The Protective Influence of Chondroitin Sulfate,a Component of Human Milk,on Intestinal Bacterial Invasion and Translocation

Abrams S. A. Schanler R. J. Lee M. L. Rechtman D. J. (2014). Greater mortality and morbidity in extremely preterm infants fed a diet containing cow milk protein products. Breastfeeding Medicine: The Official Journal of the Academy of Breastfeeding Medicine, 9(6), 281–285.

Adan A. Kiraz Y. Baran Y. (2016). Cell proliferation and cytotoxicity assays. Current Pharmaceutical Biotechnology, 17(14), 1213–1221.

Ade-Ajayi N. Spitz L. Kiely E. Drake D. Klein N. (1996). Intestinal glycosaminoglycans in neonatal necrotizing enterocolitis. The British Journal of Surgery, 83(3), 415–418.

Alex M. J. Periasamy P. Mohan K. Sekar S. Prabha K. K. Venkatachalam R. (2016). In situ synthesized TiO2-chitosan-chondroitin 4-sulphate nanocomposites for bone implant applications. IET Nanobiotechnology, 10(3), 107–113.

Andreas N. J. Kampmann B. Le-Doare K. M. (2015). Human breast milk: A review on its composition and bioactivity. Early Human Development, 91(11), 629–635.

Ardizzoni A. Neglia R. G. Baschieri M. C. Cermelli C. Caratozzolo M. Righi E. . . . Blasi E. (2011). Influence of hyaluronic acid on bacterial and fungal species, including clinically relevant opportunistic pathogens. Journal of Materials Science—Materials in Medicine, 22(10), 2329–2338.

Benkoe T. Reck C. Pones M. Weninger M. Gleiss A. Stift A. Rebhandl W. (2014). Interleukin-8 predicts 60-day mortality in premature infants with necrotizing enterocolitis. Journal of Pediatric Surgery, 49(3), 385–389.

Bischoff S. C. Barbara G. Buurman W. Ockhuizen T. Schulzke J. D. Serino M. . . . Wells J. M. (2014). Intestinal permeability—a new target for disease prevention and therapy. BMC Gastroenterology, 14, 189. doi:10.1186/s12876-014-0189-7.

Bishnoi M. Jain A. Hurkat P. Jain S. K. (2016). Chondroitin sulphate: A focus on osteoarthritis. Glycoconjugate Journal, 33(5), 693–705.

Cacho N. T. Parker L. A. Neu J. (2017). Necrotizing enterocolitis and human milk feeding: A systematic review. Clinics in Perinatology, 44(1), 49–67.

Carlson G. A. Dragoo J. L. Samimi B. Bruckner D. A. Bernard G. W Hedrick M. Benhaim P. (2004). Bacteriostatic properties of biomatrices against common orthopaedic pathogens. Biochemical and Biophysical Research Communications, 321(2), 472–478.

Canil C. Rosenshine I. Ruschkowski S. Donnenberg M. S. Kaper J. B. Finlay B. B. (1993). Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infection and Immunity, 61(7), 2755–2762.

Caron T. J. Scott K. E. Fox J. G. Hagen S. J. (2015). Tight junction disruption: Helicobacter pylori and dysregulation of the gastric mucosal barrier. World Journal of Gastroenterology, 21(40), 11411–11427.

Cartmell A. Lowe E. C. Baslé A. Firbank S. J. Ndeh D. A. Murray H. . . . Bolam D.N. (2017). How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans. Proceedings of the National Academy of Sciences of the United States of America, 114(27), 7037–7042.

Chavez-Bueno S. Day M. W. Toby I. T. Akins D. R. Dyer D. W. (2014). Genome sequence of SCB34, a sequence type 131 multidrug-resistant Escherichia coli isolate causing neonatal early-onset sepsis. Genome Announcements, 2(3), e00514-14. doi:10.1128/genomeA.00514-14

Cho S. X. Berger P. J. Nold-Petry C. A. Nold M. F. (2016). The immunological landscape in necrotising enterocolitis. Expert Reviews in Molecular Medicine, 18, E12. doi:10.1017/erm.2016.13

Ciani O. Arendsen E. Romancik M. Lunik R. Costantini E. Di Biase M. . . . Lazzeri M. (2016). Intravesical administration of combined hyaluronic acid (HA) and chondroitin sulfate (CS) for the treatment of female recurrent urinary tract infections: A European multicenter nested case-control study. BMJ Open, 6(3), E009669. doi:10.1136/bmjopen-2015-009669

Coppa G. V. Facinelli B. Magi G. Marini E. Zampini L. Mantovani V. . . . Gabrielli O. (2016). Human milk glycosaminoglycans inhibit in vitro the adhesion of Escherichia coli and Salmonella fyris to human intestinal cells. Pediatric Research, 79(4), 603–607.

Coppa G.V. Gabrielli O. Bertino E. Zampini L. Galeazzi T. Padella L. . . . Volpi N. 2013. Human milk glycosaminoglycans: The state of the art and future perspectives. Italian Journal of Pediatrics, 39. doi:10.1186/1824-7288-39-2

Coppa G. V. Gabrielli O. Buzzega D. Zampini L. Galeazzi T. Maccari F. . . . Volpi N. (2011). Composition and structure elucidation of human milk glycosaminoglycans. Glycobiology, 21(3), 295–303.

Coppa G. V. Gabrielli O. Zampini L. Galeazzi T. Maccari F. Buzzega D. . . . Volpi N. (2012). Glycosaminoglycan content in term and preterm milk during the first month of lactation. Neonatology, 101(1), 74–76.

Coppa G. V. Zampini L. Galeazzi T. Facinelli B. Ferrante L. Capretti R. Gabrielli O. (2006). Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholera and Salmonella fyris. Pediatric Research, 59(3), 377–382.

Devriese S. Van den Bossche L. Van Welden S. Holvoet T. Pinheiro I. Hindryckx P. . . . Laukens D. (2017). T84 monolayers are superior to Caco-2 as a model system of colonocytes. Histochemistry and Cell Biology, 148(1), 85–93.

Dharmsathaphorn K. Madara J. L. (1990). Established intestinal cell lines as model systems for electrolyte transport studies. Methods in Enzymology, 192, 354–389.

Dharmsathaphorn K. McRoberts J. A. Mandel K. G. Tisdale L. D. Masui H. (1984). A human colonic tumor cell line that maintains vectoral electrolyte transport. The American Journal of Physiology—Gastrointestinal and Liver Physiology, 246, G204–G208.

du Souich P. Garcia A. G. Verges J. Montell E . (2009). Immunomodulatory and anti-inflammatory effects of chondroitin sulfate. Journal of Cellular and Molecular Medicine, 13(8A), 1451–1463.

Eckmann L. Kagnoff M. F. Fierer J. (1993). Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infection and Immunity, 61(11), 4569–4574.

Egea J. Garcia A. G. Verges J. Montell E. Lopez M. G. (2010). Antioxidant anti-inflammatory and neuroprotective actions of chondroitin sulfate and proteoglycans [Supplemental material]. Osteoarthritis and Cartilage, 18, S24–S27.

Eichner M. Protze J. Piontek A. Krause G. Piontek J. (2017). Targeting and alteration of tight junctions by bacteria and their virulence factors such as Clostridium perfringens enterotoxin. European Journal of Physiology, 469(1), 77–90.

Francescone R. Hou V. Grivennikov S. I. (2015). Cytokines, IBD, and colitis-associated cancer. Inflammatory Bowel Diseases, 21(2), 409–418.

Fukui H. (2016). Increased intestinal permeability and decreased barrier function: Does it really influence the risk of inflammation? Inflammatory Intestinal Diseases, 1(3), 135–145.

GraphPad Software, Inc. (2015). Prism 6 for Windows (version 6.07) [Computer software]. Retrieved from www.graphpad.com.

Grulee C. G. Sanford H. N. Herron P. H. (1934). Breast and artificial feeding: Influence on morbidity and mortality of twenty thousand infants. JAMA: The Journal of the American Medical Association, 103(10), 735–738.

Hafez M. M. Aboulwafa M. M. Yassien M. A. Hassouna N. A. (2008). Role of different classes of mammalian cell surface molecules in adherence of coagulase positive and coagulase negative staphylococci. Journal of Basic Microbiology, 48(5), 353–362.

Hall T. Dymock D. Corfield A. P. Weaver G. Woodward M. Berry M. (2013). Bacterial invasion of HT29-MTX-E12 monolayers: Effects of human breast milk. Journal of Pediatric Surgery, 48(2), 353–358.

Henrotin Y. Mathy M. Sanchez C. Lambert C. (2010). Chondroitin sulfate in the treatment of osteoarthritis: From in vitro studies to clinical recommendations. Therapeutic Advances in Musculoskeletal Disease, 2(6), 335–348.

Hong L. Jing W. Qing W. Anxiang S. Mei X. Qin L. Qiuhui H. (2017). Inhibitory effect of Zanthoxylum bungeanum essential oil (ZBEO) on Escherichia coli and intestinal dysfunction. Food & Function, 8(4), 1569–1576.

Howie P. W. Forsyth J. S. Ogston S. A. Clark A. Florey C. D. (1990). Protective effect of breast feeding against infection. The BMJ, 300(6717), 11–16.

Jomphe C. Gabriac M. Hale T. M. Heroux L. Trudeau L. E. Deblois D. . . . du Souich P. (2008). Chondroitin sulfate inhibits the nuclear translocation of nuclear factor-kappaB in interleukin-1beta-stimulated chondrocytes. Basic & Clinical Pharmacology & Toxicology, 102(1), 59–65.

Kalayci M. Kocdor M. A. Kuloglu T. Sahin İ. Sarac M. Aksoy A. . . . Aydin S. (2017). Comparison of the therapeutic effects of sildenafil citrate, heparin and neuropeptides in a rat model of acetic acid-induced gastric ulcer. Life Sciences, 186, 102–110.

Kim Y. Kessler S. P. Obery D. R. Homer C. R. McDonald C. de la Motte C. A. (2017). Hyaluronan 35kDa treatment protects mice from Citrobacter rodentium infection and induces epithelial tight junction protein ZO-1 in vivo. Matrix Biology: Journal of the International Society for Matrix Biology, 62, 28–39.

Klein N. J. Shennan G. I. Heyderman R.S. Levin M. (1992). Alteration in glycosaminoglycan metabolism and surface charge on human umbilical vein endothelial cells induced by cytokines, endotoxin and neutrophils. Journal of Cell Science, 102, 821–832.

Kong B. S. Kim Y. Kim G. Y. Hyun J. W. Kim S. H. Jeong A. Kim H. J. (2017). Increased frequency of IL-6-producing non-classical monocytes in neuormyelitis optica spectrum disorder. Journal of Neuroinflammation, 14(1), 191. doi:10.1186/s12974-017-0961-z

Lean Q. Y. Gueven N. Eri R. D. Bhatia R. Sohal S. S. Stewart N. . . . Patel R. P. (2015). Heparins in ulcerative colitis: proposed mechanisms of action and potential reasons for inconsistent clinical outcomes. Expert Review of Clinical Pharmacology, 8(6), 795–811.

Lim J. C. Golden J. M. Ford H.R. (2015). Pathogenesis of neonatal necrotizing enterocolitis. Pediatric Surgery International, 31(6), 509–518.

Linares P. M. Chaparro M. Algaba A. Román M. Moreno Arza I. Abad Santos F. . . . Gisbert J. P. (2015). Effect of chondroitin sulphate on pro-inflammatory mediators and disease activity in patients with inflammatory bowel disease. Digestion, 92(4), 203–210.

Ling K.-H. Wan M. L. Y. El-Nezami H. Wang M. (2016). Protective capacity of resveratrol, a natural polyphenolic compound, against deoxynivalenol-induced intestinal barrier dysfunction and bacterial translocation. Chemical Research in Toxicology, 29, 823–833.

Mannello F. Maccari F. Santinelli A. Volpi N. (2011). Chondroitin sulfate structure is modified in human milk produced by breast affected by invasive carcinoma. Breast, 20(6), 586–587.

Martel-Pelletier J. Farran A. Montell E. Verges J. Pelletier J. P. (2015). Discrepancies in composition and biological effects of different formulations of chondroitin sulfate. Molecules, 20(3), 4277–4289.

Mikami T. Kitagawa H. (2017). Sulfated glycosaminoglycans: Their distinct roles in stem cell biology. Glycoconjugate Journal, 34(6), 725–735.

Misaki N. Kawano O. Uchida M. Matsueda K. Muraoka A. Umeda N. (1989). Role of the mucus gel layer in the healing of acetic acid-induced gastric ulcers in rats. Scandinavian Journal of Gastroenterology, 24(162), 158–161.

Monfort J. Martel-Pelletier J. Pelletier P. (2008). Chondroitin sulphate for symptomatic osteoarthritis: critical appraisal of meta-analyses. Current Medical Research and Opinion, 24(5), 1303–1308.

Monteville M. R. Konkel M. E. (2002). Fibronectin-facilitated invasion of T84 eukaryotic cells by Campylobacter jejuni occurs preferentially at the basolateral cell surface. Infection and Immunity, 70(12), 6665–6671.

Murch S. H. MacDonald T. T. Walker-Smith J. A. Levin M. Lionetti P. Klein N. J. (1993). Disruption of sulphated glycosaminoglycans in intestinal inflammation. Lancet, 341(8847), 711–714.

Newburg D. S. (2009). Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. Journal of Animal Science, 87(13), 26–34.

Newburg D. S. Linhardt R. J. Ampofo S. A. Yolken R. H. (1995). Human milk glycosaminoglycans inhibit HIV gp120 binding to its host cell CD4 receptor. The Journal of Nutrition, 125(3), 419–424.

Niño D. F. Sodhi C. P. Hackam D. J. (2016). Necrotizing enterocolitis: new insights into pathogenesis and mechanisms. Nature Reviews. Gastroenterology and Hepatology, 13(10), 590–600.

Nusrat A. Parkos C. A. Verkade P. Foley C. S. Liang T. W. Innis-Whitehouse W. . . . Madara J. L. (2000). Tight junctions are membrane microdomains. Journal of Cell Science, 113(pt. 10), 1771–1781.

Philpott D. McKay D. M. Sherman P. M. Perdue M. H. (1996). Infection of T84 cells with enteropathogenic Escherichia coli alters barrier and transport. American Journal of Physiology—Gastroenterology and Liver Physiology, 270, G634–G645.

Pirnazar P. Wolinsky L. Nachnani S. Haake S. Pilloni A. Bernard G. W. (1999). Bacteriostatic effects of hyaluronic acid. Journal of Periodontology, 70(4), 370–374.

Pomin V. H. (2015). Sulfated glycans in inflammation. European Journal of Medicinal Chemistry, 92, 353–369.

Poterucha T. J. Libby P. Goldhaber S. Z. (2017). More than an anticoagulant: Do heparins have direct anti-inflammatory effects? Thrombosis and Haemostasis, 117(3), 437–444.

Prasad S. Mingrino R. Kaukinen K. Hayes K. L. Powell R. M. MacDonald T. T. Collins J. E. (2005). Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Laboratory Investigation: A Journal of Technical Methods and Pathology, 85(9), 1139–1162.

Ricard-Blum S. (2017). Glycosaminoglycans: Major biological players. Glycoconjugate Journal, 34(3), 275–276.

Rich B. S. Dolgin S. E. (2017). Necrotizing enterocolitis. Pediatrics in Review, 38(12), 552–559.

Rooney P. Srivastava A. Watson L. Quinlan L. R. Pandit A. (2015). Hyaluronic acid decreases IL-6 and IL-8 secretion and permeability in an inflammatory model of interstitial cystitis. Acta Biomaterialia, 19, 66–75.

Roughley P. J. Mort J. S. (2000). Catabolism of proteoglycans. In Iozzo R. V. (Ed.), Proteoglycans: Structure, biology and molecular interactions (pp. 93–113). New York, New York: Marcel Dekker Inc.

Rozin A. P. Goldstein M. Sprecher H. (2008). Antibacterial activity of glucosamine sulfate and chondroitin sulfate? Clinical and Experimental Rheumatology, 26(3), 509–510.

Sabharwal H. Cichon C. Ölschläger T. A. Sonnenborn U. Schmidt M. A. (2016). Interleukin-8, CXCL1, and microRNA miR-146a responses to probiotic Escherichia coli Nissle 1917 and enteropathogenic E. coli in human intestinal epithelial T84 and monocytic THP-1 cells after apical or basolateral infection. Infection and Immunity, 84(9), 2482–2492.

Sakaguchi T. Köhler H. Gu X. McCormick B. A. Reinecker H.-C. (2002). Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells. Cellular Microbiology, 4(6), 367–381.

Salvatore S. Heuschkel R. Tomlin S. Davies S. E. Edwards S Walker-Smith . . . Murch S. H. (2000). A pilot study of N-acetyl glucosamine, a nutritional substrate for glycosaminoglycan synthesis, in paediatric chronic inflammatory bowel disease. Alimentary Pharmacology & Therapeutics, 14(12), 1567–1579.

Sasarman F. Maftei C. Campeau P. M. Brunel-Guitton C. Mitchell G. A. Allard P. (2016). Biosynthesis of glycosaminoglycans: Associated disorders and biochemical tests. Journal of Inherited Metabolic Disease, 39(2), 173–188.

Sava I. G. Zhang F. Toma I. Theilacker C. Li B. Baumert T. F. . . . Huebner J. (2009). Novel interactions of glycosaminoglycans and bacterial glycolipids mediate binding of enterococci to human cells. The Journal of Biological Chemistry, 284(27), 18194–18201.

Schuerer-Maly C. C. Eckmann L. Kagnoff M. F. Falco M. T. Maly F. E. (1994). Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide. Immunology, 81(1), 85–91.

Sharpton T. Lyalina S. Luong J. Pham J. Deal E. M. Armour C. . . . Pollard K. S. (2017). Development of inflammatory bowel disease is linked to a longitudinal restructuring of the gut metagenome in mice. mSystems, 2(5), E00036–17. doi:10.1128/mSystems.00036-17

Shen Y. Zhou M. Yan J. Gong Z. Xiao Y. Zhang C. . . . Chen Y. (2017). miR-200b inhibits TNF-α-induced IL-8 secretion and tight junction disruption of intestinal epithelial cells in vitro. American Journal of Physiology—Gastroenterology and Liver Physiology, 312(2), G123–G132.

Shin W. G. Park B. J. Lee S. J. Kim J. G. (2018). Infection of human intestinal epithelial cells by invasive bacteria activates NF-κB and increases ICAM-1 expression through NOD1. The Korean Journal of Internal Medicine, 33(1), 81–90.

Spitz J. Yuhan R. Koutsouris A. Blatt C. Alverdy J. Hecht G. (1995). Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function. American Journal of Physiology—Gastroenterology and Liver Physiology, 268, G374–G379.

Srinivasan B. Kolli A. R. Esch M. B. Abaci H. E. Shuler M. L. Hickman J. J. (2015). TEER measurement techniques for in vitro barrier model systems. Journal of Laboratory Automation, 20(2), 107–126.

Stabler T. V. Huang Z. Montell E. Verges J. Kraus V. B. (2017). Chondroitin sulphate inhibits NF-κB activity induced by interaction of pathogenic and damage associated molecules. Osteoarthritis and Cartilage, 25(1), 166–174.

Stålhammar M. E. Håkansson L. D. Jonzon A. Sindelar R. (2017). Differential neutrophil chemotactic response towards IL-8 and bacterial N-formyl peptides in term newborn infants. Upsala Journal of Medical Sciences, 122(1), 35–42.

Sun W. Saldaña M. D. A. Fan L. Zhao Y. Dong T. Jin Y. Zhang J. (2016). Sulfated polysaccharide heparin used as carrier to load hydrophobic lappaconitine. International Journal of Biological Macromolecules, 84, 275–280.

Tanner S. M. Berryhill T. F. Ellenburg J. L. Jilling T. Cleveland D. S. Lorenz R. G. Martin C. A. (2015). Pathogenesis of necrotizing enterocolitis: Modeling the innate immune response. The American Journal of Pathology, 185(1), 4–16.

Vallieres M. du Souich P. (2010). Modulation of inflammation by chondroitin sulfate. Osteoarthritis and Cartilage, 18(Suppl. 1), S1–S6.

Volpi N. (2009). High-performance liquid chromatography and on-line mass spectrometry detection for the analysis of chondroitin sulfates/hyaluronan disaccharides derivatized with 2-aminoacridone. Analytical Biochemistry, 397(1), 12–23.

Wang C. Lang Y. Li Q. Jin X. Li G. Yu G. (2018). Glycosaminoglycanomic profiling of human milk in different stages of lactation by liquid chromatography-tandem mass spectrometry. Food Chemistry, 258, 231–236.

Wang M. Liu X. Lyu Z. Gu H. Li D. Chen H. (2017). Glycosaminoglycans (GAGs) and GAG mimetics regulate the behavior of stem cell differentiation. Colloids and Surfaces. B, Biointerfaces, 150, 175–182.

Yan Y. Wang Z. Greenwald J. Kothapalli K. S. Park H. G. Liu R. . . .Brenna J. T . (2017). BCFA suppresses LPS induced IL-8 mRNA expression in human intestinal epithelial cells. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 116, 27–31.

Youakim A. Ahdieh M. (1999). Interferon-gamma decreases barrier function in T₈₄ cells by reducing ZO-1 levels and disrupting apical actin. The American Journal of Physiology—Gastrointestinal and Liver Physiology, 276(5 pt. 1), G1279–G1288.

Zeng J. Teng F. Weinstock G. M. Murray B. E. (2004). Translocation of Enterococcus faecalis strains across a monolayer of polarized human enterocyte-like T84 cells. Journal of Clinical Microbiology, 42(3), 1149–1154.

Zhou F. Zhang X. Cai D. Li J. Mu Q. Zhang W. . . . Ouyang H. W. (2017). Silk fibroin-chondroitin sulfate scaffold with immune-inhibition property for articular cartilage repair. Acta Biomaterialia, 63, 64–75.

Zihni C. Balda M. S. Matter K. (2014). Signalling at tight junctions during epithelial differentiation and microbial pathogenesis. Journal of Cell Science, 127, 3401–3413.