Lactoferrin up-regulates intestinal gene expression of brain-derived neurotrophic factors BDNF, UCHL1 and alkaline phosphatase activity to alleviate early weaning diarrhea in postnatal piglets

Journal of Nutritional Biochemistry

Volumn 25, Issue 8, 2014, Pages 834-842

  Yang, Changwei ^a   Zhu, Xi ^a   Liu, Ni ^a   Chen, Yue ^a   Gan, Hexia ^a   Troy, Frederic A ^a,b   Wang, Bing ^a,c  

^a XIAMEN UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHARLES STURT UNIVERSITY   (Australia)

Author keywords

BDNF; Colonic flora; Gut maturation; IAP; Lactoferrin; Neurotrophins; UCHL1

Indexed keywords

ALKALINE PHOSPHATASE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LACTOFERRIN; MESSENGER RNA; RNA 16S; UBIQUITIN THIOLESTERASE; LACTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCENDING COLON; BDNF GENE; BIFIDOBACTERIUM; COLON FLORA; CONTROLLED STUDY; DIET SUPPLEMENTATION; DUODENUM; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE; GENE EXPRESSION REGULATION; INCIDENCE; INFANTILE DIARRHEA; INTESTINE; INTESTINE CRYPT; JEJUNUM; LACTOBACILLUS; MALE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; UCHL1 GENE; ANIMAL; BODY WEIGHT; COLON; DIARRHEA; DIET THERAPY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PIG; UPREGULATION; WEANING;

ESCHERICHIA COLI; LACTOBACILLUS;

ALKALINE PHOSPHATASE; ANIMALS; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; COLON; DIARRHEA; DIETARY SUPPLEMENTS; DUODENUM; GENE EXPRESSION REGULATION; INTESTINAL MUCOSA; INTESTINES; JEJUNUM; LACTASE; LACTOFERRIN; MALE; SUS SCROFA; UBIQUITIN THIOLESTERASE; UP-REGULATION; WEANING;

EID: 84903768127     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.03.015     Document Type: Article

References (42)

1. Neu J. Gastrointestinal maturation and implications for infant feeding. Early Hum Dev 2007, 83:767-775.
2. Guerrant R.L., Kosek M., Moore S., Lorntz B., Brantley R., Lima A.A. Magnitude and impact of diarrheal diseases. Arch Med Res 2002, 33:351-355.
3. Newburg D.S., Walker W.A. Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res 2007, 61:2-8.
4. Newburg D.S. Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. J Anim Sci 2009, 87:26-34.
5. Vogel H.J. Lactoferrin, a bird's eye view. Biochem Cell Biol 2012, 90:233-244.
6. Ronayne de Ferrer P.A., Baroni A., Sambucetti M.E., Lopez N.E., Ceriani Cernadas J.M. Lactoferrin levels in term and preterm milk. J Am Coll Nutr 2000, 19:370-373.
7. Steijns J.M., van Hooijdonk A.C. Occurrence, structure, biochemical properties and technological characteristics of lactoferrin. Br J Nutr 2000, 84(Suppl. 1):S11-S17.
8. Lonnerdal B., Jiang R., Du X. Bovine lactoferrin can be taken up by the human intestinal lactoferrin receptor and exert bioactivities. J Pediatr Gastroenterol Nutr 2011, 53:606-614.
9. Singh P.K., Parsek M.R., Greenberg E.P., Welsh M.J. A component of innate immunity prevents bacterial biofilm development. Nature 2002, 417:552-555.
10. Tang Z., Yin Y., Zhang Y., Huang R., Sun Z., Li T., et al. Effects of dietary supplementation with an expressed fusion peptide bovine lactoferricin-lactoferrampin on performance, immune function and intestinal mucosal morphology in piglets weaned at age 21 d. Br J Nutr 2009, 101:998-1005.
11. Chen F.X., Yu Y.B., Yuan X.M., Zuo X.L., Li Y.Q. Brain-derived neurotrophic factor enhances the contraction of intestinal muscle strips induced by SP and CGRP in mice. Regul Pept 2012, 178:86-94.
12. Chai N.L., Dong L., Li Z.F., Du K.X., Wang J.H., Yan L.K., et al. Effects of neurotrophins on gastrointestinal myoelectric activities of rats. World J Gastroenterol 2003, 9:1874-1877.
13. Lalles J.P. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 2010, 68:323-332.
14. Lackeyram D., Yang C., Archbold T., Swanson K.C., Fan M.Z. Early weaning reduces small intestinal alkaline phosphatase expression in pigs. J Nutr 2010, 140:461-468.
15. Yang T.S., Wu S.C., Wang S.R. Serum and milk lactoferrin concentration and the correlation with some blood components in lactating sows. Res Vet Sci 2000, 69:95-97.
16. Hartke J., Monaco M., Wheeler M., Donovan S. Effect of a short-term fast on intestinal disaccharidase activity and villus morphology of piglets suckling insulin-like growth factor-I transgenic sows. J Anim Sci 2005, 83:2404-2413.
17. Lu J., Grenache D.G. High-throughput tissue homogenization method and tissue-based quality control materials for a clinical assay of the intestinal disaccharidases. Clin Chim Acta 2010, 411:754-757.
18. Nadkarni M.A., Martin F.E., Jacques N.A., Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 2002, 148:257-266.
19. Furet J.P., Firmesse O., Gourmelon M., Bridonneau C., Tap J., Mondot S., et al. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 2009, 68:351-362.
20. Penders J., Vink C., Driessen C., London N., Thijs C., Stobberingh E.E. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 2005, 243:141-147.
21. Castillo M., Martin-Orue S.M., Manzanilla E.G., Badiola I., Martin M., Gasa J. Quantification of total bacteria, enterobacteria and lactobacilli populations in pig digesta by real-time PCR. Vet Microbiol 2006, 114:165-170.
22. Correa-Matos N.J., Donovan S.M., Isaacson R.E., Gaskins H.R., White B.A., Tappenden K.A. Fermentable fiber reduces recovery time and improves intestinal function in piglets following Salmonella typhimurium infection. J Nutr 2003, 133:1845-1852.
23. Wang Y.-Z., Shan T.-Z., Xu Z.-R., Feng J., Wang Z.-Q. Effects of the lactoferrin (LF) on the growth performance, intestinal microflora and morphology of weanling pigs. Anim Feed Sci Tech 2007, 135:263-272.
24. Legrand D., Elass E., Carpentier M., Mazurier J. Lactoferrin: a modulator of immune and inflammatory responses. Cell Mol Life Sci 2005, 62:2549-2559.
25. Heo J.M., Opapeju F.O., Pluske J.R., Kim J.C., Hampson D.J., Nyachoti C.M. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr (Berl) 2013, 97:207-237.
26. Fawzy A., Arpadi S., Kankasa C., Sinkala M., Mwiya M., Thea D.M., et al. Early weaning increases diarrhea morbidity and mortality among uninfected children born to HIV-infected mothers in Zambia. J Infect Dis 2011, 203:1222-1230.
27. Wang B., Yu B., Karim M., Hu H., Sun Y., McGreevy P., et al. Dietary sialic acid supplementation improves learning and memory in piglets. Am J Clin Nutr 2007, 85:561-569.
28. Goldberg R.F., Austen W.G., Zhang X., Munene G., Mostafa G., Biswas S., et al. Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci U S A 2008, 105:3551-3556.
29. Yen C.C., Lin C.Y., Chong K.Y., Tsai T.C., Shen C.J., Lin M.F., et al. Lactoferrin as a natural regimen for selective decontamination of the digestive tract: recombinant porcine lactoferrin expressed in the milk of transgenic mice protects neonates from pathogenic challenge in the gastrointestinal tract. J Infect Dis 2009, 199:590-598.
30. Moughan P.J., Birtles M.J., Cranwell P.D., Smith W.C., Pedraza M. The piglet as a model animal for studying aspects of digestion and absorption in milk-fed human infants. World Rev Nutr Diet 1992, 67:40-113.
31. Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr 2009, 29:177-222.
32. Callesen J., Halas D., Thorup F., Bach Knudsen K.E., Kim J., Mullan B., et al. The effects of weaning age, diet composition, and categorisation of creep feed intake by piglets on diarrhoea and performance after weaning. Livest Sci 2007, 108:120-123.
33. Zavaleta N., Figueroa D., Rivera J., Sanchez J., Alfaro S., Lonnerdal B. Efficacy of rice-based oral rehydration solution containing recombinant human lactoferrin and lysozyme in Peruvian children with acute diarrhea. J Pediatr Gastroenterol Nutr 2007, 44:258-264.
34. Edde L., Hipolito R.B., Hwang F.F., Headon D.R., Shalwitz R.A., Sherman M.P. Lactoferrin protects neonatal rats from gut-related systemic infection. Am J Physiol Gastrointest Liver Physiol 2001, 281:G1140-G1150.
35. Mosquito S., Ochoa T.J., Cok J., Cleary T.G. Effect of bovine lactoferrin in Salmonella ser. Typhimurium infection in mice. Biometals 2010, 23:515-521.
36. Tori A.J., Carroll A.E., Gupta S.K. Disaccharidase activity in infants and comparison based on symptoms and histological changes. J Pediatr Gastroenterol Nutr 2007, 45:194-198.
37. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009, 9:313-323.
38. Hu W., Zhao J., Wang J., Yu T., Li N. Transgenic milk containing recombinant human lactoferrin modulates the intestinal flora in piglets. Biochem Cell Biol 2012, 90:485-496.
39. Cooper C.A., Nelson K.M., Maga E.A., Murray J.D. Consumption of transgenic cows' milk containing human lactoferrin results in beneficial changes in the gastrointestinal tract and systemic health of young pigs. Transgenic Res 2013, 22:571-578.
40. Schemann M. Control of gastrointestinal motility by the "gut brain" - the enteric nervous system. J Pediatr Gastroenterol Nutr 2005, 41(Suppl. 1):S4-S6.
41. Boesmans W., Gomes P., Janssens J., Tack J., Berghe P.V. Brain-derived neurotrophic factor amplifies neurotransmitter responses and promotes synaptic communication in the enteric nervous system. Gut 2008, 57:314-322.
42. Poon W.W., Carlos A.J., Aguilar B.L., Berchtold N.C., Kawano C.K., Zograbyan V., et al. Beta-amyloid (Abeta) oligomers impair brain-derived neurotrophic factor retrograde trafficking by down-regulating ubiquitin C-terminal hydrolase, UCH-L1. J Biol Chem 2013, 288:16937-16948.