Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function
Open accessAbstract
OBJECTIVES: Human milk oligosaccharides (HMOs) are the third most abundant component of breast milk. Our laboratory has previously revealed gene clusters specifically linked to HMO metabolism in selected bifidobacteria isolated from fecal samples of infants. Our objective was to test the hypothesis that growth of selected bifidobacteria on HMO stimulates the intestinal epithelium. METHODS: Caco-2 and HT-29 cells were incubated with lactose (LAC)- or HMO-grown Bifidobacterium longum subsp infantis (B infantis) or B bifidum. Bacterial adhesion and translocation were measured by real-time quantitative polymerase chain reaction. Expression of pro- and anti-inflammatory cytokines and tight junction proteins was analyzed by real-time reverse transcriptase. Distribution of tight junction proteins was measured using immunofluorescent microscopy. RESULTS: We showed that HMO-grown B infantis had a significantly higher rate of adhesion to HT-29 cells compared with B bifidum. B infantis also induced expression of a cell membrane glycoprotein, P-selectin glycoprotein ligand-1. Both B infantis and B bifidum grown on HMO caused less occludin relocalization and higher expression of anti-inflammatory cytokine, interleukin-10 compared with LAC-grown bacteria in Caco-2 cells. B bifidum grown on HMO showed higher expression of junctional adhesion molecule and occludin in Caco-2 cells and HT-29 cells. There were no significant differences between LAC or HMO treatments in bacterial translocation. CONCLUSIONS: The study provides evidence for the specific relation between HMO-grown bifidobacteria and intestinal epithelial cells. To our knowledge, this is the first study describing HMO-induced changes in the bifidobacteria-intestinal cells interaction.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The probiotic organism Bifidobacterium longum subsp infantis has been shown to improve gut barrier integrity.
“The probiotic organism Bifidobacterium longum subsp infantis has been shown to improve gut barrier integrity [33] and reduce expression of inflammatory genes in intestinal epithelial cells [34].”
From Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms (2019) · cites this paper as [33]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Toll-like receptors in the induction of the innate immune response
Aderem, A. A., & Ulevitch, R. J. (2000) · Nature · doi:10.1038/35021228 · Cited by 3,047 · see citing works
Pinto, M. (1983) · HAL · Cited by 1,752 · see citing works
Zeißig, S., Bürgel, N., Günzel, D., Richter, J. F., Mankertz, J., Wahnschaffe, U., Kroesen, A. J., Zeitz, M., Fromm, M., & Schulzke, J. (2006) · Gut · doi:10.1136/gut.2006.094375 · Cited by 1,218 · see citing works
Physiology and function of the tight junction
Anderson, J. M., & Van Itallie, C. M. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002584 · Cited by 1,059 · see citing works
Oligosaccharides in Human Milk: Structural, Functional, and Metabolic Aspects
Kunz, C., Rudloff, S., Baier, W., Klein, N. J., & Ströbel, S. (2000) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.20.1.699 · Cited by 1,037 · see citing works
Proinflammatory Cytokines Disrupt Epithelial Barrier Function by Apoptosis-Independent Mechanisms
Bruewer, M., Luegering, A., Kucharzik, T. F., Parkos, C. A., Madara, J., Hopkins, A. M., & Nusrat, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.11.6164 · Cited by 897 · see citing works
Sela, D. A., Chapman, J., Adeuya, A., Kim, J., Chen, F., Whitehead, T. R., Lapidus, A. L., Rokhsar, D. S., Lebrilla, C. B., German, J. B., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809584105 · Cited by 884 · see citing works
Self-citationHuman milk glycobiome and its impact on the infant gastrointestinal microbiota
Zivkovic, A. M., German, J. B., Lebrilla, C. B., & Mills, D. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000083107 · Cited by 679 · see citing works
Self-citationResta-Lenert, S., & Barrett, K. E. (2003) · Gut · doi:10.1136/gut.52.7.988 · Cited by 642 · see citing works
Ewaschuk, J. B., Diaz, H., Meddings, L., Diederichs, B., Dmytrash, A., Backer, J., Looijer-van Langen, M., & Madsen, K. L. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90227.2008 · Cited by 590 · see citing works
Molecular Basis of Epithelial Barrier Regulation
Turner, J. R. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.060681 · Cited by 542 · see citing works
Haller, D., Bode, C., Hammes, W. P., Pfeifer, A. M. A., Schiffrin, E. J., & Blum, S. (2000) · Gut · doi:10.1136/gut.47.1.79 · Cited by 466 · see citing works
Quality assurance criteria for probiotic bacteria
Tuomola, E., Crittenden, R. G., PLAYNE, M. J., Isolauri, E., & Salminen, S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.393s · Cited by 432 · see citing works
Zyrek, A. A., Cichon, C., Helms, S., Enders, C., Sonnenborn, U., & Schmidt, M. A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00836.x · Cited by 427 · see citing works
Seth, A., Yan, F., Polk, D. B., & Rao, R. K. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00202.2007 · Cited by 404 · see citing works
Candela, M., Perna, F., Carnevali, P., Vitali, B., Ciati, R., Gionchetti, P., Rizzello, F., Campieri, M., & Brigidi, P. (2008) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2008.04.012 · Cited by 400 · see citing works
Bernet‐Camard, M., Brassart, D., Neeser, J., & Servin, A. L. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.12.4121-4128.1993 · Cited by 381 · see citing works
LoCascio, R. G., Ninonuevo, M. R., Freeman, S. L., Sela, D. A., Grimm, R., Lebrilla, C. B., Mills, D. A., & German, J. B. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0710480 · Cited by 365 · see citing works
Self-citationInflammatory bowel disease is associated with changes of enterocytic junctions
Gaßler, N., Rohr, C. M., Schneider, A., Kartenbeck, J., Bach, A., Obermüller, N., Otto, H. F., & Autschbach, F. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.281.1.g216 · Cited by 363 · see citing works
Schiffrin, E., Brassart, D., Servin, A., Rochat, F., & Donnet-Hughes, A. (1997) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/66.2.515s · Cited by 354 · see citing works
Prebiotics and synbiotics: concepts and nutritional properties
Roberfroid, M. B. (1998) · British Journal Of Nutrition · doi:10.1017/s0007114500006024 · Cited by 347 · see citing works
Zweibaum, A., Pinto, M., Chevalier, G., Dussaulx, E., Triadou, N., Lacroix, B. D., HAFFEN, K., Brun, J.-F., & Rousset, M. (1985) · Journal of Cellular Physiology · doi:10.1002/jcp.1041220105 · Cited by 341 · see citing works
Resta‐Lenert, S. C., & Barrett, K. E. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.12.015 · Cited by 308 · see citing works
Mahler, G. J., Shuler, M. L., & Glahn, R. P. (2008) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2008.05.006 · Cited by 289 · see citing works
O’Hara, A. M., O'Regan, P., Fanning, A., O’Mahony, C., MacSharry, J. A., Lyons, A., Bienenstock, J., O’Mahony, L., & Shanahan, F. (2006) · Immunology · doi:10.1111/j.1365-2567.2006.02358.x · Cited by 283 · see citing works
Ward, R. E., Niñonuevo, M. R., Mills, D. A., Lebrilla, C. B., & German, J. B. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.02515-05 · Cited by 280 · see citing works
Self-citationBarrangou, R., Altermann, E., Hutkins, R. W., Cano, R. J., & Klaenhammer, T. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1332765100 · Cited by 269 · see citing works
Surface Properties of Bifidobacterial Strains of Human Origin
Pérez, P. F., Minnaard, Y., Disalvo, E. A., & Antoni, G. L. D. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.1.21-26.1998 · Cited by 268 · see citing works
Katayama, T., Sakuma, A., Kimura, T., Makimura, Y., Hiratake, J., Sakata, K., Yamanoi, T., Kumagai, H., & Yamamoto, K. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.15.4885-4893.2004 · Cited by 263 · see citing works
In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria
Ward, R. E., Niñonuevo, M. R., Mills, D. A., Lebrilla, C. B., & German, J. B. (2007) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200700150 · Cited by 239 · see citing works
Self-citationGerman, J. B., Freeman, S. L., Lebrilla, C. B., & Mills, D. A. (2008) · Nestlé Nutrition Workshop series. Pediatric program/Nestlé Nutrition Workshop series. Paediatric program · doi:10.1159/000146322 · Cited by 238 · see citing works
Self-citationLoCascio, R. G., Desai, P., Sela, D. A., Weimer, B., & Mills, D. A. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00675-10 · Cited by 229 · see citing works
Position of the American Dietetic Association: Promoting and Supporting Breastfeeding
James, D. C. S., & Dobson, B. (2005) · Journal of the American Dietetic Association · doi:10.1016/j.jada.2005.03.015 · Cited by 223 · see citing works
He, F., Ouwehand, A. C., Isolauri, E., Hashimoto, H., Benno, Y., & Salminen, S. (2001) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2001.tb01548.x · Cited by 220 · see citing works
Garrido, D. A., Kim, J., German, J. B., Raybould, H. E., & Mills, D. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017315 · Cited by 218 · see citing works
Self-citationBifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis
Khailova, L. S., Dvorak, K., Arganbright, K. M., Halpern, M. D., Kinouchi, T., Yajima, M., & Dvořák, B. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00141.2009 · Cited by 199 · see citing works
An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides
Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., Chen, X., Lebrilla, C. B., & Mills, D. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.193359 · Cited by 192 · see citing works
Increased Proteasome-Mediated Degradation of Occludin in Irritable Bowel Syndrome
Coëffier, M., Gloro, R., Boukhettala, N., Aziz, M., Lecleire, S., Vandaele, N., Antonietti, M., Savoye, G., Bôle-Feysot, C., Déchelotte, P., et al. (2010) · American Journal of Gastroenterology · doi:10.1038/ajg.2009.700 · Cited by 185 · see citing works
The Influence of Milk Oligosaccharides on Microbiota of Infants: Opportunities for Formulas
Chichlowski, M., German, J. B., Lebrilla, C. B., & Mills, D. A. (2011) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-022510-133743 · Cited by 174 · see citing works
Self-citationClark, E. C., Hoare, C. J., Tanianis-Hughes, J., Carlson, G., & Warhurst, G. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.01.046 · Cited by 171 · see citing works
Bode, L., Rudloff, S., Kunz, C., et al. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0304198 · Cited by 166 · see citing works
Functional cell models of the gut and their applications in food microbiology — A review
Čenčič, A., & Langerholc, T. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.03.026 · Cited by 166 · see citing works
Position of the American Dietetic Association: Promoting and Supporting Breastfeeding
(2009) · Journal of the American Dietetic Association · doi:10.1016/j.jada.2009.09.018 · Cited by 162 · see citing works
LoCascio, R. G., Niñonuevo, M. R., Kronewitter, S. R., Freeman, S. L., German, J. B., Lebrilla, C. B., & Mills, D. A. (2008) · Microbial Biotechnology · doi:10.1111/j.1751-7915.2008.00072.x · Cited by 140 · see citing works
Self-citationGuglielmetti, S., Tamagnini, I., Mora, D., Minuzzo, M., Scarafoni, A., Arioli, S., Hellman, J., Karp, M., & Parini, C. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00124-08 · Cited by 128 · cited 2× · see citing works
“For example, researchers noticed minimal impact of probiotic strains B animalis subsp lactis Bb12 and, to a lesser extent, B longum NCC2705 (60) on the cytokine expression induction.”
BackgroundResultLi, Q., Zhang, Q., Wang, M., Zhao, S., Ma, J., Luo, N., Li, N., Li, Y., Xu, G., & Li, J. (2007) · Clinical Immunology · doi:10.1016/j.clim.2007.08.017 · Cited by 126 · see citing works
Adhesion of Lactic Acid Bacteria to Caco‐2 Cells and Their Effect on Cytokine Secretion
Morita, H., He, F., Fuse, T., Ouwehand, A. C., Hashimoto, H., Hosoda, M., Mizumachi, K., & Kurisaki, J. (2002) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2002.tb02698.x · Cited by 121 · see citing works
Moroni, O., Kheadr, E., Boutin, Y., Lacroix, C., & Fliss, I. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00928-06 · Cited by 116 · see citing works
Ciccocioppo, R., Finamore, A., Ara, C., Sabatino, A. D., Mengheri, E., & Corazza, G. R. (2006) · American Journal of Clinical Pathology · doi:10.1309/dtyr-a91g-8r0k-tm8m · Cited by 116 · see citing works
Grimoud, J., Durand, H., Souza, S. D. M. P., MONSAN, P. F., Ouarné, F., Théodorou, V., & Roques, C. G. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.09.007 · Cited by 114 · see citing works
Bacterial-mucosal interactions in inflammatory bowel disease—an alliance gone bad
Chichlowski, M., & Hale, L. P. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90516.2008 · Cited by 114 · see citing works
Self-citationCalcium, Iron, and Zinc Uptake from Digests of Infant Formulas by Caco-2 Cells
Jovaní, M., Barberá, R., FARRÉ, R., et al. (2001) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf010106t · Cited by 110 · see citing works
Parlesak, A., Haller, D., Brinz, S., Baeuerlein, A., & Bode, C. (2004) · Scandinavian Journal of Immunology · doi:10.1111/j.0300-9475.2004.01495.x · Cited by 109 · see citing works
Crociani, J., Grill, J.-P., Huppert, M., & Ballongue, J. (1995) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.1995.tb01027.x · Cited by 109 · see citing works
Gnoth, M. J., Rudloff, S., Kunz, C., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104805200 · Cited by 107 · see citing works
In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin
Gagnon, M., Kheadr, E., Blay, G. L., & Fliss, I. (2003) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2003.07.010 · Cited by 106 · see citing works
Nakamura, N., Gaskins, H. R., Collier, C. T., Nava, G. M., Rai, D., Petschow, B. W., Russell, W. M., Harris, C. L., Mackie, R. I., Wampler, J. L., et al. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02359-07 · Cited by 95 · see citing works
Ciccocioppo, R., Finamore, A., Ara, C., et al. (2006) · American Journal of Clinical Pathology · doi:10.1309/dtyra91g8r0ktm8m · Cited by 93 · see citing works
Erickson, A. K., Willgohs, J. A., McFARLAND, S. Y., et al. (1992) · Infection and Immunity · doi:10.1128/iai.60.3.983-988.1992 · Cited by 92 · see citing works
Volatile Fatty Acids, Lactic Acid, and pH in the Stools of Breast-Fed and Bottle-Fed Infants
Ogawa, K., Ben, R. A., Pons, S., Paolo, M. I. L., & Fernández, L. B. (1992) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199210000-00004 · Cited by 90 · see citing works
Candela, M., Seibold, G. M., Vitali, B., Lachenmaier, S., Eikmanns, B. J., & Brigidi, P. (2005) · Research in Microbiology · doi:10.1016/j.resmic.2005.04.006 · Cited by 84 · see citing works
Tanabe, S. (1998) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000006 · Cited by 76 · see citing works
Preising, J., Philippe, D., Gleinser, M., Wei, H., Blum, S., Eikmanns, B. J., Niess, J. H., & Riedel, C. U. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.03127-09 · Cited by 76 · see citing works
Mass spectrometric methods for analysis of oligosaccharides in human milk
Niñonuevo, M. R., & Lebrilla, C. B. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.2009.00243.x · Cited by 74 · see citing works
Niñonuevo, M. R., Ward, R. E., LoCascio, R. G., German, J. B., Freeman, S. L., Barboza, M., Mills, D. A., & Lebrilla, C. B. (2006) · Analytical Biochemistry · doi:10.1016/j.ab.2006.11.010 · Cited by 71 · see citing works
Self-citationSheil, B., MacSharry, J. A., O'Callaghan, L., O'Riordan, A., Waters, A., Morgan, J. G., Collins, J. K., O’Mahony, L., & Shanahan, F. (2006) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2006.03051.x · Cited by 70 · see citing works
Quigley, E. M. M. (2011) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2010.12.009 · Cited by 67 · see citing works
Cluster Analysis Defines Distinct Dietary Patterns for African-American Men and Women
James, D. C. S. (2009) · Journal of the American Dietetic Association · doi:10.1016/j.jada.2008.10.052 · Cited by 65 · see citing works
Interaction of bifidobacteria with Caco-2 cells—adhesion and impact on expression profiles
Riedel, C. U., Foata, F., Goldstein, D. R., Blum, S., & Eikmanns, B. J. (2006) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2006.01.040 · Cited by 58 · see citing works
Pozo-Rubio, T., Mujico, J. R., Marcos, A., Puertollano, E., Nadal, I., Sanz, Y., & Nova, E. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511001656 · Cited by 36 · see citing works
Bifidobacterium breve – HT-29 cell line interaction: modulation of TNF-α induced gene expression
Boesten, R. J., Schuren, F. H. J., Willemsen, L. E. M., Vriesema, A. J. M., Knol, J., & Vos, W. H. D. (2011) · Beneficial Microbes · doi:10.3920/bm2011.0005 · Cited by 20 · see citing works
Butyrate and the cytokine‐induced α1‐proteinase inhibitor release in intestinal epithelial cells
Faust, D., Hormann, S., Friedrich-Sander, M., et al. (2001) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.2001.00927.x · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., Belzer, C., Delgado Palacio, S., Arboleya Montes, S., Mancabelli, L., et al. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-17 · Cited by 1,950 · see citing works
Development of the gut microbiota in infancy and its impact on health in later life
Tanaka, M., & Nakayama, J. (2017) · Allergology International · doi:10.1016/j.alit.2017.07.010 · Cited by 639 · see citing works
Breast milk, a source of beneficial microbes and associated benefits for infant health
Lyons, K. E., Ryan, C. A., Dempsey, E. M., Ross, R. P., & Stanton, C. (2020) · Nutrients · doi:10.3390/nu12041039 · Cited by 613 · see citing works
Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut
Underwood, M. A., German, J. B., Lebrilla, C. B., & Mills, D. A. (2015) · Pediatric Research · doi:10.1038/pr.2014.156 · Cited by 439 · see citing works
Self-citationBreast milk oligosaccharides: structure-function relationships in the neonate
Smilowitz, J. T., Lebrilla, C. B., Mills, D. A., German, J. B., & Freeman, S. L. (2014) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071813-105721 · Cited by 410 · see citing works
The Human Gut Microbiome and Body Metabolism: Implications for Obesity and Diabetes
Devaraj, S., Hemarajata, P., & Versalovic, J. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.187617 · Cited by 321 · see citing works
Sanctuary, M. R., Kain, J. N., Chen, S. Y., Kalanetra, K., Lemay, D. G., Rose, D. R., Yang, H. T., Tancredi, D. J., German, J. B., Slupsky, C. M., et al. (2019) · PLOS ONE · doi:10.1371/journal.pone.0210064 · Cited by 255 · see citing works
Self-citationFrese, S. A., Hutton, A. A., Contreras, L. N., Shaw, C. A., Palumbo, M. C., Casaburi, G., Xu, G., Davis, J. C. C., Lebrilla, C. B., Henrick, B. M., et al. (2017) · mSphere · doi:10.1128/msphere.00501-17 · Cited by 231 · see citing works
Self-citationGarrido, D., Dallas, D. C., & Mills, D. A. (2013) · Microbiology · doi:10.1099/mic.0.064113-0 · Cited by 228 · see citing works
Human milk and related oligosaccharides as prebiotics
Barile, D., & Rastall, R. A. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.01.008 · Cited by 193 · see citing works
Role of gut microbiota in intestinal wound healing and barrier function
Alam, A., & Neish, A. (2018) · Tissue Barriers · doi:10.1080/21688370.2018.1539595 · Cited by 166 · see citing works
Initial Intestinal Colonization in the Human Infant and Immune Homeostasis
Walker, W. A. (2013) · Annals of Nutrition and Metabolism · doi:10.1159/000354907 · Cited by 161 · see citing works
Validating bifidobacterial species and subspecies identity in commercial probiotic products
Lewis, Z. T., Shani, G., Masarweh, C. F., Popovic, M., Frese, S. A., Sela, D. A., Underwood, M. A., & Mills, D. A. (2016) · Pediatric Research · doi:10.1038/pr.2015.244 · Cited by 154 · see citing works
Self-citationA molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract
Garrido, D., Barile, D., & Mills, D. A. (2012) · Advances in Nutrition · doi:10.3945/an.111.001586 · Cited by 149 · see citing works
Self-citationUnderwood, M. A., Arriola, J., Gerber, C. W., Kaveti, A., Kalanetra, K. M., Kananurak, A., Bevins, C. L., Mills, D. A., & Dvorak, B. (2014) · Pediatric Research · doi:10.1038/pr.2014.102 · Cited by 107 · see citing works
Self-citationWickramasinghe, S., Pacheco, A. R., Lemay, D. G., & Mills, D. A. (2015) · BMC Microbiology · doi:10.1186/s12866-015-0508-3 · Cited by 86 · see citing works
Self-citationSegui-Perez, C., Huang, L. Z. X., Paganelli, F. L., Lievens, E., & Strijbis, K. (2025) · Scientific Reports · doi:10.1038/s41598-025-92125-2 · Cited by 45 · see citing works
The complex link and disease between the gut microbiome and the immune system in infants
Zhang, H., Zhang, Z., Liao, Y., Zhang, W., & Tang, D. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.924119 · Cited by 45 · see citing works
Gallier, S., Van den Abbeele, P., & Prosser, C. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.608495 · Cited by 38 · see citing works
Nam, B., Kim, S. A., Park, S. D., Kim, H. J., Kim, J. S., Bae, C. H., Kim, J. Y., Nam, W., Lee, J. L., & Sim, J. H. (2020) · PLOS ONE · doi:10.1371/journal.pone.0231268 · Cited by 35 · see citing works
Breastfeeding and early Bifidobacterium-driven microbial colonization shape the infant gut resistome
Samarra, A., Alcañiz, A. J., Martínez-Costa, C., Marina, A., Comas, I., Segata, N., Quijada, N. M., & Collado, M. C. (2025) · Nature Communications · doi:10.1038/s41467-025-61154-w · Cited by 32 · see citing works
- Authors
- Chichlowski, M., De Lartigue, G., German, J. B., Raybould, H. E., & Mills, D. A.
- Affiliations
- University of California, Davis (US)
- Foods for Health Institute University of California Davis CA
- Corresponding author
- Mills, David A.
- Venue
- Journal of Pediatric Gastroenterology and Nutrition
- Publisher
- Wiley
- Published
- 2012-09
- Volume
- 55
- Issue
- 3
- Pages
- 321-327
- ISSN
- 0277-2116 (ISSN-L)
- 1536-4801
- PMC
- PMC3381975
- OpenAlex
- W2017988783
- Cited by
- 276
- References
- 72
- Citations by year
- 2026: 13 · 2025: 15 · 2024: 24 · 2023: 23 · 2022: 26 · 2021: 23 · 2020: 30 · 2019: 16 · 2018: 21 · 2017: 21 · 2016: 11 · 2015: 17 · 2014: 18 · 2013: 14 · 2012: 3
- FWCI
- 15.46
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Pediatric Gastroenterology and Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- California Dairy Research Foundation
- National Institute of Environmental Health Sciences (P42 ES02710)
- National Institutes of Health (R01HD059127, R01HD061923, R21AT006180)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- human milk oligosaccharides, Bifidobacterium, Bifidobacterium longum subsp. infantis, Bifidobacterium bifidum, intestinal epithelial cells, bacterial adhesion, bacterial translocation, tight junction proteins, occludin, PSGL-1, IL-10, anti-inflammatory cytokines, lactose, infants, gut microbiota
- MeSH terms
- Bacterial Adhesion, Bifidobacterium, Cell Membrane, Colon, Culture Media, Humans, Intestinal Mucosa, Membrane Glycoproteins, Milk, Human, Oligosaccharides, Interleukin-10, Caco-2 Cells, HT29 Cells, Junctional Adhesion Molecules, Occludin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review