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Article: Fucosylated TLR4 mediates communication between mutualist fucotrophic microbiota and mammalian gut mucosa.

Nanthakumar, Nanda N / Meng, Di / Newburg, David S

2023 Volume 10, Page(s) 1070734

Abstract: Objective: The glycans on the mucosa of suckling mice are predominantly sialylated; upon weaning, fucosylated glycans preponderate. This manifestation of mutualism between fucotrophic bacteria and the mature host utilizes a sentinel receptor in the ... ...

Abstract	Objective: The glycans on the mucosa of suckling mice are predominantly sialylated; upon weaning, fucosylated glycans preponderate. This manifestation of mutualism between fucotrophic bacteria and the mature host utilizes a sentinel receptor in the intestinal mucosa; this receptor was isolated to distinguish its structural and functional features. Design: Provisional identification of the sentinel gut receptor as fuc-TLR4 was through colonization of germ-free mutant mice. Conventional mice whose microbiota was depleted with a cocktail of antibiotics were used to further define the nature and functions of fuc-TLR4 sentinel, and to define the role of the fucotrophic microbiota in gut homeostasis and recovery from insult. The nature of the sentinel was confirmed in cultured human HEL cells. Results: Fuc-TLR4 activity is distinct from that of TLR4. Activated mucosal fuc-TLR4 induces a fuc-TLR4 dependent non-inflammatory (ERK and JNK dependent, NF-κB independent) signaling cascade, initiating induction of fucosyltransferase 2 (secretor) gene transcription. Conclusion: In mature mice, fucosyl-TLR4 mediated gut fucosylation creates a niche that supports the healthy fucose-dependent mutualism between the mammalian gut and its fucotrophic microbes. Such microbiota-induced Fuc-TLR4 signaling supports initial colonization of the secretor gut, recovery from dysbiosis, and restoration or preservation of intestinal homeostasis.
Language	English
Publishing date	2023-03-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2775999-4
ISSN	2296-858X
ISSN	2296-858X
DOI	10.3389/fmed.2023.1070734
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Article ; Online: Glycobiology of human milk.

Newburg, D S

Biochemistry. Biokhimiia

2013 Volume 78, Issue 7, Page(s) 771–785

Abstract: Glycans are characteristic components of milk, and each species has unique patterns of specific carbohydrates. Human milk is unusually rich in glycans, with the major components being lactose and oligosaccharides, representing approximately 6.8 and 1% of ...

Abstract	Glycans are characteristic components of milk, and each species has unique patterns of specific carbohydrates. Human milk is unusually rich in glycans, with the major components being lactose and oligosaccharides, representing approximately 6.8 and 1% of the milk, respectively. Other sources of glycans in human milk include monosaccharides, mucins, glycosaminoglycans, glycoproteins, glycopeptides, and glycolipids. In human milk, the presence and patterns of these glycans vary depending upon the stage of lactation and the maternal genes and their genetic polymorphisms that control glycosyl transferases. The synthesis of milk glycans utilizes a significant portion of the metabolic energy that the mother expends when producing her milk, but other than lactose, these glycans contribute little to the nutritional needs of the infant. The data herein support several functions. 1) Many human milk glycans inhibit pathogens from binding to the intestinal mucosa. 2) Human milk glycans attenuate inflammation. 3) Glycans also directly stimulate the growth of beneficial (mutualist) bacteria of the microbiota (formerly considered commensal microflora of the intestine); these mutualists and their fermentation products can, in turn, (a) inhibit pathogens, (b) modulate signaling and inflammation, and (c) the fermentation products can be absorbed and utilized as a source of dietary calories. These functions can help direct and support intestinal postnatal growth, development, and ontogeny of colonization. The many functions of the milk glycans may synergistically protect infants from disease. Hence, human milk glycans and their homologs may serve as novel prophylactic or therapeutic agents for a diverse range of deleterious conditions.
MeSH term(s)	Female ; Glycolipids/chemistry ; Glycolipids/metabolism ; Glycomics ; Glycoproteins/chemistry ; Glycoproteins/metabolism ; Glycosaminoglycans/chemistry ; Glycosaminoglycans/metabolism ; Humans ; Immunity, Innate ; Lactose/chemistry ; Lactose/metabolism ; Milk, Human/chemistry ; Milk, Human/immunology ; Milk, Human/metabolism ; Monosaccharides/chemistry ; Monosaccharides/metabolism ; Mucins/chemistry ; Mucins/metabolism ; Oligosaccharides/chemistry ; Oligosaccharides/metabolism
Chemical Substances	Glycolipids ; Glycoproteins ; Glycosaminoglycans ; Monosaccharides ; Mucins ; Oligosaccharides ; Lactose (J2B2A4N98G)
Language	English
Publishing date	2013-09-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1109-5
ISSN	1608-3040 ; 0006-2979 ; 0320-9717
ISSN (online)	1608-3040
ISSN	0006-2979 ; 0320-9717
DOI	10.1134/S0006297913070092
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Article ; Online: Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans.

Newburg, D S

Journal of animal science

2009 Volume 87, Issue 13 Suppl, Page(s) 26–34

Abstract: This review discusses the role of human milk glycans in protecting infants, but the conclusion that the human milk glycans constitute an innate immune system whereby the mother protects her offspring may have general applicability in all mammals, ... ...

Abstract	This review discusses the role of human milk glycans in protecting infants, but the conclusion that the human milk glycans constitute an innate immune system whereby the mother protects her offspring may have general applicability in all mammals, including species of commercial importance. Infants that are not breastfed have a greater incidence of severe diarrhea and respiratory diseases than those who are breastfed. In the past, this had been attributed primarily to human milk secretory antibodies. However, the oligosaccharides are major components of human milk, and milk is also rich in other glycans, including glycoproteins, mucins, glycosaminoglycans, and glycolipids. These milk glycans, especially the oligosaccharides, are composed of thousands of components. The milk factor that promotes gut colonization by Bifidobacterium bifidum was found to be a glycan, and such prebiotic characteristics may contribute to protection against infectious agents. However, the ability of human milk glycans to protect the neonate seems primarily to be due to their inhibition of pathogen binding to their host cell target ligands. Many such examples include specific fucosylated oligosaccharides and glycans that inhibit specific pathogens. Most human milk oligosaccharides are fucosylated, and their production depends on fucosyltransferase enzymes; mutations in these fucosyltransferase genes are common and underlie the various Lewis blood types in humans. Variable expression of specific fucosylated oligosaccharides in milk, also a function of these genes (and maternal Lewis blood type), is significantly associated with the risk of infectious disease in breastfed infants. Human milk also contains major quantities and large numbers of sialylated oligosaccharides, many of which are also present in bovine colostrum. These could similarly inhibit several common viral pathogens. Moreover, human milk oligosaccharides strongly attenuate inflammatory processes in the intestinal mucosa. These results support the hypothesis that oligosaccharides and other glycans are the major constituents of an innate immune system of human milk whereby the mother protects her infant from enteric and other pathogens through breastfeeding. These protective glycans may prove useful as a basis for the development of novel prophylactic and therapeutic agents that inhibit disease by mucosal pathogens in many species.
MeSH term(s)	Bacterial Toxins/immunology ; Gastrointestinal Diseases/immunology ; Gastrointestinal Diseases/microbiology ; Gastrointestinal Diseases/virology ; Genotype ; Humans ; Immunity, Innate/immunology ; Milk, Human/immunology ; Oligosaccharides/immunology ; Polysaccharides/immunology
Chemical Substances	Bacterial Toxins ; Oligosaccharides ; Polysaccharides
Language	English
Publishing date	2009-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	390959-1
ISSN	1525-3163 ; 0021-8812
ISSN (online)	1525-3163
ISSN	0021-8812
DOI	10.2527/jas.2008-1347
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Article: Prenatal SARS-CoV-2 infection alters postpartum human milk-derived extracellular vesicles.

Chutipongtanate, Somchai / Cetinkaya, Hatice / Zhang, Xiang / Kuhnell, Damaris / Benefield, Desirée / Haffey, Wendy / Wyder, Michael / Patel, Richa / Conrey, Shannon C / Burrell, Allison R / Langevin, Scott / Nommsen-Rivers, Laurie / Newburg, David S / Greis, Kenneth D / Staat, Mary A / Morrow, Ardythe L

bioRxiv : the preprint server for biology

2023

Abstract: Human milk-derived extracellular vesicles (HMEVs) are crucial functional components in breast milk, contributing to infant health and development. Maternal conditions could affect HMEV cargos; however, the impact of SARS-CoV-2 infection on HMEVs remains ... ...

Abstract	Human milk-derived extracellular vesicles (HMEVs) are crucial functional components in breast milk, contributing to infant health and development. Maternal conditions could affect HMEV cargos; however, the impact of SARS-CoV-2 infection on HMEVs remains unknown. This study evaluated the influence of SARS-CoV-2 infection during pregnancy on postpartum HMEV molecules. Milk samples (9 prenatal SARS-CoV-2 vs. 9 controls) were retrieved from the IMPRINT birth cohort. After defatting and casein micelle disaggregation, 1 mL milk was subjected to a sequential process of centrifugation, ultrafiltration, and qEV-size exclusion chromatography. Particle and protein characterizations were performed following the MISEV2018 guidelines. EV lysates were analyzed through proteomics and miRNA sequencing, while the intact EVs were biotinylated for surfaceomic analysis. Multi-Omics was employed to predict HMEV functions associated with prenatal SARS-CoV-2 infection. Demographic data between the prenatal SARS-CoV-2 and control groups were similar. The median duration from maternal SARS-CoV-2 test positivity to milk collection was 3 months (range: 1-6 months). Transmission electron microscopy showed the cup-shaped nanoparticles. Nanoparticle tracking analysis demonstrated particle diameters of <200 nm and yields of >1e11 particles from 1 mL milk. Western immunoblots detected ALIX, CD9 and HSP70, supporting the presence of HMEVs in the isolates. Thousands of HMEV cargos and hundreds of surface proteins were identified and compared. Multi-Omics predicted that mothers with prenatal SARS-CoV-2 infection produced HMEVs with enhanced functionalities involving metabolic reprogramming and mucosal tissue development, while mitigating inflammation and lower EV transmigration potential. Our findings suggest that SARS-CoV-2 infection during pregnancy boosts mucosal site-specific functions of HMEVs, potentially protecting infants against viral infections. Further prospective studies should be pursued to reevaluate the short- and long-term benefits of breastfeeding in the post-COVID era.
Language	English
Publishing date	2023-06-01
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.06.01.543234
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Article ; Online: Gut Microbiome Composition and Metabolic Capacity Differ by

Thorman, Alexander W / Adkins, Grace / Conrey, Shannon C / Burrell, Allison R / Yu, Ying / White, Brendon / Burke, Rachel / Haslam, David / Payne, Daniel C / Staat, Mary A / Morrow, Ardythe L / Newburg, David S

Nutrients

2023 Volume 15, Issue 2

Abstract: ... the abundance of a breastfeeding mother’s fucosylated milk oligosaccharides. We compared the impact of maternal ...

Abstract	A major polymorphism in the fucosyltransferase2 (FUT2) gene influences risk of multiple gut diseases, but its impact on the microbiome of breastfed infants was unknown. In individuals with an active FUT2 enzyme (“secretors”), the intestinal mucosa is abundantly fucosylated, providing mutualist bacteria with a rich endogenous source of fucose. Non-secretors comprise approximately one-fifth of the population, and they lack the ability to create this enzyme. Similarly, maternal secretor status influences the abundance of a breastfeeding mother’s fucosylated milk oligosaccharides. We compared the impact of maternal secretor status, measured by FUT2 genotype, and infant secretor status, measured by FUT2 genotype and phenotype, on early infant fecal microbiome samples collected from 2-month-old exclusively breastfed infants (n = 59). Infant secretor status (19% non-secretor, 25% low-secretor, and 56% full-secretor) was more strongly associated with the infant microbiome than it was with the maternal FUT2 genotype. Alpha diversity was greater in the full-secretors than in the low- or non-secretor infants (p = 0.049). Three distinct microbial enterotypes corresponded to infant secretor phenotype (p = 0.022) and to the dominance of Bifidobacterium breve, B. longum, or neither (p < 0.001). Infant secretor status was also associated with microbial metabolic capacity, specifically, bioenergetics pathways. We concluded that in exclusively breastfed infants, infant—but not maternal—secretor status is associated with infant microbial colonization and metabolic capacity.
MeSH term(s)	Fucosyltransferases/genetics ; Gastrointestinal Microbiome ; Genotype ; Microbiota ; Milk, Human/metabolism ; Humans ; Female ; Infant ; Galactoside 2-alpha-L-fucosyltransferase
Chemical Substances	Fucosyltransferases (EC 2.4.1.-)
Language	English
Publishing date	2023-01-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2518386-2
ISSN	2072-6643 ; 2072-6643
ISSN (online)	2072-6643
ISSN	2072-6643
DOI	10.3390/nu15020471
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Article: Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans

Newburg, D.S

Journal of animal science. 2009 Apr., v. 87, no. 13_suppl

2009

Abstract	This review discusses the role of human milk glycans in protecting infants, but the conclusion that the human milk glycans constitute an innate immune system whereby the mother protects her offspring may have general applicability in all mammals, including species of commercial importance. Infants that are not breastfed have a greater incidence of severe diarrhea and respiratory diseases than those who are breastfed. In the past, this had been attributed primarily to human milk secretory antibodies. However, the oligosaccharides are major components of human milk, and milk is also rich in other glycans, including glycoproteins, mucins, glycosaminoglycans, and glycolipids. These milk glycans, especially the oligosaccharides, are composed of thousands of components. The milk factor that promotes gut colonization by Bifidobacterium bifidum was found to be a glycan, and such prebiotic characteristics may contribute to protection against infectious agents. However, the ability of human milk glycans to protect the neonate seems primarily to be due to their inhibition of pathogen binding to their host cell target ligands. Many such examples include specific fucosylated oligosaccharides and glycans that inhibit specific pathogens. Most human milk oligosaccharides are fucosylated, and their production depends on fucosyltransferase enzymes; mutations in these fucosyltransferase genes are common and underlie the various Lewis blood types in humans. Variable expression of specific fucosylated oligosaccharides in milk, also a function of these genes (and maternal Lewis blood type), is significantly associated with the risk of infectious disease in breastfed infants. Human milk also contains major quantities and large numbers of sialylated oligosaccharides, many of which are also present in bovine colostrum. These could similarly inhibit several common viral pathogens. Moreover, human milk oligosaccharides strongly attenuate inflammatory processes in the intestinal mucosa. These results support the hypothesis that oligosaccharides and other glycans are the major constituents of an innate immune system of human milk whereby the mother protects her infant from enteric and other pathogens through breastfeeding. These protective glycans may prove useful as a basis for the development of novel prophylactic and therapeutic agents that inhibit disease by mucosal pathogens in many species.
Keywords	Bifidobacterium bifidum ; antibodies ; blood groups ; breast feeding ; breast milk ; cow colostrum ; diarrhea ; enzymes ; genes ; glycolipids ; glycosaminoglycans ; humans ; immunity ; infectious diseases ; intestinal mucosa ; milk ; mucins ; mutation ; neonates ; oligosaccharides ; pathogens ; prebiotics ; progeny ; respiratory tract diseases ; risk
Language	English
Dates of publication	2009-04
Size	p. 26-34.
Publishing place	American Society of Animal Science
Document type	Article
ZDB-ID	390959-1
ISSN	1525-3163 ; 0021-8812
ISSN (online)	1525-3163
ISSN	0021-8812
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: A longitudinal study of human milk composition in the second year postpartum: implications for human milk banking.

Perrin, Maryanne T / Fogleman, April D / Newburg, David S / Allen, Jonathan C

Maternal & child nutrition

2016 Volume 13, Issue 1

Abstract: While the composition of human milk has been studied extensively in the first year of lactation, there is a paucity of data regarding human milk composition beyond one year postpartum. Policies vary at milk banks around the world regarding how long ... ...

Abstract	While the composition of human milk has been studied extensively in the first year of lactation, there is a paucity of data regarding human milk composition beyond one year postpartum. Policies vary at milk banks around the world regarding how long lactating women are eligible to donate their milk. The primary purpose of this study is to describe longitudinal changes in human milk composition in the second year postpartum to support the development of evidence based guidelines regarding how long lactating women can donate human milk to a milk bank. Nineteen lactating women in North Carolina provided monthly milk samples from 11 months to 17 months postpartum (N = 131), and two non-profit milk banks provided (N = 33) pooled, unpasteurized milk samples from 51 approved donors less than one year postpartum. There was a significant increase (P < 0.05) in the concentration of total protein, lactoferrin, lysozyme, Immunoglobulin A, oligosaccharides and sodium in longitudinal samples of mother's milk between 11 and 17 months postpartum, while zinc and calcium concentrations declined, and no changes were observed in lactose, fat, iron and potassium. Human milk in the second year postpartum contained significantly higher concentrations of total protein, lactoferrin, lysozyme and Immunoglobulin A, than milk bank samples, and significantly lower concentrations of zinc, calcium, iron and oligosaccharides. Accepting milk bank donations beyond one year postpartum is a potential strategy for increasing the supply of donor milk, but may require mineral fortification.
MeSH term(s)	Calcium/analysis ; Dietary Fats/analysis ; Female ; Humans ; Immunoglobulin A/analysis ; Iron/analysis ; Lactation ; Lactoferrin/analysis ; Lactose/analysis ; Longitudinal Studies ; Milk Banks ; Milk Proteins/analysis ; Milk, Human/chemistry ; Muramidase/analysis ; North Carolina ; Oligosaccharides/analysis ; Postpartum Period ; Potassium/analysis ; Time Factors ; Zinc/analysis
Chemical Substances	Dietary Fats ; Immunoglobulin A ; Milk Proteins ; Oligosaccharides ; Iron (E1UOL152H7) ; Muramidase (EC 3.2.1.17) ; Lactoferrin (EC 3.4.21.-) ; Lactose (J2B2A4N98G) ; Zinc (J41CSQ7QDS) ; Potassium (RWP5GA015D) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2016-01-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2175105-5
ISSN	1740-8709 ; 1740-8695
ISSN (online)	1740-8709
ISSN	1740-8695
DOI	10.1111/mcn.12239
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Article ; Online: Translational Proteomic Approach for Cholangiocarcinoma Biomarker Discovery, Validation, and Multiplex Assay Development: A Pilot Study.

Watcharatanyatip, Kamolwan / Chutipongtanate, Somchai / Chokchaichamnankit, Daranee / Weeraphan, Churat / Mingkwan, Kanokwan / Luevisadpibul, Virat / Newburg, David S / Morrow, Ardythe L / Svasti, Jisnuson / Srisomsap, Chantragan

Molecules (Basel, Switzerland)

2022 Volume 27, Issue 18

Abstract: Cholangiocarcinoma (CCA) is a highly lethal disease because most patients are asymptomatic until they progress to advanced stages. Current CCA diagnosis relies on clinical imaging tests and tissue biopsy, while specific CCA biomarkers are still lacking. ... ...

Abstract	Cholangiocarcinoma (CCA) is a highly lethal disease because most patients are asymptomatic until they progress to advanced stages. Current CCA diagnosis relies on clinical imaging tests and tissue biopsy, while specific CCA biomarkers are still lacking. This study employed a translational proteomic approach for the discovery, validation, and development of a multiplex CCA biomarker assay. In the discovery phase, label-free proteomic quantitation was performed on nine pooled plasma specimens derived from nine CCA patients, nine disease controls (DC), and nine normal individuals. Seven proteins (S100A9, AACT, AFM, and TAOK3 from proteomic analysis, and NGAL, PSMA3, and AMBP from previous literature) were selected as the biomarker candidates. In the validation phase, enzyme-linked immunosorbent assays (ELISAs) were applied to measure the plasma levels of the seven candidate proteins from 63 participants: 26 CCA patients, 17 DC, and 20 normal individuals. Four proteins, S100A9, AACT, NGAL, and PSMA3, were significantly increased in the CCA group. To generate the multiplex biomarker assays, nine machine learning models were trained on the plasma dynamics of all seven candidates (All-7 panel) or the four significant markers (Sig-4 panel) from 45 of the 63 participants (70%). The best-performing models were tested on the unseen values from the remaining 18 (30%) of the 63 participants. Very strong predictive performances for CCA diagnosis were obtained from the All-7 panel using a support vector machine with linear classification (AUC = 0.96; 95% CI 0.88-1.00) and the Sig-4 panel using partial least square analysis (AUC = 0.94; 95% CI 0.82-1.00). This study supports the use of the composite plasma biomarkers measured by clinically compatible ELISAs coupled with machine learning models to identify individuals at risk of CCA. The All-7 and Sig-4 assays for CCA diagnosis should be further validated in an independent prospective blinded clinical study.
MeSH term(s)	Bile Duct Neoplasms/pathology ; Bile Ducts, Intrahepatic/metabolism ; Bile Ducts, Intrahepatic/pathology ; Biomarkers, Tumor/metabolism ; Calgranulin B ; Cholangiocarcinoma/pathology ; Humans ; Lipocalin-2 ; Pilot Projects ; Prospective Studies ; Proteomics/methods
Chemical Substances	Biomarkers, Tumor ; Calgranulin B ; Lipocalin-2
Language	English
Publishing date	2022-09-11
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	1413402-0
ISSN	1420-3049 ; 1431-5165 ; 1420-3049
ISSN (online)	1420-3049
ISSN	1431-5165 ; 1420-3049
DOI	10.3390/molecules27185904
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Article: Introduction to the Macy-György award lecture.

Newburg, D S

Advances in experimental medicine and biology

2001 Volume 501, Page(s) 31–33

MeSH term(s)	Awards and Prizes ; History, 19th Century ; History, 20th Century ; Humans ; Hungary ; Lactation ; Milk, Human ; Societies, Medical ; United States
Language	English
Publishing date	2001
Publishing country	United States
Document type	Biography ; Historical Article ; Journal Article ; Portrait
ISSN	2214-8019 ; 0065-2598
ISSN (online)	2214-8019
ISSN	0065-2598
DOI	10.1007/978-1-4615-1371-1_3
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Article: Bioactive components of human milk: evolution, efficiency, and protection.

Newburg, D S

Advances in experimental medicine and biology

2001 Volume 501, Page(s) 3–10

MeSH term(s)	Biological Evolution ; Female ; Humans ; Immunity ; Infant ; Infant Food ; Infant Nutritional Physiological Phenomena ; Infant, Newborn ; Lactation ; Milk, Human/chemistry
Language	English
Publishing date	2001
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, P.H.S. ; Review
ISSN	2214-8019 ; 0065-2598
ISSN (online)	2214-8019
ISSN	0065-2598
DOI	10.1007/978-1-4615-1371-1_1
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