Lactoferrin Promotes Early Neurodevelopment and Cognition in Postnatal Piglets by Upregulating the BDNF Signaling Pathway and Polysialylation

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 256-269

  Chen, Yue ^a   Zheng, Zhiqiang ^a   Zhu, Xi ^a   Shi, Yujie ^b   Tian, Dandan ^a   Zhao, Fengjuan ^a   Liu, Ni ^a   Hüppi, Petra S ^c   Troy, Frederic A ^a,d   Wang, Bing ^a,e  

^a XIAMEN UNIVERSITY   (China)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e CHARLES STURT UNIVERSITY   (Australia)

Author keywords

BDNF signaling pathway; Cognition; CREB; Gene microarray and qPCR; Lactoferrin; Neurodevelopment; Polysialic acid NCAMs

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LACTOFERRIN; POLYSIALIC ACID; HYDROCORTISONE; N ACETYLNEURAMINIC ACID; NERVE GROWTH FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; COGNITION; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; FOOD INTAKE; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; MALE; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; PIGLET; POSTNATAL DEVELOPMENT; RADIAL ARM MAZE TEST; SIALYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BLOOD; BODY WEIGHT; BOVINE; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVOUS SYSTEM; NEWBORN; PIG;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CATTLE; COGNITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HYDROCORTISONE; LACTOFERRIN; MALE; MEMORY; N-ACETYLNEURAMINIC ACID; NERVE GROWTH FACTORS; NERVOUS SYSTEM; NEURONAL PLASTICITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SUS SCROFA; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84937950414     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8856-9     Document Type: Article

References (54)

1. Wang B (2012) Molecular mechanism underlying sialic acid as an essential nutrient for brain development and cognition. Adv Nutr 3(3):465S–472S. doi:10.3945/an.112.0018753/3/465S
2. Wang B (2009) Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr 29:177–222. doi:10.1146/annurev.nutr.28.061807.155515
3. Serpero LD, Frigiola A, Gazzolo D (2012) Human milk and formulae: neurotrophic and new biological factors. Early Hum Dev 88(Suppl 1):S9–S12. doi:10.1016/j.earlhumdev.2011.12.021S0378-3782(11)00391-4
4. Montagne P, Cuilliere ML, Mole C, Bene MC, Faure G (2001) Changes in lactoferrin and lysozyme levels in human milk during the first twelve weeks of lactation. Adv Exp Med Biol 501:241–247
5. Adamkin DH (2012) Mother’s milk, feeding strategies, and lactoferrin to prevent necrotizing enterocolitis. JPEN J Parenter Enteral Nutr 36(1 Suppl):25S–29S. doi:10.1177/0148607111420158
6. Sanchez L, Aranda P, Perez MD, Calvo M (1988) Concentration of lactoferrin and transferrin throughout lactation in cow’s colostrum and milk. Biol Chem Hoppe Seyler 369(9):1005–1008
7. Levay PF, Viljoen M (1995) Lactoferrin: a general review. Haematologica 80(3):252–267
8. Wolfson DR, Robbins JB (1971) Heterogeneity of human lactoferrin due to differences in sialic acid content. Pediatr Res 5:514–517
9. Lonnerdal B, Iyer S (1995) Lactoferrin: molecular structure and biological function. Annu Rev Nutr 15:93–110. doi:10.1146/annurev.nu.15.070195.000521
10. Legrand D, Pierce A, Elass E, Carpentier M, Mariller C, Mazurier J (2008) Lactoferrin structure and functions. Adv Exp Med Biol 606:163–194. doi:10.1007/978-0-387-74087-4_6
11. Orsi N (2004) The antimicrobial activity of lactoferrin: current status and perspectives. Biometals 17(3):189–196
12. Legrand D (2012) Lactoferrin, a key molecule in immune and inflammatory processes. Biochem Cell Biol 90(3):252–268. doi:10.1139/o11-056
13. Tsuda H, Kozu T, Iinuma G, Ohashi Y, Saito Y, Saito D, Akasu T, Alexander DB, Futakuchi M, Fukamachi K, Xu J, Kakizoe T, Iigo M (2010) Cancer prevention by bovine lactoferrin: from animal studies to human trial. Biometals 23(3):399–409. doi:10.1007/s10534-010-9331-3
14. Ward PP, Conneely OM (2004) Lactoferrin: role in iron homeostasis and host defense against microbial infection. Biometals 17(3):203–208
15. Naot D, Grey A, Reid IR, Cornish J (2005) Lactoferrin—a novel bone growth factor. Clin Med Res 3(2):93–101
16. Manzoni P, Stolfi I, Messner H, Cattani S, Laforgia N, Romeo MG, Bollani L, Rinaldi M, Gallo E, Quercia M, Maule M, Mostert M, Decembrino L, Magaldi R, Mosca F, Vagnarelli F, Memo L, Betta PM, Stronati M, Farina D (2012) Bovine lactoferrin prevents invasive fungal infections in very low birth weight infants: a randomized controlled trial. Pediatrics 129(1):116–123. doi:10.1542/peds.2011-0279
17. Manzoni P, Decembrino L, Stolfi I, Pugni L, Rinaldi M, Cattani S, Romeo MG, Messner H, Laforgia N, Vagnarelli F, Memo L, Bordignon L, Saia OS, Maule M, Gallo E, Mostert M, Magnani C, Quercia M, Bollani L, Pedicino R, Renzullo L, Betta P, Ferrari F, Magaldi R, Mosca F, Stronati M, Farina D (2010) Lactoferrin and prevention of late-onset sepsis in the pre-term neonates. Early Hum Dev 86(Suppl 1):59–61. doi:10.1016/j.earlhumdev.2010.01.009S0378-3782(10)00011-3
18. Kamemori N, Takeuchi T, Sugiyama A, Miyabayashi M, Kitagawa H, Shimizu H, Ando K, Harada E (2008) Trans-endothelial and trans-epithelial transfer of lactoferrin into the brain through BBB and BCSFB in adult rats. J Vet Med Sci 70(3):313–315
19. Kamemori N, Takeuchi T, Hayashida K, Harada E (2004) Suppressive effects of milk-derived lactoferrin on psychological stress in adult rats. Brain Res 1029(1):34–40. doi:10.1016/j.brainres.2004.09.015
20. Pond WG, Boleman SL, Fiorotto ML, Ho H, Knabe DA, Mersmann HJ, Savell JW, Su DR (2000) Perinatal ontogeny of brain growth in the domestic pig. Proc Soc Exp Biol Med 223(1):102–108
21. Moughan PJ, Birtles MJ, Cranwell PD, Smith WC, Pedraza M (1992) The piglet as a model animal for studying aspects of digestion and absorption in milk-fed human infants. World Rev Nutr Diet 67:40–113
22. Wang B, Yu B, Karim M, Hu H, Sun Y, McGreevy P, Petocz P, Held S, Brand-Miller J (2007) Dietary sialic acid supplementation improves learning and memory in piglets. Am J Clin Nutr 85(2):561–569
23. Kornum BR, Knudsen GM (2011) Cognitive testing of pigs (Sus scrofa) in translational biobehavioral research. Neurosci Biobehav Rev 35(3):437–451. doi:10.1016/j.neubiorev.2010.05.004
24. Raymond F, Metairon S, Borner R, Hofmann M, Kussmann M (2006) Automated target preparation for microarray-based gene expression analysis. Anal Chem 78(18):6299–6305. doi:10.1021/ac060097t
25. Gomez-Palacio-Schjetnan A, Escobar ML (2013) Neurotrophins and synaptic plasticity. Curr Top Behav Neurosci. doi:10.1007/7854_2012_231
26. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35(4):605–623
27. Park H, Poo MM (2013) Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14(1):7–23. doi:10.1038/nrn3379
28. Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361(1473):1545–1564. doi:10.1098/rstb.2006.1894
29. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4(4):299–309. doi:10.1038/nrn1078
30. Lee YS, Silva AJ (2009) The molecular and cellular biology of enhanced cognition. Nat Rev Neurosci 10(2):126–140. doi:10.1038/nrn2572
31. Oltmann-Norden I, Galuska SP, Hildebrandt H, Geyer R, Gerardy-Schahn R, Geyer H, Muhlenhoff M (2008) Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 283(3):1463–1471. doi:10.1074/jbc.M708463200
32. Kanato Y, Kitajima K, Sato C (2008) Direct binding of polysialic acid to a brain-derived neurotrophic factor depends on the degree of polymerization. Glycobiology 18(12):1044–1053. doi:10.1093/glycob/cwn084
33. Ono S, Hane M, Kitajima K, Sato C (2012) Novel regulation of fibroblast growth factor 2 (FGF2)-mediated cell growth by polysialic acid. J Biol Chem 287(6):3710–3722. doi:10.1074/jbc.M111.276618
34. Olton DS, Samuelson RJ (1976) Remembrance of places passed: spatial memory in rats. J Exp Psychol Anim Behav Process 2(2):97–116
35. Ahissar M, Hochstein S (1997) Task difficulty and the specificity of perceptual learning. Nature 387(6631):401–406. doi:10.1038/387401a0
36. Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89(3):312–323. doi:10.1016/j.nlm.2007.08.018
37. Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29(41):12764–12767. doi:10.1523/JNEUROSCI.3566-09.2009
38. Tan NY, Khachigian LM (2009) Sp1 phosphorylation and its regulation of gene transcription. Mol Cell Biol 29(10):2483–2488. doi:10.1128/MCB.01828-08
39. Giubellino A, Burke TR Jr, Bottaro DP (2008) Grb2 signaling in cell motility and cancer. Expert Opin Ther Targets 12(8):1021–1033. doi:10.1517/14728222.12.8.1021
40. Cargnello M, Roux PP (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75(1):50–83. doi:10.1128/MMBR.00031-10
41. Coultrap SJ, Bayer KU (2012) CaMKII regulation in information processing and storage. Trends Neurosci 35(10):607–618. doi:10.1016/j.tins.2012.05.003
42. Cavallaro S, D’Agata V, Manickam P, Dufour F, Alkon DL (2002) Memory-specific temporal profiles of gene expression in the hippocampus. Proc Natl Acad Sci U S A 99(25):16279–16284. doi:10.1073/pnas.242597199
43. Shanware NP, Zhan L, Hutchinson JA, Kim SH, Williams LM, Tibbetts RS (2010) Conserved and distinct modes of CREB/ATF transcription factor regulation by PP2A/B56gamma and genotoxic stress. PLoS One 5(8):e12173. doi:10.1371/journal.pone.0012173
44. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127–148. doi:10.1146/annurev.neuro.21.1.127
45. Benito E, Barco A (2010) CREB’s control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33(5):230–240. doi:10.1016/j.tins.2010.02.001
46. Rutishauser U (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9(1):26–35
47. Muhlenhoff M, Rollenhagen M, Werneburg S, Gerardy-Schahn R, Hildebrandt H (2013) Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem Res 38(6):1134–1143. doi:10.1007/s11064-013-0979-2
48. Foley AG, Ronn LC, Murphy KJ, Regan CM (2003) Distribution of polysialylated neural cell adhesion molecule in rat septal nuclei and septohippocampal pathway: transient increase of polysialylated interneurons in the subtriangular septal zone during memory consolidation. J Neurosci Res 74(6):807–817
49. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S et al (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367(6462):455–459. doi:10.1038/367455a0
50. Murphy KJ, O'Connell AW, Regan CM (1996) Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrial spatial training. J Neurochem 67(3):1268–1274
51. Fox GB, Fichera G, Barry T, O'Connell AW, Gallagher HC, Murphy KJ, Regan CM (2000) Consolidation of passive avoidance learning is associated with transient increases of polysialylated neurons in layer II of the rat medial temporal cortex. J Neurobiol 45(3):135–141
52. Foley AG, Hedigan K, Roullet P, Moricard Y, Murphy KJ, Sara SJ, Regan CM (2003) Consolidation of memory for odour-reward association requires transient polysialylation of the neural cell adhesion molecule in the rat hippocampal dentate gyrus. J Neurosci Res 74(4):570–576
53. Hadders-Algra M (2011) Prenatal and early postnatal supplementation with long-chain polyunsaturated fatty acids: neurodevelopmental considerations. Am J Clin Nutr 94(6 Suppl):1874S–1879S. doi:10.3945/ajcn.110.001065
54. Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3(1):79–83