切除肩胛间褐色脂肪组织对雌性黑线仓鼠免疫功能的影响

doi:10.16829/j.slxb.150989

摘要/Abstract

摘要： 为了解产热对动物免疫能力的影响，通过肩胛间褐色脂肪组织(interscapular brown adipose tissue,IBAT)切除术和低温处理，将雌性黑线仓鼠(Cricetulus barabensis)随机分为常温假切组(warm BAT sham-removed group,WS, n=5)、低温假切组(cold BAT sham-removed group,CS,n=7)和低温切除组(cold BAT removed group, CR, n=8)，比较了产热和免疫器官大小及血液指标和免疫功能的差异。结果发现，切除IBAT或逐渐降温均不影响雌性黑线仓鼠的体质量和身体成分，但低温导致总脂肪质量下降。切除IBAT不影响肝脏、脾脏和胸腺等器官的鲜质量，提示器官水平产热和免疫之间无权衡关系，但逐渐降温增加了小肠鲜质量及长度、结肠鲜质量、总消化道长，暗示为满足低温下的高能量需求，其加工食物的能力和消化能力均有所增强。切除IBAT或逐渐降温不影响植物血球凝集素反应峰值，以及白细胞、淋巴细胞、中间粒细胞和中性粒细胞的数量。低温或切除IBAT不影响雌性黑线仓鼠的免疫功能。

关键词: 黑线仓鼠, 褐色脂肪组织切除,免疫功能, 血液学, 逐渐降温

Abstract: In order to understand the effect of thermogenic capacity on immune function in animals, female striped hamsters (Cricetulus barabensis) were randomly assigned into the warm interscapular brown adipose tissue (IBAT) sham-removed group (WS, n = 5), the cold IBAT sham-removed group (CS, n = 7), and the cold IBAT removed group (CS, n = 8). IBAT removal or gradually decreased temperature had no effect on body mass and body composition. However, low temperature reduced total body fat mass. IBAT removal did not affect organ wet masses including liver, thymus, and spleen, indicating there was no trade-off between thermogenesis and immunity at organ size levels. However, gradually decreased temperature increased the wet mass of small intestine and colon, the length of small intestine and total digestive tract, indicating the increase of the food processing and digestive capacities to satisfy the enhancement of energy requirements under the condition of low temperature. IBAT removal or gradually decreased temperature had no influence on the wet mass of thymus and spleen, the maximal phytohaemagglutinin (PHA) response, as well as the number of white blood cells, lymphocytes, intermediate granulocytes, and neutrophil granulocytes, suggesting that no trade-offs relationship might occur between immune function and thermogenic capacity. In summary, IBAT removal or gradually decreased temperature had no effect on immune function in striped hamsters.

Key words: Striped hamsters (Cricetulus barabensis), Brown adipose tissue removal, Immune function, Hematology, Gradually decreased temperature

中图分类号:

Q958.1

徐德立, 王逸, 张学英, 王德华. 切除肩胛间褐色脂肪组织对雌性黑线仓鼠免疫功能的影响[J]. 兽类学报, 2025, 45(4): 457-467.

XU Deli, WANG Yi, ZHANG Xueying, WANG Dehua. Effect of interscapular brown adipose tissue removal on immune function in female striped hamsters[J]. ACTA THERIOLOGICA SINICA, 2025, 45(4): 457-467.

参考文献

Ahima R S, Flier J S. 2000. Adipose tissue as an endocrine organ [J]. Trends in Endocrinology and Metabolism, 11: 327-332.
Bellocq J G, Krasnov B R, Khokhlova I S, Pinshow B. 2006. Temporal dynamics of a T-cell mediated immune response in desert rodents [J]. Comparative Biochemistry and Physiology Part A, 145:554-559.
Calder P C, Kew S. 2002. The immune system: a target for functional foods? [J]. British Journal of Nutrition, 88: S165-176.
Cannon B, Nedergaard J A N. 2004. Brown adipose tissue: function and physiological significance [J]. Physiological Reviews, 84:277-359.
Chi Q S, Wang D H. 2011. Thermal physiology and energetics in male desert hamsters (Phodopus roborovskii) during cold acclimation [J]. Journal of Comparative Physiology B, 181: 91-103.
Demas G E, Chefer V, Talan M I, Nelson R J. 1997. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice [J]. American Journal of Physiology-Regulatory, Intergrative and Comparative Physiology, 273: 1631-1637.
Demas G E, Drazen D L, Nelson R J. 2003. Reductions in total body fat decrease humoral immunity [J]. Proceedings of the Royal Society B, 270: 905-911.
Demas G E, Nelson R J. 1998. Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus) [J]. Journal of Biological Rhythms, 13: 253-262.
Demas G E. 2004. The energetics of immunity: a neuroendocrine link between energy balance and immune function [J]. Hormone and Behavior, 45: 173-180.
Daan S, Masman D, Groenewold A. 1990. Avian basal metabolic rates: their association with body composition and energy expenditure in nature [J]. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 259: R333-340.
Hadri L E, Garlich J D, Qureshi M A, Ferket P R, Odetallah N H. 2004. Glucose and electrolyte supplementation of drinking water improve the immune responses of poults with inanition [J]. Poultry Science, 83: 803-809.
Hammond K A, Wunder B A. 1995. Effect of cold temperatures on the morphology of gastrointestinal tracts of two microtine rodents [J]. Journal of Mammalogy, 76: 232-239.
Hayward J, Davies P. 1972. Evidence for the mediatory role of brown adipose tissue during nonshivering thermogenesis in the cold-acclimated mouse [J]. Canadian Journal of Physiology and Pharmacology, 50: 168-170.
Heldmaier G, Buchberger A. 1985. Sources of heat during nonshivering thermogenesis in Djungarian hamsters: a dominant role of brown adipose tissue during cold adaptation [J]. Journal of Comparative Physiology B, 156: 237-245.
Heldmaier G, Steinlechner S, Rafael J, Latteier B. 1982. Photoperiod and ambient temperature as environmental cues for seasonal thermogenic adaptation in the Djungarian hamster, Phodopus sungorus [J]. International Journal of Biometeorology, 26: 339-345.
Horwitz B A, Detrick J F, Smith R E. 1972. Norepinephrine-induced thermogenesis: effect of interscapular brown fat [J]. Cellular and Molecular Life Sciences, 28: 284-286.
Houston A I, McNamara J M, Barta Z, Klasing K C. 2007. The effect of energy reserves and food availability on optimal immune defence [J]. Proceedings of the Royal Society B, 274: 2835-2842.
Hull D, Segall M. 1965. The contribution of brown adipose tissue to heat production in the new-born rabbit [J]. The Journal of Physiology, 181: 449-457.
Janković B D, Janezíc A, Popesković L. 1975. Brown adipose tissue and immunity: effect of neonatal adipectomy on humoral and cellular immune reactions in the rat [J]. Immunology, 28: 597-609.
Kaminogawa S, Nanno M. 2004. Modulation of immune functions by foods [J]. eCAM, 1. DOI: 10. 1093/ecam/neh042.
Keipert S, Gaudry M J, Kutschke M, Keuper M, Dela Rosa M A S, Cheng Y M, Kuhn J M M, Laterveer R, Cotrim C A, Giere P, Perocchi F, Feederle R, Crichton P G, Lutter D, Jastroch M. 2024. Two-stage evolution of mammalian adipose tissue thermogenesis [J]. Science, 384: 1111-1117.
Kim J H, Kang J C. 2016. Changes in hematological parameters, plasma cortisol, and acetylcholinesterase of juvenile rockfish, Sebastes schlegelii supplemented with the dietary ascorbic acid [J]. Aquaculture Reports, 4: 80-85.
Liu M, Zhang X Y, Wang C Z, Wang D H. 2023. Recruitment of muscle genes as an effect of brown adipose tissue ablation in cold-acclimated Brandt’s voles (Lasiopodomys brandtii) [J]. International Journal of Molecular Sciences, 24 (1). DOI: 10. 3390/ijms24010342.
Lu H Q, Li Y C, Zhang X D. 1987. Age determination, age structure and population dynamics of striped hamster [J]. Acta Theriologica Sinica, 7: 28-34. (in Chinese)
Maciver N J, Jacobs S R, Wieman H L, Wofford J A, Coloff J L, Rathmell J C. 2008. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival [J]. Journal of Leukocyte Biology, 84: 949-957.
Martin L B, Weil Z M, Nelson R J. 2007. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs [J]. Philosophical Transactions of the Royal Society B, 363 (1490):321-339.
Martin L B, Weil Z M, Bowers S L, Nelson R J. 2008. Sex-specific effects of glucose deprivation on cell-mediated immunity and reproduction in Siberian hamsters (Phodopus sungorus) [J]. Journal of Comparative Physiology B, 178: 623-628.
Matarese G, Cava A L. 2004. The intricate interface between immune system and metabolism [J]. Trends in Immunology, 25: 193-200.
Moret Y, Schmid-Hempel P. 2000. Survival for immunity: the price of immune system activation for bumblebee workers [J]. Science, 290: 1166-1168.
Nelson R J, Demas G E. 1996. Seasonal changes in immune function [J]. Quarterly Review of Biology, 71: 511-548.
Nelson R J. 2004. Seasonal immune function and sickness responses [J]. Trends in Immunology, 25: 187-192.
Sakers A, Siqueira M K D, Seale P, Villanueva C J. 2022.Adipose-tissue plasticity in health and disease [J]. Cell, 185:419-446.
Schäffler A, Schölmerich J, Salzberger B. 2007. Adipose tissue as an immunological organ: Toll-like receptors, C1q/TNFs and CTRPs [J]. Trends in Immunology, 28: 393-399.
Schwenke R A, Lazzaro B P, Wolfner M F. 2016.Reproduction-immunity trade-offs in insects [J]. Annual Review of Entomology, 61: 239-256.
Smith K G, Hunt J L. 2004. On the use of spleen mass as a measure of avian immune system strength [J]. Oecologia, 138: 28-31.
Smits J E, Bortolotti G R, Tella J L. 1999. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence [J]. Functional Ecology, 13: 567-572.
Trayhurn P. 2005. Endocrine and signalling role of adipose tissue:new perspectives on fat [J]. Acta Physiologica Scandinavica, 184: 285-293.
Xu D L, Hu X K, Tian Y F. 2017. Effect of temperature and food restriction on immune function in striped hamsters (Cricetulus barabensis) [J]. Journal of Experimental Biology, 220: 2187-2195.
Xu D L, Hu X K. 2017. Photoperiod and temperature differently affect immune function in striped hamsters (Cricetulus barabensis) [J]. Comparative Biochemistry and Physiology Part A, 204:211-218.
Xu D L, Hu X K, Tian Y F. 2018. Seasonal variations in cellular and humoral immunity in male striped hamsters (Cricetulus barabensis) [J]. Biology Open, 7: 1-8.
Xu D L, Hu X K. 2020. Season and sex have different effects on hematology and cytokines in striped hamsters (Cricetulusbarabensis) [J]. Journal of Comparative Physiology B, 190: 87-100.
Xu D L, Hu X K, Tian Y F, Wang D H. 2021. Seasonal changes in immune function in female striped hamsters [J]. Acta Ecologica Sinica, 41 (2): 182-192. (in Chinese)
Xu D L, Xu L X. 2015. Effect of food restriction on immune function in the striped hamster (Cricetulus barabensis) [J]. Acta Ecologica Sinica, 35: 1882-1890. (in Chinese)
Xu D L, Xu M M, Wang D H. 2019b. Effects of air temperatures on antioxidant defense and immunity in Mongolian gerbils [J]. Journal of Thermal Biology, 84: 111-120.
Xu D L, Xu M M, Wang D H. 2019a. Effect of temperature on antioxidant defense and innate immunity in Brandt’s voles [J]. Zoological Research, 40: 305-316.
Xu D L, Wang D H. 2010. Fasting suppresses T cell-mediated immunity in female Mongolian gerbils (Meriones unguiculatus) [J]. Comparative Biochemistry and Physiology Part A, 155: 25-33.
Xu D L, Wang D H. 2011. Glucose supplement reverses the fasting-induced suppression of cellular immunity in Mongolian gerbils (Meriones unguiculatus) [J]. Zoology, 114: 306-312.
Xu D L, Wang D H. 2012. Advances in ecological immunology [J]. Acta Ecologica Sinica, 32: 6251-6258. (in Chinese)
Xu D L, Zhao M X. 2022. Leptin mediates the suppressive effect of partial fat removal on cellular and humoral immunity in striped hamsters [J]. Comparative Biochemistry and Physiology Part A, 271. DOI: 10. 1016/j. cbpa. 2022. 111256.
Xu D L, Wang Y H. 2023. Effect of gradual increase and decrease in temperature on innate, cellular and humoral immunity in striped hamsters [J]. Mammalian Biology, 103: 265-276.
Yang D B, Xu Y C, Wang D H. 2012. Partial removal of brown adipose tissue enhances humoral immunity in warm-acclimated Mongolian gerbils (Meriones unguiculatus) [J]. General and Comparative Endocrinology, 175: 144-152.
Yu Y, Zhao M X, Wang Y H, Zhang X Y, Xu D L, Wang D H. 2022. Seasonal changes in immune function in female striped hamsters [J]. Acta Theriologica Sinica, 42: 286-294. (in Chinese)
Zang Z Q, Huang S L, Zhao Z J. 2015a. Response patterns of phytohemagglutinin-induced skin swelling at different reproductive phases in female striped hamster (Cricetulus barabensis) [J]. Acta Theriologica Sinica, 35: 74-79. (in Chinese)
Zang Z Q, Huang S L, Zhao Z J. 2015b. No simultaneous increase of humoral immune response and resting metabolic rate in striped hamsters followed a single KLH challenge [J]. Acta Theriologica Sinica, 35: 405-411. (in Chinese)
Zhang X Y, Wang D H. 2007. Thermogenesis, food intake and serum leptin in cold-exposed lactating Brandt’s voles (Lasiopodomys brandtii) [J]. Journal of Experimental Biology, 210: 512-521.
Zhang X Y, Wang D H. 2006. Energy metabolism, thermogenesis and body mass regulation in Brandt’s voles (Lasiopodomys brandtii) during cold acclimation and rewarming [J]. Hormones and Behavior, 50: 61-69.
Zhang Z Q, Wang D H. 2006. Seasonal changes in immune function, body fat mass and organ mass in Mongolian gerbils (Meriones unguiculatus) [J]. Acta Theriologica Sinica, 26: 338-345. (in Chinese)
Zhang Z Q, Zhao Z J. 2015. Correlations between phytohemagglutinin response and leukocyte profile, and bactericidal capacity in a wild rodent [J]. Integrative Zoology, 10: 302-310.
Zhang Z B, Wang Z W. 1998. Ecology and Management of Rodent Pests in Agriculture [M]. Beijing: Ocean Publishing House.
Zhao Z J, Cao J. Meng X L, Li Y B. 2010. Seasonal variations in metabolism and thermoregulation in the striped hamster (Cricetulus barabensis) [J]. Journal of Thermal Biology, 35: 52-57.
Zhao Z J. 2011. Serum leptin, energy budget and thermogenesis in striped hamsters exposed to consecutive decrease in ambient temperatures [J]. Physiological and Biochemical Zoology, 84:560-72.
Zysling D A, Demas G E. 2007. Metabolic stress suppresses humoral immune function in long-day, but not short-day, Siberian hamsters(Phodopus sungorus) [J]. Journal of Comparative Physiology B, 177: 339-347.
于祎, 赵明星, 王玉辉, 张学英, 徐德立, 王德华. 2022. 花生对非繁殖期雌性黑线仓鼠细胞免疫和血液指标的影响 [J]. 兽类学报, 42 (3): 286-294.
卢浩泉, 李玉春, 张学栋. 1987. 黑线仓鼠种群年龄组成及其数量季节消长的研究 [J]. 兽类学报, 7 (1): 28-34.
张志强, 王德华. 2006. 长爪沙鼠免疫功能、体脂含量和器官重量的季节变化 [J]. 兽类学报, 26 (4): 338-345.
张志强, 黄淑丽, 赵志军. 2015a. 不同繁殖状态雌性黑线仓鼠对植物血凝素的反应模式 [J]. 兽类学报, 35 (1): 74-79.
张志强, 黄淑丽, 赵志军. 2015b. KLH 单独刺激不影响黑线仓鼠的静止代谢率 [J]. 兽类学报, 35 (4): 405-411.
张知彬, 王祖望. 1998. 农业重要害鼠的生态学及控制对策 [M]. 北京: 海洋出版社, 1-286.
徐德立, 王德华. 2012. 生态免疫学研究进展 [J]. 生态学报, 32(19): 6251-6258.
徐德立, 胡晓凯, 田玉芬, 王德华. 2021. 雌性黑线仓鼠免疫功能的季节变化 [J]. 兽类学报, 41 (2): 182-192.
徐德立, 徐来祥. 2015. 食物限制对黑线仓鼠免疫功能的影响 [J]. 生态学报, 35 (6): 1882-1890.

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