Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-18T10:31:31.901Z Has data issue: false hasContentIssue false
  • English
  • Français

Responses of plasma glucose metabolism to exogenous insulin infusion in sheep-fed forage herb plantain and exposed to heat

Published online by Cambridge University Press:  16 January 2017

M. Al-Mamun ,
K. Shibuya ,
M. Kajita ,
Y. Tamura  and
H. Sano
M. Al-Mamun
Affiliation:
Deptartment of Animal Science, Iwate University, Morioka 020-8550, Japan
K. Shibuya
Affiliation:
Deptartment of Animal Science, Iwate University, Morioka 020-8550, Japan
M. Kajita
Affiliation:
Deptartment of Animal Science, Iwate University, Morioka 020-8550, Japan
Y. Tamura
Affiliation:
Forage Production and Utilization Research Team, Tohoku Agricultural Experimental Station, Morioka 020-0123, Japan
H. Sano*
Affiliation:
Deptartment of Animal Science, Iwate University, Morioka 020-8550, Japan
*
†E-mail: sano@iwate-u.ac.jp
Get access

Abstract

The use of herbal plants as traditional medicines has a century long history. Plantain (Plantago lanceolata L.) is a perennial herb containing bioactive components with free radical scavenging activities. An isotope dilution technique using [U-13C]glucose was conducted to determine the effect of plantain on the responses of plasma glucose metabolism to exogenous insulin infusion in sheep. Six crossbred sheep (three wethers and three ewes; mean initial BW=40±2 kg) were fed either a mixed hay of orchardgrass (Dactylis glomerata) and reed canarygrass (Phalaris arundinacea) (MH-diet) or mixed hay and fresh plantain (1 : 1 ratio, dry matter basis, PL-diet) and exposed to a thermoneutral (TN, 20°C; 70% relative humidity (RH)) environment or a heat exposure (HE, 30°C; 70% RH) for 5 days using a crossover design for two 23-day periods. The isotope dilution was conducted on days 18 and 23 of the experimental period during TN and HE, respectively. Plasma concentration of α-tocopherol was greater (P<0.0001) for the PL-diet than the MH-diet and remained comparable between environmental treatments. Plasma glucose concentration before isotope dilution technique was reduced for sheep (P=0.05) during HE compared with TN and remained comparable between diets. Plasma glucose turnover rate during the preinfusion period of insulin did not differ (P=0.10) between dietary treatments and between environments (P=0.65). The response of plasma glucose utilization to exogenous insulin administration was lower (P=0.04) for the PL-diet than the MH-diet. Under present experimental conditions, the plantain group was found to be resistant to the effects of insulin infusion.

Keywords

glucose metabolismplantaininsulinheat stresssheep
Type
Research Article
Information
animal , Volume 11 , Issue 8 , August 2017 , pp. 1287 - 1294
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: Department of Animal Nutrition, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.

References

Achmadi, J, Yanagisawa, T, Sano, H and Terashima, Y 1993. Pancreatic insulin secretory response and insulin action in heat-exposed sheep given a concentrate or roughage diet. Domestic Animal Endocrinology 10, 279–287.CrossRefGoogle ScholarPubMed
Al-Mamun, M, Abe, D, Kofujita, H, Tamura, Y and Sano, H 2008a. Comparison of the bioactive components of the ecotypes and cultivars of plantain (Plantago lanceolata L.) herbs. Animal Science Journal 79, 83–88.Google Scholar
Al-Mamun, M, Hanai, Y, Tanaka, C, Tamura, Y and Sano, H 2008b. Responses of whole body protein synthesis and degradation to plantain in sheep exposed to heat. Archive of Animal Nutrition 62, 219–229.Google Scholar
Al-Mamun, M, Hanai, Y, Tanaka, C, Tamura, Y and Sano, H 2007b. Effects of plantain (Plantago lanceolata L.) herb and heat exposure on plasma glucose metabolism in sheep. Asian-Australasian Journal of Animal Sciences 20, 894–899.Google Scholar
Al-Mamun, M, Yamaki, K, Masumizu, T, Nakai, Y, Saito, K, Sano, H and Tamura, Y 2007a. Superoxide anion radical scavenging activities of herbs and pastures in northern Japan determined using electron spin resonance spectrometry. International Journal of Biological Sciences 3, 349–355.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists 1995. Official methods of analysis, volume 2, 16th edition. AOAC, Arlington, VA, USA.Google Scholar
Badamchian, M, Spangelo, B, Hagiwara, Y, Hagiwara, H, Veyama, H and Goldstein, AL 1994. Alpha-tocopherol succinate, but not alpha-tocopherol or other vitamin E analogs stimulates prolactin and growth hormone release from rat anterior pituitary cells in vitro. Neuropsychopharmacology 11, 265.CrossRefGoogle Scholar
Barre, P, Emile, JC, Betin, M, Surault, F, Ghesquière, M and Hazard, L 2006. Morphological characteristics of perennial ryegrass leaves that influence short-term intake in dairy cows. Agronomy Journal 98, 978–985.Google Scholar
Beara, IN, Orčić, DZ, Lesjak, MM, Mimica-Dukić, NM, Peković, BA and Popović, MR 2010. Liquid chromatography/tandem mass spectrometry study of anti-inflammatory activity of Plantain (Plantago L.) species. Journal of Pharmaceutical and Biomedical Analysis 52, 701–706.Google Scholar
Brockman, RP 1979. Effect of somatostatin on plasma glucagons and insulin, and glucose turnover in exercising sheep. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology 47, 273–278.CrossRefGoogle ScholarPubMed
Buckley, BA, Herbein, JH and Young, JW 1982. Glucose kinetics in lactating and nonlactating dairy goats. Journal of Dairy Science 65, 371–384.Google Scholar
Buckley, DJ, Morrissey, PA and Gray, JI 1995. Influence of dietary vitamin E on the oxidative stability and quality of pig meat. Journal of Animal Science 73, 3122–3130.Google Scholar
Chauhan, SS, Celi, P, Fahri, FT, Leury, BJ and Dunshea, FR 2014. Dietary antioxidants at supranutritional doses modulate skeletal muscle heat shock protein and inflammatory gene expression in sheep exposed to heat stress. Journal of Animal Science 92, 4897–4908.Google Scholar
Christison, GI and Johnson, HD 1972. Cortisol turnover in heat-stressed cows. Journal of Animal Science 35, 1005–1010.Google Scholar
Cohen, N, Audehm, R, Pretorius, E, Kaye, J, Chapman, L and Colagiuri, S 2013. The rationale for combining GLP-1 receptor agonists with basal insulin. Medical Journal of Australia 199, 246–249.CrossRefGoogle ScholarPubMed
Costacou, T, Ma, B, King, IB and Mayer-Davis, EJ 2008. Plasma and dietary vitamin E in relation to insulin secretion and sensitivity. Diabetes, Obesity and Metabolism 10, 223–228.Google Scholar
Cowan, J, McKay, G and Fisher, M 2012. GLP-1 receptor agonists and insulin: where are we now? Practical Diabetes 29, 351–352.Google Scholar
Cowan, JS and Hetenyi, G Jr 1971. Glucoregulatory responses in normal and diabetic dogs recorded by a new tracer method. Metabolism 20, 360–372.Google Scholar
Etherton, TD and Walton, PE 1986. Hormonal and metabolic regulation of lipid metabolism in domestic livestock. Journal of Animal Science 63, 76–188.Google Scholar
Evans, E and Buchanan-Smith, JG 1975. Effects upon glucose metabolism of feeding a low-or high roughage diet at two levels of intake to sheep. British Journal of Nutrition 33, 33–44.CrossRefGoogle ScholarPubMed
Gelardi, NL, Rapoza, RE, Renzulli, JF and Cowett, RM 1999. Insulin resistance and glucose transporter expression during the euglycemic hyperinsulinemic clamp in the lamb. American Journal of Physiology 277, E1142–E1149.Google Scholar
Huggett, AG and Nixon, DA 1957. Enzymatic determination of blood glucose. Biochemical Journal 66, 12.Google Scholar
Ishiguro, K, Yamaki, M and Takagi, S 1982. Studies on the iridoid related compounds. I. On the antimicrobial activity of aucubigenin and certain iridoid aglycones. Yakugaku Zasshi 102, 755–759.Google Scholar
Itoh, F, Hodate, K, Koyama, S, Rose, MT, Matsumoto, M, Ozawa, A and Obara, Y 2001. Effects of heat exposure on adrenergic modulation of insulin and glucagons secretion in sheep. Endocrine Journal 48, 193–198.Google Scholar
Jia, Y, Gong, N, Li, TF, Zhu, B and Wang, YX 2015. Peptidic exenatide and herbal catalpol mediate neuroprotection via the hippocampal GLP-1 receptor/β-endorphin pathway. Pharmacological Research 102, 276–285.Google Scholar
Juan, CC, Fang, VS, Kwok, CF, Perng, JC, Chou, YC and Ho, LT 1999. Exogenous hyperinsulinemia causes insulin resistance, hyperendothelinemia, and subsequent hypertension in rats. Metabolism 48, 465–471.Google Scholar
Kim, DY, Kim, J, Ham, HJ and Choue, R 2013. Effects of d-α-tocopherol supplements on lipid metabolism in a high-fat diet-fed animal model. Nutrition Research and Practice 7, 481–487.Google Scholar
Landau, S, Madar, Z, Nitsan, Z and Zoref, Z 1992. Estimation of energy status in non-pregnant and pregnant prolific ewes according to plasma levels of non-esterified fatty acids. In Etat corporel des brebis et chèvres (ed. A Purroy), pp. 57–62. CIHEAM, Zaragoza, Spain.Google Scholar
Leslie, AC, Jill, AB and Joseph, AH 2009. Intramuscular lipid metabolism, insulin action and obesity. International Union of Biochemistry and Molecular Biology Life 61, 47–55.Google Scholar
Mook, JH, Haeck, J, van der Toorn, J and van Tienderen, PH 1989. Comparative demography of Plantago I. Observations on eight populations of Plantago lanceolata . Acta Botanica Neerlandica 38, 67–78.Google Scholar
National Research Council 1985. Nutrient requirements of sheep, 6th edition. National Academiy Press, Washington, DC, USA.Google Scholar
Nishibe, S and Murai, M 1995. Bioactive components of Plantago herb. Foods and Food Ingredients Journal 166, 43–49.Google Scholar
Park, KS and Chang, IM 2004. Anti-inflammatory activity of aucubin by inhibition of tumor necrosis factor-alpha production in RAW 264.7 cells. Planta Medica 70, 778–779.Google Scholar
Provenza, FD 2003. Foraging behavior: managing to survive in a world of change. USDA, Washington, DC, USA.Google Scholar
Purushotham, A, Wendel, AA, Liu, L-F and Belury, MA 2007. Maintenance of adiponectin attenuates insulin resistance induced by dietary conjugated linoleic acid in mice. Journal of Lipid Research 48, 444–452.CrossRefGoogle ScholarPubMed
Rose, MT, Obara, Y, Fuse, H, Itoh, F, Ozawa, A, Takahashi, Y, Hodate, K and Ohashi, S 1996. Effect of growth hormone-releasing factor on the response to insulin of cows during early and late lactation. Journal of Dairy Science 79, 1734–1745.Google Scholar
Rumball, W, Keogh, RG, Lane, GE, Miller, JE and Claydon, RB 1997. Grasslands Lancelot plantain (Plantago lanceolata L.). New Zealand Journal of Agricultural Research 40, 373–377.Google Scholar
Rupérez, FJ, Mach, M and Barbas, C 2004. Direct liquid chromatography method for retinol, alpha- and gamma-tocopherols in rat plasma. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 800, 225–230.Google Scholar
Sano, H, Fujita, T, Murakami, M and Shiga, A 1996. Stimulative effect of epinephrine on glucose production and utilization rates in sheep using a stable isotope. Domestic Animal Endocrinology 13, 445–451.Google Scholar
Sano, H, Konno, S and Shiga, A 2000. Effects of supplemental chromium and heat exposure on glucose metabolism and insulin action in sheep. Journal of Agricultural Science 134, 319–325.Google Scholar
Sano, H, Takahashi, K, Ambo, K and Tsuda, T 1983. Turnover and oxidation rates of blood glucose and heat production in sheep exposed to heat. Journal of Dairy Science 66, 856–861.Google Scholar
Sano, H, Takebayashi, A, Kodama, Y, Nakamura, K, Ito, H, Arino, Y, Fujita, T, Takahashi, H and Ambo, K 1999. Effects of feed restriction and cold exposure on glucose metabolism in response to feeding and insulin in sheep. Journal of Animal Science 77, 2564–2573.Google Scholar
Sano, H, Tamura, Y and Shiga, A 2002. Metabolism and glucose kinetics in sheep fed plantain and orchardgrass and exposed to heat. New Zealand Journal of Agricultural Research 45, 171–177.Google Scholar
SAS Institute Inc. 1996. SAS/STAT® software: changes and enhancements through release 6.11. SAS, Cary, NC, USA.Google Scholar
Smit, HJ, Tas, BM, Taweel, HZ, Tamminga, S and Elgersma, A 2005. Effects of perennial ryegrass (Lolium perenne L.) cultivars on herbage production, nutritional quality and herbage intake of grazing dairy cows. Grass and Forage Science 60, 297–309.Google Scholar
Stewart, AV 1996. Plantain (Plantago lanceolata) – a potential pasture species. Proceedings of the New Zealand Grassland Association 58, 77–86.Google Scholar
Sudarman, A and Ito, T 2000. Heat production and thermoregulatory responses of sheep fed different roughage proportion diets and intake levels when exposed to a high ambient temperature. Asian-Australasian Journal of Animal Sciences 13, 625–629.Google Scholar
Tserng, K-Y and Kalhan, SC 1983. Calculation of substrate turnover rate in stable isotope tracer studies. American Journal of Physiology 245, E308–E311.Google Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA 1991. Carbohydrate methodology, metabolism and nutritional implications in dairy cattle. Methods of dietary fibre, neutral detergent fibre and non starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Vernon, RG 1982. Effects of growth hormone on fatty acid synthesis in sheep adipose tissue. International Journal of Biochemistry 14, 255–258.Google Scholar
Weekes, TEC, Sasaki, Y and Tsuda, T 1983. Enhanced responsiveness to insulin in sheep exposed to cold. American Journal of Physiology 244, E335–E345.Google Scholar
Wolfe, RR (ed.) 1984. Tracers in metabolic research. Radioisotope and stable isotope/mass spectrometry methods. Alan R Liss Inc., New York, NY, USA.Google Scholar
Yoshida, T, Rikimaru, K, Sakai, M, Nishibe, S, Fujikawa, T and Tamura, Y 2012. Plantago lanceolata L. leaves prevent obesity in C57BL/6 J mice fed a high-fat diet. Natural Product Research: Formerly Natural Product Letters 27, 982–987.Google Scholar
Supplementary material: File

Al-Mamun supplementary material

Al-Mamun supplementary material

Download Al-Mamun supplementary material(File)
File 19.7 KB