Hormonal and neural regulation of intestinal function in pigs

Livestock Science

Volumn 108, Issue 1-3, 2007, Pages 32-40

  Zabielski, R ^a,b  

^a KIELANOWSKI INSTITUTE OF ANIMAL PHYSIOLOGY AND NUTRITION   (Poland)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Apoptosis; Ghrelin; Glucagon like peptide 2; Leptin; Mucosa remodeling; Neonate

Indexed keywords

RODENTIA; SUIDAE;

EID: 34247503776     PISSN: 18711413     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.livsci.2007.01.022     Document Type: Article

References (84)

1. Aoki N., Kawamura M., and Matsuda T. Lactation-dependent down regulation of leptin production in mouse mammary gland. Biochim. Biophys. Acta 1427 (1999) 298-306
2. Barada K.A., Atallah J.B., and Nassar C.F. Age influence of intestinal taurine transport in mice. Comp. Biochem. Physiol. 118A (1997) 159-163
3. Barrenetxe J., Villaro A.C., Guembe L., Pascual I., Muñoz-Navas M., Barber A., and Lostao M.P. Distribution of the long leptin receptor isoform in brush border, basolateral membrane, and cytoplasm of enterocytes. Gut 50 (2002) 797-802
4. Biernat M., Zabielski R., Yao G., Marion J., le Huërou-Luron I., and Le Dividich J. Effect of formula vs. sow's milk feeding on the gut morphology in neonatal piglets. In: Lindberg J.E., and Ogle B. (Eds). Digestive Physiology in Pigs (2001), CABI Publishing, Wallingford 43-45
5. Biernat M., Woliński J., Godlewski M.M., Motyl T., Morisset J., and Zabielski R. Apoptosis in the gut of neonatal piglets. Proceedings of the 9th International Symposium on Digestive Physiology in Pigs (2003), University of Alberta, Edmonton 46-48
6. Blum J.W., and Hammon H. Colostrum effects on the gastrointestinal tract, and on nutritional, endocrine and metabolic parameters in neonatal calves. Livest. Poult. Prod. 66 (2000) 151-159
7. Brzozowski T., Konturek P.C., Konturek S.J., Pajdo R., Duda A., Pierzchalski P., Bielański W., and Hahn E.G. Leptin in gastroprotection induced by cholecystokinin or by a meal. Role of vagal and sensory nerves and nitric oxide. Eur. J. Pharmacol. 374 (1999) 263-276
8. Burrin D.G., Shulman R.J., Reeds P.J., Davis T.A., and Gravitt K.R. Porcine colostrums and milk stimulate visceral organ and skeletal muscle protein synthesis in neonatal piglets. J. Nutr. 122 (1992) 1205-1213
9. Burrin D., Guan X., Stoll B., Petersen Y.M., and Sangild P.T. Glucagon-like peptide 2: a key link between nutrition and intestinal adaptation in neonates?. J. Nutr. 133 (2003) 3712-3716
10. Burrin D.G., Stoll B., Guan X., Cui L., Chang X., and Holst J.J. Glucagon-like peptide 2 dose-dependently activates intestinal cell survival and proliferation in neonatal piglets. Endocrinology 146 (2005) 22-32
11. Casabiell X., Pineiro V., Tome M.A., Peino R., Dieguez C., and Casanueva F.F. Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J. Clin. Endocrinol. Metab. 82 (1997) 4270-4273
12. Ceregrzyn M., and Kuwahara A. The role of nitric oxide in motility of the developing gastrointestinal tract. In: Zabielski R., Gregory P.C., and Weström B. (Eds). Biology of the Intestine in Growing Animals (2002), Elsevier, Amsterdam 271-324
13. Date Y., Mondal M.S., Matsukura S., Ueta Y., Yamashita H., Kaiya H., Kangawa K., and Nakazato M. Distribution of orexin/hypocretin in the rat median eminence and pituitary. Brain Res. Mol. Brain Res. 76 (2000) 1-6
14. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., Fukuhara C., Battenberg E.L., Gautvik V.T., Bartlett II F.S., Frankel W.N., van den Pol A.N., Bloom F.E., Gautvik K.M., and Sutcliffe J.G. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 322-327
15. Dembiński A., Konturek P.K., and Konturek S.J. Role of gastrin and cholecystokinin in the growth-promoting action of bombesin on the gastroduodenal mucosa and the pancreas. Regul. Pept. 27 (1990) 343-354
16. Dembiński A., Warzecha Z., Ceranowicz P., Bielański W., Cieszkowski J., Dembiński M., Pawlik W.W., Kuwahara A., Kato I., and Konturek P.C. Variable effect of ghrelin administration on pancreatic development in young rats. Role of insulin-like growth factor-1. J. Physiol. Pharmacol. 56 (2005) 555-570
17. Eder K. Effects of l-carnitine supplementation in sows. Chem. Mon. 136 (2005) 1535-1544
18. Ekblad E., and Sundler F. Innervation of the small intestine. In: Zabielski R., Gregory P.C., and Weström B. (Eds). Biology of the Intestine in Growing Animals (2002), Elsevier, Amsterdam 235-270
19. Estienne M.J., Harper A.F., Barb C.R., and Azain M.J. Concentrations of leptin in serum and milk collected from lactating sows differing in body condition. Domest. Anim. Endocrinol. 19 (2000) 275-280
20. Gacsalyi U., Zabielski R., and Pierzynowski S.G. Telemetry facilitates long-term recording of gastrointestinal myoelectrical activity in pigs. Exp. Physiol. 85 (2000) 239-241
21. Godlewski M.M., Słupecka M., Woliński J., Skrzypek T., Skrzypek H., Motyl T., and Zabielski R. Into the unknown - the death pathways in the neonatal gut epithelium. J. Physiol. Pharmacol. 56 Supp. 3 (2005) 7-24
22. Guan X., Karpen H.E., Stephens J., Bukowski J.T., Niu S., Zhang G., Stoll B., Finegold M.J., Holst J.J., Hadsell D., Nichols B.L., and Burrin D.G. GLP-2 receptor localizes to enteric neurons and endocrine cells expressing vasoactive peptides and mediates increased blood flow. Gastroenterology 130 (2006) 150-164
23. Guilloteau P., Le Huërou-Luron I., Le Drean G., Gestin M., Philouze-Rome V., Artiaga A., Bernard C., and Chayvialle J.A. Gut regulatory peptide levels in bovine fetuses and their dams between the 3rd and 9th months of gestation. Biol. Neonate 74 (1998) 430-438
24. Hansen L., Lampert S., Mineo H., and Holst J.J. Neural regulation of glucagon-like peptide-1 secretion in pigs. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E939-E947
25. Hayashida T., Murakami K., Mogi K., Nishihara M., Nakazato M., Mondal M.S., Horii Y., Kojima M., Kangawa K., and Murakami N. Ghrelin in domestic animals: distribution in stomach and its possible role. Domest. Anim. Endocrinol. 21 (2001) 17-24
26. Hogg J., Hill D.J., and Han V.K.M. The ontogeny of insulin-like growth factor (IGF) and IGF binding protein gene expression in the rat pancreas. J. Mol. Endocrinol. 13 (1994) 49-58
27. Houseknecht K.L., McGuire M.K., Portocarrero C.P., McGuire M.A., and Beerman K. Leptin is present in human milk and is related to maternal plasma leptin concentration and adiposity. Biochem. Biophys. Res. Commun. 240 (1997) 742-747
28. Huizinga J.D., Berezin I., Sircar K., Hewlett B., Donnelly G., Bercik P., Ross C., Algoufi T., Fitzgerald P., Der T., Riddell R.H., Collins S.M., and Jacobson K. Development of interstitial cells of Cajal in a full-term infant without an enteric nervous system. Gastroenterology 120 (2001) 561-567
29. Kirchgessner A.L., and Liu M. Orexin synthesis and response in the gut. Neuron 24 (1999) 941-951
30. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., and Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402 (1999) 656-660
31. Korczyński W., Ceregrzyn M., Matyjek R., Kato I., Kuwahara A., Woliński J., and Zabielski R. Central and local (enteric) action of orexins. J. Physiol. Pharmaccol. 57 S6 (2006) 17-42
32. Kotunia A., Woliński J., Słupecka M., Dolman D., Kato I., Kuwahara A., and Zabielski R. Exogenous ghrelin retards the development of the small intestine in pig neonates fed with artificial milk formula. Book of Abstracts, Digestive Physiology in Pigs (2006) May 25-27, 2006, Vejle, Denmark, p. 82
33. Lake N., Wright E.D., and Lapp W.S. Effects of taurine deficiency on immune function in mice. Adv. Exp. Med. Biol. 315 (1992) 241-243
34. Larsson K.P., Akerman K.E., Magga J., Uotila S., Kukkonen J.P., Nasman J., and Herzig K.H. The STC-1 cells express functional orexin-A receptors coupled to CCK release. Biochem. Biophys. Res. Commun. 309 (2003) 209-216
35. Lee C.Y., Bazer F.W., Etherton T.D., and Simmen F.A. Ontogeny of insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in porcine serum during fetal and postnatal development. Endocrinology 128 (1991) 2336-2344
36. Lipkin M., Sherlock P., and Bell B. Cell proliferation kinetics in the gastrointestinal tract of man. II. Cell renewal in stomach, ileum, colon and rectum. Gastroenterology 45 (1963) 721-729
37. Marion J., Biernat M., Thomas F., Savary G., Le Breton Y., Zabielski R., Le Huërou-Luron I., and Le Dividich J. Small intestine growth and morphometry in piglets weaned at 7 days of age. Effects of level of energy intake. Reprod. Nutr. Dev. 42 (2002) 339-354
38. Menard D., Arsenault P., and Pothier P. Biologic effects of epidermal growth factor in human fetal jejunum. Gastroenterology 94 (1988) 656-663
39. Metges C.C., and Hammon H.M. Nutritional programming: prenatal nutrition effects on the regulation of growth and metabolism. J. Anim. Feed Sci. 14 (2005) 15-30
40. Morton N.M., Emilsson V., Liu Y.L., and Cawthorne M.A. Leptin action in intestinal cells. J. Biol. Chem. 273 (1998) 26194-26201
41. Nagashima K., Itoh K., and Kuroume T. Levels of insulin-like growth factor I in full-and preterm human milk in comparison to levels in cow's milk and in milk formulas. Biol. Neonate 58 (1990) 343-346
42. Nankervis C.A., Reber K.M., and Nowicki P.T. Age-dependent changes in the postnatal intestinal microcirculation. Microcirculation 8 (2001) 377-387
43. Natarajan D., and Pachnis V. Development of the enteric nervous system. In: Sanderson I.R., and Walker W.A. (Eds). Development of the Gastrointestinal Tract (2000), B.C. Decker, Inc., Hamilton 197-210
44. Nowak K.W., Strowski M.Z., Świtońska M.M., Kaczmarek P., Singh V., Fabis M., Mackowiak P., Nowak M., and Malendowicz L.K. Evidence that orexins A and B stimulate insulin secretion from rat pancreatic islets via both receptor subtypes. Int. J. Mol. Med. 15 (2005) 969-972
45. Owen C.G., Martin R.M., Whincup P.H., Davey-Smith G., Gillman M.W., and Cook D.G. The effect of breastfeeding on mean body mass index throughout life: a quantitative review of published and unpublished observational evidence. Am. J. Clin. Nutr. 82 (2005) 1298-1307
46. Pan W., Tu H., and Kasin A.J. Differential BBB interactions of three ingestive peptides: obestatin, ghrelin, and adiponectin. Peptides 27 (2006) 911-916
47. Peeters T.L. Central and peripheral mechanisms by which ghrelin regulates gut motility. J. Physiol. Pharmacol. 54 Suppl 4 (2003) 95-103
48. Petersen Y.M., Hartmann B., Holst J.J., Le Huerou-Luron I., Bjornvad C.R., and Sangild P.T. Introduction of enteral food increases plasma GLP-2 and decreases GLP-2 receptor mRNA abundance during pig development. J. Nutr. 133 (2003) 1781-1786
49. Polk B., and Barnard J.A. Hormones and growth factors in intestinal development. In: Sanderson I.R., and Walker W.A. (Eds). Development of the Gastrointestinal Tract (2000), B.C. Decker, Inc., Hamilton 37-56
50. Puzio I., Kapica M., Bieńko M., Valverde Piedra J.L., Gajewski Z., Kulasek G., and Zabielski R. Dietary bioactive substances influenced perinatal bone development in piglets. Livest. Sci. 108 (2007) 68-71 10.1016/j.livsci.2007.01.047 (this issue)
51. Ramanau A., Kluge H., Spilke J., and Eder K. Supplementation of sows with l-carnitine during pregnancy and lactation improves growth of the piglets during the suckling period through increased milk production. J. Nutr. 134 (2004) 86-92
52. Read L.C., Upton F.M., Francis G.L., Wallace J.C., Dahlenberg G.W., and Ballard F.J. Growth factor concentrations and growth-promoting activity of human milk following premature birth. J. Dev. Physiol. 7 (1985) 135-145
53. Riva E., Verduci E., Agostoni C., and Giovannini M. Closer to the gold standard: an appraisal of formulae available in Italy for use in formula-fed infants. J. Int. Med. Res. 33 (2005) 595-611
54. Rudloff S., and Kunz C. Protein and nonprotein nitrogen components in human milk, bovine milk, and infant formula: quantitative and qualitative aspects in infant nutrition. J. Pediatr. Gastroenterol. Nutr. 24 (1997) 328-344
55. Sakurai T., Amemiya A., Ishii M., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (1998) 573-585
56. Salfen B.E., Carroll J.A., Keisler D.H., and Strauch T.A. Effects of exogenous ghrelin on feed intake, weight gain, behavior, and endocrine responses in weanling pigs. J. Anim. Sci. 82 (2004) 1957-1966
57. Sánchez de Miguel M.J., and Burrell M.A. Immunocytochemical detection of orexin A in endocrine cells of the developing mouse gut. J. Histochem. Cytochem. 50 (2002) 63-69
58. Schanbacher F.L., Talhouk R.S., and Murray F.A. Biology and origin of bioactive peptides in milk. Livest. Poult. Prod. 50 (1997) 105-123
59. Schlimme E., and Meisel H. Bioactive peptides derived from milk proteins. Structural, physiological and analytical aspects. Nahrung 39 (1995) 1-20
60. Shin E.D., Estall J.L., Izzo A., Drucker D.J., and Brubaker P.L. Mucosal adaptation to enteral nutrients is dependent on the physiologic actions of glucagon-like peptide-2 in mice. Gastroenterology 128 (2005) 1340-1353
61. Słupecka M., Woliński J., and Zabielski R. Leptin affects the p53 expression in the gut mucosa of neonatal piglets. 13th Euroconference on Apoptosis, Budapest, Hungary, October 1-4, Abstract P-207 (2005)
62. Smith-Kirwin S.M., O'Connor D.M., De Johnston J., Lancey E.D., Hassink S.G., and Funanage V.L. Leptin expression in human mammary epithelial cells and breast milk. J. Clin. Endocrinol. Metab. 83 (1998) 1810-1813
63. Stephens J., Stoll B., Cottrell J., Chang X., Helmrath M., and Burrin D.G. Glucagon-like peptide-2 acutely increases proximal small intestinal blood flow in TPN-fed neonatal piglets. Am. J. Physiol., Regul. Integr. Comp. Physiol. 290 (2006) R283-R289
64. Svendsen L.S., Weström B.R., Svendsen J., Ohlsson B.G., Ekman R., and Karlsson B.W. Insulin involvement in intestinal macromolecular transmission and closure in neonatal pigs. J. Pediatr. Gastroenterol. Nutr. 5 (1986) 299-304
65. Ucar B., Kirel B., Bor O., Kilic F.S., Dogruel N., Aydogdu S.D., and Tekin N. Breast milk leptin concentrations in initial and terminal milk samples: relationships to maternal and infant plasma leptin concentrations, adiposity, serum glucose, insulin, lipid and lipoprotein levels. J. Pediatr. Endocrinol. Metab. 13 (2000) 149-156
66. Usami M., Komurasaki T., Hanada A., Kinoshita K., and Ohata A. Effect of γ-linolenic acid or docosahexoenoic acid on tight junction permeability in intestinal monolayer cells and their mechanism by protein kinase C activation and/or eicosanoid formation. Nutrition 19 (2003) 150-156
67. Van Ginneken C., and Weyns A. A stereological evaluation of secretin and gastric inhibitory peptide-containing mucosal cells of the perinatal small intestine of the pig. J. Anat. 205 (2004) 267-275
68. Varga G., Kisfalvi K., Pelosini I., D'Amato M., and Scarpignato C. Different actions of CCK on pancreatic and gastric growth in the rat: effect of CCK(A) receptor blockade. Br. J. Pharmacol. 124 (1998) 435-440
69. Warzecha Z., Dembiński A., Ceranowicz P., Dembiński M., Cieszkowski J., Bielañski W., Pawlik W.W., Kuwahara A., and Kato I. Dual age-dependent effect of ghrelin administration on serum level of insulin-like growth factor-1 and gastric growth in young rats. Eur. J. Pharmacol. 529 (2006) 145-150
70. Wester T., O'Briain D.S., and Puri P. Notable postnatal alterations in the myenteric plexus of normal human bowel. Gut 44 (1999) 666-674
71. Weström B.R., Ekman R., Svendsen L., Svendsen J., and Karlsson B.W. Levels of immunoreactive insulin, neurotensin, and bombesin in porcine colostrum and milk. J. Pediatr. Gastroenterol. Nutr. 6 (1987) 460-465
72. Woliński J., Leśniewska V., Biernat M., Ba{ogonek}belewska M., Korczyński W., and Zabielski R. Exogenous leptin influences gastrointestinal growth and in vitro small intestinal motility in neonatal piglets - preliminary results. J. Anim. Feed Sci. 10 Suppl 2 (2001) 249-254
73. Woliński J., Biernat M., Guilloteau P., Weström B., and Zabielski R. Exogenous leptin controls the development of the small intestine in neonatal piglets. J. Endocrinol. 177 (2003) 215-222
74. Xu R.-J. Bioactive peptides in milk and their biological and health implications. Food Rev. Int. 14 (1998) 1
75. Xu R.J., Mellor D.J., Tungthanathanich P., Birtles M.J., Reynolds G.W., and Simpson H.V. Growth and morfological changes in the small intestine in piglets during the first three days after birth. J. Dev. Physiol. 18 (1992) 161-172
76. Xu R.J., Wang F., and Zhang S.H. Postnatal adaptation of the gastrointestinal tract in neonatal pigs: a possible role of milk-borne growth factors. Livest. Poult. Prod. 66 (2000) 95-107
77. Xu L., Depoortere I., Tomasetto C., Zandecki M., Tang M., Timmermans J.P., and Peeters T.L. Evidence for the presence of motilin, ghrelin, and the motilin and ghrelin receptor in neurons of the myenteric plexus. Regul. Pept. 124 (2005) 119-125
78. Yuan C.S., Attele A.S., Wu J.A., Zhang L., and Shi Z.Q. Peripheral gastric leptin modulates brain stem neuronal activity in neonates. Am. J. Physiol. 277 (1999) G626-G630
79. Zabielski R. Regulatory peptides in milk, food, and in the gastrointestinal lumen of young animals and children. J. Anim. Feed Sci. 7 Suppl 1 (1998) 65-78
80. Zabielski R., Laubitz D., Woliński J., and Guilloteau P. Nutritional and hormonal control of gut epithelium remodeling in neonatal piglets. J. Anim. Feed Sci. 14 Suppl 1 (2005) 99-112
81. Zabielski R., Gajewski Z., Valverde Pietra J.L., Woliński J., Laubitz D., Wilczak J., and Kulasek G. The perinatal development of the gastrointestinal tract in piglets can be modified by supplementation of sow diet with bioactive substances. Livest. Sci. (2007) doi:10.1016/j.livsci.2007.01.037
82. Zhang Y., Proenca R., Maffei M., Barone M., Leopold I., and Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 372 (1994) 425-432
83. Zhang H., Malo C., and Buddington R. Suckling induces rapid intestinal growth and changes in brush border digestive functions of newborn pigs. J. Nutr. 127 (1997) 418-426
84. Zhang J.V., Ren P.G., Avsian-Kretchmer O., Luo C.W., Rauch R., Klein C., and Hsueh A.J. Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake. Science 310 (2005) 996-999