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Breast Milk Oligosaccharides: Structure-Function Relationships in the Neonate
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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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B. infantis grows exceptionally well in the presence of complex milk oligosaccharides to the exclusion of other potentially harmful bacteria.
“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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“To cite just a few examples, the following glycans were mostly unknown when the previous version of this review was being written: functional sialylation in the fly nervous system (181); O-fucose and O-glucose glycans on Notch (182–184), and O-fucose on thrombospondin repeats (185); mucin type O-glycosylation in proti…”
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“Human milk is composed of many bioactive substances, including a diverse repertoire of human milk oligosaccharides (HMOs) that may be decoratedwith fucose and/or sialic acidmoieties (Coppa et al., 2011; Smilowitz et al., 2014).”
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“HMOs are structurally diverse and composed of several monosaccharides (glucose, galactose, N -acetylglucosamine, fucose, or sialic acid), and they mainly consist of a lactose core linked to units (n = 0 to 15) of lacto-N -biose (type I) or to N -acetyl- lactosamine (type II) (21).”
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“Human milk oligosaccharides (HMOs) are complex carbohydrates that are highly abundant in human milk, but are absent from most infant formulas (10–12).”
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“Therefore, breast milk can be assigned to one of the four groups based on the expression of FUT2 and FUT3: Le-positive secretors (Le+Se+), Le-negative secretors (Le-Se+), Le-positive nonsecretors (Le+Se-), and Le-negative nonsecretors (Le-Se+) (Table 1) [9,10,14]:”
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“Twenty-one percent of mothers do not have the functional FUT2 enzyme and produce milk without the α1,2-fucosylated oligosaccharides 2′FL and LNFP I [5,8,15].”
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“development of a healthy microbiome (Smilowitz et al. 2014).”
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“HMOs are clearly a factor that influences populations of beneficial microorganisms, such as Bifidobacterium, in the infant gut (22, 24).”
BackgroundStudying Lactoferrin N-Glycosylation
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“Elongation with NeuAC and Fuc increases the diversity and complexity of the N-glycan structure [53,54].”
BackgroundInfluence of Maternal Milk on the Neonatal Intestinal Microbiome
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“They are not broken down by the digestive enzymes of the infant and thus can reach to the distal ileum and colon [68].”
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“Lactose concentration increases with lactation stage, with the lowest concentration (around 56 g/L) in colostrum to reach an average content of 69 g/L at 120 days postpartum (58).”
BackgroundBenefits of Lactoferrin, Osteopontin and Milk Fat Globule Membranes for Infants
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“Furthermore, lactadherin might contribute to establishing the intestinal barrier in the neonate [127].”
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“HMO fucosylation is regulated by enzymes encoded by the fucosyltransferase 2 (FUT2) and FUT3 genes, which determine secretor status and Lewis blood group status, respectively (23, 24).”
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Human milk oligosaccharides: The role in the fine-tuning of innate immune responses
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“The HMO structure can be elongated further via addition of: (1) lacto-N-biose and N-acetyllactosamine units (by β1-3 and β1-6 linkages); (2) Fuc connected with α1-2, α1-3, or α1-4 linkages; (3) and/or sialic acid residues attached by α2-3 or α2-6 linkages at terminal positions [190].”
BackgroundEnzymatic and cell factory approaches to the production of human milk oligosaccharides
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“HMOs make up about 10% of the dry weight of mother’s milk, making them the third most abundant solid component after lipids and lactose 150 .”
BackgroundProduction of human milk oligosaccharides by enzymatic and whole-cell microbial biotransformations
Sprenger, G. A., Baumgärtner, F., & Albermann, C. (2017) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2017.07.030 · Cited by 139
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The Interaction of the Gut Microbiota with the Mucus Barrier in Health and Disease in Human
Corfield, A. P. (2018) · Microorganisms · doi:10.3390/microorganisms6030078 · Cited by 139
Human Milk Oligosaccharides: Their Effects on the Host and Their Potential as Therapeutic Agents
Rousseaux, A., Brosseau, C., Gall, S. L., Piloquet, H., Barbarot, S., & Bodinier, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.680911 · Cited by 136
Hegar, B., Wibowo, Y., Basrowi, R. W., Ranuh, R. G., Sudarmo, S. M., Munasir, Z., Atthiyah, A. F., Widodo, A. D., Supriatmo, Kadim, M., et al. (2019) · Pediatric Gastroenterology Hepatology & Nutrition · doi:10.5223/pghn.2019.22.4.330 · Cited by 140
“The human breast milk contains three major HMO types: fucosylated HMOs (35%–50%), sialylated HMOs (12%–14%), and nonfucosylated neutral HMOs (42%–55%) [10].”
BackgroundGut Microbiota and Mucosal Immunity in the Neonate
Dzidic, M., Boix-Amorós, A., Selma‐Royo, M., Mira, Á., & Collado, M. C. (2018) · Medical Sciences · doi:10.3390/medsci6030056 · Cited by 139
“Importantly, specific HMOs can act as homologous to infant gut cell receptors, inhibiting the binding of pathogens to the intestinal epithelium and therefore offering protection against infections [160,164].”
BackgroundZhang, S., Li, T., Xie, J., Zhang, D., Pi, C., Zhou, L., & Yang, W. (2021) · Microbial Cell Factories · doi:10.1186/s12934-021-01599-y · Cited by 135
“Although the combination of these five building blocks in diverse directions and sequences is immense, only approximately 200 different HMOs have been characterized so far and 50 compositions of HMOs are assumed to represent 99% of HMO abundance in human mother’s milk [19, 24].”
BackgroundFostering of advanced mutualism with gut microbiota by Immunoglobulin A
Sutherland, D. B., Suzuki, K., & Fagarasan, S. (2016) · Immunological Reviews · doi:10.1111/imr.12384 · Cited by 115
“Indeed, besides the core microbiome, milk contains essential nutrients, bioactive oligosaccharides (26, 27), protective white blood cells, and functional proteins of which secretory IgA is the main immunoglobulin constituent.”
BackgroundMilk Glycans and Their Interaction with the Infant-Gut Microbiota
Kirmiz, N., Robinson, R. C., Shah, I. M., Barile, D., & Mills, D. A. (2018) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030216-030207 · Cited by 124
“Many pathogens adhere to the intestinal epithelial surfaces, and milk glycans have epitopes identical to the intestinal surfaces, as they are generated from similar enzymes (Smilowitz et al. 2014).”
BackgroundZhu, Y., Wan, L., Li, W., Ni, D., Zhang, W., Yan, X., & Mu, W. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1850413 · Cited by 124
“Furthermore, several studies have been reported on other effects such as modulating the immune system and promoting brain development for the newborn (Smilowitz et al. 2014; Wang 2012; Yatsunenko et al. 2012).”
BackgroundPetschacher, B., & Nidetzky, B. (2016) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2016.03.052 · Cited by 120
Borewicz, K., Gu, F., Saccenti, E., Arts, I. C. W., Penders, J., Thijs, C. T., van Leeuwen, S. S., Lindner, C., Nauta, A., van Leusen, E., et al. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801214 · Cited by 121
Ambrogi, V., Bottacini, F., Cao, L., Kuipers, B. J. H., Schoterman, M. H. C., & van Sinderen, D. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1953437 · Cited by 126
“Notably, breast milk is rich in HMOs, a group of oligosaccharides that have been described to function as highly effective and selective bifidobacteria-specific prebiotics for infants (Smilowitz et al. 2014).”
BackgroundZhang, N., Jin, M., Wang, K., Zhang, Z., Shah, N. P., & Wei, H. (2021) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2021.119043 · Cited by 126
Xu, G., Amicucci, M. J., Cheng, Z., Galermo, A. G., & Lebrilla, C. B. (2017) · The Analyst · doi:10.1039/c7an01530e · Cited by 117
Plant Glycan Metabolism by Bifidobacteria
Kelly, S. M., Muñoz-Muñoz, J., & van Sinderen, D. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.609418 · Cited by 116
Lis-Kuberka, J., & Orczyk‐Pawiłowicz, M. (2019) · Nutrients · doi:10.3390/nu11020306 · Cited by 113
“The main sialylated structures of human milk oligosaccharides and glycoconjugates (glycoproteins and glycolipids) [35,41,43,44].”
BackgroundInfluentialde Almeida, C. C., Pereira, B. F. D. M., Leandro, K. C., da Costa, M. P., Spisso, B. F., & Conte‐Júnior, C. A. (2021) · International Journal of Food Science · doi:10.1155/2021/8850080 · Cited by 119
Lordan, C., Roche, A. K., Delsing, D. J. M., Nauta, A., Groeneveld, A., MacSharry, J. A., Cotter, P. D., & van Sinderen, D. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00094-23 · Cited by 117
“The biosynthesis of oligosaccharides occurs following the formation of the lactose core when Gal and Glc are coupled by β-galactotransferase in the presence of α-lactalbumin, which is expressed during lactation (44).”
BackgroundProspecting Human Milk Oligosaccharides as a Defense Against Viral Infections
Moore, R. E., Xu, L. L., & Townsend, S. D. (2021) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.0c00807 · Cited by 109
Doherty, A. M., Lodge, C., Dharmage, S. C., Dai, X., Bode, L., & Lowe, A. J. (2018) · Frontiers in Pediatrics · doi:10.3389/fped.2018.00091 · Cited by 105
He, X., Parenti, M., Grip, T., Lönnerdal, B. L., Timby, N., Domellöf, M., Hernell, O., & Slupsky, C. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-47953-4 · Cited by 107
Engineering two species of yeast as cell factories for 2′-fucosyllactose
Hollands, K., Baron, C. M., Gibson, K. J., Kelly, K. J., Krasley, E., Laffend, L. A., Lauchli, R. M., Maggio‐Hall, L. A., Nelson, M. J., Prasad, J. C., et al. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.12.005 · Cited by 102
Salli, K. M., Anglenius, H., Hirvonen, J., Hibberd, A. A., Ahonen, I., Saarinen, M., Tiihonen, K., Maukonen, J., & Ouwehand, A. C. (2019) · Scientific Reports · doi:10.1038/s41598-019-49497-z · Cited by 104
Kong, C., Elderman, M. E., Cheng, L., de Haan, B. J., Nauta, A., & de Vos, P. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201900303 · Cited by 104
Boudry, G., Hamilton, M. K., Chichlowski, M., Wickramasinghe, S., Barile, D., Kalanetra, K. M., Mills, D. A., & Raybould, H. E. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-11890 · Cited by 101
“Milk oligosaccharides are complex sugars that selectively enhance the growth of specific beneficial bacteria in the gastrointestinal system (Smilowitz et al., 2014).”
BackgroundEngineering mucus to study and influence the microbiome
Werlang, C. A., Cárcamo‐Oyarce, G., & Ribbeck, K. (2019) · Nature Reviews Materials · doi:10.1038/s41578-018-0079-7 · Cited by 99
Cheng, L., Kong, C., Walvoort, M. T. C., Faas, M. M., & de Vos, P. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201900976 · Cited by 96
Borewicz, K., Gu, F., Saccenti, E., Hechler, C., Beijers, R., de Weerth, C., van Leeuwen, S. S., Schols, H. A., & Smidt, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-61024-z · Cited by 97
Punia, H., Tokas, J., Malik, A., Sangwan, S., Baloda, S., Singh, N., Singh, S., Bhuker, A., Singh, P. K., Yashveer, S., et al. (2020) · Molecules · doi:10.3390/molecules25153328 · Cited by 95
Untangling human milk oligosaccharides and infant gut microbiome
Masi, A. C., & Stewart, C. J. (2021) · iScience · doi:10.1016/j.isci.2021.103542 · Cited by 97
“…liquid chromatography coupled with online fluorescence detection (HPLC-FL) and liquid chromatography mass spectrometry (LCMS) are frequently used in HMO studies, where relative or absolute abundances of HMOs can be determined with these methods (Smilowitz et al., 2014; van Leeuwen, 2019).”
BackgroundMethodThe connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · Cited by 92
Dong, X., Zhou, S., & Mechref, Y. S. (2016) · Electrophoresis · doi:10.1002/elps.201500561 · Cited by 92
Nagy, G., Attah, I. K., Garimella, S., Tang, K., Ibrahim, Y., Baker, E. S., & Smith, R. D. (2018) · Chemical Communications · doi:10.1039/c8cc06966b · Cited by 89
Potential Benefits of Bovine Colostrum in Pediatric Nutrition and Health
Sangild, P. T., Vonderohe, C. E., Hebib, V. M., & Burrin, D. G. (2021) · Nutrients · doi:10.3390/nu13082551 · Cited by 109
Xiao, L., Leusink-Muis, T., Kettelarij, N., van Ark, I., Blijenberg, B., Hesen, N. A., Stahl, B., Overbeek, S. A., Garssen, J., Folkerts, G., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00452 · Cited by 91
Liquid Chromatography–Tandem Mass Spectrometry Approach for Determining Glycosidic Linkages
Galermo, A. G., Nandita, E., Barboza, M., Amicucci, M. J., Vo, T.-T. T., & Lebrilla, C. B. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b04124 · Cited by 84
Anti-Pathogenic Functions of Non-Digestible Oligosaccharides In Vitro
Asadpoor, M., Peeters, C., Henricks, P. A. J., Varasteh, S., Pieters, R. J., Folkerts, G., & Braber, S. (2020) · Nutrients · doi:10.3390/nu12061789 · Cited by 87
“Fucose is present in human milk and the proportion of fucosylated HMOs in term breast milk was recently reported as 35–50% [23].”
BackgroundInfluentialCui, Y., & Qu, X. (2021) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2021.06.058 · Cited by 82
Miliku, K., & Azad, M. B. (2018) · Nutrients · doi:10.3390/nu10080995 · Cited by 82
Cheng, L., Kiewiet, M. B. G., Groeneveld, A., Nauta, A., & de Vos, P. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.05.023 · Cited by 79
“HMOs can be found in mother’s milk in concentrations varying between 5 and 20 mg/ mL (Bode, 2012; Petherick, 2010), depending on the stage of lactation and may provide a variety of health-promoting effects (Bode, 2012; Kunz et al., 2000; Smilowitz, Lebrilla, Mills, German, & Freeman, 2014).”
BackgroundVongbhavit, K., & Underwood, M. A. (2016) · Clinical Therapeutics · doi:10.1016/j.clinthera.2016.01.006 · Cited by 79
Salcedo, J., Frese, S. A., Mills, D. A., & Barile, D. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-10966 · Cited by 87
“Taken together, these bioactivities favor the establishment of a protective and healthful intestinal environment (Smilowitz et al., 2014).”
BackgroundSingh, R. P., Niharika, J., Kondepudi, K. K., Bishnoi, M., & Tingirikari, J. M. R. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110884 · Cited by 81
Siméoni, U., Berger, B. W., Junick, J., Blaut, M., Pecquet, S., Rezzonico, E., Grathwohl, D., Sprenger, N., Brüssow, H., The Study Team, et al. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13144 · Cited by 79
“Human milk oligosaccharides (HMOs) are natural prebiotics because they represent the bifidogenic factors that favour the growth of bifidobacteria, which typically dominate the gut microbiota of breastfed infants (Garrido et al., 2013; Smilowitz et al., 2014).”
BackgroundLactose and lactose-derived oligosaccharides: More than prebiotics?
Chen, X. Y., & Gänzle, M. G. (2016) · International Dairy Journal · doi:10.1016/j.idairyj.2016.10.001 · Cited by 77
“Most HMO contain 158 lactose at the reducing end and are elongated with galactose and N-acetyglucosamine units to 159 form linear or branched oligosaccharides (Smilowitz et al., 2014).”
BackgroundZhao, C., Wu, Y., Yu, H., Shah, I. M., Li, Y., Zeng, J., Liu, B., Mills, D. A., & Chen, X. (2016) · Chemical Communications · doi:10.1039/c5cc10646j · Cited by 76
Duar, R. M., Casaburi, G., Mitchell, R. D., Scofield, L. N. C., Ramírez, C. A. O., Barile, D., Henrick, B. M., & Frese, S. A. (2020) · Nutrients · doi:10.3390/nu12113247 · Cited by 72
“These core structures can be further elongated with residues of galactose, N-acetylglucosamine, and decorated with fucose or sialic acid [8].”
BackgroundTerm Infant Formulas Influencing Gut Microbiota: An Overview
Fabiano, V., Indrio, F., Verduci, E., Calcaterra, V., Pop, T. L., Mari, A., Zuccotti, G., Cokugras, F. C., Pettoello‐Mantovani, M., & Goulet, O. (2021) · Nutrients · doi:10.3390/nu13124200 · Cited by 78
“Compared to formula-fed infants, studies of the “intestinal flora” of BF infants showed differences, especially regarding Bifidobacteria species [9,10].”
BackgroundResultQuin, C., Vicaretti, S. D., Mohtarudin, N. A., Garner, A. M., Vollman, D. M., Gibson, D. L., & Zandberg, W. F. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011351 · Cited by 75
“Obesity (21),malnourishment (7), andhyperglycemia (21) impactboth HMO concentrations and structures; it is possible that these conditions affect the levels of nucleotide-activated GlcNAc and Neu5Ac available forHMObiosynthesis, as obesity and hyperglycemia are both linked to alteredmetabolic flux through the hexosamin…”
BackgroundHow far is it from infant formula to human milk? A look at the human milk oligosaccharides
Li, W., Wang, J., Lin, Y., Li, Y., Ren, F., & Guo, H. (2021) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2021.09.021 · Cited by 74
Smilowitz, J. T., Moya, J. J., Breck, M. A., Cook, C., Fineberg, A. E., Angkustsiri, K., & Underwood, M. A. (2017) · BMC Pediatrics · doi:10.1186/s12887-017-0886-9 · Cited by 71
“Advances in mass spectrometry have revealed detailed chemical structures of the complex and diverse free and conjugated glycans in human milk [1].”
BackgroundSelf-citationEnzymatic and chemoenzymatic synthesis of human milk oligosaccharides and derivatives
Zheng, J., Han, X., Fang, J., & Zhang, X. (2022) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2022.119564 · Cited by 70
Yu, H., Li, Y., Wu, Z., Li, L., Zeng, J., Zhao, C., Wu, Y., Tasnima, N., Wang, J., Liu, H., et al. (2017) · Chemical Communications · doi:10.1039/c7cc05403c · Cited by 70
Zabel, B., Yde, C. C., Roos, P., Marcussen, J., Jensen, H. M., Salli, K. M., Hirvonen, J., Ouwehand, A. C., & Morovic, W. (2019) · Scientific Reports · doi:10.1038/s41598-019-43780-9 · Cited by 70
Hamilton, M. K., Ronveaux, C. C., RUST, B. M., Newman, J. W. I., Hawley, M. M., Barile, D., Mills, D. A., & Raybould, H. E. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00427.2016 · Cited by 70
Insights into human evolution from ancient and contemporary microbiome studies
Schnorr, S. L., Sankaranarayanan, K., Lewis, C. M., & Warinner, C. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.07.003 · Cited by 71
Walsh, C., Lane, J. A., van Sinderen, D., & Hickey, R. M. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104052 · Cited by 66
“Due to the structure–function relationships of HMOs and other oligosaccharides, correct branching and stereospecific linkages are required for biological function to be preserved (Smilowitz et al., 2014).”
InfluentialInfant Complementary Feeding of Prebiotics for the Microbiome and Immunity
McKeen, S., Young, W., Mullaney, J. A., Fraser, K., McNabb, W. C., & Roy, N. C. (2019) · Nutrients · doi:10.3390/nu11020364 · Cited by 66
“HMO consumption has only been identified in select Bacteroides (Bifidobacterium) and Lactobacillus species, and different species and subspecies have been found to utilise different protein-substrate binding and enzymatic mechanisms to metabolise HMOs [113,114].”
BackgroundInfluentialKnoop, K. A., Coughlin, P. E., Floyd, A. N., Ndao, I. M., Hall-Moore, C. M., Shaikh, N., Gasparrini, A. J., Rusconi, B. A., ESCOBEDO, M. B., Good, M. L., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1912022117 · Cited by 64
O’Brien, C. E., Meier, A., Cernioglo, K., Mitchell, R. D., Casaburi, G., Frese, S. A., Henrick, B. M., Underwood, M. A., & Smilowitz, J. T. (2021) · Pediatric Research · doi:10.1038/s41390-020-01350-0 · Cited by 67
Self-citationHuman milk oligosaccharides as prebiotics
Okburan, G., & Kızıler, S. (2023) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2022.09.017 · Cited by 70
Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus
Hu, L., Ramani, S., Czakó, R., Sankaran, B., Yu, Y. Q., Smith, D. F., Cummings, R. D., Estes, M. K., & Prasad, B. V. V. (2015) · Nature Communications · doi:10.1038/ncomms9346 · Cited by 63
“Since human milk oligosaccharides (HMOs) beyond lactose are not readily digested by human enzymes, these glycans may have evolved as natural prebiotics to support the growth of gut microbiota in the newborn 31 .”
Henrick, B. M., Yao, X.-D., Nasser, L., Roozrogousheh, A., & Rosenthal, K. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01631 · Cited by 86
Translational Advances in Pediatric Nutrition and Gastroenterology: New Insights from Pig Models
Burrin, D. G., Sangild, P. T., Stoll, B., Thymann, T., Buddington, R. K., Marini, J. C., Olutoye, O. O., & Shulman, R. J. (2020) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-115142 · Cited by 63
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Influence of gut microbiota on mucosal IgA antibody response to the polio vaccine
Zhao, T., Li, J., Fu, Y., Ye, H., Liu, X., Li, G., Yang, X., & Yang, J. (2020) · npj Vaccines · doi:10.1038/s41541-020-0194-5 · Cited by 63
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“In humans, one of the most well-known sources of variation in OS composition is genetic variability (Ninonuevo et al. 2006), specifically Lewis blood group and secretor status (Smilowitz et al. 2014).”
BackgroundInfluentialKilogram scale chemical synthesis of 2′-fucosyllactose
Ágoston, K., Hederos, M. J., Bajza, I., & Dékány, G. (2019) · Carbohydrate Research · doi:10.1016/j.carres.2019.03.006 · Cited by 60
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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