Volume 36 Issue 2
Mar.  2015
Turn off MathJax
Article Contents

Guo-Xiao ZHENG, Jiang-Tao LIN, Wei-Hong ZHENG, Jing CAO, Zhi-Jun ZHAO. Energy intake, oxidative stress and antioxidant in mice during lactation. Zoological Research, 2015, 36(2): 95-102.
Citation: Guo-Xiao ZHENG, Jiang-Tao LIN, Wei-Hong ZHENG, Jing CAO, Zhi-Jun ZHAO. Energy intake, oxidative stress and antioxidant in mice during lactation. Zoological Research, 2015, 36(2): 95-102.

Energy intake, oxidative stress and antioxidant in mice during lactation

Funds:  This work was supported by grants from Wenzhou University (14SK51A, 14SK52A), the National Natural Science Foundation of China (31270458) and grant from Zhejiang Province (pd2013374)
More Information
  • Corresponding author: Zhi-Jun ZHAO
  • Received Date: 2014-10-14
  • Rev Recd Date: 2014-12-16
  • Publish Date: 2015-03-08
  • Reproduction is the highest energy demand period for small mammals, during which both energy intake and expenditure are increased to cope with elevated energy requirements of offspring growth and somatic protection. Oxidative stress life history theory proposed that reactive oxygen species (ROS) were produced in direct proportion to metabolic rate, resulting in oxidative stress and damage to macromolecules. In the present study, several markers of oxidative stress and antioxidants activities were examined in brain, liver, kidneys, skeletal muscle and small intestine in non-lactating (Non-Lac) and lactating (Lac) KM mice. Uncoupling protein (ucps) gene expression was examined in brain, liver and muscle. During peak lactation, gross energy intake was 254% higher in Lac mice than in Non-Lac mice. Levels of H2O2 of Lac mice were 17.7% higher in brain (P<0.05), but 21.1% (P<0.01) and 14.5% (P<0.05) lower in liver and small intestine than that of Non-Lac mice. Malonadialdehyde (MDA) levels of Lac mice were significantly higher in brain, but lower in liver, kidneys, muscle and small intestine than that of Non-Lac mice. Activity of glutathione peroxidase (GSH-PX) was significantly decreased in brain and liver in the Lac group compared with that in the Non-Lac group. Total antioxidant capacity (T-AOC) activity of Lac mice was significantly higher in muscle, but lower in kidneys than Non-Lac mice. Ucp4 and ucp5 gene expression of brain was 394% and 577% higher in Lac mice than in Non-Lac mice. These findings suggest that KM mice show tissue-dependent changes in both oxidative stress and antioxidants. Activities of antioxidants may be regulated physiologically in response to the elevated ROS production in several tissues during peak lactation. Regulations of brain ucp4 and ucp5 gene expression may be involved in the prevention of oxidative damage to the tissue.
  • 加载中
  • [1] Aloise King ED, Garratt M, Brooks R. 2013. Manipulating reprodu­ctive effort leads to changes in female reproductive scheduling but not oxidative stress. Ecology and Evolution, 3(12): 4161-4171.
    [2] Beckman KB, Ames BN. 1998. The free radical theory of aging matures. Physiological Reviews, 78(2): 547-581.
    [3] Bergeron P, Careau V, Humphries MM, Réale D, Speakman JR, Garant D. 2011. The energetic and oxidative costs of reproduction in a free-ranging rodent. Functional Ecology, 25(5): 1063-1071.
    [4] Boveris A, Valdez LB, Zaobornyj T, Bustamante J. 2006. Mitochondrial metabolic states regulate nitric oxide and hydrogen peroxide diffusion to the cytosol. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1757(5-6): 535-542.
    [5] Brand MD. 2000. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Experimental Gerontology, 35(6-7): 811-820.
    [6] Brand MD, Buckingham JA, Esteves TC, Green K, Lambert AJ, Miwa S, Murphy MP, Pakay JL, Talbot DA, Echtay KS. 2004. Mitochondrial superoxide and aging: uncoupling-protein activity and superoxide production. Biochemical Society Symposium, 71: 203-213.
    [7] Chen KX, Wang CM, Wang GY, Zhao ZJ. 2014. Energy budget, oxidative stress and antioxidant in striped hamster acclimated to moderate cold and warm temperatures. Journal of Thermal Biology, 44: 35-40.
    [8] Davidovi? V, ?joki? I, Petrovi? N, ?uraševi? S, Cviji? G. 1999. Activity of antioxidant enzymes in rat skeletal muscle and brown fat: effect of cold and propranolol. Journal of Thermal Biology, 24(5-6): 385-389.
    [9] Dowling DK, Simmons LW. 2009. Reactive oxygen species as universal constraints in life-history evolution. Proceedings of the Royal Society B: Biological Sciences, 276(1663): 1737-1745.
    [10] Fletcher QE, Selman C, Boutin S, McAdam AG, Woods SB, Seo AY, Leeuwenburgh C, Speakman JR, Humphries MM. 2013. Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution, 67(5): 1527-1536.
    [11] Garratt M, Pichaud N, Aloise King ED, Brooks RC. 2013. Physiol­ogical adaptations to reproduction. I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice. The Journal of Experimental Biology, 216(Pt 15): 2879-2888.
    [12] Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, Hurst JL. 2011. Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proceedings of the Royal Society B: Biological Sciences, 278(1708): 1098-1106.
    [13] Garratt M, McArdle F, Stockley P, Vasilaki A, Beynon RJ, Jackson MJ, Hurst JL. 2012. Tissue-dependent changes in oxidative damage with male reproductive effort in house mice. Functional Ecology, 26(2): 423-433.
    [14] Grodziński W, Wunder BA. 1975. Ecological energetics of small mammals. In: Golley EB, Petrusewicz K, Ryszkowski L. Small Mammals: Their Productivity and Population Dynamics. Cambridge: Cambridge University Press, 173-204.
    [15] Hammond KA, Diamond J. 1997. Maximal sustained energy budgets in humans and animals. Nature, 386(6624): 457-462.
    [16] Je?ek P. 2002. Possible physiological roles of mitochondrial uncoupling proteins-UCPn. The International Journal of Biochemistry & Cell Biology, 34(10): 1190-1206.
    [17] Johnson MS, Thomson SC, Speakman JR. 2001. Limits to sustained energy intake I. Lactation in the laboratory mouse Mus musculus. The Journal of Experimental Biology, 204(11): 1925-1935.
    [18] Król E, Speakman JR. 2003. Limits to sustained energy intake VII. Milk energy output in laboratory mice at thermoneutrality. The Journal of Experimental Biology, 206(23): 4267-4281.
    [19] Li XS, Wang DH. 2005. Suppression of thermogenic capacity during reproduction in primiparous brandt's voles (Microtus brandtii). Journal of Thermal Biology, 30(6): 431-436.
    [20] Liu H, Wang DH, Wang ZW. 2003. Energy requirements during reproduction in female Brandt's voles (Microtus brandtii). Journal of Mammalogy, 84(4): 1410-1416.
    [21] Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measu­r­ement with the Folin phenol reagent. Journal of Biological Chemistry, 193: 265-275.
    [22] Manivannan J, Sinha S, Ghosh M, Mukherjee A. 2013. Evaluation of multi-endpoint assay to detect genotoxicity and oxidative stress in mice exposed to sodium fluoride. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 751(1): 59-65.
    [23] Martin I, Giralt M, Viñas O, Iglesias R, Mampel T, Villarroya F. 1989. Adaptative decrease in expression of the mRNA for uncoupling protein and subunit II of cytochrome c oxidase in rat brown adipose tissue during pregnancy and lactation. Biochemical Journal, 263(3): 965-968.
    [24] Miwa S, Brand MD. 2003. Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling. Biochemical Society Transactions, 31(6): 1300-1301.
    [25] Monaghan P, Metcalfe NB, Torres R. 2009. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters, 12(1): 75-92.
    [26] Nussey DH, Pemberton JM, Pilkington JG, Blount JD. 2009. Life history correlates of oxidative damage in a free-living mammal population. Functional Ecology, 23(4): 809-817.
    [27] Paul MJ, Tuthill C, Kauffman AS, Zucker I. 2010. Pelage insulation, litter size, and ambient temperature impact maternal energy intake and offspring development during lactation. Physiology & Behavior, 100(2): 128-134.
    [28] Pedraza N, Solanes G, Carmona MC, Iglesias R, Viñas O, Mampel T, Vazquez M, Giralt M, Villarroya F. 2000. Impaired expression of the uncoupling protein-3 gene in skeletal muscle during lactation: fibrates and troglitazone reverse lactation-induced downregulation of the uncoupling protein-3 gene. Diabetes, 49(7): 1224-1230.
    [29] Ramsden DB, Ho PWL, Ho JWM, Liu HF, So DHF, Tse HM, Chan KH, Ho SL. 2012. Human neuronal uncoupling proteins 4 and 5 (UCP4 and UCP5): structural properties, regulation, and physiological role in protection against oxidative stress and mitochondrial dysfunction. Brain and Behavior, 2(4): 468-478.
    [30] Salmon AB, Marx DB, Harshman LG. 2001. A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution, 55(8): 1600-1608.
    [31] Selman C, McLaren JS, Himanka MJ, Speakman JR. 2000. Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radical Biology and Medicine, 28(8): 1279-1285.
    [32] Selman C, Blount JD, Nussey DH, Speakman JR. 2012. Oxidative damage, ageing, and life-history evolution: where now?. Trends in Ecology & Evolution, 27(10): 570-577.
    [33] Selman C, Grune T, Stolzing A, Jakstadt M, McLaren JS, Speakman JR. 2002. The consequences of acute cold exposure on protein oxidation and proteasome activity in short-tailed field voles, microtus agrestis. Free Radical Biology and Medicine, 33(2): 259-265.
    [34] Speakman JR. 2008. The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1490): 375-398.
    [35] Speakman JR, Król E. 2005. Limits to sustained energy intake IX: a review of hypotheses. Journal of Comparative Physiology B, 175(6): 375-394.
    [36] Speakman JR, Król E. 2011. Limits to sustained energy intake. XIII. Recent progress and future perspectives. The Journal of Experimental Biology, 214(2): 230-241.
    [37] Speakman JR, Selman C. 2011. The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. BioEssays, 33(4): 255-259.
    [38] Speakman JR, Garratt M. 2014. Oxidative stress as a cost of reproduction: Beyond the simplistic trade-off model. BioEssays, 36(11): 93-106.
    [39] Toime LJ, Brand MD. 2010. Uncoupling protein-3 lowers reactive oxygen species production in isolated mitochondria. Free Radical Biology and Medicine, 49(4): 606-611.
    [40] Venditti P, De Rosa R, Portero-Otin M, Pamplona R, Di Meo S. 2004. Cold-induced hyperthyroidism produces oxidative damage in rat tissues and increases susceptibility to oxidants. The International Journal of Biochemistry & Cell Biology, 36(7): 1319-1331.
    [41] Xiao XQ, Grove KL, Grayson BE, Smith MS. 2004. Inhibition of uncoupling protein expression during lactation: role of leptin. Endocrinology, 145(2): 830-838.
    [42] Xu YC, Yang DB, Speakman JR, Wang DH. 2014. Oxidative stress in response to natural and experimentally elevated reproductive effort is tissue dependent. Functional Ecology, 28(2): 402-410.
    [43] Yang DB, Xu YC, Wang DH, Speakman JR. 2013. Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent. The Journal of Experimental Biology, 216(22): 4242-4250.
    [44] Zhang XY, Wang DH. 2007. Thermogenesis, food intake and serum leptin in cold-exposed lactating Brandt's voles Lasiopodomys brandtii. The Journal of Experimental Biology, 210(3): 512-521.
    [45] Zhao ZJ, Cao J. 2009. Effect of fur removal on the thermal conductance and energy budget in lactating Swiss mice. The Journal of Experimental Biology, 212(16): 2541-2549.
    [46] Zhao ZJ, Chi QS, Cao J, Han YD. 2010. The energy budget, thermogenic capacity and behavior in Swiss mice exposed to a consecutive decrease in temperatures. The Journal of Experimental Biology, 213(23): 3988-3997.
    [47] Zhao ZJ. 2011. Relationship between reproductive output and basal metabolic rate in striped hamster (Cricetulus barabensis). Acta Theriologica Sinica, 31(1): 69-78. (in Chinese)
    [48] Zhao ZJ, Wei WT, Li MZ, Cao J. 2013. Body mass, energy budget and leptin of mice under stochastic food restriction and refeeding. Zoological Research, 34(6): 574-581.
    [49] Zhao ZJ, Liu YA, Xing YJ, Zhang ML, Ni XY, Cao J. 2014a. The role of leptin in striped hamsters subjected to food restriction and refeeding. Zoological Research, 35(4): 262-271.
    [50] Zhao ZJ, Chen KX, Liu YA, Wang CM, Cao J. 2014b. Decreased circulating leptin and increased neuropeptide Y gene expression are implicated in food deprivation-induced hyperactivity in striped hamsters, Cricetulus barabensis. Hormones and Behavior, 65(4): 355-362.
  • 加载中
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Article Metrics

Article views(501) PDF downloads(1120) Cited by()

Related
Proportional views

Energy intake, oxidative stress and antioxidant in mice during lactation

Funds:  This work was supported by grants from Wenzhou University (14SK51A, 14SK52A), the National Natural Science Foundation of China (31270458) and grant from Zhejiang Province (pd2013374)
    Corresponding author: Zhi-Jun ZHAO

Abstract: Reproduction is the highest energy demand period for small mammals, during which both energy intake and expenditure are increased to cope with elevated energy requirements of offspring growth and somatic protection. Oxidative stress life history theory proposed that reactive oxygen species (ROS) were produced in direct proportion to metabolic rate, resulting in oxidative stress and damage to macromolecules. In the present study, several markers of oxidative stress and antioxidants activities were examined in brain, liver, kidneys, skeletal muscle and small intestine in non-lactating (Non-Lac) and lactating (Lac) KM mice. Uncoupling protein (ucps) gene expression was examined in brain, liver and muscle. During peak lactation, gross energy intake was 254% higher in Lac mice than in Non-Lac mice. Levels of H2O2 of Lac mice were 17.7% higher in brain (P<0.05), but 21.1% (P<0.01) and 14.5% (P<0.05) lower in liver and small intestine than that of Non-Lac mice. Malonadialdehyde (MDA) levels of Lac mice were significantly higher in brain, but lower in liver, kidneys, muscle and small intestine than that of Non-Lac mice. Activity of glutathione peroxidase (GSH-PX) was significantly decreased in brain and liver in the Lac group compared with that in the Non-Lac group. Total antioxidant capacity (T-AOC) activity of Lac mice was significantly higher in muscle, but lower in kidneys than Non-Lac mice. Ucp4 and ucp5 gene expression of brain was 394% and 577% higher in Lac mice than in Non-Lac mice. These findings suggest that KM mice show tissue-dependent changes in both oxidative stress and antioxidants. Activities of antioxidants may be regulated physiologically in response to the elevated ROS production in several tissues during peak lactation. Regulations of brain ucp4 and ucp5 gene expression may be involved in the prevention of oxidative damage to the tissue.

Guo-Xiao ZHENG, Jiang-Tao LIN, Wei-Hong ZHENG, Jing CAO, Zhi-Jun ZHAO. Energy intake, oxidative stress and antioxidant in mice during lactation. Zoological Research, 2015, 36(2): 95-102.
Citation: Guo-Xiao ZHENG, Jiang-Tao LIN, Wei-Hong ZHENG, Jing CAO, Zhi-Jun ZHAO. Energy intake, oxidative stress and antioxidant in mice during lactation. Zoological Research, 2015, 36(2): 95-102.
Reference (50)

Catalog

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return