Diet effects on glucose absorption in the small intestine of neonatal calves: Importance of intestinal mucosal growth, lactase activity, and glucose transporters

Journal of Dairy Science

Volumn 97, Issue 10, 2014, Pages 6358-6369

  Steinhoff Wagner, Julia ^a   Zitnan, Rudolf ^b   Schönhusen, Ulrike ^a   Pfannkuche, Helga ^c   Hudakova, Monika ^d   Metges, Cornelia C ^a   Hammon, Harald M ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b Institute of Nutrition National Centre of Agriculture and Food Nitra   (Slovakia)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d School of Economics and Management in Public Administration in Bratislava Slovak Republic   (Slovakia)

Author keywords

Colostrum; Glucose transporter; Intestinal mucosa growth; Lactase

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 2; LACTASE; SODIUM GLUCOSE COTRANSPORTER 1;

ANIMAL; BOVINE; COLOSTRUM; DIET; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE MUCOSA; MALE; METABOLISM; MILK; NEWBORN; PREGNANCY; SMALL INTESTINE; VETERINARY;

ANIMALS; ANIMALS, NEWBORN; CATTLE; COLOSTRUM; DIET; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLUCOSE TRANSPORTER TYPE 2; INTESTINAL MUCOSA; INTESTINE, SMALL; LACTASE; MALE; MILK; PREGNANCY; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 84908027555     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2014-8391     Document Type: Article

References (59)

1. Alexander A.N., Carey H.V. Oral IGF-I enhances nutrient and electrolyte absorption in neonatal piglet intestine. Am. J. Physiol. 1999, 277:G619-G625.
2. Arsenault P., Menard D. Stimulatory effects of epidermal growth factor on deoxyribonucleic acid synthesis in the gastrointestinal tract of the suckling mouse. Comp. Biochem. Physiol. B 1987, 86:123-127.
3. Au A., Gupta A., Schembri P., Cheeseman C.I. Rapid insertion of GLUT2 into the rat jejunal brush-border membrane promoted by glucagon-like peptide 2. Biochem. J. 2002, 367:247-254.
4. + intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R738-R743.
5. Bauer M.L., Harmon D.L., Bohnert D.W., Branco A.F., Huntington G.B. Influence of alpha-linked glucose on sodium-glucose cotransport activity along the small intestine in cattle. J. Anim. Sci. 2001, 79:1917-1924.
6. Baumrucker C.R., Blum J.W. Effects of dietary recombinant human insulin-like growth factor-I on concentrations of hormones and growth factors in the blood of newborn calves. J. Endocrinol. 1994, 140:15-21.
7. Baumrucker C.R., Hadsell D.L., Blum J.W. Effects of dietary insulin-like growth factor I on growth and insulin-like growth factor receptors in neonatal calf intestine. J. Anim. Sci. 1994, 72:428-433.
8. Berseth C.L. Enhancement of intestinal growth in neonatal rats by epidermal growth factor in milk. Am. J. Physiol. 1987, 253:G662-G665.
9. Bird A.R., Croom W.J., Fan Y.K., Black B.L., McBride B.W., Taylor I.L. Peptide regulation of intestinal glucose absorption. J. Anim. Sci. 1996, 74:2523-2540.
10. Blättler U., Hammon H.M., Morel C., Philipona C., Rauprich A., Rome V., Le Huerou-Luron I., Guilloteau P., Blum J.W. Feeding colostrum, its composition and feeding duration variably modify proliferation and morphology of the intestine and digestive enzyme activities of neonatal calves. J. Nutr. 2001, 131:1256-1263.
11. Blum J.W. Nutritional physiology of neonatal calves. J. Anim. Physiol. Anim. Nutr. (Berl.) 2006, 90:1-11.
12. Blum J.W., Hammon H. Colostrum effects on the gastrointestinal tract, and on nutritional, endocrine and metabolic parameters in neonatal calves. Livest. Prod. Sci. 2000, 66:151-159.
13. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
14. Bühler C., Hammon H., Rossi G.L., Blum J.W. Small intestinal morphology in eight-day-old calves fed colostrum for different durations or only milk replacer and treated with long-R-3-insulin-like growth factor I and growth hormone. J. Anim. Sci. 1998, 76:758-765.
15. Burrin D.G., Davis T.A., Ebner S., Schoknecht P.A., Fiorotto M.L., Reeds P.J., McAvoy S. Nutrient-independent and nutrient-dependent factors stimulate protein synthesis in colostrum-fed newborn pigs. Pediatr. Res. 1995, 37:593-599.
16. Burrin D.G., Stoll B., Fan M.Z., Dudley M.A., Donovan S.M., Reeds P.J. Oral IGF-I alters the posttranslational processing but not the activity of lactase-phlorizin hydrolase in formula-fed neonatal pigs. J. Nutr. 2001, 131:2235-2241.
17. Burrin D.G., Wester T.J., Davis T.A., Amick S., Heath J.P. Orally administered IGF-I increases intestinal mucosal growth in formula-fed neonatal pigs. Am. J. Physiol. 1996, 270:R1085-R1091.
18. Drozdowski L.A., Clandinin T., Thomson A.B. Ontogeny, growth and development of the small intestine: Understanding pediatric gastroenterology. World J. Gastroenterol. 2010, 16:787-799.
19. +/glucose cotransporter (SGLT1) gene in lamb small intestine during postnatal development. Biochim. Biophys. Acta 1993, 1146:203-212.
20. Fujita M., Matsui H., Nagano K., Nakao M. Asymmetric distribution of ouabain-sensitive ATPase activity in rat intestinal mucosa. Biochim. Biophys. Acta 1971, 233:404-408.
21. Gauthier S.F., Pouliot Y., Maubois J.L. Growth factors from bovine milk and colostrum: Composition, extraction and biological activities. Lait 2006, 86:99-125.
22. Girard J. Metabolic adaptations to change of nutrition at birth. Biol. Neonate 1990, 58(Suppl. 1):3-15.
23. Grütter R., Blum J.W. Insulin and glucose in neonatal calves after peroral insulin and intravenous glucose-administration. Reprod. Nutr. Dev. 1991, 31:389-397.
24. Guilloteau P., Zabielski R., Blum J.W. Gastrointestinal tract and digestion in the young ruminant: Ontogenesis, adaptations, consequences and manipulations. J. Physiol. Pharmacol. 2009, 60:37-46.
25. Hammon H., Blum J.W. Prolonged colostrum feeding enhances xylose absorption in neonatal calves. J. Anim. Sci. 1997, 75:2915-2919.
26. Hammon H., Blum J.W. The somatotropic axis in neonatal calves can be modulated by nutrition, growth hormone, and long-R-3-IGF-I. Am. J. Physiol. 1997, 273:130-138.
27. Hammon H.M., Schönhusen U. Effects of colostrum (C) feeding and dexamethasone (Dexa) treatment on sodium-dependent glucose co-transporter-1 (SGLT1) in the small intestine of neonatal calves. J. Anim. Sci. 2006, 84(Suppl. 1):31.
28. Hammon H.M., Steinhoff-Wagner J., Flor J., Schönhusen U., Metges C.C. Role of colostrum and colostrum components on glucose metabolism in neonatal calves. J. Anim. Sci. 2013, 91:685-695.
29. Hammon H.M., Steinhoff-Wagner J., Schönhusen U., Metges C.C., Blum J.W. Energy metabolism in the newborn farm animal with emphasis on the calf: Endocrine changes and responses to milk-born and systemic hormones. Domest. Anim. Endocrinol. 2012, 43:171-185.
30. Hammon H.M., Stürmer G., Schneider F., Tuchscherer A., Blum H., Engelhard T., Genzel A., Staufenbiel R., Kanitz W. Performance and metabolic and endocrine changes with emphasis on glucose metabolism in high-yielding dairy cows with high and low fat content in liver after calving. J. Dairy Sci. 2009, 92:1554-1566.
31. Kellett G.L., Brot-Laroche E., Mace O.J., Leturque A. Sugar absorption in the intestine: The role of GLUT2. Annu. Rev. Nutr. 2008, 28:35-54.
32. Kellett G.L., Helliwell P.A. The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. Biochem. J. 2000, 350:155-162.
33. Kelly D., King T.P., McFadyen M., Coutts A.G. Effect of preclosure colostrum intake on the development of the intestinal epithelium of artificially reared piglets. Biol. Neonate 1993, 64:235-244.
34. Kühne S., Hammon H.M., Bruckmaier R.M., Morel C., Zbinden Y., Blum J.W. Growth performance, metabolic and endocrine traits, and absorptive capacity in neonatal calves fed either colostrum or milk replacer at two levels. J. Anim. Sci. 2000, 78:609-620.
35. Lee C.Y., Head H.H., Feinstein C.R., Hayen J., Simmen F.A. Endocrine changes and circulating insulin-like growth factors in newborn calves fed colostrum, milk or milk replacer. Asian-australas. J. Anim. Sci. 1995, 8:51-58.
36. Lohrenz A.K., Duske K., Schönhusen U., Losand B., Seyfert H.M., Metges C.C., Hammon H.M. Glucose transporter and enzymes related to glucose synthesis in small intestinal mucosa of dairy cows fed either a starch-based or a diet containing rumen-protected fat. J. Dairy Sci. 2011, 94:4546-4555.
37. Michanek P., Ventorp M., Westrom B. Milk intake before first colostrum in newborn dairy calves-Effect on intestinal transmission of macromolecules. J. Dairy Sci. 1990, 73:480-483.
38. Mir P.S., Bailey D.R.C., Mir Z., Morgan Jones S.D., Douwes H., McAllister T.A., Weselake R.J., Lozeman F.J. Activity of intestinal mucosal membrane carbohydrases in cattle of different breeds. Can. J. Anim. Sci. 1997, 77:441-446.
39. Odle J., Zijlstra R.T., Donovan S.M. Intestinal effects of milkborne growth factors in neonates of agricultural importance. J. Anim. Sci. 1996, 74:2509-2522.
40. Ontsouka E.C., Korczak B., Hammon H.M., Blum J.W. Real-time PCR quantification of bovine lactase mRNA: Localization in the gastrointestinal tract of milk-fed calves. J. Dairy Sci. 2004, 87:4230-4237.
41. Oste M., van Haver E., Thymann T., Sangild P., Weyns A., van Ginneken C.J. Formula induces intestinal apoptosis in preterm pigs within a few hours of feeding. JPEN J. Parenter. Enteral. Nutr. 2010, 34:271-279.
42. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
43. Pfannkuche H., Gäbel G. Glucose, epithelium, and enteric nervous system: Dialogue in the dark. J. Anim. Physiol. Anim. Nutr. (Berl.) 2009, 93:277-286.
44. Pfannkuche H., Taifour F., Steinhoff-Wagner J., Hammon H.M., Gäbel G. Postnatal changes of MCT1 expression in the forestomach of calves. J. Anim. Physiol. Anim. Nutr. (Berl.) 2014, 98:140-148.
45. Rauprich A.B.E., Hammon H.M., Blum J.W. Effects of feeding colostrum and a formula with nutrient contents as colostrum on metabolic and endocrine traits in neonatal calves. Biol. Neonate 2000, 78:53-64.
46. Roffler B., Fah A., Sauter S.N., Hammon H.M., Gallmann P., Brem G., Blum J.W. Intestinal morphology, epithelial cell proliferation, and absorptive capacity in neonatal calves fed milk-born insulin-like growth factor-I or a colostrum extract. J. Dairy Sci. 2003, 86:1797-1806.
47. Sauter S.N., Roffler B., Philipona C., Morel C., Rome V., Guilloteau P., Blum J.W., Hammon H.M. Intestinal development in neonatal calves: Effects of glucocorticoids and dependence on colostrum feeding. Biol. Neonate 2004, 85:94-104.
48. +-Dependent transport of d-xylose by bovine intestinal brush border membrane vesicles (BBMV) is inhibited by various pentoses and hexoses. J. Vet. Med. A. Physiol. Clin. Med. 2000, 47:617-626.
49. Schröder B., Breves G. Mechanisms of phosphate uptake into brush border membrane vesicles from goat jejunum. J. Comp. Physiol. B 1996, 166:230-240.
50. Shirazi-Beechey S.P., Wood I.S., Dyer J., Scott D., King T.P. Intestinal sugar transport in ruminants. Ruminant Physiology 1995, 117-133. Ferdinand Enke Verlag, Stuttgart, Germany, . W. von Engelhardt, S. Leonhard-Marek, G. Breves, D. Gieseke (Eds.).
51. Simmen F.A., Cera K.R., Mahan D.C. Stimulation by colostrum or mature milk of gastrointestinal tissue-development in newborn pigs. J. Anim. Sci. 1990, 68:3596-3603.
52. Steinhoff-Wagner J., Görs S., Junghans P., Bruckmaier R.M., Kanitz E., Metges C.C., Hammon H.M. Intestinal glucose absorption but not endogenous glucose production differs between colostrum- and formula-fed neonatal calves. J. Nutr. 2011, 141:48-55.
53. Thymann T., Burrin D.G., Tappenden K.A., Bjornvad C.R., Jensen S.K., Sangild P.T. Formula-feeding reduces lactose digestive capacity in neonatal pigs. Br. J. Nutr. 2006, 95:1075-1081.
54. Tivey D.R., Le Dividich J., Herpin P., Brown D., Dauncey M.J. Differential effects of lipid and carbohydrate on enterocyte lactase activity in newborn piglets. Exp. Physiol. 1994, 79:189-201.
55. Vacher P.Y., Bestetti G., Blum J.W. Insulin-like growth factor I absorption in the jejunum of neonatal calves. Biol. Neonate 1995, 68:354-367.
56. Widdowson E.M., Colombo V.E., Artavanis C.A. Changes in the organs of pigs in response to feeding for the first 24h after birth. II. The digestive tract. Biol. Neonate 1976, 28:272-281.
57. Xu R.J., Sangild P.T., Zhang Y.Q., Zhang S.H. Bioactive compounds in porcine colostrum and milk and their effects on intestinal development in neonatal pigs. Biology of the Intestine in Growing Animals: Developments in Animal and Veterinary Sciences 2002, 169-192. Elsevier, Amsterdam, the Netherlands. R. Zabielski, S. Pierzynowski, B. Westrom (Eds.).
58. Xu R.J., Wang F., Zhang S.H. Postnatal adaptation of the gastrointestinal tract in neonatal pigs: A possible role of milk-borne growth factors. Livest. Prod. Sci. 2000, 66:95-107.
59. Zitnan R., Voigt J., Kuhla S., Wegner J., Chudy A., Schönhusen U., Brna M., Zupcanova M., Hagemeister H. Morphology of small intestinal mucosa and intestinal weight change with metabolic type of cattle. Vet. Med. (Praha) 2008, 53:525-532.