Neonatal administration of goat whey modulates memory and cortical spreading depression in rats previously suckled under different litter sizes: Possible role of sialic acid

References

• Lovik M. Impact of a New European regulations on functional food market—an overview. Clin Transl Allergy 2011;1:S55. doi: 10.1186/2045-7022-1-S1-S55
   Google Scholar
• Silanikove N, Leitner G, Merin Y, Prosser CG. Recent advances in exploiting goat's milk: quality, safety and production aspects. Small Rumin Res 2010;89:110–24. doi: 10.1016/j.smallrumres.2009.12.033
   Web of Science ®Google Scholar
• Ribeiro AC, Ribeiro SDA. Specialty products made from goat milk. Small Rumin Res 2010;89:225–33. doi: 10.1016/j.smallrumres.2009.12.048
   Web of Science ®Google Scholar
• El-Agamy EI. The challenge of cow milk protein allergy. Small Rumin Res 2007;68:64–72. doi: 10.1016/j.smallrumres.2006.09.016
   Web of Science ®Google Scholar
• Haenlein GFW. Goat milk in human nutrition. Small Rumin Res 2004;51:155–63. doi: 10.1016/j.smallrumres.2003.08.010
   Web of Science ®Google Scholar
• Martinez-Ferez A, Rudloff S, Guadix A, Henkel CA, Pohlentz G, Boza JJ, et al. Goats’ milk as a natural source of lactose-derived oligosaccharides: isolation by membrane technology. Int Dairy J 2006;16:173–81. doi: 10.1016/j.idairyj.2005.02.003
   Web of Science ®Google Scholar
• Lara-Villoslada F, Debras E, Nieto A, Concha A, Gálvez J, López-Huertas E, et al. Oligosaccharides isolated from goat milk reduce intestinal inflammation in a rat model of dextran sodium sulfate-induced colitis. Clin Nutr 2006;25:477–88. doi: 10.1016/j.clnu.2005.11.004
   PubMed Web of Science ®Google Scholar
• Wang B. Molecular mechanism underlying sialic acid as an essential nutrient for brain development and cognition. Adv Nutr 2012;3:465S–72. doi: 10.3945/an.112.001875
   PubMed Web of Science ®Google Scholar
• Wang B, Brand-Miller J. The role and potential of sialic acid in human nutrition. Eur J Clin Nutr 2003;57:1351–69. doi: 10.1038/sj.ejcn.1601704
   PubMed Web of Science ®Google Scholar
• Urashima T, Taufik E, Fukuda K, Asakuma S. Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci Biotechnol Biochem 2013;77:455–66. doi: 10.1271/bbb.120810
   PubMed Web of Science ®Google Scholar
• Kiskini A, Difilippo E. Oligosaccharides in goat milk: structure, health effects and isolation. Mol Cell Biol 2013;59:25–30.
   Web of Science ®Google Scholar
• Morgan BLG, Winick M. Effects of administration of N-acetylneuraminic acid (NANA) on brain NANA content and behavior. J Nutr 1980;110:416–24.
   PubMed Web of Science ®Google Scholar
• Wang B, Yu B, Karim M, Hu M, Sun Y, Mcgreevy P, et al. Dietary SA supplementation improves learning and memory in piglets. Am J Clin Nutr 2007;85:561–69.
   PubMed Web of Science ®Google Scholar
• Isaeva E, Lushnikova I, Savrasova A, Skibo G, Holmes GL, Isaev D. Short communication—effect of neuraminidase treatment on persistent epileptiform activity in the rat hippocampus. Pharmacol Rep 2011;63:840–44. doi: 10.1016/S1734-1140(11)70597-7
   PubMed Web of Science ®Google Scholar
• Peng XQ, Zhang XL, Fang Y, Xie WR, Xie YK. Sialic acid contributes to hyperexcitability of dorsal root ganglion neurons in rats with peripheral nerve injury. Brain Res 2004;1026:185–93. doi: 10.1016/j.brainres.2004.07.075
   PubMed Web of Science ®Google Scholar
• Yoo SW, Motari MG, Susuki K, Prendergast J, Mountney A, Hurtado A, et al. Sialylation regulates brain structure and function. FASEB J 2015;29:3040–53. doi: 10.1096/fj.15-270983
   PubMed Web of Science ®Google Scholar
• Wielgat P, Braszko JJ. The participation of sialic acids in microglia–neuron interactions. Cell Immunol 2012;273:17–22. doi: 10.1016/j.cellimm.2011.12.002
   PubMed Web of Science ®Google Scholar
• Oliveira DL, Wilbey RA, Grandison AS, Duarte LC, Roseiro LB. Separation of oligosaccharides from caprine milk whey, prior to prebiotic evaluation. Int Dairy J 2012;24:102–6. doi: 10.1016/j.idairyj.2011.12.012
   Web of Science ®Google Scholar
• Oliveira DL, Costabile A, Wilbey RA, Grandison AS, Duarte LC, Roseiro LB. In vitro evaluation of the fermentation properties and potential prebiotic activity of caprine cheese whey oligosaccharides in batch culture systems. Biofactors 2012;38:440–49. doi: 10.1002/biof.1043
   PubMed Web of Science ®Google Scholar
• Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol 1944;7:359–90.
   Google Scholar
• Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol 2008;119:1973–84. doi: 10.1016/j.clinph.2008.05.025
   PubMed Web of Science ®Google Scholar
• Ghadiri MK, Kozian M, Ghaffarian N, Stummer W, Kazemi H, Speckmann EJ, et al. Sequential changes in neuronal activity in single neocortical neurons after spreading depression. Cephalalgia 2012;32:116–24. doi: 10.1177/0333102411431308
   PubMed Web of Science ®Google Scholar
• Ferrari MD, Klever RR, Terwindt GM, Ayata C, Van Den Maagdenberg AMJM. Migraine pathophysiology: lessons from mouse models and human genetics. Lancet Neurol 2015;14:65–80. doi: 10.1016/S1474-4422(14)70220-0
   PubMed Web of Science ®Google Scholar
• Pusic DA, Mitchell HM, Kunkler PE, Klauer N, Kraig RP. Spreading depression transiently disrupts myelin via interferon-gamma signaling. Exp Neurol 2015;264:43–54. doi: 10.1016/j.expneurol.2014.12.001
   PubMed Web of Science ®Google Scholar
• Wei Y, Ullah G, Schiff SJ. Unification of neuronal spikes, seizures, and spreading depression. J Neurosci 2014;34:11733–43. doi: 10.1523/JNEUROSCI.0516-14.2014
   PubMed Web of Science ®Google Scholar
• Guedes RCA. Cortical spreading depression: a model for studying brain consequences of malnutrition. In: Preedy VR, Watson RR and Martin CR (eds.), Handbook of behavior. Food and nutrition; 2011. p. 2343–55.
   Google Scholar
• Alamy M, Bengelloun WA. Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat. Neurosci Biobehav Rev 2012;36:1463–80. doi: 10.1016/j.neubiorev.2012.03.009
   PubMed Web of Science ®Google Scholar
• Morgane PJ, Miller M, Kemper T, Stern W, Forbes W, Hall R, et al. The effects of protein malnutrition on the developing central nervous system in the rat. Neurosci Biobehav Rev 1978;2:137–230. doi: 10.1016/0149-7634(78)90059-3
   Web of Science ®Google Scholar
• Francisco ES, Guedes RCA. Neonatal taurine and alanine modulate anxiety-like behavior and decelerate cortical spreading depression in rats previously suckled under different litter sizes. Amino Acids 2015;47:2437–45. doi: 10.1007/s00726-015-2036-8
   PubMed Web of Science ®Google Scholar
• Garcia EF, De Oliveira ME, Queiroga RC, Machado TA, De Souza EL. Development and quality of a Brazilian semi-hard goat cheese (coalho) with added probiotic lactic acid bacteria. Int J Food Sci Nutr 2012;63:947–56. doi: 10.3109/09637486.2012.687367
   PubMed Web of Science ®Google Scholar
• de Sousa YRF, da Silva Vasconcelos MAV, Costa RG, de Azevedo Filho CA, de Paiva EP, Queiroga RCER. Sialic acid content of goat milk during lactation. Livest Sci 2015;177:175–80. doi: 10.1016/j.livsci.2015.04.005
   Web of Science ®Google Scholar
• Carlson SE, House SG. Oral and intraperitoneal administration of N-acetylneuraminic acid: effect on rat cerebral and cerebellar N-acetylneuraminic acid. J Nutr 1986;116:881–86.
   PubMed Web of Science ®Google Scholar
• Ennaceur A, Delacour J. Effect of combined or separate administration of piracetam and choline on learning and memory in the rat. Psychopharmacology 1987;92:58–67. doi: 10.1007/BF00215480
   PubMed Web of Science ®Google Scholar
• Han M, Kim J. Effect of dietary iron loading on recognition memory in growing rats. PLoS One 2015;6.
   Google Scholar
• Xu M, Wei L, Dai Z, Zhang Y, Li Y, Wang J. Effects of goat milk-based formula on development in weaned rats. Food Nutr Res 2015;59.
   Google Scholar
• Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008;9:26–35. doi: 10.1038/nrn2285
   PubMed Web of Science ®Google Scholar
• Markram K, Gerardy-Schahn R, Sandi C. Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 2007;144:788–96. doi: 10.1016/j.neuroscience.2006.10.024
   PubMed Web of Science ®Google Scholar
• Florian C, Foltz J, Norreel JC, Rougon G, Roullet P. Post-training intrahippocampal injection of synthetic poly-alpha-2,8-sialic acid-neural cell adhesion molecule mimetic peptide improves spatial long-term performance in mice. Learn Mem 2006;13:335–41. doi: 10.1101/lm.187506
   PubMed Web of Science ®Google Scholar
• Rutherfurd SM, Moughan PJ, Lowry D, Prosser CG. Amino acid composition determined using multiple hydrolysis times for three goat milk formulations. Int J Food Sci Nutr 2008;59:679–90. doi: 10.1080/09637480701705424
   PubMed Web of Science ®Google Scholar
• Kim HY, Kim HV, Yoon JH, Kang BR, Cho SM, Lee S, et al. Taurine in drinking water recovers learning and memory in the adult APP/PS1 mouse model of Alzheimer's disease. Sci Rep 2014;4.
   Web of Science ®Google Scholar
• Wenting L, Ping L, Haitao J, Meng Q, Xiaofei R. Therapeutic effect of taurine against aluminum-induced impairment on learning, memory and brain neurotransmitters in rats. Neurol Sci 2014;35:1579–84. doi: 10.1007/s10072-014-1801-x
   PubMed Web of Science ®Google Scholar
• Soares JKB, Rocha-de-Melo APR, Medeiros MC, Queiroga RCRE, Bomfim MAD, de Souza AFO, et al. Conjugated linoleic acid in the maternal diet differentially enhances growth and cortical spreading depression in the rat progeny. Biochim Biophys Acta 2012;1820:1490–95. doi: 10.1016/j.bbagen.2012.05.010
   PubMed Web of Science ®Google Scholar
• Gama MA, Raposo NR, Mury FB, Lopes FC, Dias-Neto E, Talib LL, et al. Conjugated linoleic acid-enriched butter improved memory and up-regulated phospholipase A2 encoding-genes in rat brain tissue. J Neural Transm (Vienna) 2015;122:1371–80. doi: 10.1007/s00702-015-1401-9
   PubMed Web of Science ®Google Scholar
• Gattaz WF, Cairns NJ, Levy R, Förstl H, Braus DF, Maras A. Decreased phospholipase A2 activity in the brain and in platelets of patients with Alzheimer's disease. Eur Arch Psychiatry Clin Neurosci 1996;246:129–31. doi: 10.1007/BF02189113
   PubMed Web of Science ®Google Scholar
• Merkler D, Klinker F, Jürgens T, Glaser R, Paulus W, Brinkmann BG, et al. Propagation of spreading depression inversely correlates with cortical myelin content. Ann Neurol 2009;66:355–65. doi: 10.1002/ana.21746
   PubMed Web of Science ®Google Scholar
• Scholtz SA, Gottipati BS, Gajewski BJ, Carlson SE. Dietary sialic acid and cholesterol influence cortical composition in developing rats. J Nutr 2013;143:132–35. doi: 10.3945/jn.112.169508
   PubMed Web of Science ®Google Scholar
• Linnartz-Gerlach B, Mathews M, Neumann H. Sensing the neuronal glycocalyx by glial sialic acid Binding immunoglobulin-like lectins. Neuroscience 2014;275:113–24. doi: 10.1016/j.neuroscience.2014.05.061
   PubMed Web of Science ®Google Scholar
• Fewou SN, Ramakrishnan H, Bussow H, Gieselmann V, Eckhardt M. Down-regulation of polysialic acid is required for efficient myelin formation. J Biol Chem 2007;282:16700–11. doi: 10.1074/jbc.M610797200
   PubMed Web of Science ®Google Scholar
• Largo C, Ibarz JM, Herreras O. Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J Neurophysiol 1997;78:295–307.
   PubMed Web of Science ®Google Scholar
• Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, et al. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA 2003;100:12045–50. doi: 10.1073/pnas.2131556100
   PubMed Web of Science ®Google Scholar
• Chen Y, Pan L, Liu N, Troy II FA, Wang B. LC–MS/MS quantification of N-acetylneuraminic acid, N-glycolylneuraminic acid and ketodeoxynonulosonic acid levels in the urine and potential relationship with dietary sialic acid intake and disease in 3- to 5-year-old children. Br J Nutr 2014;111:332–41. doi: 10.1017/S0007114513002468
   PubMed Web of Science ®Google Scholar
• da Silva Hernandes AS, Françolin-Silva AL, Valadares CT, Fukuda MTH, Almeida SS. Effects of different malnutrition techniques on the behavior of rats tested in the elevated T-maze. Behav Brain Res 2005;162:240–45. doi: 10.1016/j.bbr.2005.03.008
   PubMed Web of Science ®Google Scholar
• Yida Z, Imam MU, Ismail M, Ismail N, Ideris A, Abdullah MA. High fat diet-induced inflammation and oxidative stress are attenuated by N-acetylneuraminic acid in rats. J Biomed Sci 2015;22:755. doi: 10.1186/s12929-015-0211-6
   Web of Science ®Google Scholar
• Lindberg G. Resialylation of sialic acid deficit vascular endothelium, circulating cells and macromolecules may counteract the development of atherosclerosis: a hypothesis. Atherosclerosis 2007;192:243–5. doi: 10.1016/j.atherosclerosis.2007.03.011
   PubMed Web of Science ®Google Scholar
• Duncan PI, Raymond F, Fuerholz A, Sprenger N. Sialic acid utilisation and synthesis in the neonatal rat revisited. Plos One 2009;4:e8241. doi: 10.1371/journal.pone.0008241
   PubMed Web of Science ®Google Scholar
• Cabral FR, Priel MR, Silva Araujo BH, Brito Torres L, de Lima E, Gurgel do Vale T. Malnutrition in infancy as a susceptibility factor for temporal lobe epilepsy in adulthood induced by the pilocarpine experimental model. Dev Neurosci 2011;33:469–78. doi: 10.1159/000330707
   PubMed Web of Science ®Google Scholar
• Florian ML, Nunes ML. Effects of intra-uterine and early extra-uterine malnutrition on seizure threshold and hippocampal morphometry of pup rats. Nutr Neurosci 2011;14:151–8. doi: 10.1179/147683010X12611460764804
   PubMed Web of Science ®Google Scholar
• Feoli AM, Siqueira I, Almeida LMV, Tramontina AC, Battu C, Wofchuk ST, et al. Brain glutathione content and glutamate uptake are reduced in rats exposed to pre- and postnatal protein malnutrition. J Nutr 2006;136:2357–61.
   PubMed Web of Science ®Google Scholar
• Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, Santello M, et al. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in CaV2.1 knockin migraine mice. Neuron 2009;61:762–73. doi: 10.1016/j.neuron.2009.01.027
   PubMed Web of Science ®Google Scholar