Oral supplementation of 2'-fucosyllactose during lactation improves memory and learning in rats

Journal of Nutritional Biochemistry

Volumn 31, Issue , 2016, Pages 20-27

  Oliveros, Elena ^a   Ramirez, María ^a   Vazquez, Enrique ^a   Barranco, Alejandro ^a   Gruart, Agnes ^c   Delgado Garcia, Jose Maria ^c   Buck, Rachael ^b   Rueda, Ricardo ^a   Martin, Maria J ^a  

^a ABBOTT LABORATORIES   (Spain)

^b ABBOTT LABORATORIES   (United States)

^c UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

2' Fucosyllactose; Cognitive development; Early Nutrition; Infant formula; Milk oligosaccharides

Indexed keywords

2' FUCOSYLLACTOSE; LACTOSE; UNCLASSIFIED DRUG; 2'-FUCOSYLLACTOSE; TRISACCHARIDE;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; DIET SUPPLEMENTATION; EXPERIMENTAL BEHAVIORAL TEST; LACTATION; LEARNING; LONG TERM POTENTIATION; MEMORY; MORRIS WATER MAZE TEST; NEWBORN; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; RAT; Y-MAZE TEST; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; FEMALE; MALE; MAZE TEST; ORAL DRUG ADMINISTRATION; PREGNANCY;

ADMINISTRATION, ORAL; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; PREGNANCY; RATS; TRISACCHARIDES;

EID: 84974566770     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.12.014     Document Type: Article

References (63)

1. Le Huerou-Luron I., Blat S., Boudry G. Breast- v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev 2010, 23:23-36.
2. Schanler R.J., Shulman R.J., Lau C. Feeding strategies for premature infants: beneficial outcomes of feeding fortified human milk versus preterm formula. Pediatrics 1999, 103:1150-1157.
3. Howie P.W., Forsyth J.S., Ogston S.A., Clark A., Florey C.D. Protective effect of breast feeding against infection. BMJ 1990, 300:11-16.
4. Saarinen U.M., Kajosaari M. Breastfeeding as prophylaxis against atopic disease: prospective follow-up study until 17 years old. Lancet 1995, 346:1065-1069.
5. Virtanen S.M., Knip M. Nutritional risk predictors of beta cell autoimmunity and type 1 diabetes at a young age. Am J Clin Nutr 2003, 78:1053-1067.
6. Ikeda N., Shoji H., Murano Y., Mori M., Matsunaga N., Suganuma H., et al. Effects of breastfeeding on the risk factors for metabolic syndrome in preterm infants. J Dev Orig Health Dis 2014, 5:459-464.
7. Mortensen E.L., Michaelsen K.F., Sanders S.A., Reinisch J.M. The association between duration of breastfeeding and adult intelligence. JAMA 2002, 287:2365-2371.
8. Chichlowski M., German J.B., Lebrilla C., Mills D.A. The influence of milk oligosaccharides on microbiota of infants: opportunities for formulas. Annu Rev Food Sci Technol 2011, 2:331-351.
9. Martin-Sosa S., Martin M.J., Hueso P. The sialylated fraction of milk oligosaccharides is partially responsible for binding to enterotoxigenic and uropathogenic Escherichia coli human strains. J Nutr 2002, 132:3067-3072.
10. Morrow A.L., Ruiz-Palacios G.M., Altaye M., Jiang X., Guerrero M.L., Meinzen-Derr J.K., et al. Human milk oligosaccharides are associated with protection against diarrhea in breast-fed infants. J Pediatr 2004, 145:297-303.
11. Leach J.L., Garber S.A., Marcon A.A., Prieto P.A. In vitro and in vivo effects of soluble, monovalent globotriose on bacterial attachment and colonization. Antimicrob Agents Chemother 2005, 49:3842-3846.
12. Coppa G.V., Bruni S., Morelli L., Soldi S., Gabrielli O. The first prebiotics in humans: human milk oligosaccharides. J Clin Gastroenterol 2004, 38:80-83.
13. Bode L. Human milk oligosaccharides: prebiotics and beyond. Nutr Rev 2009, 67:183-191.
14. Kunz C., Rudloff S., Baier W., Klein N., Strobel S. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 2000, 20:699-722.
15. Coppa G.V., Gabrielli O., Pierani P., Catassi C., Carlucci A., Giorgi P.L. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 1993, 91:637-641.
16. Newburg D.S., Ruiz-Palacios G.M., Morrow A.L. Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 2005, 25:37-58.
17. Bode L. Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr 2006, 136:2127-2130.
18. Smith D.F., Zopf D.A., Ginsburg V. Sialyl oligosaccharides from milk. Methods Enzymol 1978, 50:221-226.
19. Castanys-Muñoz E., Martin M.J., Prieto P.A. 2'-Fucosyllactose: an abundant, genetically determined soluble glycan present in human milk. Nutr Rev 2013, 71:773-789.
20. Akasuma S., Urashima T., Akahori M., Obayashi H., Nakamura T., Kimura K., et al. Variation of major neutral oligosaccharides levels in human colostrum. Eur J Clin Nutr 2008, 62:488-494.
21. Erney R.M., Malone W.T., Skelding M.B., Marcon A.A., Kleman-Leyer K.M., O'Ryan M.L., et al. Variability of human milk neutral oligosaccharides in a diverse population. J Pediatr Gastroenterol Nutr 2000, 30:181-192.
22. Chaturvedi P., Warren C.D., Altaye M., Morrow A.L., Ruiz-Palacios G., Pickering L.K., et al. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 2001, 11:365-372.
23. Marino K., Lane J.A., Abrahams J.L., Struwe W.B., Harvey D.J., Marotta M., et al. Method for milk oligosaccharide profiling by 2-aminobenzamide labeling and hydrophilic interaction chromatography. Glycobiology 2011, 21:1317-1330.
24. Aldredge D.L., Geronimo M.R., Hua S., Nwosu C.C., Lebrilla C.B., Barile D. Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures. Glycobiology 2013, 23:664-676.
25. Urashima T., Saito T., Nakamura T., Messer M. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J 2001, 18:357-371.
26. Bienenstock J., Buck R.H., Linke H., Forsythe P., Stanisz A.M., Kunze W.A. Fucosylated but not sialylated milk oligosaccharides diminish colon motor contractions. PLoS One 2014, 8.
27. Murrey H.E., Hsieh-Wilson L.C. The chemical neurobiology of carbohydrates. Chem Rev 2008, 108:1708-1731.
28. Wetzel W., Popov N., Lossner B., Schulzeck S., Honza R., Matthies H. Effect of l-fucose on brain protein metabolism and retention of a learned behavior in rats. Pharmacol Biochem Behav 1980, 13:765-771.
29. McCabe N., Rose S.P. Increased fucosylation of chick brain proteins following training: effects of cycloheximide. J Neurochem 1987, 48:538-542.
30. Matthies H., Staak S., Krug M. Fucose and fucosyllactose enhance in-vitro hippocampal long-term potentiation. Brain Res 1996, 725:276-280.
31. Goehring K.C., Kennedy A.D., Prieto P.A., Buck R.H. Direct evidence for the presence of human milk oligosaccharides in the circulation of breastfed infants. PLoS One 2014, 9.
32. Reeves P.G., Nielsen F.H., Fahey G.C.J. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993, 123:1939-1951.
33. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, New York.
34. Gureviciene I., Ikonen S., Gurevicius K., Sarkaki A., Van Groen T., Pussinen R., et al. Normal induction but accelerated decay of LTP in APP+PS1 transgenic mice. Neurobiol Dis 2004, 26:1077-1087.
35. Bliss T.V.P., Gardner-Medwin A.R. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol 1973, 232:357-374.
36. Gruart A., Muñoz M., Delgado-García J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 2006, 26:1077-1087.
37. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res 1988, 31:47-59.
38. Dellu F., Mayo W., Le Moal M., Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res 1992, 588:132-139.
39. Koletzko B., Brands B., Poston L., Godfrey K., Demmelmair H. Early nutrition programming of long-term health. Proc Nutr Soc 2012, 71:371-378.
40. Anjos T., Altmae S., Emmett P., Tiemeier H., Closa-Monasterolo R., Luque V., et al. Nutrition and neurodevelopment in children: focus on NUTRIMENTHE project. Eur J Nutr 2013, 52:1825-1842.
41. Kafouri S., Kramer M., Leonard G., Perron M., Pike B., Richer L., et al. Breastfeeding and brain structure in adolescence. Int J Epidemiol 2013, 42:150-159.
42. Newton N. The uniqueness of human milk. Psychological differences between breast and bottle feeding. Am J Clin Nutr 1971, 24:993-1004.
43. Caspi A., Williams B., Kim-Cohen J., Craig I.W., Milne B.J., Poulton R., et al. Moderation of breastfeeding effects on the IQ by genetic variation in fatty acid metabolism. Proc Natl Acad Sci U S A 2007, 104:18860-18865.
44. Isaacs E.B., Fischl B.R., Quinn B.T., Chong W.K., Gadian D.G., Lucas A. Impact of breast milk on intelligence quotient, brain size, and white matter development. Pediatr Res 2010, 67:357-362.
45. Makrides M., Neumann M.A., Byard R.W., Simmer K., Gibson R.A. Fatty acid composition of brain, retina, and erythrocytes in breast and formula-fed infants. Am J Clin Nutr 1994, 60:189-194.
46. Makrides M., Smithers L.G., Gibson R.A. Role of long-chain polyunsaturated fatty acids in neurodevelopment and growth. Nestle Nutr Workshop Ser Pediatr Program 2010, 65:123-133.
47. Gibson R.A., Makrides M. Long-chain polyunsaturated fatty acids in breast milk: are they essential?. Adv Exp Med Biol 2001, 501:375-383.
48. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 2012, 22:1147-1162.
49. Ruiz-Palacios G.M., Cervantes L.E., Ramos P., Chavez-Munguia B., Newburg D.S. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha1,2Gal beta1,4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 2003, 278:14112-14120.
50. Jantscher-Krenn E., Bode L. Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatr 2012, 64:83-99.
51. Wang J., Cheng A., Wakade C., Yu R.K. Ganglioside GD3 is required for neurogenesis and long-term maintenance of neural stem cells in the postnatal mouse brain. J Neurosci 2014, 34:13790-13800.
52. 13C-Labeled oligosaccharides in breastfed infants' urine: individual-, structure- and time-dependent differences in the excretion. Glycobiology 2014, 24:185-194.
53. Krug M., Wagner M., Staak S., Smalla K.H. Fucose and fucose-containing sugar epitopes enhance hippocampal long-term potentiation in the freely moving rat. Brain Res 1994, 643:130-135.
54. Vazquez E., Barranco A., Ramirez M., Gruart A., Delgado-García J.M., Martinez-Lara E., et al. Effects of a human milk oligosaccharide, 2'-fucosyllactose, on hippocampal long term potentiation and learning capabilities in rodents. JNB 2015, 26:455-465.
55. Albrecht S., Lane J.A., Mariño K., Al Busadah K.A. A comparative study of free oligosaccharides in the milk of domestic animals. Br J Nutr 2014, 111:1313-1328.
56. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci U S A 2004, 101:14515-14520.
57. Antunes M., Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012, 13:93-110.
58. Cutuli D., De Bartolo P., Caporali P., Laricchiuta D., Foti F., Ronci M., et al. n-3 polyunsaturated fatty acids supplementation enhances hippocampal functionality in aged mice. Front Aging Neurosci 2014, 6:220.
59. Hiratsuka S., Honma H., Saitoh Y., Yasuda Y., Yokogoshi H. Effects of dietary sialic acid in n-3 fatty acid-deficient dams during pregnancy and lactation on the learning abilities of their pups after weaning. J Nutr Sci Vitaminol (Tokyo) 2013, 59:136-143.
60. Karimi S.A., Salehi I., Komaki A., Sarihi A., Zarei M., Shahidi S. Effect of high-fat diet and antioxidants on hippocampal long-term potentiation in rats: an in vivo study. Brain Res 2013, 1539:1-6.
61. Leussis M.P., Bolivar V.J. Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 2006, 30:1045-1064.
62. Burke S.N., Wallace J.L., Hartzell A.L., Nematollahi S., Plange K., Barnes C.A. Age-associated deficits in pattern separation functions of the perirhinal cortex: a cross-species consensus. Behav Neurosci 2011, 125:836-847.
63. Ryan M.M., Guévremont D., Luxmanan C., Abraham W.C., Williams J.M. Aging alters long-term potentiation-related gene networks and impairs synaptic protein synthesis in the rat hippocampus. Neurobiol Aging 2015, 36:1868-1880.