Sialylated Milk Oligosaccharides Promote Microbiota-Dependent Growth in Models of Infant Undernutrition

Cell

Volumn 164, Issue 5, 2016, Pages 859-871

  Charbonneau, Mark R ^a   O'Donnell, David ^a   Blanton, Laura V ^a   Totten, Sarah M ^b   Davis, Jasmine C C ^b   Barratt, Michael J ^a   Cheng, Jiye ^a   Guruge, Janaki ^a   Talcott, Michael ^a   Bain, James R ^c,d   Muehlbauer, Michael J ^c   Ilkayeva, Olga ^c   Wu, Chao ^e   Struckmeyer, Tedd ^e   Barile, Daniela ^b   Mangani, Charles ^f   Jorgensen, Josh ^b   Fan, Yue Mei ^g   Maleta, Kenneth ^f   Dewey, Kathryn G ^b   Ashorn, Per ^g,h   Newgard, Christopher B ^c,d   Lebrilla, Carlito ^b   Mills, David A ^b   Gordon, Jeffrey I ^a   more..

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e Hilmar Cheese Company   (United States)

^f UNIVERSITY OF MALAWI   (Malawi)

^g TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^h TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOSACCHARIDE; SIALYLATED BOVINE MILK OLIGOSACCHARIDE; UNCLASSIFIED DRUG; SIALOOLIGOSACCHARIDES;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; BODY GROWTH; BONE STRUCTURE; BRAIN METABOLISM; CONTROLLED STUDY; EXPLORATORY RESEARCH; FECES MICROFLORA; LEAN BODY WEIGHT; LIVER METABOLISM; MALNUTRITION; MOUSE; MUSCLE METABOLISM; NONHUMAN; NUTRIENT UPTAKE; PRIORITY JOURNAL; STUNTING; ANIMAL; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; BRAIN CHEMISTRY; BREAST MILK; C57BL MOUSE; CHEMISTRY; CHILD DEVELOPMENT; CLASSIFICATION; DIET THERAPY; DISEASE MODEL; ESCHERICHIA COLI; FECES; GENETICS; GERMFREE ANIMAL; HUMAN; INFANT; MALAWI; MALE; METABOLISM; METABOLOMICS; MICROBIOLOGY; MICROFLORA; MILK;

ANIMALS; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; BRAIN CHEMISTRY; CHILD DEVELOPMENT; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; FECES; GERM-FREE LIFE; HUMANS; INFANT; MALAWI; MALE; MALNUTRITION; METABOLOMICS; MICE; MICE, INBRED C57BL; MICROBIOTA; MILK; MILK, HUMAN; OLIGOSACCHARIDES;

EID: 84959476433     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.01.024     Document Type: Article

References (43)

1. D.L. Aldredge, M.R. Geronimo, S. Hua, C.C. Nwosu, C.B. Lebrilla, and D. Barile Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures Glycobiology 23 2013 664 676
2. S. Almagro-Moreno, and E.F. Boyd Sialic acid catabolism confers a competitive advantage to pathogenic vibrio cholerae in the mouse intestine Infect. Immun. 77 2009 3807 3816
3. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
4. P. Ashorn, L. Alho, U. Ashorn, Y.B. Cheung, K.G. Dewey, U. Harjunmaa, A. Lartey, M. Nkhoma, N. Phiri, J. Phuka, and et al. The impact of lipid-based nutrient supplement provision to pregnant women on newborn size in rural Malawi: A randomized controlled trial Am. J. Clin. Nutr. 101 2015 387 397
5. S. Bartz, A. Mody, C. Hornik, J. Bain, M. Muehlbauer, T. Kiyimba, E. Kiboneka, R. Stevens, J. Bartlett, J.V. St Peter, and et al. Severe acute malnutrition in childhood: hormonal and metabolic status at presentation, response to treatment, and predictors of mortality J. Clin. Endocrinol. Metab. 99 2014 2128 2137
6. R.E. Black, C.G. Victora, S.P. Walker, Z.A. Bhutta, P. Christian, M. de Onis, M. Ezzati, S. Grantham-McGregor, J. Katz, R. Martorell, R. Uauy Maternal and Child Nutrition Study Group Maternal and child undernutrition and overweight in low-income and middle-income countries Lancet 382 2013 427 451
7. L. Bode Human milk oligosaccharides: every baby needs a sugar mama Glycobiology 22 2012 1147 1162
8. P. Chen, D.E. Goldberg, B. Kolb, M. Lanser, and L.I. Benowitz Inosine induces axonal rewiring and improves behavioral outcome after stroke Proc. Natl. Acad. Sci. USA 99 2002 9031 9036
9. L. Chen, Z. Xiong, L. Sun, J. Yang, and Q. Jin VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors Nucleic Acids Res. 40 2012 D641 D645
10. G.V. Coppa, O. Gabrielli, L. Zampini, T. Galeazzi, A. Ficcadenti, L. Padella, L. Santoro, S. Soldi, A. Carlucci, E. Bertino, and L. Morelli Oligosaccharides in 4 different milk groups, Bifidobacteria, and Ruminococcus obeum J. Pediatr. Gastroenterol. Nutr. 53 2011 80 87
11. S. Dachir, D. Shabashov, V. Trembovler, A.G. Alexandrovich, L.I. Benowitz, and E. Shohami Inosine improves functional recovery after experimental traumatic brain injury Brain Res. 1555 2014 78 88
12. K.G. Dewey, and S. Adu-Afarwuah Systematic review of the efficacy and effectiveness of complementary feeding interventions in developing countries Matern. Child Nutr. 4 Suppl 1 2008 24 85
13. M.B. Engfer, B. Stahl, B. Finke, G. Sawatzki, and H. Daniel Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract Am. J. Clin. Nutr. 71 2000 1589 1596
14. J.B. Ewaschuk, H. Diaz, L. Meddings, B. Diederichs, A. Dmytrash, J. Backer, M. Looijer-van Langen, and K.L. Madsen Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function Am. J. Physiol. Gastrointest. Liver Physiol. 295 2008 G1025 G1034
15. B.B. Fredholm, J.F. Chen, S.A. Masino, and J.M. Vaugeois Actions of adenosine at its receptors in the CNS: insights from knockouts and drugs Annu. Rev. Pharmacol. Toxicol. 45 2005 385 412
16. S. Fukuda, H. Toh, K. Hase, K. Oshima, Y. Nakanishi, K. Yoshimura, T. Tobe, J.M. Clarke, D.L. Topping, T. Suzuki, and et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate Nature 469 2011 543 547
17. B. Gal, M.J. Ruano, R. Puente, L.A. García-Pardo, R. Rueda, A. Gil, and P. Hueso Developmental changes in UDP-N-acetylglucosamine 2-epimerase activity of rat and guinea-pig liver Comp. Biochem. Physiol. B Biochem. Mol. Biol. 118 1997 13 15
18. M.N. Huda, Z. Lewis, K.M. Kalanetra, M. Rashid, S.M. Ahmad, R. Raqib, F. Qadri, M.A. Underwood, D.A. Mills, and C.B. Stephensen Stool microbiota and vaccine responses of infants Pediatrics 134 2014 e362 e372
19. Y. Kodama, H.P. Dimai, J. Wergedal, M. Sheng, R. Malpe, S. Kutilek, W. Beamer, L.R. Donahue, C. Rosen, D.J. Baylink, and J. Farley Cortical tibial bone volume in two strains of mice: effects of sciatic neurectomy and genetic regulation of bone response to mechanical loading Bone 25 1999 183 190
20. M.S. Kramer, and R. Kakuma Optimal duration of exclusive breastfeeding Cochrane Database Syst. Rev. 8 2012 CD003517
21. C. Mangani, K. Maleta, J. Phuka, Y.B. Cheung, C. Thakwalakwa, K. Dewey, M. Manary, T. Puumalainen, and P. Ashorn Effect of complementary feeding with lipid-based nutrient supplements and corn-soy blend on the incidence of stunting and linear growth among 6- to 18-month-old infants and children in rural Malawi Matern. Child Nutr. 11 Suppl 4 2015 132 143
22. R. Martorell, and A. Zongrone Intergenerational influences on child growth and undernutrition Paediatr. Perinat. Epidemiol. 26 Suppl 1 2012 302 314
23. J. McFie, and H.F. Welbourn Effect of malnutrition in infancy on the development of bone, muscle and fat J. Nutr. 76 1962 97 105
24. N.P. McNulty, T. Yatsunenko, A. Hsiao, J.J. Faith, B.D. Muegge, A.L. Goodman, B. Henrissat, R. Oozeer, S. Cools-Portier, G. Gobert, and et al. The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins Sci. Transl. Med. 3 2011 106ra106
25. E.R. Miller, and D.E. Ullrey The pig as a model for human nutrition Annu. Rev. Nutr. 7 1987 361 382
26. D.M. Muoio Metabolic inflexibility: when mitochondrial indecision leads to metabolic gridlock Cell 159 2014 1253 1262
27. C.B. Newgard, J. An, J.R. Bain, M.J. Muehlbauer, R.D. Stevens, L.F. Lien, A.M. Haqq, S.H. Shah, M. Arlotto, C.A. Slentz, and et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance Cell Metab. 9 2009 311 326
28. K.M. Ng, J.A. Ferreyra, S.K. Higginbottom, J.B. Lynch, P.C. Kashyap, S. Gopinath, N. Naidu, B. Choudhury, B.C. Weimer, D.M. Monack, and J.L. Sonnenburg Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens Nature 502 2013 96 99
29. D.M. Scholtens, M.J. Muehlbauer, N.R. Daya, R.D. Stevens, A.R. Dyer, L.P. Lowe, B.E. Metzger, C.B. Newgard, J.R. Bain, W.L. Lowe Jr. HAPO Study Cooperative Research Group Metabolomics reveals broad-scale metabolic perturbations in hyperglycemic mothers during pregnancy Diabetes Care 37 2014 158 166
30. K. Sjögren, C. Engdahl, P. Henning, U.H. Lerner, V. Tremaroli, M.K. Lagerquist, F. Bäckhed, and C. Ohlsson The gut microbiota regulates bone mass in mice J. Bone Miner. Res. 27 2012 1357 1367
31. J.T. Smilowitz, C.B. Lebrilla, D.A. Mills, J.B. German, and S.L. Freeman Breast milk oligosaccharides: structure-function relationships in the neonate Annu. Rev. Nutr. 34 2014 143 169
32. S. Subramanian, S. Huq, T. Yatsunenko, R. Haque, M. Mahfuz, M.A. Alam, A. Benezra, J. DeStefano, M.F. Meier, B.D. Muegge, and et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children Nature 510 2014 417 421
33. N. Tao, E.J. DePeters, J.B. German, R. Grimm, and C.B. Lebrilla Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography-chip/mass spectrometry J. Dairy Sci. 92 2009 2991 3001
34. T. Thomas, B. Burguera, L.J. Melton 3rd, E.J. Atkinson, W.M. O'Fallon, B.L. Riggs, and S. Khosla Role of serum leptin, insulin, and estrogen levels as potential mediators of the relationship between fat mass and bone mineral density in men versus women Bone 29 2001 114 120
35. C.G. Victora, L. Adair, C. Fall, P.C. Hallal, R. Martorell, L. Richter, H.S. Sachdev Maternal and Child Undernutrition Study Group Maternal and child undernutrition: consequences for adult health and human capital Lancet 371 2008 340 357
36. B. Wang, and J. Brand-Miller The role and potential of sialic acid in human nutrition Eur. J. Clin. Nutr. 57 2003 1351 1369
37. B. Wang, J. Brand-Miller, P. McVeagh, and P. Petocz Concentration and distribution of sialic acid in human milk and infant formulas Am. J. Clin. Nutr. 74 2001 510 515
38. B. Wang, B. Yu, M. Karim, H. Hu, Y. Sun, P. McGreevy, P. Petocz, S. Held, and J. Brand-Miller Dietary sialic acid supplementation improves learning and memory in piglets Am. J. Clin. Nutr. 85 2007 561 569
39. Q. Wang, G.M. Garrity, J.M. Tiedje, and J.R. Cole Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy Appl. Environ. Microbiol. 73 2007 5261 5267
40. P.J. Wijtten, J. van der Meulen, and M.W. Verstegen Intestinal barrier function and absorption in pigs after weaning: A review Br. J. Nutr. 105 2011 967 981
41. D.S. Wishart, T. Jewison, A.C. Guo, M. Wilson, C. Knox, Y. Liu, Y. Djoumbou, R. Mandal, F. Aziat, E. Dong, and et al. HMDB 3.0 - The Human Metabolome Database in 2013 Nucleic Acids Res. 41 2013 D801 D807
42. T. Yatsunenko, F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, M. Contreras, M. Magris, G. Hidalgo, R.N. Baldassano, A.P. Anokhin, and et al. Human gut microbiome viewed across age and geography Nature 486 2012 222 227
43. T. Yonekawa, M.C. Malicdan, A. Cho, Y.K. Hayashi, I. Nonaka, T. Mine, T. Yamamoto, I. Nishino, and S. Noguchi Sialyllactose ameliorates myopathic phenotypes in symptomatic GNE myopathy model mice Brain 137 2014 2670 2679