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Female athlete triad affects rat intestinal morphology and sucrase-isomaltase expression

Published online by Cambridge University Press:  04 November 2022

Kai Aoki
Affiliation:
Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8575, Japan Research Fellow of the Japan Society for the Promotion of Science, Tokyo, Japan
Kei Ebina
Affiliation:
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
Hana Shingu
Affiliation:
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
Kazuki Kioka
Affiliation:
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
Takehito Sugasawa
Affiliation:
Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8575, Japan
Yasushi Kawakami
Affiliation:
Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8575, Japan
Kazuhiro Takekoshi*
Affiliation:
Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8575, Japan
Naomi Omi*
Affiliation:
Faculty of Health and Sport Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
*
*Corresponding authors: K. Takekoshi, email k-takemd@md.tsukuba.ac.jp; N. Omi, email omi.naomi.gn@u.tsukuba.ac.jp
*Corresponding authors: K. Takekoshi, email k-takemd@md.tsukuba.ac.jp; N. Omi, email omi.naomi.gn@u.tsukuba.ac.jp

Abstract

Female athletes follow a strict diet and perform rigorous exercise to boost their performance, which induces health issues called the female athlete triad (FAT), defined as the combination of disordered eating, amenorrhoea and low bone mineral density. It is known to have a significant effect on bones. However, its effects on the small intestine, which is responsible for nutrient uptake into the body, remain unclear. In this study, we created an animal model of FAT to examine its effects on digestive and absorptive molecules in the small intestine. Thirty 5-week-old female Sprague-Dawley (sd) rats with an initial body weight of about 147 g were divided into control (Con, n = 7), exercise (Ex, n = 7), food restriction (FR, n = 8) and exercise plus food restriction (FAT, n = 8) groups. The rats were subjected to 4 weeks of wheel running (Ex, FAT) and 50–40 % food restriction (FR, FAT) to examine the effects on bone and typical digestive enzymes and transporters in the jejunum. Two-way ANOVA and the Kruskal–Wallis test were used for statistical analysis of normal and non-normal data, respectively. Four weeks of exercise and food restriction decreased bone weight (vs. other group P < 0·01) and bone breaking power (vs. other group P < 0·01). Villus height decreased in the jejunum (vs. other group P < 0·01), but the expression of typical macronutrients digestive enzyme and absorptive molecules remained unchanged. In contrast, sucrase-isomaltase gene (v. Ex P = 0·02) and protein expression were increased (vs. other group P < 0·05). The study findings show that FAT affects sucrase-isomaltase without histone methylation changes.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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Footnotes

These authors contributed equally to this work

References

Joy, E, De Souza, MJ, Nattiv, A, et al. (2014) Female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad. Curr Sports Med Rep 13, 219232.CrossRefGoogle ScholarPubMed
Ackland, TR, Lohman, TG, Sundgot-Borgen, J, et al. (2012) Current status of body composition assessment in sport: review and position statement on behalf of the ad hoc research working group on body composition health and performance, under the auspices of the I.O.C. Medical Commission. Sports Med 42, 227249.CrossRefGoogle Scholar
Sundgot-Borgen, J, Meyer, NL, Lohman, TG, et al. (2013) How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the ad hoc research working group on body composition, health and performance, under the auspices of the IOC Medical Commission. Br J Sports Med 47, 10121022.CrossRefGoogle Scholar
Wheatley, S, Khan, S, Székely, AD, et al. (2012) Expanding the female athlete triad concept to address a public health issue. Perform Enhancement Health 1, 1027.CrossRefGoogle Scholar
Lifshitz, F (2009) Nutrition and growth. J Clin Res Pediatr Endocrinol 1, 157163.CrossRefGoogle ScholarPubMed
Aparisi Gómez, MP, Weidekamm, C, Aparisi, F, et al. (2020) Sports and metabolic bone disease. Semin Musculoskelet Radiol 24, 277289.Google ScholarPubMed
Loucks, AB (2006) The response of luteinizing hormone pulsatility to 5 d of low energy availability disappears by 14 years of gynecological age. J Clin Endocrinol Metab 91, 31583164.CrossRefGoogle ScholarPubMed
Loucks, AB & Heath, EM (1994) Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J Clin Endocrinol Metab 78, 910915.Google ScholarPubMed
Loucks, AB & Verdun, M (1998) Slow restoration of LH pulsatility by refeeding in energetically disrupted women. Am J Physiol 275, R1218R1226.Google ScholarPubMed
Loucks, AB, Verdun, M & Heath, EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 84, 3746.CrossRefGoogle Scholar
Ribeiro, FM, Petriz, B, Marques, G, et al. (2021) Is there an exercise-intensity threshold capable of avoiding the leaky gut? Front Nutr 8, 627289.CrossRefGoogle ScholarPubMed
Aoki, K, Yanazawa, K, Tokinoya, K, et al. (2021) Renalase is localized to the small intestine crypt and expressed upon the activation of NF-κB p65 in mice model of fasting-induced oxidative stress. Life Sci 267, 118904.CrossRefGoogle Scholar
Catalioto, RM, Maggi, CA & Giuliani, S (2011) Intestinal epithelial barrier dysfunction in disease and possible therapeutical interventions. Curr Med Chem 18, 398426.CrossRefGoogle ScholarPubMed
Peterson, LW & Artis, D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14, 141153.CrossRefGoogle ScholarPubMed
Beumer, J, Gehart, H & Clevers, H (2020) Enteroendocrine dynamics – new tools reveal hormonal plasticity in the gut. Endocr Rev 41, 695706.CrossRefGoogle ScholarPubMed
Aoki, K, Suzuki, T, Hui, F, et al. (2021) Acute low-intensity treadmill running upregulates the expression of intestinal glucose transporters via GLP-2 in mice. Nutrients 13, 1735.CrossRefGoogle ScholarPubMed
Todorov, H, Kollar, B, Bayer, F, et al. (2020) α-linolenic acid-rich diet influences microbiota composition and villus morphology of the mouse small intestine. Nutrients 12, 732.CrossRefGoogle ScholarPubMed
Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402408.CrossRefGoogle ScholarPubMed
Suzuki, T, Mayanagi, Y, Keta, A, et al. (2019) Oral administration of fructose improves jejunal villous morphology and nutrient digestion and absorption capabilities in a rat model of total parenteral nutrition. Biomed Res Clin Prac 4, 18.CrossRefGoogle Scholar
Dahlqvist, A (1984) Assay of intestinal disaccharidases. Scand J Clin Lab Invest 44, 169172.CrossRefGoogle ScholarPubMed
Inoue, S, Honma, K, Mochizuki, K, et al. (2015) Induction of histone H3K4 methylation at the promoter, enhancer, and transcribed regions of the Si and Sglt1 genes in rat jejunum in response to a high-starch/low-fat diet. Nutrition 31, 366372.CrossRefGoogle Scholar
Inoue, S, Mochizuki, K & Goda, T (2011) Jejunal induction of SI and SGLT1 genes in rats by high-starch/low-fat diet is associated with histone acetylation and binding of GCN5 on the genes. J Nutr Sci Vitaminol 57, 162169.CrossRefGoogle ScholarPubMed
Aikawa, Y, Wakasugi, Y, Narukawa, T, et al. (2019) Jump exercise and food restriction on bone parameters in young female rats. Calcif Tissue Int 105, 557566.CrossRefGoogle Scholar
Aikawa, Y, Agata, U, Kakutani, Y, et al. (2015) The interaction of voluntary running exercise and food restriction induces low bone strength and low bone mineral density in young female rats. Calcif Tissue Int 97, 9099.CrossRefGoogle ScholarPubMed
Yanaka, K, Higuchi, M & Ishimi, Y (2019) Anti-osteoporotic effect of soy isoflavones intake on low bone mineral density caused by voluntary exercise and food restriction in mature female rats. J Nutr Sci Vitaminol 65, 335342.CrossRefGoogle ScholarPubMed
Woods, DJ & Routtenberg, A (1971) “Self-starvation” in activity wheels: developmental and chlorpromazine interactions. J Comp Physiol Psychol 76, 8493.CrossRefGoogle ScholarPubMed
Shin, HE, Kwak, SE, Zhang, DD, et al. (2020) Effects of treadmill exercise on the regulation of tight junction proteins in aged mice. Exp Gerontol 141, 111077.CrossRefGoogle ScholarPubMed
Carbajo-Pescador, S, Porras, D, Garcia-Mediavilla, MV, et al. (2019) Beneficial effects of exercise on gut microbiota functionality and barrier integrity, and gut-liver crosstalk in an in vivo model of early obesity and non-alcoholic fatty liver disease. Dis Model Mech 12, dmm039206.CrossRefGoogle Scholar
Costa, RJS, Snipe, RMJ, Kitic, CM, et al. (2017) Systematic review: exercise-induced gastrointestinal syndrome-implications for health and intestinal disease. Aliment Pharmacol Ther 46, 246265.CrossRefGoogle ScholarPubMed
Tang, D, Zeng, T, Wang, Y, et al. (2020) Dietary restriction increases protective gut bacteria to rescue lethal methotrexate-induced intestinal toxicity. Gut Microbes 12, 1714401.CrossRefGoogle ScholarPubMed
Heyman, M, Boudraa, G, Sarrut, S, et al. (1984) Macromolecular transport in jejunal mucosa of children with severe malnutrition: a quantitative study. J Pediatr Gastroenterol Nutr 3, 357363.CrossRefGoogle ScholarPubMed
Hampson, DJ (1986) Attempts to modify changes in the piglet small intestine after weaning. Res Vet Sci 40, 313317.CrossRefGoogle ScholarPubMed
Pinheiro, DF, Cruz, VC, Sartori, JR, et al. (2004). Effect of early feed restriction and enzyme supplementation on digestive enzyme activities in broilers. Poult Sci 83, 15441550.CrossRefGoogle ScholarPubMed
Trotta, RJ, Vasquez-Hidalgo, MA, Vonnahme, KA, et al. (2020) Effects of nutrient restriction during midgestation to late gestation on maternal and fetal postruminal carbohydrase activities in sheep. J Anim Sci 98, skz393.CrossRefGoogle ScholarPubMed
Freetly, HC, Ferrell, CL, Jenkins, TG, et al. (1995) Visceral oxygen consumption during chronic feed restriction and realimentation in sheep. J Anim Sci 73, 843852.CrossRefGoogle ScholarPubMed
Meyer, AM, Reed, JJ, Neville, TL, et al. (2012) Effects of nutritional plane and selenium supply during gestation on visceral organ mass and indices of intestinal growth and vascularity in primiparous ewes at parturition and during early lactation. J Anim Sci 90, 27332749.CrossRefGoogle ScholarPubMed
Andersen, MK, Skotte, L, Jørsboe, E, et al. (2022) Loss of sucrase-isomaltase function increases acetate levels and improves metabolic health in Greenlandic cohorts. Gastroenterology 162, 1171.e31182.e3.CrossRefGoogle ScholarPubMed
Deng, YX, Chen, YS, Zhang, WR, et al. (2011) Polysaccharide from Gynura divaricata modulates the activities of intestinal disaccharidases in streptozotocin-induced diabetic rats. Br J Nutr 106, 13231329.CrossRefGoogle ScholarPubMed
Dyer, J, Wood, IS, Palejwala, A, et al. (2002) Expression of monosaccharide transporters in intestine of diabetic humans. Am J Physiol Gastrointest Liver Physiol 282, G241G248.CrossRefGoogle ScholarPubMed
Liu, L, Yu, YL, Liu, C, et al. (2011) Insulin deficiency induces abnormal increase in intestinal disaccharidase activities and expression under diabetic states, evidences from in vivo and in vitro study. Biochem Pharmacol 82, 19631970.CrossRefGoogle ScholarPubMed
Buckley, GL, Hall, LE, Lassemillante, AM, et al. (2019) Retired athletes and the intersection of food and body: a systematic literature review exploring compensatory behaviours and body change. Nutrients 11, 1395.CrossRefGoogle Scholar
Saarni, SE, Rissanen, A, Sarna, S, et al. (2006) Weight cycling of athletes and subsequent weight gain in middleage. Int J Obes 30, 16391644.CrossRefGoogle ScholarPubMed
Roostaee, A, Guezguez, A, Beauséjour, M, et al. (2015) Histone deacetylase inhibition impairs normal intestinal cell proliferation and promotes specific gene expression. J Cell Biochem 116, 26952708.CrossRefGoogle ScholarPubMed
Mehraban, MH, Motovali-Bashi, M & Ghasemi, Y (2019) MiR-26a and miR-26b downregulate the expression of sucrase-isomaltase enzyme: a new chapter in diabetes treatment. Biochem Biophys Res Commun 519, 192197.CrossRefGoogle ScholarPubMed
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