Sialylated human milk oligosaccharides program cognitive development through a non-genomic transmission mode.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
26
08
2020
accepted:
12
02
2021
revised:
26
01
2021
pubmed:
6
3
2021
medline:
27
1
2022
entrez:
5
3
2021
Statut:
ppublish
Résumé
Breastmilk contains bioactive molecules essential for brain and cognitive development. While sialylated human milk oligosaccharides (HMOs) have been implicated in phenotypic programming, their selective role and underlying mechanisms remained elusive. Here, we investigated the long-term consequences of a selective lactational deprivation of a specific sialylated HMO in mice. We capitalized on a knock-out (KO) mouse model (B6.129-St6gal1
Identifiants
pubmed: 33664475
doi: 10.1038/s41380-021-01054-9
pii: 10.1038/s41380-021-01054-9
pmc: PMC8505264
doi:
Substances chimiques
Oligosaccharides
0
Lactose
J2B2A4N98G
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2854-2871Informations de copyright
© 2021. The Author(s).
Références
Horta BL, Loret de Mola C, Victora CG. Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: a systematic review and meta-analysis. Acta Paediatr. 2015;104:30–7.
pubmed: 26192560
doi: 10.1111/apa.13133
Victora CG, Horta BL, de Mola CL, Quevedo L, Pinheiro RT, Gigante DP, et al. Association between breastfeeding and intelligence, educational attainment, and income at 30 years of age: a prospective birth cohort study from Brazil. Lancet Glob Health. 2015;3:E199–205.
pubmed: 25794674
pmcid: 4365917
doi: 10.1016/S2214-109X(15)70002-1
Isaacs EB, Fischl BR, Quinn BT, Chong WK, Gadian DG, Lucas A. Impact of breast milk on intelligence quotient, brain size, and white matter development. Pediatr Res. 2010;67:357–62.
pubmed: 20035247
pmcid: 2939272
doi: 10.1203/PDR.0b013e3181d026da
Anderson JW, Johnstone BM, Remley DT. Breast-feeding and cognitive development: a meta-analysis. Am J Clin Nutr. 1999;70:525–35.
pubmed: 10500022
doi: 10.1093/ajcn/70.4.525
Kramer MS, Aboud F, Mironova E, Vanilovich I, Platt RW, Matush L, et al. Breastfeeding and child cognitive development: new evidence from a large randomized trial. Arch Gen Psychiatry. 2008;65:578–84.
pubmed: 18458209
doi: 10.1001/archpsyc.65.5.578
Kramer MS, Chalmers B, Hodnett ED, Sevkovskaya Z, Dzikovich I, Shapiro S, et al. Promotion of breastfeeding intervention trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA. 2001;285:413–20.
pubmed: 11242425
doi: 10.1001/jama.285.4.413
Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr. 2009;29:177–222.
pubmed: 19575597
doi: 10.1146/annurev.nutr.28.061807.155515
Fuhrer A, Sprenger N, Kurakevich E, Borsig L, Chassard C, Hennet T. Milk sialyllactose influences colitis in mice through selective intestinal bacterial colonization. J Exp Med. 2010;207:2843–54.
pubmed: 21098096
pmcid: 3005226
doi: 10.1084/jem.20101098
ten Bruggencate SJ, Bovee-Oudenhoven IM, Feitsma AL, van Hoffen E, Schoterman MH. Functional role and mechanisms of sialyllactose and other sialylated milk oligosaccharides. Nutr Rev. 2014;72:377–89.
pubmed: 24828428
doi: 10.1111/nure.12106
Victora CG, Bahl R, Barros AJ, Franca GV, Horton S, Krasevec J, et al. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet. 2016;387:475–90.
pubmed: 26869575
doi: 10.1016/S0140-6736(15)01024-7
Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013;60:49–74.
pubmed: 23178060
pmcid: 3586783
doi: 10.1016/j.pcl.2012.10.002
Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22:1147–62.
pubmed: 22513036
pmcid: 3406618
doi: 10.1093/glycob/cws074
Schnaar RL, Gerardy-Schahn R, Hildebrandt H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 2014;94:461–518.
pubmed: 24692354
pmcid: 4044301
doi: 10.1152/physrev.00033.2013
Sheikh KA, Sun J, Liu Y, Kawai H, Crawford TO, Proia RL, et al. Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc Natl Acad Sci USA. 1999;96:7532–7.
pubmed: 10377449
pmcid: 22120
doi: 10.1073/pnas.96.13.7532
Senkov O, Sun M, Weinhold B, Gerardy-Schahn R, Schachner M, Dityatev A. Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci. 2006;26:10888–9898.
pubmed: 17050727
pmcid: 6674738
doi: 10.1523/JNEUROSCI.0878-06.2006
Weinhold B, Seidenfaden R, Rockle I, Muhlenhoff M, Schertzinger F, Conzelmann S, et al. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem. 2005;280:42971–7.
pubmed: 16267048
doi: 10.1074/jbc.M511097200
Nakano T, Sugawara M, Kawakami H. Sialic acid in human milk: composition and functions. Acta Paediatr Taiwan. 2001;42:11–17.
pubmed: 11270179
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.
pubmed: 17284758
doi: 10.1093/ajcn/85.2.561
Oliveros E, Vazquez E, Barranco A, Ramirez M, Gruart A, Delgado-Garcia JM, et al. Sialic acid and sialylated oligosaccharide supplementation during lactation improves learning and memory in rats. Nutrients. 2018;10:1519.
pmcid: 6212975
doi: 10.3390/nu10101519
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.
pmcid: 6628371
doi: 10.3390/nu11061335
Cryan JF, O’Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23:187–92.
pubmed: 21303428
doi: 10.1111/j.1365-2982.2010.01664.x
Aarts E, Ederveen THA, Naaijen J, Zwiers MP, Boekhorst J, Timmerman HM, et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS ONE. 2017;12:e0183509.
pubmed: 28863139
pmcid: 5581161
doi: 10.1371/journal.pone.0183509
Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF. Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Transl Res. 2017;179:223–44.
pubmed: 27832936
doi: 10.1016/j.trsl.2016.10.002
O’Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2015;277:32–48.
pubmed: 25078296
doi: 10.1016/j.bbr.2014.07.027
Hennet T, Chui D, Paulson JC, Marth JD. Immune regulation by the ST6Gal sialyltransferase. Proc Natl Acad Sci USA. 1998;95:4504–9.
pubmed: 9539767
pmcid: 22519
doi: 10.1073/pnas.95.8.4504
Castelhano-Carlos MJ, Sousa N, Ohl F, Baumans V. Identification methods in newborn C57BL/6 mice: a developmental and behavioural evaluation. Lab Anim. 2010;44:88–103.
pubmed: 19854756
doi: 10.1258/la.2009.009044
Macrì S, Pasquali P, Bonsignore LT, Pieretti S, Cirulli F, Chiarotti F, et al. Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice. PLoS ONE. 2007;2:e1015.
pubmed: 17925863
pmcid: 2000350
doi: 10.1371/journal.pone.0001015
Fox WM. Reflex-ontogeny and behavioural development of the mouse. Anim Behav. 1965;13:234–41.
pubmed: 5835840
doi: 10.1016/0003-3472(65)90041-2
Nisticò R, Cavallucci V, Piccinin S, Macrì S, Pignatelli M, Mehdawy B, et al. Insulin receptor beta-subunit haploinsufficiency impairs hippocampal late-phase LTP and recognition memory. Neuromolecular Med. 2012;14:262–9.
pubmed: 22661254
doi: 10.1007/s12017-012-8184-z
Macrì S, Spinello C, Widomska J, Magliozzi R, Poelmans G, Invernizzi RW, et al. Neonatal corticosterone mitigates autoimmune neuropsychiatric disorders associated with streptococcus in mice. Sci Rep. 2018;8:10188.
pubmed: 29976948
pmcid: 6033871
doi: 10.1038/s41598-018-28372-3
Deacon RM, Rawlins JN. T-maze alternation in the rodent. Nat Protoc. 2006;1:7–12.
pubmed: 17406205
doi: 10.1038/nprot.2006.2
Zoratto F, Sbriccoli M, Martinelli A, Glennon JC, Macrì S, Laviola G. Intranasal oxytocin administration promotes emotional contagion and reduces aggression in a mouse model of callousness. Neuropharmacology. 2018;143:250–67.
pubmed: 30213592
doi: 10.1016/j.neuropharm.2018.09.010
Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol. 1979;93:74–104.
pubmed: 221551
doi: 10.1037/h0077579
Proietti Onori M, Ceci C, Laviola G, Macrì S. A behavioural test battery to investigate tic-like symptoms, stereotypies, attentional capabilities, and spontaneous locomotion in different mouse strains. Behav Brain Res. 2014;267:95–105.
pubmed: 24675156
doi: 10.1016/j.bbr.2014.03.023
Birrell JM, Brown VJ. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci. 2000;20:4320–4.
pubmed: 10818167
pmcid: 6772641
doi: 10.1523/JNEUROSCI.20-11-04320.2000
Colacicco G, Welzl H, Lipp HP, Wurbel H. Attentional set-shifting in mice: modification of a rat paradigm, and evidence for strain-dependent variation. Behav Brain Res. 2002;132:95–102.
pubmed: 11853862
doi: 10.1016/S0166-4328(01)00391-6
Macrì S, Granstrem O, Shumilina M, Antunes Gomes dos Santos FJ, Berry A, Saso L, et al. Resilience and vulnerability are dose-dependently related to neonatal stressors in mice. Horm Behav. 2009;56:391–8.
pubmed: 19632235
doi: 10.1016/j.yhbeh.2009.07.006
Paxinos G, Franklin KB. Paxinos and Franklin’s the mouse brain in stereotaxic coordinates. Academic Press: Cambridge, Massachusetts, 2019.
Martire A, Lambertucci C, Pepponi R, Ferrante A, Benati N, Buccioni M, et al. Neuroprotective potential of adenosine A1 receptor partial agonists in experimental models of cerebral ischemia. J Neurochem. 2019;149:211–30.
pubmed: 30614535
doi: 10.1111/jnc.14660
Anderson WW, Collingridge GL. The LTP program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events. J Neurosci Methods. 2001;108:71–83.
pubmed: 11459620
doi: 10.1016/S0165-0270(01)00374-0
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
doi: 10.1093/bioinformatics/bts635
pubmed: 23104886
Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9.
pubmed: 25260700
doi: 10.1093/bioinformatics/btu638
Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:R25.
pubmed: 20196867
pmcid: 2864565
doi: 10.1186/gb-2010-11-3-r25
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.
doi: 10.1093/bioinformatics/btp616
pubmed: 19910308
Wold S, Esbensen K, Geladi P. Principal component analysis. Chemom Intell Lab. 1987;2:37–52.
doi: 10.1016/0169-7439(87)80084-9
Trygg J, Wold S. Orthogonal projections to latent structures (O-PLS). J Chemom. 2002;16:119–28.
doi: 10.1002/cem.695
Pinheiro J, Bates D. Mixed-effects models in S and S-PLUS. Springer Science & Business Media: Berlin, 2006.
Macrì S, Wurbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav. 2006;50:667–80.
pubmed: 16890940
doi: 10.1016/j.yhbeh.2006.06.015
Takashima S, Tsuji S, Tsujimoto M. Characterization of the second type of human beta-galactoside alpha 2,6-sialyltransferase (ST6Gal II), which sialylates Galbeta 1,4GlcNAc structures on oligosaccharides preferentially. Genomic analysis of human sialyltransferase genes. J Biol Chem. 2002;277:45719–28.
pubmed: 12235148
doi: 10.1074/jbc.M206808200
Tebano MT, Martire A, Rebola N, Pepponi R, Domenici MR, Gro MC, et al. Adenosine A2A receptors and metabotropic glutamate 5 receptors are co-localized and functionally interact in the hippocampus: a possible key mechanism in the modulation of N-methyl-D-aspartate effects. J Neurochem. 2005;95:1188–1200.
pubmed: 16271052
doi: 10.1111/j.1471-4159.2005.03455.x
Romijn HJ, Hofman MA, Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev. 1991;26:61–67.
pubmed: 1914989
doi: 10.1016/0378-3782(91)90044-4
Huttenlocher PR. Synaptic density in human frontal cortex—developmental changes and effects of aging. Brain Res. 1979;163:195–205.
pubmed: 427544
doi: 10.1016/0006-8993(79)90349-4
Heisler JM, Morales J, Donegan JJ, Jett JD, Redus L, O’Connor JC. The attentional set shifting task: a measure of cognitive flexibility in mice. J Vis Exp. 2015;96:51944.
Swerdlow NR, Taaid N, Oostwegel JL, Randolph E, Geyer MA. Towards a cross-species pharmacology of sensorimotor gating: effects of amantadine, bromocriptine, pergolide and ropinirole on prepulse inhibition of acoustic startle in rats. Behav Pharm. 1998;9:389–96.
doi: 10.1097/00008877-199809000-00002
Lacroix L, Spinelli S, White W, Feldon J. The effects of ibotenic acid lesions of the medial and lateral prefrontal cortex on latent inhibition, prepulse inhibition and amphetamine-induced hyperlocomotion. Neuroscience. 2000;97:459–68.
pubmed: 10828529
doi: 10.1016/S0306-4522(00)00013-0
Russell WMS, Burch RL. The principles of humane experimental technique. Methuen: Slingsby, York, 1959.
Voelkl B, Altman NS, Forsman A, Forstmeier W, Gurevitch J, Jaric I, et al. Reproducibility of animal research in light of biological variation. Nat Rev Neurosci. 2020;21:384–93.
pubmed: 32488205
doi: 10.1038/s41583-020-0313-3
Richter SH, von Kortzfleisch V. It is time for an empirically informed paradigm shift in animal research. Nat. Rev. Neurosci. 2020;21:660.
pubmed: 32826977
doi: 10.1038/s41583-020-0369-0
Matias S, Lottem E, Dugue GP, Mainen ZF. Activity patterns of serotonin neurons underlying cognitive flexibility. eLife. 2017;6:e20552.
pubmed: 28322190
pmcid: 5360447
doi: 10.7554/eLife.20552
Biggio G, Fadda F, Fanni P, Tagliamonte A, Gessa GL. Rapid depletion of serum tryptophan, brain tryptophan, serotonin and 5-hydroxyindoleacetic acid by a tryptophan-free diet. Life Sci. 1974;14:1321–9.
pubmed: 4823644
doi: 10.1016/0024-3205(74)90440-8
Puig MV, Gulledge AT. Serotonin and prefrontal cortex function: neurons, networks, and circuits. Mol Neurobiol. 2011;44:449–64.
pubmed: 22076606
pmcid: 3282112
doi: 10.1007/s12035-011-8214-0
Perez-De La Cruz V, Konigsberg M, Santamaria A. Kynurenine pathway and disease: an overview. CNS Neurol Disord Drug Targets. 2007;6:398–410.
pubmed: 18220779
doi: 10.2174/187152707783399229
Grant RS, Coggan SE, Smythe GA. The physiological action of picolinic acid in the human brain. Int J Tryptophan Res. 2009;2:71–9.
pubmed: 22084583
pmcid: 3195224
doi: 10.4137/IJTR.S2469
Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe. 2018;23:716–24.
pubmed: 29902437
doi: 10.1016/j.chom.2018.05.003
Kaur H, Bose C, Mande SS. Tryptophan metabolism by gut microbiome and gut-brain-axis: an in silico Analysis. Front Neurosci. 2019;13:1365.
pubmed: 31920519
pmcid: 6930238
doi: 10.3389/fnins.2019.01365
Mullineaux-Sanders C, Sanchez-Garrido J, Hopkins EGD, Shenoy AR, Barry R, Frankel G. Citrobacter rodentium-host-microbiota interactions: immunity, bioenergetics and metabolism. Nat Rev Microbiol. 2019;17:701–15.
pubmed: 31541196
doi: 10.1038/s41579-019-0252-z
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.
pubmed: 31323174
pmcid: 6852474
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.
pubmed: 26144888
pmcid: 4631662
doi: 10.1016/j.bbi.2015.06.025
Wang Y-C, Stein JW, Lynch CL, Tran HT, Lee C-Y, Coleman R, et al. Glycosyltransferase ST6GAL1 contributes to the regulation of pluripotency in human pluripotent stem cells. Sci Rep. 2015;5:13317.
pubmed: 26304831
pmcid: 4548446
doi: 10.1038/srep13317
Jones MB. IgG and leukocytes: targets of immunomodulatory α2, 6 sialic acids. Cell Immunol. 2018;333:58–64.
pubmed: 29685495
pmcid: 6167213
doi: 10.1016/j.cellimm.2018.03.014
Doyle KP, Quach LN, Solé M, Axtell RC, Nguyen T-VV, Soler-Llavina GJ, et al. B-lymphocyte-mediated delayed cognitive impairment following stroke. J Neurosci. 2015;35:2133–45.
pubmed: 25653369
pmcid: 4315838
doi: 10.1523/JNEUROSCI.4098-14.2015
Macrì S. Neonatal corticosterone administration in rodents as a tool to investigate the maternal programming of emotional and immune domains. Neurobiol Stress. 2017;6:22–30.
pubmed: 28229106
doi: 10.1016/j.ynstr.2016.12.001