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Seasonal plasticity in immunocompetent cytokines (IL-2, IL-6, and TNF-α), myeloid progenitor cell (CFU-GM) proliferation, and LPS-induced oxido-inflammatory aberrations in a tropical rodent Funambulus pennanti: role of melatonin

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Cell Stress and Chaperones Aims and scope

Abstract

In seasonal breeders, photoperiods regulate the levels of circulatory melatonin, a well-known immunomodulator and an antioxidant. Melatonin is known to play a complex physiological role in maintaining the immune homeostasis by affecting cytokine production in immunocompetent cells. In this study, we have quantified seasonal and temporal variations in immunocompetent cytokines—IL-2, IL-6, and TNF-α—and circulatory corticosterone along with in- vitro proliferation of bone marrow-derived granulocyte macrophage-colony forming unit (CFU-GM) progenitor cells of a tropical seasonal breeder Funambulus pennanti (northern palm squirrel). Transient variations in antioxidant status of seasonal breeders might be due to the fluctuations associated with immunity and inflammation. Further, to establish a direct immunomodulatory effect of photoperiod, we recorded the LPS-induced oxidative and inflammatory responses of squirrels by housing them in artificial photoperiodic chambers mimicking summer and winter seasons respectively. We observed a marked variation in cytokines level, melatonin, and corticosterone , and CFU-GM cell proliferation during summer and winter seasons. High Peripheral melatonin levels directly correlated with cytokine IL-2 levels, and inversely correlated with TNF-α, and circulatory corticosterone level. LPS-challenged squirrels housed in short photoperiod (10L:14D; equivalent to winter days) showed a marked reduction in the components of the inflammatory cascade, CRP, TNF-α, IL-6, NOx, NF-κB, Cox-2, and PGES, with an overall improvement in antioxidant status when compared to squirrels maintained under a long photoperiod (16L:8D; equivalent to summer days). Our results underline the impact of seasonality, photoperiod, and melatonin in maintaining an intrinsic redox-immune homeostasis which helps the animal to withstand environmental stresses.

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Acknowledgements

The authors are thankful to the University Grants Commission, Center for Advanced Studies Scheme-R/Dev/IX-Sch. SRF-JRF-CAS-Zoology/78184, New Delhi, for providing financial assistance to Ms. Shraddha Rastogi. The instrument subsidiary award from the Alexander Von Humboldt Foundation, Bonn, Germany, to Prof. C. Haldar is gratefully acknowledged.

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Shraddha Rastogi: study conception and design, data collection, analysis and interpretation of the result, and manuscript preparation. Chandana Haldar: conceptualization and supervision, funding acquisition, and critical revision of the article. The authors have read and approved the manuscript.

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Correspondence to Chandana Haldar.

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Rastogi, S., Haldar, C. Seasonal plasticity in immunocompetent cytokines (IL-2, IL-6, and TNF-α), myeloid progenitor cell (CFU-GM) proliferation, and LPS-induced oxido-inflammatory aberrations in a tropical rodent Funambulus pennanti: role of melatonin. Cell Stress and Chaperones 28, 567–582 (2023). https://doi.org/10.1007/s12192-022-01313-w

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