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Influence of obestatin on the histological development of the small intestine in piglets during the first week of postnatal life

Published online by Cambridge University Press:  13 May 2020

J. Woliński ,
P. Szczurek ,
K. Pierzynowska ,
P. Wychowański ,
B. Seklecka ,
M. Boryczka ,
A. Kuwahara ,
I. Kato ,
O. Drahanchuk  and
K. Zaworski
...Show all authors
J. Woliński*
Affiliation:
Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3, 05-110Jabłonna, Poland
P. Szczurek
Affiliation:
Department of Animal Nutrition and Feed Sciences, National Research Institute of Animal Production, Krakowska 1, 32-083Balice, Poland
K. Pierzynowska
Affiliation:
Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3, 05-110Jabłonna, Poland Department of Biology, Lund University, Sölvegatan 35, 223 62Lund, Sweden Department of Medical Biology, Institute of Rural Health, Jaczewskiego 2, 20-090Lublin, Poland
P. Wychowański
Affiliation:
Department of Dental Surgery, Warsaw Medical University, Nowogrodzka 59, 02-006Warszawa, Poland
B. Seklecka
Affiliation:
Early Clinical Trials Unit, University Clinical Centre, Smoluchowskiego 17, 80-214Gdańsk, Poland Department of Oncology and Radiotherapy, Medical University of Gdansk, M. Skłodowskiej-Curie 3a, 80-210Gdańsk, Poland
M. Boryczka
Affiliation:
Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3, 05-110Jabłonna, Poland
A. Kuwahara
Affiliation:
Laboratory of Physiology, Institute for Environmental Sciences and Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, 52-1 Yada, Shizuoka, 422-8526, Japan
I. Kato
Affiliation:
Department of Medical Biochemistry, Kobe Pharmaceutical University, 4-19-1, Motoyama-Kita-Machi, Higashinada-ku, Kobe, 658-8558, Japan
O. Drahanchuk
Affiliation:
Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3, 05-110Jabłonna, Poland
K. Zaworski
Affiliation:
Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3, 05-110Jabłonna, Poland
S. G. Pierzynowski
Affiliation:
Department of Biology, Lund University, Sölvegatan 35, 223 62Lund, Sweden Department of Medical Biology, Institute of Rural Health, Jaczewskiego 2, 20-090Lublin, Poland
M. Słupecka-Ziemilska
Affiliation:
Department of Human Epigenetics, Mossakowski Medical Research Centre, Polish Academy of Sciences, Pawińskiego 5, 02-106Warszawa, Poland
*
†E-mail: j.wolinski@ifzz.pl.
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Abstract

Obestatin is a gastrointestinal peptide having wide-ranging effects on cell proliferation; however, its mechanism of action remains poorly understood. Thus, the aim of the study was to elucidate the effect of exogenous obestatin on the postnatal structural development of the small intestine. Seven-day-old piglets with an average BW of 1.56 ± 0.23 kg were divided into four groups (n = 10) that received intragastrically obestatin (2, 10 or 15 μg/kg BW) or vehicle. After a 6-day experimental period, morphological analysis of gastrointestinal tract and small intestine wall (mitosis and apoptosis indexes, histomorphometry of mucosa and muscularis layers) was performed. The study revealed a seemingly incoherent pattern of the histological structure of the small intestine among the experimental groups, suggesting that the effect of obestatin is both intestinal segment specific and dose dependent. Histomorphometric analysis of the small intestine showed that higher doses of obestatin seem to promote the structural development of the duodenum while simultaneously hindering the maturation of more distal parts of the intestine. Intragastric administration of obestatin increased the crypt mitotic index in all segments of the small intestine with the strongest pro-mitotic activity following the administration of obestatin at a dose of 10 and 15 μg/kg BW. The significant differences in the number of apoptotic cells in the intestinal villi among the groups were observed only in proximal jejunum and ileum. In conclusion, it seems that obestatin shows a broad-spectrum of activity in the gastrointestinal tract of newborn piglets, being able to accelerate its structural development. However, the varied effect depending on the intestinal segment or the concentration of exogenous obestatin causes that further research is needed to clarify the exact mechanism of this phenomenon.

Keywords

obestatinintestinal mucosaenterocytesmaturationneonatal piglets
Type
Research Article
Information
animal , Volume 14 , Issue 10 , October 2020 , pp. 2129 - 2137
Copyright
© The Kielanowski Institute of Animal Physiology and Nutrition Polish Academy of Sciences, and The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Asakawa, A, Ataka, K, Fujino, K, Chen, CY, Kato, I, Fujimiya, M and Inui, A 2011. Ghrelin family of peptides and gut motility. Journal of Gastroenterology and Hepatology 26, 73–74.CrossRefGoogle ScholarPubMed
Baintner, K 1986. Intestinal absorption of macromolecules and immune transmission from mother to young. CRC Press, Boca Raton, Florida, USA.Google Scholar
Biernat, M, Zabielski, R, Yao, G, Marion, J, le Huërou-Luron, I and Le Dividich, J 2001. Effect of formula vs. sow’s milk feeding on the gut morphology in neonatal piglets. In Proceedings of the 8th Digestive Physiology in Pigs Symposium, 20–22 June 2000, Uppsala, Sweden, pp. 43–45.CrossRefGoogle Scholar
Blättler, U, Hammon, HM, Morel, C, Philipona, C, Rauprich, A, Romé, V, Le Huërou-Luron, I, Guilloteau, P and Blum, JW 2001. Feeding colostrum, its composition and feeding duration variably modify proliferation and morphology of the intestine and digestive enzyme activities of neonatal calves. Journal of Nutrition 131, 1256–1263.CrossRefGoogle ScholarPubMed
Bühler, C, Hammon, H, Rossi, GL and Blum, JW 1998. Small intestinal morphology in eight-day-old calves fed colostrum for different durations or only milk replacer and treated with long-R3-insulin-like growth factor I and growth hormone. Journal of Animal Science 76, 758–765.CrossRefGoogle ScholarPubMed
Fisher, DA and Lakshmanan, J 1990. Metabolism and effects of epidermal growth factor and related growth factors in mammals. Endocrine Reviews 11, 418–442.CrossRefGoogle ScholarPubMed
Granata, R, Settanni, F, Gallo, D, Trovato, L, Biancone, L, Cantaluppi, V, Nano, R, Annunziata, M, Campiglia, P, Arnoletti, E, Ghè, C, Volante, M, Papotti, M, Muccioli, G and Ghigo, E 2008. Obestatin promotes survival of pancreatic beta-cells and human islets and induces expression of genes involved in the regulation of beta-cell mass and function. Diabetes 57, 967–979.CrossRefGoogle ScholarPubMed
Green, BD, Irwin, N and Flatt, PR 2007. Direct and indirect effects of obestatin peptides on food intake and the regulation of glucose homeostasis and insulin secretion in mice. Peptides 28, 981–987.CrossRefGoogle ScholarPubMed
Green, BD and Grieve, DJ 2018. Biochemical properties and biological actions of obestatin and its relevance in type 2 diabetes. Peptides 100, 249–259.CrossRefGoogle ScholarPubMed
Jeffery, PL, Murray, RE, Yeh, AH, McNamara, JF, Duncan, RP, Francis, GD, Herington, AC and Chopin, LK 2005. Expression and function of the ghrelin axis including a novel preproghrelin isoform in human breast cancer tissues and cell lines. Endocrine-Related Cancer 12, 839–850.CrossRefGoogle ScholarPubMed
Kisfalvi, K, Hajnal, F, Varga, G and Papp, M 1993. Influence of gastrointestinal (GI) hormones on suckling, gastric emptying and pancreatic trypsin content in the developing rat. Journal of Developmental Physiology 19, 149–155.Google ScholarPubMed
Kobelt, P, Wisser, AS, Stengel, A, Goebel, M, Bannert, N, Gourcerol, G, Inhoff, T, Noetzel, S, Wiedenmann, B, Klapp, BF, Taché, Y and Mönnikes, H 2008. Peripheral obestatin has no effect on feeding behavior and brain Fos expression in rodents. Peptides 29, 1018–1027.CrossRefGoogle ScholarPubMed
Lang, W 1982. Nomarski differential interference-contrast microscopy. Carl Zeiss, Oberkochen, Germany.Google Scholar
Meszarosova, M, Sirotkin, AV, Grossmann, R, Darlak, K and Valenzuela, F 2008. The effect of obestatin on porcine ovarian granulosa cells. Animal Reproduction Science 108, 196–207.CrossRefGoogle ScholarPubMed
Mondal, MS, Toshinai, K, Ueno, H, Koshinaka, K and Nakazato, M 2008. Characterization of obestatin in rat and human stomach and plasma, and its lack of acute effect on feeding behavior in rodents. Journal of Endocrinology 198, 339–346.CrossRefGoogle ScholarPubMed
Nakazato, M, Murakami, N, Date, Y, Kojima, M, Matsuo, H, Kangawa, K and Matsukura, S 2001. A role for ghrelin in the central regulation of feeding. Nature 409, 194–198.CrossRefGoogle ScholarPubMed
Nogueiras, R, Pfluger, P, Tovar, S, Arnold, M, Mitchell, S, Morris, A, Perez-Tilve, D, Vazquez, MJ, Wiedmer, P, Casteñeda, TR, DiMarchi, R, Tschöp, M, Schurmann, A, Joost, HG, Williams, LM, Langhans, W and Diéguez, C 2007. Effects of obestatin on energy balance and growth hormone secretion in rodents. Endocrinology 148, 21–26.CrossRefGoogle ScholarPubMed
Ren, AJ, Guo, ZF, Wang, YK, Wang, LG, Wang, WZ, Lin, L, Zheng, X and Yuan, WJ 2008. Inhibitory effect of obestatin on glucose-induced insulin secretion in rats. Biochemical and Biophysical Research Communications 369, 969–972.CrossRefGoogle ScholarPubMed
Seim, I, Herington, AC and Chopin, LK 2009. New insights into the molecular complexity of the ghrelin gene locus. Cytokine and Growth Factor Reviews 20, 297–304.CrossRefGoogle ScholarPubMed
Seim, I, Amorim, L, Walpole, C, Carter, S, Chopin, LK and Herington, AC 2010. Ghrelin gene-related peptides: multifunctional endocrine/autocrine modulators in health and disease. Clinical and Experimental Pharmacology and Physiology 37, 125–131.CrossRefGoogle Scholar
Seoane, LM, Al-Massadi, O, Pazos, Y, Pagotto, U and Casanueva, FF 2006. Central obestatin administration does not modify either spontaneous or ghrelin-induced food intake in rats. Journal of Endocrinological Investigation 29, RC13–RC15.CrossRefGoogle ScholarPubMed
Słupecka, M, Woliński, J and Pierzynowski, SG 2012. The effects of enteral ghrelin administration on the remodeling of the small intestinal mucosa in neonatal piglets. Regulatory Peptides 174, 38–45.CrossRefGoogle ScholarPubMed
Słupecka, M, Pierzynowski, SG, Kuwahara, A, Kato, I and Woliński, J 2014. Age-dependent effect of obestatin on intestinal contractility in Wistar rats. General and Comparative Endocrinology 208, 109–115.CrossRefGoogle ScholarPubMed
Unniappan, S, Speck, M and Kieffer, TJ 2008. Metabolic effects of chronic obestatin infusion in rats. Peptides 29, 1354–1361.CrossRefGoogle ScholarPubMed
Volante, M, Rosas, R, Ceppi, P, Rapa, I, Cassoni, P, Wiedenmann, B, Settanni, F, Granata, R and Papotti, M 2009. Obestatin in human neuroendocrine tissues and tumours: expression and effect on tumour growth. Journal of Pathology 218, 458–466.CrossRefGoogle ScholarPubMed
Walia, P, Asadi, A, Kieffer, TJ, Johnson, JD and Chanoine, JP 2009. Ontogeny of ghrelin, obestatin, preproghrelin and prohormone convertases in rat pancreas and stomach. Pediatric Research 65, 39–44.CrossRefGoogle ScholarPubMed
Woliński, J, Biernat, M, Guilloteau, P, Weström, BR and Zabielski, R 2003. Exogenous leptin controls the development of the small intestine in neonatal piglets. Journal of Endocrinology 177, 215–222.CrossRefGoogle ScholarPubMed
Woliński, J 2012. The influence of exogenous obestatin on the gastrointestinal tract in newborn piglets. Habilitation thesis, Kielanowski Institute of Animal Physiology and Nutrition Polish Academy of Sciences, Jabłonna, Poland.Google Scholar
Xu, RJ, Mellor, DJ, Birtles, MJ, Breier, BH and Gluckman, PD 1994. Effects of oral IGF-I or IGF-II on digestive organ in newborn piglets. Biology of the Neonate 66, 280–287.CrossRefGoogle ScholarPubMed
Yeh, AH, Jeffery, PL, Duncan, RP, Herington, AC and Chopin, LK 2005. Ghrelin and a novel preproghrelin isoform are highly expressed in prostate cancer and ghrelin activates mitogen-activated protein kinase in prostate cancer. Clinical Cancer Research 11, 8295–8303.CrossRefGoogle Scholar
Zhang, JV, Ren, PG, Avsian-Kretchmer, O, Luo, CW, Rauch, R, Klein, C and Hsueh, AJW 2005. Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin’s effects on food intake. Science 310, 996–999.CrossRefGoogle ScholarPubMed
Zhang, JV, Klein, C, Ren, PG, Kass, S, Donck, LV, Moechars, D and Hsueh, AJW 2007. Response to comment on obestatin, a peptide encoded by the ghrelin gene opposes ghrelin’s effect on food intake. Science 315, 766.CrossRefGoogle Scholar
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