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Breast Milk Oligosaccharides: Structure-Function Relationships in the Neonate
Open accessAbstract
In addition to providing complete postnatal nutrition, breast milk is a complex biofluid that delivers bioactive components for the growth and development of the intestinal and immune systems. Lactation is a unique opportunity to understand the role of diet in shaping the intestinal environment including the infant microbiome. Of considerable interest is the diversity and abundance of milk glycans that are energetically costly for the mammary gland to produce yet indigestible by infants. Milk glycans comprise free oligosaccharides, glycoproteins, glycopeptides, and glycolipids. Emerging technological advances are enabling more comprehensive, sensitive, and rapid analyses of these different classes of milk glycans. Understanding the impact of inter- and intraindividual glycan diversity on function is an important step toward interventions aimed at improving health and preventing disease. This review discusses the state of technology for glycan analysis and how specific structure-function knowledge is enhancing our understanding of early nutrition in the neonate.
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“This bacteria grows exceptionally well in the presence of complex milk oligosaccharides to the exclusion of other potentially harmful bacteria [27–29].”
From Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms (2019) · cites this paper as [29]
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Genome of Bifidobacteria and Carbohydrate Metabolism
Bondue, P., & Delcenserie, V. (2015) · Korean Journal for Food Science of Animal Resources · doi:10.5851/kosfa.2015.35.1.1 · Cited by 32
“It passes through the membrane, with an ABC transporter associated with a specific SBP, and is then degraded intracellularly (Sela, 2011; Smilowitz et al., 2014).”
BackgroundResultInfluentialLee, H., de MeloSilva, V. L., Liu, Y., & Barile, D. (2015) · Journal of Dairy Science · doi:10.3168/jds.2015-9882 · Cited by 32
“Milk oligosaccharides have received a lot of interest for their biological activities as prebiotics (promoting the growth of beneficial microbiota), antiinfective agents, and immune modulators (Smilowitz et al., 2014).”
Safety and efficacy of probiotic administration to preterm infants: ten common questions
Underwood, M. A., Umberger, E., & Patel, R. M. (2020) · Pediatric Research · doi:10.1038/s41390-020-1080-6 · Cited by 33
Human milk oligosaccharides, infant growth, and adiposity over the first 4 months of lactation
Binia, A., Lavalle, L., Chen, C., Austin, S., Agosti, M. A., Al-Jashi, I., Pereira, A. B., Costeira, M. J., Silva, M. G., Marchini, G., et al. (2021) · Pediatric Research · doi:10.1038/s41390-020-01328-y · Cited by 32
Bhattacharya, M., Salcedo, J., Robinson, R. C., Henrick, B. M., & Barile, D. (2019) · npj Science of Food · doi:10.1038/s41538-019-0037-9 · Cited by 30
Bifidobacteria and Their Health-Promoting Effects
Hidalgo-Cantabrana, C., Delgado, S., Ruíz, L., Ruas‐Madiedo, P., Sánchez, B., & Margollés, A. (2018) · ASM Press eBooks · doi:10.1128/9781555819705.ch3 · Cited by 32
Role of milk glycome in prevention, treatment, and recovery of COVID-19
Kaplan, M., Şahutoğlu, A. S., Sarıtaş, S., Duman, H., Arslan, A., Pekdemir, B., & Karav, S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1033779 · Cited by 31
Sischo, W. M., Short, D. M., Geissler, M., Bunyatratchata, A., & Barile, D. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-12388 · Cited by 31
“The 5 monosaccharides that comprise OS are attached in various ways through at least 12 possible linkages, resulting in many possible structural combinations (Smilowitz et al., 2014).”
Profile and content of sialylated oligosaccharides in donkey milk at early lactation
Licitra, R., Li, J., Liang, X., Altomonte, I., Salari, F., Yan, J., & Martini, M. (2019) · LWT · doi:10.1016/j.lwt.2019.108437 · Cited by 30
Giampaoli, O., Conta, G., Calvani, R., & Miccheli, A. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.606171 · Cited by 30
“Fucosylated oligosaccharydes such as 2-fucosyllactose (2 FL), 3-fucosyllactose (3 FL), and lacto-N-fucopentaose I/II/III (LNFP I/II/III) are higher in secretors compared to non-secretors (12, 55, 56) but, in general, the HMOs content changes during the lactation period (57).”
BackgroundDuman, H., Kaplan, M., Arslan, A., Şahutoğlu, A. S., Kayılı, H. M., Frese, S. A., & Karav, S. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.646275 · Cited by 32
“There are three main HMO categories: neutral N-containing (non-fucosylated) (42–55%), neutral (fucosylated) (35–50%), and acidic (sialylated) (12–14%) (39).”
BackgroundWang, X., Liu, J., Li, C., Xu, Y., Wang, X., Lu, Y., Zhang, T., Cao, H., Huang, L., & Wang, Z. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.2c00147 · Cited by 31
O’Connell Motherway, M., O’Brien, F., O’Driscoll, T., Casey, P. G., Shanahan, F., & van Sinderen, D. (2018) · Scientific Reports · doi:10.1038/s41598-018-29034-0 · Cited by 29
Vicaretti, S. D., Mohtarudin, N. A., Garner, A. M., & Zandberg, W. F. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b01041 · Cited by 29
Lawley, B., Otal, A., Moloney‐Geany, K., Diana, A., Houghton, L. A., Heath, A. M., Taylor, R. W., & Tannock, G. W. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.01105-19 · Cited by 29
“These findings suggest a relatively stable environment with direct reliance on environmental resources by bacteria with special trophic adaptations that permit cohabitation (for example, differential utilization of HMOs for growth [22, 38, 44]).”
BackgroundPhylogenomic disentangling of the Bifidobacterium longum subsp. infantis taxon
Tarracchini, C., Milani, C., Lugli, G. A., Mancabelli, L., Fontana, F., Alessandri, G., Longhi, G., Anzalone, R., Viappiani, A., Turroni, F., et al. (2021) · Microbial Genomics · doi:10.1099/mgen.0.000609 · Cited by 29
Human milk oligosaccharides and the infant gut microbiome from an eco-evolutionary perspective
Kijner, S., Kolodny, O., & Yassour, M. (2022) · Current Opinion in Microbiology · doi:10.1016/j.mib.2022.102156 · Cited by 31
Dietary sialic acids: distribution, structure, and functions
Zhang, T., Wu, J., & Zhan, X. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2023.2202254 · Cited by 30
“Sialoglycans are not present in plants but are abundant in vertebrates and invertebrates (Baydas et al. 2002; Crocker and Varki 2001), such as in beef, mutton, pork, edible bird’s nest (EBN), milks, and eggs (Ma and Liu 2012; Morrissey 1973; Powell, Liu, and Pekosz 2021; Smilowitz et al. 2014).”
Sialyllactose suppresses angiogenesis by inhibiting VEGFR-2 activation, and tumor progression
Chung, T., Kim, E. Y., Kim, S.-J., Choi, H.-J., Jang, S. B., Kim, K., Ha, S., Abekura, F., Kwak, C.-H., Kim, C., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.16192 · Cited by 29
“Human milk is composed of many bioactive ingredients, including milk oligosaccharides [1, 2].”
BackgroundEl-Hawiet, A., Chen, Y., Shams‐Ud‐Doha, K., Kitova, E. N., St‐Pierre, Y., & Klassen, J. S. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b00542 · Cited by 29
Bandara, M. D., Stine, K. J., & Demchenko, A. V. (2019) · The Journal of Organic Chemistry · doi:10.1021/acs.joc.9b02701 · Cited by 29
Wang, M., Monaco, M. H., Hauser, J., Yan, J., Dilger, R. N., & Donovan, S. M. (2021) · Microorganisms · doi:10.3390/microorganisms9050884 · Cited by 32
Akkerman, R., Logtenberg, M. J., An, R., van den Berg, M. A., de Haan, B. J., Faas, M. M., Zoetendal, E. G., de Vos, P., & Schols, H. A. (2020) · Nutrients · doi:10.3390/nu12061660 · Cited by 29
“prebiotics that guide immune development and gut barrier maturation [4,5].”
BackgroundÖztürk, G., German, J. B., & Bell, J. M. L. N. D. M. (2019) · npj Science of Food · doi:10.1038/s41538-019-0046-8 · Cited by 27
Hanau, S., Almugadam, S. H., Sapienza, E., Cacciari, B., Manfrinato, M. C., Trentini, A., & Kennedy, J. F. (2020) · Carbohydrate Polymer Technologies and Applications · doi:10.1016/j.carpta.2020.100013 · Cited by 28
Changes to the Oligosaccharide Profile of Bovine Milk at the Onset of Lactation
Quinn, E. M., O’Callaghan, T. F., Tobin, J. T., Murphy, J. P., Sugrue, K., Slattery, H., O’Donovan, M., & Hickey, R. M. (2020) · Dairy · doi:10.3390/dairy1030019 · Cited by 26
“Furthermore, HMOs can directly modulate the host’s epithelial responses by blocking the binding of pathogens to intestinal epithelial cells, or by acting as decoy receptors, inhibiting the binding of enteric pathogens [3].”
BackgroundBai, Y., Yang, X., Yu, H., & Chen, X. (2022) · ChemSusChem · doi:10.1002/cssc.202102539 · Cited by 26
Building Robust Assemblages of Bacteria in the Human Gut in Early Life
Tannock, G. W. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.01449-21 · Cited by 24
Metadata
- Authors
- Smilowitz, J. T., Lebrilla, C. B., Mills, D. A., German, J. B., & Freeman, S. L.
- Affiliations
- Department of Food Science and Technology,
- Department of Chemistry, and
- University of California, Davis (US)
- Venue
- Annual Review of Nutrition
- Publisher
- Annual Reviews
- Published
- 2014-07-17
- Volume
- 34
- Issue
- 1
- Pages
- 143-169
- ISSN
- 0199-9885 (ISSN-L)
- 1545-4312
- PMC
- PMC4348064
- OpenAlex
- W2157542971
- Cited by
- 410
- References
- 154
- Citations by year
- 2026: 15 · 2025: 19 · 2024: 30 · 2023: 33 · 2022: 27 · 2021: 57 · 2020: 64 · 2019: 51 · 2018: 36 · 2017: 29 · 2016: 33 · 2015: 15 · 2014: 1
- FWCI
- 2.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Bill and Melinda Gates Foundation
- California Dairy Research Foundation
- National Institutes of Health
- University of California, Davis
- National Center for Complementary and Integrative Health (R01AT007079, R21AT006180)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD065122, R01HD061923, R01HD059127)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Health Sciences › Medicine › Epidemiology › Breastfeeding Practices and Influences
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- human milk oligosaccharides, structure-function relationship, neonatal nutrition, infant microbiome, intestinal development, immune system development, glycoproteins, glycopeptides, glycolipids, lactation
- MeSH terms
- Bifidobacterium, Breast Feeding, Carbohydrate Sequence, Child Development, Female, Glycolipids, Glycopeptides, Glycoproteins, Humans, Immunity, Innate, Infant, Newborn, Intestinal Mucosa, Lactation, Male, Milk Proteins, Milk, Human, Models, Biological, Oligosaccharides
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