研究论文

麋鹿角脱落和再生与血液激素含量的关系

  • 孟庆辉 ,
  • 夏志强 ,
  • 单云芳 ,
  • 李俊芳 ,
  • 贺永惠 ,
  • 崔艳红 ,
  • 胡华刚 ,
  • 肖璇 ,
  • 白加德 ,
  • 钟震宇 ,
  • 孟秀祥 ,
  • 张付贤 ,
  • 柏超 ,
  • 张成林
展开
  • 1 北京市科学技术研究院北京麋鹿生态实验中心, 北京 100076;
    2 麋鹿国家保护研究中心, 北京 100076;
    3 河南科技学院, 新乡 453003;
    4 北京小汤山医院, 北京 102211;
    5 中国人民大学环境学院, 北京 100081;
    6 长江大学动物科学学院, 荆州 434023;
    7 北京动物园, 北京 100044
孟庆辉(1982-),男,博士,研究员,主要从事动物生态及麋鹿保护研究.

收稿日期: 2023-03-16

  修回日期: 2024-01-25

  网络出版日期: 2025-01-23

基金资助

北京自然科学基金(5212003,5252004);北京动物园圈养野生动物技术北京市重点实验室开放课题(ZDK202101)

Relationship between the level of blood hormones and the shedding and regeneration of male Père David’s deer (Elaphurus davidianus) antlers

  • MENG Qinghui ,
  • XIA Zhiqiang ,
  • SHAN Yunfang ,
  • LI Junfang ,
  • HE Yonghui ,
  • CUI Yanhong ,
  • HU Huagang ,
  • XIAO Xuan ,
  • BAI Jiade ,
  • ZHONG Zhenyu ,
  • MENG Xiuxiang ,
  • ZHANG Fuxian ,
  • BAI Chao ,
  • ZHANG Chenglin
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  • 1 Beijing Père David's Deer Ecological Research Center, Beijing Academy of Science and Technology, Beijing 100076, China;
    2 National Deer Conversation and Research Center, Beijing 100076, China;
    3 Henan Institute of Science and Technology, Xinxiang 453003, China;
    4 Beijing Xiaotangshan Hospital, Beijing 102211, China;
    5 School of Environmental Sciences, Renmin University of China, Beijing 100081, China;
    6 College of Animal Science, Yangtze University, Jingzhou 434023, China;
    7 Beijing Zoo, Beijing 100044, China

Received date: 2023-03-16

  Revised date: 2024-01-25

  Online published: 2025-01-23

摘要

麋鹿(Elaphurus davidianus)冬至解角,激素在茸软骨再生过程中起重要作用。本文采集麋鹿血液样品,测定激素含量,进行年度节律、冬至前(11—12月)后(翌年1—3月)比对及茸生长期(冬至—惊蛰,12月至翌年3月)波动变化的递进分析,以期为鹿茸软骨再生与激素含量关系的研究提供进一步印证。结果显示:(1)血液雌二醇(Estradiol,E2)、睾酮(Testosterone,T)、生长激素(Growth Hormone,GH)、胰岛素样生长因子1(Insulin-likeGrowth Factor 1,IGF-1)、褪黑素(Melatonin,MT)的含量均存在显著(F11,486=3.98,n=507,P=0.004)的年节律变化;血液甲状旁腺激素(Parathyroid hormone,PTH)含量与茸骨化呈现同步(F11,486=1.72,n=507,P=0.081)的月规律变化。(2)冬至后麋鹿茸血液中E2、GH、T和PTH含量开始逐渐提升,IGF-1含量上升滞后。(3)整个生茸期,血液IGF-1、MT、GH、T、E2含量与麋鹿茸再生速度显著正相关,血液PTH含量与鹿茸增重显著正相关。其中在麋鹿茸胚孕育的Ⅰ期和茸的萌发Ⅱ期,大雪节气(12月初)时,血液MT、GH、IGF-1含量开始增加,E2与T的含量处于年度的次高峰期;麋鹿茸的缓慢生长Ⅲ期和级数增长Ⅳ期,冬至(12月22日)后,麋鹿茸血中MT、GH、IGF-1含量急剧上升(F3,80=4.69,n=84,P=0.002);E2的含量先下降后上升,差异显著(F3,80=3.14,n=84,P=0.045),T的含量则由(0.696 9 ±0.09) ng/mL (n=84)下降至(0.664 7 ±0.06) ng/mL (n=84),差异不显著(F3,80=5.79,P=0.178)。茸增长停滞的Ⅴ期,雨水节气(2月底)后,血液中GH含量明显回落,差异显著(F3,80=3.25,n=84,P=0.037),E2与T的含量则持续提升。PTH含量在脱角前及整个生茸期均处于不断提升中,由立冬节气的(11.78 ±2.54) pg/mL (n=22)上升到春分节气的(69.23 ±7.89) pg/mL (n=22),两者差异极显著(F1,20=4.44,P=0.001)。可见,E2、MT、GH、IGF-1、T和PTH均参与冬季麋鹿茸再生全过程,冬至低生理浓度褪黑素和睾酮与麋鹿角脱落相关。本研究可为冬季改善雄性麋鹿的饲养条件提供依据,同时为激素对软骨增殖调控及茸再生多样化机制的研究提供助益。

本文引用格式

孟庆辉 , 夏志强 , 单云芳 , 李俊芳 , 贺永惠 , 崔艳红 , 胡华刚 , 肖璇 , 白加德 , 钟震宇 , 孟秀祥 , 张付贤 , 柏超 , 张成林 . 麋鹿角脱落和再生与血液激素含量的关系[J]. 兽类学报, 2025 , 45(1) : 86 -95 . DOI: 10.16829/j.slxb.150791

Abstract

The antlers of male Père David’s deer (Elaphurus davidianus) were shed during the winter solstice, and hormones play a crucial role in the regeneration of antler cartilage. This study collected blood samples from male Père David’s deer (Elaphurus davidianus) to measure hormone levels, comparing pre-winter solstice (November-December) and post-winter solstice (January-March) periods, as well as analyzing the fluctuations during the antler growth period (Winter Solstice-Start of Insects Awakening, December to March of the following year). The aim is to provide further evidence for the relationship between antler cartilage regeneration and hormone levels. Results showed that blood estradiol (E2), testosterone (T), growth hormone (GH), insulin-like growth factor-1 (IGF-1), and melatonin (MT) levels exhibited significant annual rhythmic changes (F11,486= 3. 98, n = 507, P = 0.004). Blood parathyroid hormone (PTH) levels showed synchronous monthly changes with antler ossification (F11,486= 1. 72, n = 507, P = 0.081). After the winter solstice, blood E2, GH, T, and PTH levels in deer antlers began to gradually increase, while IGF-1 levels increased later. Throughout the antler growth period, blood IGF-1, MT, GH, T, and E2 levels were significantly positively correlated with the regeneration speed of deer antlers, while blood PTH levels were significantly positively correlated with antler weight gain. During the Major Snow solar term (early December), the content of MT, GH, and IGF-1 in the blood began to increase, and the content of E2 and T was at the second peak of the year, which was extremely significantly different from the content of E2 and T during the breeding season of male deer (F7,152 = 4. 08, n = 160, P = 0.003). During the winter solstice, the slow growth phase Ⅲ and the rapid growth phase Ⅳ of the antlers, the content of MT, GH, and IGF-1 in the blood of deer antlers increased sharply (F3,80 = 4. 69, n = 84, P = 0.002); the content of E2 first decreased and then increased, with significant differences (F3,80 = 3. 14, n = 84, P = 0.045), while the content of T decreased from (0. 696 9 ±0. 09) ng/mL (n = 84) to (0. 664 7 ±0. 06) ng/mL (n = 84), with no significant difference (F3,80 = 5. 79, P = 0.178). After the Rainwater solar term (late February), during the stagnation and ossification phase V of antler growth, the content of GH in the blood decreased significantly, with significant differences (F3,80 = 3. 25, n = 84, P = 0.037), while the content of E2 and T continued to increase. PTH levels continued to rise before shedding and throughout the antler growth period, increasing from (11. 78 ±2. 54) pg/mL (n = 22) during the Major Snow solar term to (69. 23 ±7. 89) pg/mL (n = 22) during the Vernal Equinox solar term, with extremely significant differences (F1,20 = 4. 44, P = 0.001). In conclusion, E2, MT, GH, IGF-1, T, and PTH are all involved in the entire process of winter antler regeneration in deer antlers. Low physiological concentrations of melatonin and testosterone during the winter solstice are directly related to antler shedding. This study can provide a basis for improving the breeding conditions of male deer in winter and contribute to research on the regulation of cartilage proliferation by hormones and the diverse mechanisms of antler regeneration.

参考文献

Bao J R, Li C Y, Xing X M, Yang F H. 2008. Research progress in deer antler regeneration and stem cells. Journal of Clinical Reha-bilitative Tissue Engineering Research, 12 (51):10163-10166.(in Chinese)
Bowyer R T. 1991. Timing of parturition and lactation in southern mule deer. Journal of Mammalogy, 72 (1):138-145.
Chen L, Qiu Q, Jiang Y, Wang K, Lin Z S, Li Z P, Bibi F, Yang Y Z, Wang J H, Nie W H, Su W T, Liu G C, Li Q Y, Fu W W, Pan X Y, Liu C, Yang J, Zhang C Z, Yin Y, Wang Y, Zhao Y, Zhang C, Wang Z K, Qin Y L, Liu W, Wang B, Ren Y D, Zhang R, Zeng Y, Da Fonseca R R, Wei B, Li R, Wan W T, Zhao R P, Zhu W B, Wang Y J, Duan S C, Gao Y, Zhang Y E, Chen C Y, Hvilsom C, Epps C W, Chemnick L G, Dong Y, Mirarab S, Siegismund H R, Ryder O A, Gilbert M T P, Lewin H A, Zhang G J, Heller R, Wang W. 2019. Large-scale ruminant genome sequencing provides in-sights into their evolution and distinct traits. Science, 364 (6446).DOI:10.1126/science. aav6202.
Clements M N, Clutton-Brock T H, Albon S D, Pemberton J M, Kruuk L E B. 2010.Getting the timing right:antler growth phenology and sexual selection in a wild red deer population. Oecologia, 164 (2):357-368.
Clutton-Brock T H, Albon S D, Guinness F E. 1989. Fitness costs of gestation and lactation in wild mammals. Nature, 337 (6204):260-262.
Festa-Bianchet M, Coltman D W, Turelli L, Jorgenson J T. 2004.Relative allocation to horn and body growth in bighorn rams var-ies with resource availability. Behavioral Ecology, 15 (2):305-312.
Goss R J. 1980. Photoperiodic control of antler cycles in deer. V. Re-versed seasons. Journal of Experimental Zoology, 211 (1):101-105.
Hu P F, Xu J P, Ai C, Shao X J, Wang H L, Dong Y M, Cui X Z, Xing X M. 2017. Screening weight related genes of velvet antlers by whole genome re-sequencing. Hereditas, 39 (11):1090-1101.(in Chinese)
Hu T C, Liu Y M, Tao R S, Su F Y, hang J, Gu X Y, Li Q J, Wang Q K. 2015. Advances on the chemical components and pharmacologi-cal activities of velvet antler. Journal of Economic Animal, 19(3):156-162. (in Chinese)
Li C W, Jiang Z G, Zeng Y, You Z Q. 2005. Rutting tactics in Père Da-vid's deer stags under different population densities and during different rut periods. Biodiversity Science, 13 (5):424-431. (in Chinese)
Li C Y, Liu Z A, Zhao S Z, Du Y C. 1988. Variation of testosterone and estradiol levels in plasma during every stage of growth of sika deer antler. Acta Theriologica Sinica, 8 (3):224-231. (in Chinese)
Li C Y, Suttie J M. 2001. Deer antlerogenic periosteum:a piece of postnatally retained embryonic tissue? Anatomy and Embryology, 204 (11):375-388.
Li C Y. 2017. Progress on the mechanism underlying full regeneration of mammalianorgan deer antlers. Journal of Agricultural Bio-technology, 25 (1):1-10.(in Chinese)
Li H D, Zhou Y, Zhang H Y, Zheng J J, Liu L L, Ba H X, Wang G W. 2023. Correlation and regression analysis between body mass and body ruler index of sika deer. Special Wild Economic Animal and Plant Research, 45 (3):127-133. (in Chinese)
Li K K, Sun X Y, Chen C, Jing H S, Xu X L, You S, Zhao J B, Xiong J J. 2020. Effect of exogenous melatonin on the growth and devel-opment of antler chondrocytes. China Animal Husbandry & Vet-erinary Medicine, 47 (7):1997-2004. (in Chinese)
Li Y W. 2022. Analysis and guiding significance of examination re-sults of six levels of sex hormones in 91 infertile women. Journal of Rare and Uncommon Diseases, 29 (2):108-110.(in Chinese)
Lin Z S, Chen L, Chen X Q, Zhong Y B, Yang Y, Xia W H, Liu C, Zhu W B, Wang H, Yan B Y, Yang Y F, Liu X, Kvie K S, Røed K H, Wang K, Xiao W H, Wei H J, Li G Y, Heller R, Gilbert M T P, Qiu Q, Wang W, Li Z P. 2019. Biological adaptations in the Arc-tic cervid, the reindeer (Rangifer tarandus). Science, 364 (6446):DOI:10.1126/science. aav6312.
Liu H, Liu Z, Wang Q W, Zhang W, Wang W Y, Li C Y, Wang G W. 2017. Effect of androgen on development and regeneration of ant-ler. Progress in Veterinary Medicine, 38 (5):113-116. (in Chinese)
Liu W, Li T, Yu R, Xie L, Gao X. 2017. Analysis of the pathological changes and sex hormones in 147 cases of Sertoli cell only syn-drome. Journal of Shandong University (Health Sciences), 55(1):75-79, 84. (in Chinese)
Liu Z K, Zhou S L, Wu S Z. 1982. Some experiments concerning the effect of androgen on the growth of antlers. Journal of Sichuan University (Natural Science Edition), 19 (1):83-88. (in Chinese)
Meng Q H, Bai C, Song Y, Shan Y F, Li J F, Zhang S M, Bai J D, Zhong Z Y, Zhang C L, Meng X X. 2022. Timing and synchrony of births in reintroduced Père David's deer (Elaphurus davidi-anus). Acta Theriologica Sinica, 42 (4):379-386. (in Chinese)
Meng Q H, Xia Z Q, Shan Y F, Li J F, Hu H G, Xiao X, Bai J D, Zhong Z Y, Meng X X, Zhang F X, Bai C, Zhang C L. 2024a. Ef-fects of light duration times on the ecological overflow of antler growth and reproductive dominance of male Père David's deer(Elaphurus davidianus). Acta Ecologica Sinica, 44 (10):4368-4376. (in Chinese)
Meng Q H, Xia Z Q, Shan Y F, Li J F, Hu H G, Xiao X, Bai J D, Zhong Z Y, Meng X X, Bai C, Zhang C L. 2024b. Analysis of age factors affecting the branching velvet and weight of antlers in Père David's deer (Elaphurus davidianus). Acta Theriologica Si-nica, 44 (3):377-384. (in Chinese)
Qin T, Zhang G K, Zheng Y, Li S Y, Yuan Y, Li Q J, Hu M L, Si H Z, Wei G N, Gao X L, Cui X X, Xia B, Ren J, Wang K, Ba H X, Liu Z, Rasmus Heller, Li Z P, Wang W, Huang J H, Li C Y, Qiu Q. 2023. A population of stem cells with strong regenerative poten-tial discovered in deer antlers. Science, 379 (6634):840-847.
Tao D Y. 2016. Study on velvet antler ossification and the relationship between the calcification and its related factors in Tarim red deer(Cervus elaphus). Ph. D thesis. Wuhan:Huazhong Agricultural University.
Wang Y, Zhang C, Wang N, Li Z, Heller R, Liu R, Zhao Y, Han J, Pan X, Zheng Z, Dai X, Chen C, Dou M, Peng S, Chen X, Liu J, Li M, Wang K, Liu C, Lin Z, Chen L, Hao F, Zhu W, Song C, Zhao C, Zheng C, Wang J, Hu S, Li C, Yang H, Jiang L, Li G, Liu M, Sonstegard T S, Zhang G, Jiang Y, Wang W, Qiu Q. 2019. Ge-netic basis of ruminant headgear and rapid antler regeneration. Science, 364 (6446). DOI:10.1126/science. aav6335.
Wei M L, Chu W H, Zhao H P, Li C Y. 2011. Antler stem cells and antler regeneration. Special Wild Economic Animal and Plant Re-search, 33 (2):47-51. (in Chinese)
Xia Z Q, Shan Y F, Li J F, Zhang Q X, He Y H, Cui Y H, Zhong Z Y, Bai C, Zhang C L, Bai J D, Meng Q H. 2023. Development of antler pedicle in male Père David's deer and related endocrine and signaling pathways detection. Chinese Journal of Wildlife, 44(3):565-571. (in Chinese)
Xing B R, Zhao H P, Li G Y, Sun H M, Ma Z F, Tan Z Q, Hu X, Li C Y, Wu J H, Liu Z. 2023. Effect of steroid hormones on osteopro-tegerin expression in antler mesenchymal stem cells of the sika deer. Acta Theriologica Sinica, 43 (4):443-449.
Yao X Y, Li B Y, Zhang Q L, Yue Z P, Yang Z Q, Guo B. 2022. Ef-fects of testosterone on proliferation and differentiation of sika deer antler mesenchymal cells. Chinese Journal of Veterinary Sci-ence, 42 (12):2500-2504. (in Chinese)
Zhang F, Zhang B, Wang Y Y, Jiang R M, Liu J, Wei Y X, Gao X Y, Zhu Y C, Wang X L, Sun M, Kang J J, Liu Y Y, You G X, Wei D, Xin J J, Bao J X, Wang M Q, Gu Y, Wang Z, Ye J, Guo S P, Huang H Y, Sun Q. 2023. An extra-erythrocyte role of haemo-globin body in chondrocyte hypoxia adaptation. Nature, 622(7984):834-841.
Zhang F X, Meng Q H, Jiang Z G, Meng X G, Cheng Z B, Song Y, Bai J D, Ding Y H, Wen H J. 2022. The vicissitudes of fate and future protection prospects of Père David's deer. Acta Ecologica Sinica, 42 (1):1-10.(in Chinese)
Zhang S M, Li Y P, Chen Q, Meng Q H, Cheng Z B, Chen X, Bai J D. 2021. Fecal cortisol steroids assay for tourist disturbance on cap-tive Père David's deer during spring in Beijing Nanhaizi milu park. Chinese Journal of Wildlife, 42 (2):522-527. (in Chinese)
邢宝瑞, 赵海平, 李光玉, 孙红梅, 马泽芳, 谭展清, 胡肖, 李晨莹, 吴建华, 刘振. 2023. 甾体类激素对梅花鹿鹿茸间充质干细胞骨保护素表达的影响. 兽类学报, 43 (4):443-449.
刘仲康, 周世朗, 伍善志. 1982. 雄激素对鹿茸生长作用的试验. 四川大学学报 (自然科学版), 19 (1):83-88.
刘雯, 李婷, 于瑞梅, 解磊, 高选. 2017. 147 例唯支持细胞综合征患者的睾丸病理分型和性激素分析. 山东大学学报 (医学版), 55(1):75-79, 84.
刘慧, 刘振, 王权威, 张伟, 杨万云, 李春义, 王桂武. 2017. 雄激素对鹿茸发生和再生的影响. 动物医学进展, 38 (5):113-116.
李长生, 王喜萍, 马丽娟. 2001. 梅花鹿茸角生长规律与体内激素关系的研究进展. 中国草食动物, 20 (6):36-38.
李可可, 孙旭阳, 陈超, 荆焕松, 许学林, 游思, 赵靖波, 熊家军. 2020. 外源褪黑素对鹿茸软骨细胞生长发育的影响. 中国畜牧兽医, 47 (7):1997-2004.
李春义, 刘钟安, 赵世臻, 杜玉川. 1988. 梅花鹿 (Cervus nippon hor-tulorum) 茸角生长发育各阶段血浆睾酮、雌二醇的含量变化.兽类学报, 8 (3):224-231.
李春义. 2017. 鹿茸完全再生机制研究进展. 农业生物技术学报, 25 (1):1-10.
李春旺, 蒋志刚, 曾岩, 游章强. 2005. 不同密度下和不同发情期时段中雄性麋鹿的繁殖计策. 生物多样性, 13 (5):424-431.
李浩东, 周雅, 张禾垟, 郑军军, 刘琳玲, 巴恒星, 王桂武. 2023. 梅花鹿 体 重 与 体 尺 指 标 的 相 关 及 回 归 分 析. 特 产 研 究, 45 (3):127-133.
李耀伟. 2022. 91 例不孕女性需求性激素六项水平检查结果分析及指导意义. 罕少疾病杂志, 29 (2):108-110.
张付贤, 孟庆辉, 蒋志刚, 孟秀祥, 程志斌, 宋苑, 白加德, 丁玉华, 温华军. 2022. 麋鹿沧桑命运与未来保护展望. 生态学报, 42(1):1-10.
张树苗, 李夷平, 陈颀, 孟庆辉, 程志斌, 陈星, 白加德. 2021. 北京南海子麋鹿苑春季麋鹿粪样皮质醇激素变化及其指示作用. 野生动物学报, 42 (2):522-527.
林仲凡. 1985. 有关鹿茸 (角) 的生物学研究进展. 国外畜牧学 (草食家畜), 3 (4):7-10.
孟庆辉, 柏超, 宋苑, 单云芳, 李俊芳, 张树苗, 白加德, 钟震宇, 张成林, 孟秀祥. 2022. 重引入对麋鹿种群分娩定时及同步化的影响. 兽类学报, 42 (4):379-386.
孟庆辉, 夏志强, 单云芳, 李俊芳, 胡华刚, 肖璇, 白加德, 钟震宇, 孟秀祥, 张付贤, 柏超, 张成林. 2024a. 不同光照时长对麋鹿茸生长和繁殖季的溢出效应. 生态学报, 44 (10):4368-4376.
孟庆辉, 夏志强, 单云芳, 李俊芳, 胡华刚, 肖璇, 白加德, 钟震宇, 孟秀祥, 柏超, 张成林. 2024b. 影响麋鹿茸分枝和角重量的年龄因素分析. 兽类学报, 44 (3):377-384.
胡太超, 刘玉敏, 陶荣珊, 苏凤艳, 张晶, 顾效瑜, 李庆杰, 王全凯. 2015. 鹿茸的化学成分及药理作用研究概述. 经济动物学报, 19 (3):156-162.
胡鹏飞, 徐佳萍, 艾成, 邵秀娟, 王洪亮, 董依萌, 崔学哲, 杨福合, 邢秀梅. 2017. 利用全基因组重测序分析鹿茸重量相关基因. 遗传, 39 (11):1090-1101.
姚雪原, 李柏余, 张巧玲, 岳占碰, 杨占清, 郭斌. 2022. 睾酮对梅花鹿鹿茸间充质细胞增殖与分化的影响. 中国兽医学报, 42 (12):2500-2504.
陶大勇. 2016. 塔里木马鹿鹿茸骨化及其相关因子关系研究. 武汉:华中农业大学博士学位论文.
夏志强, 单云芳, 李俊芳, 张庆勋, 贺永惠, 崔艳红, 钟震宇, 柏超, 张成林, 白加德, 孟庆辉. 2023. 麋鹿角柄发育规律与相关内分泌及信号通路检测. 野生动物学报, 44 (3):565-571.
鲍加荣, 李春义, 邢秀梅, 杨福合. 2008. 鹿茸再生及干细胞研究进展. 中国组织工程研究与临床康复, 12 (51):10163-10166.
魏明立, 褚文辉, 赵海平, 李春义. 2011. 鹿茸干细胞与鹿茸再生.
特产研究, 33 (2):47-51.
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