Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 25, 2022 - Issue 12
1,965
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Dietary sialylated oligosaccharides in early-life may promote cognitive flexibility during development in context of obesogenic dietary intake

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon

References

  • Bode L. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology. 2012;22:1147–62. doi:10.1093/glycob/cws074.
  • Donovan SM, Comstock SS. Human milk oligosaccharides Influence neonatal mucosal and systemic immunity. Ann Nutr Metab. 2016;69(Suppl 2):42–51. doi:10.1159/000452818.
  • Kirmiz N, Robinson RC, Shah IM, Barile D, Mills DA. Milk glycans and their interaction with the infant-Gut microbiota. Annu Rev Food Sci Technol. 2018;9:429–50. doi:10.1146/annurev-food-030216-030207.
  • Urashima T, Saito T, Nakamura T, Messer M. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J. 2001;18:357–71. doi:10.1023/A:1014881913541.
  • Sakai F, Ikeuchi Y, Urashima T, Fujihara M, Ohtsuki K, Yanahira S. Effects of feeding sialyllactose and galactosylated N-acetylneuraminic acid on swimming learning ability and brain lipid composition in adult rats. J Appl Glycosci. 2006;53:249–54. doi:10.5458/jag.53.249.
  • Tarr AJ, Galley JD, Fisher SE, Chichlowski M, Berg BM, Bailey MT. The prebiotics 3′sialyllactose and 6′sialyllactose diminish stressor-induced anxiety-like behavior and colonic microbiota alterations: evidence for effects on the gut–brain axis. Brain Behav Immun. 2015;50:166–77. doi:10.1016/j.bbi.2015.06.025.
  • Vázquez E, Barranco A, Ramírez M, Gruart A, Delgado-García JM, Martínez-Lara E, et al. Effects of a human milk oligosaccharide, 2′-fucosyllactose, on hippocampal long-term potentiation and learning capabilities in rodents. J Nutr Biochem. 2015;26:455–65. doi:10.1016/j.jnutbio.2014.11.016.
  • Vázquez E, Barranco A, Ramírez M, Gruart A, Delgado-García JM, Jimenez ML, et al. Dietary 2’-fucosyllactose enhances operant conditioning and long-term potentiation via gut-brain communication through the vagus nerve in rodents. PLoS One. 2016;11:1–14. doi:10.1371/journal.pone.0166070.
  • Jacobi SK, Yatsunenko T, Li D, Dasgupta S, Yu RK, Berg BM, et al. Dietary isomers of sialyllactose increase ganglioside sialic Acid Concentrations in the Corpus Callosum and cerebellum and modulate the colonic Microbiota of formula-Fed piglets. J Nutr. 2016;146:200–8. doi:10.3945/jn.115.220152.
  • Kao ACC, Harty S, Burnet PWJ. The Influence of prebiotics on neurobiology and behavior. Int Rev Neurobiol. 2016;131:21–48. doi:10.1016/bs.irn.2016.08.007.
  • Oliveros E, Ramirez M, Vazquez E, Barranco A, Gruart A, Delgado-Garcia JM, et al. Oral supplementation of 2′-fucosyllactose during lactation improves memory and learning in rats. J Nutr Biochem. 2016;31:20–7. doi:10.1016/j.jnutbio.2015.12.014.
  • Mudd AT, Fleming SA, Labhart B, Chichlowski M, Berg BM, Donovan SM, et al. Dietary Sialyllactose influences Sialic Acid Concentrations in the prefrontal cortex and magnetic resonance imaging Measures in Corpus Callosum of Young pigs. Nutrients. 2017;9:1297. doi:10.3390/nu9121297.
  • Obelitz-Ryom K, Bering SB, Overgaard SH, Eskildsen SF, Ringgaard S, Olesen JL, et al. Bovine Milk Oligosaccharides with sialyllactose improves cognition in preterm pigs. Nutrients. 2019;11:1335. doi:10.3390/nu11061335.
  • Berger PK, Plows JF, Jones RB, Alderete TL, Yonemitsu C, Poulsen M, et al. Human milk oligosaccharide 2’-fucosyllactose links feedings at 1 month to cognitive development at 24 months in infants of normal and overweight mothers. PLoS One. 2020;15:e0228323. doi:10.1371/journal.pone.0228323.
  • Hauser J, Pisa E, Arias Vásquez A, Tomasi F, Traversa A, Chiodi V, et al. Sialylated human milk oligosaccharides program cognitive development through a non-genomic transmission mode. Mol Psychiatry. 2021. doi:10.1038/s41380-021-01054-9.
  • McGuire MK, Meehan CL, McGuire MA, Williams JE, Foster J, Sellen DW, et al. What’s normal? Oligosaccharide concentrations and profiles in milk produced by healthy women vary geographically. Am J Clin Nutr. 2017: ajcn 139980. doi:10.3945/ajcn.116.139980.
  • Nishtar S, Gluckman P, Armstrong T. Ending childhood obesity: a time for action. Lancet (London, England). 2016;387:825–7. doi:10.1016/S0140-6736(16)00140-9.
  • Isganaitis E, Venditti S, Matthews TJ, Lerin C, Demerath EW, Fields DA. Maternal obesity and the human milk metabolome: associations with infant body composition and postnatal weight gain. Am J Clin Nutr. 2019;110:111–20. doi:10.1093/ajcn/nqy334.
  • Alderete TL, Autran C, Brekke BE, Knight R, Bode L, Goran MI, et al. Associations between human milk oligosaccharides and infant body composition in the first 6 mo of life. Am J Clin Nutr. 2015;102:1381–8. doi:10.3945/ajcn.115.115451.
  • Reinert KRS, Po’e EK, Barkin SL. The relationship between executive function and obesity in children and adolescents: a systematic literature review. J Obes. 2013;2013:820956. doi:10.1155/2013/820956.
  • Galván M, Uauy R, López-Rodríguez G, Kain J. Association between childhood obesity, cognitive development, physical fitness and social-emotional wellbeing in a transitional economy. Ann Hum Biol. 2014;41:101–6. doi:10.3109/03014460.2013.841288.
  • Wang C, Chan JSY, Ren L, Yan JH. Obesity reduces cognitive and motor functions across the lifespan. Neural Plast. 2016;2016; doi:10.1155/2016/2473081.
  • Li N, Yolton K, Lanphear BP, Chen A, Kalkwarf HJ, Braun JM. Impact of early-life weight status on cognitive abilities in children. Obesity. 2018;26:1088–95. doi:10.1002/oby.22192.
  • Litten-Brown JC, Corson AM, Clarke L. Porcine models for the metabolic syndrome, digestive and bone disorders: a general overview. Animal. 2010;4:899–920. doi:10.1017/S1751731110000200.
  • Odle J, Lin X, Jacobi SK, Kim SW, Stahl CH. The suckling piglet as an agrimedical model for the study of pediatric nutrition and metabolism. Annu Rev Anim Biosci. 2014;2:419–44. doi:10.1146/annurev-animal-022513-114158.
  • Lind NM, Moustgaard A, Jelsing J, Vajta G, Cumming P, Hansen AK. The use of pigs in neuroscience: modeling brain disorders. Neurosci Biobehav Rev 2007;31:728–51. doi:10.1016/j.neubiorev.2007.02.003.
  • Gieling ET, Nordquist RE, van der Staay FJ. Assessing learning and memory in pigs. Anim Cogn. 2011;14:151–73. doi:10.1007/s10071-010-0364-3.
  • Conrad MS, Dilger RN, Johnson RW. Brain growth of the domestic pig (Sus scrofa) from 2 to 24 weeks of age: a longitudinal MRI study. Dev Neurosci. 2012;34:291–8. doi:10.1159/000339311.
  • Conrad MS, Johnson RW. The domestic piglet: An important model for investigating the neurodevelopmental consequences of early life insults. Annu Rev Anim Biosci. 2015;3:245–64. doi:10.1146/annurev-animal-022114-111049.
  • Mudd AT, Dilger RN. Early-life nutrition and neurodevelopment: use of the piglet as a translational model. Adv Nutr. 2017;8:92–104. doi:10.3945/an.116.013243.
  • Fleming SA, Mudd AT, Hauser J, Yan J, Metairon S, Steiner P, et al. Dietary oligofructose alone or in combination with 2′-fucosyllactose differentially improves Recognition memory and hippocampal mRNA expression. Nutrients. 2020;12:2131. doi:10.3390/nu12072131.
  • Fleming SA, Mudd AT, Hauser J, Yan J, Metairon S, Steiner P, et al. Human and bovine milk oligosaccharides elicit improved recognition memory concurrent with alterations in regional brain volumes and hippocampal mRNA expression. Front Neurosci. 2020;14:1–14. doi:10.3389/fnins.2020.00770.
  • Peter B, De Rijk EPCT, Zeltner A, Emmen HH. Sexual maturation in the female Göttingen minipig. Toxicol Pathol. 2016;44:482–5. doi:10.1177/0192623315621413.
  • van der Staay FJ, Gieling ET, Pinzón NE, Nordquist RE, Ohl F. The appetitively motivated “cognitive” holeboard: A family of complex spatial discrimination tasks for assessing learning and memory. Neurosci Biobehav. Rev. 2012;36:379–403. doi:10.1016/j.neubiorev.2011.07.008.
  • Mudd AT, Salcedo J, Alexander LS, Johnson SK, Getty CM, Chichlowski M, et al. Porcine milk oligosaccharides and Sialic Acid Concentrations vary throughout lactation. Front Nutr. 2016;3; doi:10.3389/fnut.2016.00039.
  • Nadel L, Hardt O. Update on memory systems and processes. Neuropsychopharmacology. 2011;36:251–73. doi:10.1038/npp.2010.169.
  • Gieling ET, Antonides A, Fink-Gremmels J, ter Haar K, Kuller WI, Meijer E, et al. Chronic allopurinol treatment during the last trimester of pregnancy in sows: effects on Low and normal birth weight offspring. PLoS One. 2014;9:e86396. doi:10.1371/journal.pone.0086396.
  • Antonides A, Schoonderwoerd AC, Scholz G, Berg BM, Nordquist RE, van der Staay FJ. Pre-weaning dietary iron deficiency impairs spatial learning and memory in the cognitive holeboard task in piglets. Front Behav Neurosci. 2015;9; doi:10.3389/fnbeh.2015.00291.
  • Elmore MRP, Dilger RN, Johnson RW. Place and direction learning in a spatial T-maze task by neonatal piglets. Anim Cogn. 2012;15:667–76. doi:10.1007/s10071-012-0495-9.
  • Dilger RN, Johnson RW. Behavioral assessment of cognitive function using a translational neonatal piglet model. Brain Behav Immun. 2010;24:1156–65. doi:10.1016/j.bbi.2010.05.008.
  • Izquierdo A, Brigman JL, Radke AK, Rudebeck PH, Holmes A. The neural basis of reversal learning: An updated perspective. Neuroscience. 2017;345:12–26. doi:10.1016/j.neuroscience.2016.03.021.
  • Pagani JH, Brown KL, Stanton ME. Contextual modulation of spatial discrimination reversal in developing rats. Dev Psychobiol. 2005;46:36–46. doi:10.1002/dev.20041.
  • Watson DJ, Sullivan JR, Frank JG, Stanton ME. Serial reversal learning of position discrimination in developing rats. Dev Psychobiol. 2006;48:79–94. doi:10.1002/dev.20106.
  • Saperstein LA, Kucharski D, Stanton ME, Hall WG. Developmental change in reversal learning of an olfactory discrimination. Psychobiology. 1989;17:293–9. doi:10.1007/BF03337783.
  • Willing J, Drzewiecki CM, Cuenod BA, Cortes LR, Juraska JM. A role for puberty in water maze performance in male and female rats. Behav Neurosci. 2016;130:422–7. doi:10.1037/bne0000145.
  • 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;85:561–9. doi:10.1093/ajcn/85.2.561.
  • Fleming S, Chichlowski M, Berg B, Donovan S, Dilger R. Dietary sialyllactose does not influence measures of recognition memory or diurnal activity in the young pig. Nutrients. 2018;10:395. doi:10.3390/nu10040395.
  • Palmano K, Rowan A, Guillermo R, Guan J, McJarrow P. The role of gangliosides in neurodevelopment. Nutrients. 2015;7:3891–913. doi:10.3390/nu7053891.
  • Vickers MH, Guan J, Gustavsson M, Krägeloh CU, Breier BH, Davison M, et al. Supplementation with a mixture of complex lipids derived from milk to growing rats results in improvements in parameters related to growth and cognition. Nutr Res. 2009;29:426–35. doi:10.1016/j.nutres.2009.06.001.
  • Chen Y, Zheng Z, Zhu X, Shi Y, Tian D, Zhao F, et al. Lactoferrin promotes early neurodevelopment and cognition in postnatal piglets by upregulating the BDNF signaling pathway and polysialylation. Mol Neurobiol. 2015;52:256–69. doi:10.1007/s12035-014-8856-9.
  • Wang B. Molecular mechanism underlying sialic acid as an essential Nutrient for brain development and cognition. Adv Nutr. 2012;3:465S–472S. doi:10.3945/an.112.001875.
  • Laube C, van den Bos W, Fandakova Y. The relationship between pubertal hormones and brain plasticity: implications for cognitive training in adolescence. Dev Cogn Neurosci. 2020;42:100753. doi:10.1016/j.dcn.2020.100753.
  • Koss WA, Belden CE, Hristov AD, Juraska JM. Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse. 2014;68:61–72. doi:10.1002/syn.21716.
  • Drzewiecki CM, Willing J, Juraska JM. Synaptic number changes in the medial prefrontal cortex across adolescence in male and female rats: A role for pubertal onset. Synapse. 2016;70:361–8. doi:10.1002/syn.21909.
  • Jia S, Lu Z, Gao Z, An J, Wu X, Li X, et al. Chitosan oligosaccharides alleviate cognitive deficits in an amyloid-β1–42-induced rat model of Alzheimer’s disease. Int J Biol Macromol. 2016;83:416–25. doi:10.1016/j.ijbiomac.2015.11.011.
  • Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, et al. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry. 2017;82:472–87. doi:10.1016/j.biopsych.2016.12.031.
  • Chen D, Yang X, Yang J, Lai G, Yong T, Tang X, et al. Prebiotic effect of fructooligosaccharides from Morinda officinalis on Alzheimer’s disease in rodent models by targeting the microbiota-gut-brain axis. Front Aging Neurosci. 2017;9:403. doi:10.3389/fnagi.2017.00403.
  • Savignac HM, Corona G, Mills H, Chen L, Spencer JPE, Tzortzis G, et al. Prebiotic feeding elevates central brain derived neurotrophic factor, N-methyl-d-aspartate receptor subunits and d-serine. Neurochem Int. 2013;63:756–64. doi:10.1016/j.neuint.2013.10.006.
  • Yen C-H, Wang C-H, Wu W-T, Chen H-L. Fructo-oligosaccharide improved brain β-amyloid, β-secretase, cognitive function, and plasma antioxidant levels in D-galactose-treated balb/cJ mice. Nutr Neurosci. 2017;20:228–37. doi:10.1080/1028415X.2015.1110952.
  • Savignac HM, Couch Y, Stratford M, Bannerman DM, Tzortzis G, Anthony DC, et al. Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain Behav Immun. 2016;52:120–31. doi:10.1016/j.bbi.2015.10.007.
  • Williams S, Chen L, Savignac HM, Tzortzis G, Anthony DC, Burnet PW. Neonatal prebiotic (BGOS) supplementation increases the levels of synaptophysin. GluN. 2A), -subunits and BDNF proteins in the adult rat hippocampus. Synapse. 2016;70:121–4. doi:10.1002/syn.21880.
  • Fleming SA, Monaikul S, Patsavas AJ, Waworuntu RV, Berg BM, Dilger RN. Dietary polydextrose and galactooligosaccharide increase exploratory behavior, improve recognition memory, and alter neurochemistry in the young pig. Nutr Neurosci. 2017;22:499–512. doi:10.1080/1028415X.2017.1415280.
  • Gronier B, Savignac HM, Di Miceli M, Idriss SM, Tzortzis G, Anthony D, et al. Increased cortical neuronal responses to NMDA and improved attentional set-shifting performance in rats following prebiotic (B-GOS®) ingestion. Eur Neuropsychopharmacol. 2018;28:211–24. doi:10.1016/j.euroneuro.2017.11.001.
  • Kao A, Spitzer S, Anthony DC, Lennox B, Burnet PWJ. Prebiotic attenuation of olanzapine-induced weight gain in rats: analysis of central and peripheral biomarkers and gut microbiota. Transl Psychiatry. 2018;8:66. doi:10.1038/s41398-018-0116-8.
  • Jorgensen JM, Young R, Ashorn P, Ashorn U, Chaima D, Davis JCC, et al. Associations of human milk oligosaccharides and bioactive proteins with infant growth and development among Malawian mother-infant dyads. Am J Clin Nutr. 2020: 1–12. doi:10.1093/ajcn/nqaa272.
  • Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe. 2015;17:565–76. doi:10.1016/j.chom.2015.04.011.
  • Schmidt K, Cowen PJ, Harmer CJ, Tzortzis G, Errington S, Burnet PWJ. Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology (Berl). 2015;232:1793–801. doi:10.1007/s00213-014-3810-0.
  • Thompson RS, Roller R, Mika A, Greenwood BN, Knight R, Chichlowski M, et al. Dietary prebiotics and bioactive milk fractions improve NREM Sleep, enhance REM Sleep rebound and attenuate the stress-induced decrease in diurnal temperature and Gut microbial alpha diversity. Front Behav Neurosci. 2017;10:240. doi:10.3389/fnbeh.2016.00240.
  • Xu L-Z, Xu D-F, Han Y, Liu L-J, Sun C-Y, Deng J-H, et al. BDNF-GSK-3β-β-Catenin Pathway in the mPFC Is involved in antidepressant-like effects of Morinda officinalis oligosaccharides in rats. Int J Neuropsychopharmacol. 2017;20:83–93. doi:10.1093/ijnp/pyw088.
  • Li H, Wang P, Huang L, Li P, Zhang D. Effects of regulating gut microbiota on the serotonin metabolism in the chronic unpredictable mild stress rat model. Neurogastroenterol Motil. 2019;31:e13677. doi:10.1111/nmo.13677.