by 49 · see citing works
Gather, L., Nath, N., Falckenhayn, C., Oterino-Sogo, S., Bosch, T. C. G., Wenck, H., Winnefeld, M., Grönniger, E., Simm, S., & Siracusa, A. (2022) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2022.06.023 · Cited by 47 · see citing works
Salminen, A., Kaarniranta, K., & Kauppinen, A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102296 · Cited by 49 · see citing works
Du, M., Sun, L., Guo, J. J., & Lv, H. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107198 · Cited by 49 · see citing works
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Considerations for successful cancer immunotherapy in aged hosts
Hurez, V. J., Padron, A. S., Svatek, R. S., & Curiel, T. J. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.10.002 · Cited by 46 · see citing works
“Other factors include tumor cells that can attract detrimental MDSC, neutrophils or Tregs that blunt anti-tumor immunity and can generate pro-tumorigenic molecules (Jackaman and Nelson, 2014; Jackaman et al., 2013).”
BackgroundInfluentialSingh, M. P., Sethuraman, S. N., Ritchey, J. W., Fiering, S., Guha, C., Malayer, J. R., & Ranjan, A. (2019) · International Journal of Hyperthermia · doi:10.1080/02656736.2019.1663280 · Cited by 46 · see citing works
Common Pathogenetic Mechanisms Underlying Aging and Tumor and Means of Interventions
Shen, W., He, J., Hou, T., Si, J., & Chen, S. (2022) · Aging and Disease · doi:10.14336/ad.2021.1208 · Cited by 45 · see citing works
Research Progress of Macrophages in Bone Regeneration
Zhang, D., Dang, Y., Deng, R., Ma, Y., Wang, J., Ao, J., & Wang, X. (2022) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1155/2023/1512966 · Cited by 44 · see citing works
“Mahbub et al. reported that aging results in a decrease in both M1 and M2 macrophages [93], while other investigators reported that aging leads to the increase of M2 macrophages in the retina, spleen, lymph nodes, and bone marrow [94, 95].”
Markers of the ageing macrophage: a systematic review and meta-analysis
Moss, C. E., Phipps, H., Wilson, H. L., & Kiss‐Toth, E. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1222308 · Cited by 43 · see citing works
“It is widely thought that overall, tissue macrophage numbers do not change with age (81–83), although expansion of infiltrating macrophages has been reported (84).”
BackgroundCancer Immunotherapies: Are They as Effective in the Elderly?
Poropatich, K., Fontanarosa, J., Samant, S., Sosman, J., & Zhang, B. (2017) · Drugs & Aging · doi:10.1007/s40266-017-0479-1 · Cited by 39 · see citing works
“Additionally, age-related increases in tumor-resident antigen-presenting cell subsets, specifically pro-inflammatory macrophages, have been found in both murine and human subjects [19, 23].”
BackgroundNormal Aging and Its Role in Cancer MetastasisPreprint
Fane, M. E., & Weeraratna, A. T. (2019) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a037341 · Cited by 42 · see citing works
“Studies have shown that M2 tumor-associated macrophages (TAMs), which have an immunosuppressive phenotype, are significantly higher in the spleen and bone marrow of aged mice (Jackaman et al. 2013).”
ResultGardner, J. K., Mamotte, C. D. S., Jackaman, C., & Nelson, D. J. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.07.002 · Cited by 40 · see citing works
“lymphoid M2 macrophages (Jackaman et al., 2014; Jackaman et al., 2013) and MDSCs in tumours increases with age (Chandra et al.”
Self-citationHe, W., Yuan, T., Choezom, D., Hunkler, H. J., Annamalai, K., Lupše, B., & Maedler, K. (2018) · Scientific Reports · doi:10.1038/s41598-018-20909-w · Cited by 40 · see citing works
Orchestration of the Adipose Tissue Immune Landscape by Adipocytes
Bradley, D. P., Deng, T., Shantaram, D., & Hsueh, W. A. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042222-024353 · Cited by 38 · see citing works
Salminen, A., Kaarniranta, K., & Kauppinen, A. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109771 · Cited by 36 · see citing works
Therapies for sarcopenia and regeneration of old skeletal muscles
Grounds, M. D. (2014) · BioArchitecture · doi:10.4161/bioa.29668 · Cited by 35 · see citing works
Implications of inflammatory states on dysfunctional immune responses in aging and obesity
Thomas, A. L., Alarcon, P. C., Divanovic, S., Chougnet, C. A., Hildeman, D. A., & Moreno-Fernandez, M. E. (2021) · Frontiers in Aging · doi:10.3389/fragi.2021.732414 · Cited by 35 · see citing works
“Additionally, macrophages with anti-inflammatory characteristics, including increased secretion of Interleukin-10 (IL-10) and Transforming Growth Factor Beta (TGFβ) are more frequent in aged bone marrow, lymph nodes, and skeletal muscle (Jackaman et al., 2013; Wang et al., 2015).”
BackgroundProinflammatory profile of in vitro monocytes in the ageing is affected by lymphocytes presence
Pinke, K. H., Calzavara, B., Faria, P. F., do Nascimento, M. P. P., Venturini, J., & Lara, V. S. (2013) · Immunity & Ageing · doi:10.1186/1742-4933-10-22 · Cited by 36 · see citing works
“Unlike our findings, other studies showed higher levels of TGF-β from macrophages with aging [48,49].”
ResultMyeloid-Derived Suppressor Cells at the Intersection of Inflammaging and Bone Fragility
Kirkwood, K. L., Zhang, L., Thiyagarajan, R., Seldeen, K. L., & Troen, B. R. (2018) · Immunological Investigations · doi:10.1080/08820139.2018.1552360 · Cited by 36 · see citing works
“…of cancer immunology, MDSCs have also been shown to contribute to chronic and acute inflammatory processes associated with aging (Gabrilovich and Nagaraj, 2009; Jackaman and Nelson, 2014; Jackaman et al., 2013) and are recurrently detected in different inflammatory-based pathological disorders.”
BackgroundImmunometabolism at the Nexus of Cancer Therapeutic Efficacy and Resistance
Traba, J., Sack, M. N., Waldmann, T. A., & Antón, O. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.657293 · Cited by 35 · see citing works
“It has been suggested that upregulation of the gluconeogenic enzyme Fructose-1,6-bisphosphatase 1 (FBP1) in NK cells of lung cancer, which inhibits their glycolytic metabolism, is caused by high levels of TGF-b in the TME (94).”
BackgroundInfluentialImmune checkpoint protein VSIG4 as a biomarker of aging in murine adipose tissue
Hall, B. M., Gleiberman, A. S., Strom, E., Krasnov, P. A., Frescas, D., Vujcic, S., Leontieva, O. V., Antoch, M. P., Kogan, V., Koman, I. E., et al. (2020) · Aging Cell · doi:10.1111/acel.13219 · Cited by 33 · see citing works
“…lymphocytes is highly relevant to aging and represents a potential area of therapeutic intervention, as the modulation of Mφ (via activation by IL-2/agonist anti-CD40 immunotherapy) was shown to rescue age-related deficiencies in T lymphocytes (Jackaman, Dye, & Nelson, 2014; Jackaman et al., 2013).”
BackgroundSalminen, A. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102694 · Cited by 33 · see citing works
“There is abundant evidence indicating that the number of M2 macrophages is elevated in certain tissues of aged mice, such as the BM, spleen, lymph nodes, lungs, and skeletal muscles (Jackaman et al., 2013; Wang et al., 2015).”
Jackaman, C., & Nelson, D. J. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.11.009 · Cited by 31 · see citing works
“We have shown that macrophages from elderly, but not young, mice exposed to tumor conditioned media from murine mesothelioma and lewis lung carcinoma tumor cells produced IL-4 and high levels of immune-suppressive TGFβ (Jackaman et al., 2013).”
BackgroundResultInfluentialMicrovasculature remodeling in the mouse lower gut during inflammaging
Jeong, J., Kim, K., Lim, D., Kim, K.-H., Kim, H.-S., Lee, S., Song, J., Moon, B.-G., Choy, H. E., & Park, S. C. (2017) · Scientific Reports · doi:10.1038/srep39848 · Cited by 30 · see citing works
Immune aging and infectious diseases
Chen, R., Zou, J., Chen, J., Wang, L., Kang, R., & Tang, D. (2024) · Chinese Medical Journal · doi:10.1097/cm9.0000000000003410 · Cited by 33 · see citing works
“[ 160 , 161 ] Autophagy regulates key aging features in macrophages, such as phagocytosis and nitrite production.”
IL-2/CD40-activated macrophages rescue age and tumor-induced T cell dysfunction in elderly mice
Jackaman, C., Dye, D. E., & Nelson, D. J. (2014) · AGE · doi:10.1007/s11357-014-9655-y · Cited by 30 · see citing works
“Nonetheless, elderly-derived macrophages maintained their ability to respond to stimuli but lost their ability to induce T cells to secrete IFN-γ; a function that could be restored by activating macrophages using a combination of IL-2 with agonist anti-CD40 antibody (IL-2/ CD40; Jackaman et al. 2013).”
InfluentialAn old problem with new solutions: Strategies to improve vaccine efficacy in the elderly
Bell, M. R., & Kutzler, M. A. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114175 · Cited by 29 · see citing works
The Central Nervous Mechanism of Stress-Promoting Cancer Progression
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“Although age does not result in a skew towards either phenotype [36], old mice seem to have higher numbers of M2 macrophages in the spleen, lymph nodes, and bone marrow [37].”
Park, H.-E., Lee, W., Choi, S., Jung, M., Shin, M., & Shin, S. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.931876 · Cited by 27 · see citing works
Counteracting Immunosenescence—Which Therapeutic Strategies Are Promising?
Hieber, C., Grabbe, S., & Bros, M. (2023) · Biomolecules · doi:10.3390/biom13071085 · Cited by 28 · see citing works
“In a geriatric mouse model, increased numbers of macrophages were observed in the bone marrow and in the spleen [43].”
BackgroundGDF15/MIC-1: a stress-induced immunosuppressive factor which promotes the aging process
Salminen, A. (2024) · Biogerontology · doi:10.1007/s10522-024-10164-0 · Cited by 29 · see citing works
“For instance, the presence of the M2 macrophages is upregulated not only in mouse bone marrow, spleen, and lymph nodes but also in lungs and skeletal muscles (Jackaman et al. 2013; Wang et al. 2015).”
Kassem, K. M., Ali, M., & Rhaleb, N. (2019) · Journal of Cardiovascular Pharmacology and Therapeutics · doi:10.1177/1074248419868699 · Cited by 26 · see citing works
“Furthermore, aging has been associated with suppressed M2 macrophage polarization and increased M1 macrophage polarization leading to enhanced inflammation and myocardial dysfunction as evident in SAMP8 aging mice heart.(82,86)”
BackgroundBloomer, S. A., Moyer, E. D., Brown, K. E., & Kregel, K. C. (2019) · Histochemistry and Cell Biology · doi:10.1007/s00418-019-01827-y · Cited by 26 · see citing works
Age-related macrophage alterations are associated with carcinogenesis of colorectal cancer
Li, Y., Zhao, Y., Gao, Y., Yu, L., Liu, M., Xu, N., & Zhu, H. (2022) · Carcinogenesis · doi:10.1093/carcin/bgac088 · Cited by 25 · see citing works
The role of immunosuppressive myofibroblasts in the aging process and age-related diseases
Salminen, A. (2023) · Journal of Molecular Medicine · doi:10.1007/s00109-023-02360-1 · Cited by 26 · see citing works
Duong, L., Pixley, F. J., Nelson, D. J., & Jackaman, C. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.848925 · Cited by 23 · see citing works
“, 2017), with expansion of monocyte and macrophage numbers (Strohacker et al., 2012; Jackaman et al., 2013; Puchta et al., 2016; Duong et al., 2018).”
BackgroundTakahashi, R., Totsuka, S., Ishigami, A., Kobayashi, Y., & Nagata, K. (2015) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/ggi.12436 · Cited by 24 · see citing works
Hepatic macrophage accumulation with aging: cause for concern?
Bloomer, S. A., & Moyer, E. D. (2021) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00286.2020 · Cited by 24 · see citing works
Immune senescence and periodontitis: From mechanism to therapy
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Immunoregulation of synovial macrophages for the treatment of osteoarthritis
Xu, M., & Ji, Y. (2023) · Open Life Sciences · doi:10.1515/biol-2022-0567 · Cited by 23 · see citing works
Ni, N. C., Jin, C. S., Cui, L., Shao, Z., Wu, J., Li, S.-H., Weisel, R. D., Zheng, G., & Li, R. (2016) · Molecular Imaging and Biology · doi:10.1007/s11307-015-0922-9 · Cited by 23 · see citing works
“Macrophages affect, and are affected by, environmental factors including local stem cells [5, 32] and organism aging [33, 34].”
BackgroundDAMPs and influenza virus infection in ageing
Samy, R. P., & Lim, L. H. K. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.005 · Cited by 22 · see citing works
Mikovic, J., Sadler, K. J., Butchart, L., Voisin, S. A. C., Gerlinger‐Romero, F., Gatta, P. A. D., Grounds, M. D., & Lamon, S. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00548 · Cited by 21 · see citing works
Hirata, H., Zhang, N., Ueno, M., Barati, D., Kushioka, J., Shen, H., Tsubosaka, M., Toya, M., Lin, T., Huang, E. E., et al. (2022) · Immunity & Ageing · doi:10.1186/s12979-022-00272-1 · Cited by 21 · see citing works
Aging on a different scale – chronological versus pathology-related aging
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“Immune responses, cell motility/adhesion and oxidative stress have been previously linked to (hepatic) injury and aging [87-98] and according to our results these related processes might be contributing factors to the biological diversity in hepatic injury and aging per individual.”
BackgroundImmunosenescence and age-related immune cells: causes of age-related diseases
Kim, N., Sim, S.-J., Han, H.-G., Yoon, J.-H., & Han, Y. (2024) · Archives of Pharmacal Research · doi:10.1007/s12272-024-01529-7 · Cited by 21 · see citing works
“Research also indicates an increase in CX3CR1 hi Ly6 lo macrophages in the peritoneum of aged mice, exhibiting an anti-inflammatory phenotype (Jackaman et al. 2013).”
Salminen, A. (2024) · Biogerontology · doi:10.1007/s10522-024-10114-w · Cited by 20 · see citing works
“For instance, several investigators have revealed that the populations of regulatory T cells (Treg), myeloid-derived suppressor cells (MDSC), and M2 macrophages were augmented in aged tissues (Griz-zle et al. 2007; Enioutina et al. 2011; Jackaman et al. 2013; Garg et al. 2014; Ruhland et al. 2016).”
BackgroundThe emerging importance of lymphangiogenesis in aging and aging-associated diseases
Ji, R. (2024) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2024.111975 · Cited by 19 · see citing works
“IL-2-/CD40-activated macrophages rescue T-cell production of IFN-γ in geriatric mice, thus targeting these factors can improve innate and T-cell immunity in aging hosts (Jackaman et al., 2013).”
BackgroundZiogas, D. C., Theocharopoulos, C., Aravantinou-Fatorou, K., Boukouris, A. E., Stefanou, D. T., Anastasopoulou, A. N., Lialios, P., Lyrarakis, G., & Gogas, H. J. (2025) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2025.104635 · Cited by 19 · see citing works
- Authors
- Jackaman, C., Radley‐Crabb, H. G., Soffe, Z., Shavlakadze, T., Grounds, M. D., & Nelson, D. J.
- Affiliations
- Curtin University (AU)
- The University of Western Australia (AU)
- Corresponding author
- Jackaman, Connie
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2013-03-27
- Volume
- 12
- Issue
- 3
- Pages
- 345-357
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- OpenAlex
- W2097861054
- Cited by
- 162
- References
- 45
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 19 · 2023: 14 · 2022: 20 · 2021: 15 · 2020: 11 · 2019: 13 · 2018: 8 · 2017: 14 · 2016: 11 · 2015: 7 · 2014: 4 · 2013: 5
- FWCI
- 4.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- eSpace (Curtin University) (submittedVersion)
- Funders
- Australian Government
- Curtin University of Technology
- Cancer Council Western Australia
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- macrophages, myeloid-derived suppressor cells, aging, M2 macrophages, CD40, CX3CR1, TGF-beta, IL-4, tumor microenvironment, mesothelioma, lung cancer, allogeneic T cell proliferation, interferon-gamma, anti-CD40 antibody, interleukin-2, immunotherapy
- MeSH terms
- CX3C Chemokine Receptor 1, Aging, Animals, Immunity, Innate, Interferon-gamma, Interleukin-2, Lung Neoplasms, Lymphocyte Activation, Macrophages, Mesothelioma, Mice, Inbred C57BL, CD4-Positive T-Lymphocytes, Interleukin-4, Transforming Growth Factor beta, Cellular Senescence, Culture Media, Conditioned, CD8-Positive T-Lymphocytes, CD40 Antigens, Receptors, Chemokine, Cell Line, Tumor, Cell Proliferation, Mice, Tumor Microenvironment
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