Human milk oligosaccharides inhibit Candida albicans invasion of human premature intestinal epithelial cells

Journal of Nutrition

Volumn 145, Issue 9, 2015, Pages 1992-1998

  Gonia, Sara ^a   Tuepker, Michele ^a   Heisel, Timothy ^a   Autran, Chloe ^c   Bode, Lars ^c   Gale, Cheryl A ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Candida albicans; Fungal invasion; Fungal pathogenesis; Human milk oligosaccharides; Hyphal morphogenesis; Intestinal epithelial cells; Premature infants

Indexed keywords

ANTIFUNGAL AGENT; CELL MEMBRANE PROTEIN; FUNGAL PROTEIN; HUMAN MILK OLIGOSACCHARIDE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIFUNGAL ACTIVITY; ARTICLE; BREAST MILK; CANDIDA ALBICANS; CANDIDIASIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; FUNGAL VIABILITY; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; HUMAN; HUMAN CELL; HUMAN PREMATURE INTESTINAL EPITHELIAL CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; MORPHOGENESIS; NONHUMAN; QUANTITATIVE ANALYSIS; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INTESTINE; MICROBIOLOGY; TUMOR CELL LINE;

CANDIDA ALBICANS; CELL LINE, TUMOR; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYPHAE; INTESTINES; MILK, HUMAN; OLIGOSACCHARIDES; VIRULENCE FACTORS;

EID: 84941125075     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.214940     Document Type: Article

References (49)

1. Gibertoni D, Corvaglia L, Vandini S, Rucci P, Savini S, Alessandroni R, Sansavini A, Fantini MP, Faldella G. Positive effect of human milk feeding during NICU hospitalization on 24 month neurodevelopment of very low birth weight infants: an Italian cohort study. PLoS One 2015;10:e0116552.
2. Johnson TJ, Patel AL, Bigger HR, Engstrom JL, Meier PP. Economic benefits and costs of human milk feedings: a strategy to reduce the risk of prematurity-related morbidities in very-low-birth-weight infants. Adv Nutr 2014;5:207-12.
3. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 2012;22:1147-62.
4. Srinivasjois R, Rao S, Patole S. Prebiotic supplementation in preterm neonates: updated systematic review and meta-analysis of randomised controlled trials. Clin Nutr 2013;32:958-65.
5. Albrecht S, Schols HA, van den Heuvel EG, Voragen AG, Gruppen H. Occurrence of oligosaccharides in feces of breast-fed babies in their first six months of life and the corresponding breast milk. Carbohydr Res 2011;346:2540-50.
6. Albrecht S, Schols HA, van Zoeren D, van Lingen RA, Groot Jebbink LJ, van den Heuvel EG, Voragen AG, Gruppen H. Oligosaccharides in feces of breast-and formula-fed babies. Carbohydr Res 2011;346:2173-81.
7. Kuntz S, Kunz C, Rudloff S. Oligosaccharides from human milk induce growth arrest via G2/M by influencing growth-related cell cycle genes in intestinal epithelial cells. Br J Nutr 2009;101:1306-15.
8. Kuntz S, Rudloff S, Kunz C. Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-transformed intestinal cells. Br J Nutr 2008;99:462-71.
9. Jantscher-Krenn E, Lauwaet T, Bliss LA, Reed SL, Gillin FD, Bode L. Human milk oligosaccharides reduce Entamoeba histolytica attachment and cytotoxicity in vitro. Br J Nutr 2012;108:1839-46.
10. Newburg DS, Ruiz-Palacios GM, Morrow AL. Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 2005;25: 37-58.
11. Jantscher-Krenn E, Zherebtsov M, Nissan C, Goth K, Guner YS, Naidu N, Choudhury B, Grishin AV, Ford HR, Bode L. The human milk oligosaccharide disialyllacto-N-tetraose prevents necrotising enterocolitis in neonatal rats. Gut 2012;61:1417-25.
12. Fridkin SK, Kaufman D, Edwards JR, Shetty S, Horan T. Changing incidence of Candida bloodstream infections among NICU patients in the United States: 1995-2004. Pediatrics 2006;117:1680-7.
13. Heisel T, Podgorski H, Staley CM, Knights D, Sadowsky MJ, Gale CA. Complementary amplicon-based genomic approaches for the study of fungal communities in humans. PLoS One 2015;10:e0116705.
14. LaTuga MS, Ellis JC, Cotton CM, Goldberg RN, Wynn JL, Jackson RB, Seed PC. Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants. PLoS One 2011;6:e27858.
15. Saiman L, Ludington E, Dawson JD, Patterson JE, Rangel-Frausto S, Wiblin RT, Blumberg HM, Pfaller M, Rinaldi M, Edwards JE, et al. Risk factors for Candida species colonization of neonatal intensive care unit patients. Pediatr Infect Dis J 2001;20:1119-24.
16. Cole GT, Halawa AA, Anaissie EJ. The role of the gastrointestinal tract in hematogenous candidiasis: from the laboratory to the bedside. Clin Infect Dis: an official publication of the Infectious Diseases Society of America 1996;22 Suppl 2:S73-88.
17. Cutler JE. Putative virulence factors of Candida albicans. Annu Rev Microbiol 1991;45:187-218.
18. Odds FC. Pathogenesis of Candida infections. J Am Acad Dermatol 1994;31:S2-5.
19. Coates EW, Karlowicz MG, Croitoru DP, Buescher ES. Distinctive distribution of pathogens associated with peritonitis in neonates with focal intestinal perforation compared with necrotizing enterocolitis. Pediatrics 2005;116:e241-6.
20. Ragouilliaux CJ, Keeney SE, Hawkins HK, Rowen JL. Maternal factors in extremely low birth weight infants who develop spontaneous intestinal perforation. Pediatrics 2007;120:e1458-64.
21. Parra-Herran CE, Pelaez L, Sola JE, Urbiztondo AK, Rodriguez MM. Intestinal candidiasis: an uncommon cause of necrotizing enterocolitis (NEC) in neonates. Fetal Pediatr Pathol 2010;29:172-80.
22. Falgier C, Kegley S, Podgorski H, Heisel T, Storey K, Bendel CM, Gale CA. Candida species differ in their interactions with immature human gastrointestinal epithelial cells. Pediatr Res 2011;69:384-9.
23. Cummings NP, Neifert MR, Pabst MJ, Johnston RB, Jr. Oxidative metabolic response and microbicidal activity of human milk macrophages: effect of lipopolysaccharide and muramyl dipeptide. Infect Immun 1985;49:435-9.
24. Mete E, Bavbek N, Dayi S, Erkmen M, Andiran F. In vitro antifungal effect of human milk. Allergy Asthma Proc 2006;27:412-4.
25. Robinson JE, Harvey BA, Soothill JF. Phagocytosis and killing of bacteria and yeast by human milk cells after opsonisation in aqueous phase of milk. BMJ 1978;1:1443-5.
26. Sanderson IR, Ezzell RM, Kedinger M, Erlanger M, Xu ZX, Pringault E, Leon-Robine S, Louvard D, Walker WA. Human fetal enterocytes in vitro: modulation of the phenotype by extracellular matrix. Proc Natl Acad Sci USA 1996;93:7717-22.
27. Gillum AM, Tsay EY, Kirsch DR. Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 1984;198: 179-82.
28. Sherman F. Getting Started with Yeast. In: Methods Enzymol; Guide to yeast genetics and molecular biology. Editors: Fink G and Guthrie C. Publisher: Harcourt Brace Jovanovich 1991:3-20.
29. Brand A, Vacharaksa A, Bendel C, Norton J, Haynes P, Henry-Stanley M, Wells C, Ross K, Gow NA, Gale CA. An internal polarity landmark is important for externally induced hyphal behaviors in Candida albicans. Eukaryot Cell 2008;7:712-20.
30. Lawless C, Wilkinson DJ, Young A, Addinall SG, Lydall DA. Colonyzer: automated quantification of micro-organism growth characteristics on solid agar. BMC Bioinformatics 2010;11:287.
31. Berman J. Morphogenesis and cell cycle progression in Candida albicans. Curr Opin Microbiol 2006;9:595-601.
32. Pulver R, Heisel T, Gonia S, Robins R, Norton J, Haynes P, Gale CA. Rsr1 focuses Cdc42 activity at hyphal tips and promotes maintenance of hyphal development in Candida albicans. Eukaryot Cell 2013;12:482-95.
33. Bassilana M, Hopkins J, Arkowitz RA. Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot Cell 2005;4:588-603.
34. Lin AE, Autran CA, Espanola SD, Bode L, Nizet V. Human milk oligosaccharides protect bladder epithelial cells against uropathogenic Escherichia coli invasion and cytotoxicity. J Infect Dis 2014;209:389-98.
35. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 2003; 278:14112-20.
36. Kaufman DA. Epidemiology and prevention of neonatal candidiasis: fluconazole for all neonates? Adv Exp Med Biol 2010;659:99-119.
37. Austin N, McGuire W. Prophylactic systemic antifungal agents to prevent mortality and morbidity in very low birth weight infants. Cochrane Database Syst Rev 2013;4:CD003850.
38. Bendel CM, Hess DJ, Garni RM, Henry-Stanley M, Wells CL. Comparative virulence of Candida albicans yeast and filamentous forms in orally and intravenously inoculated mice. Crit Care Med 2003;31:501-7.
39. Dalle F, Wachtler B, L'Ollivier C, Holland G, Bannert N, Wilson D, Labruere C, Bonnin A, Hube B. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol 2010;12:248-71.
40. Naglik J, Albrecht A, Bader O, Hube B. Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 2004;6:915-26.
41. Grubb SE, Murdoch C, Sudbery PE, Saville SP, Lopez-Ribot JL, Thornhill MH. Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infect Immun 2009;77:3872-8.
42. Rotrosen D, Edwards JE, Jr., Gibson TR, Moore JC, Cohen AH, Green I. Adherence of Candida to cultured vascular endothelial cells: mechanisms of attachment and endothelial cell penetration. J Infect Dis 1985;152:1264-74.
43. Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA, Yeater K, Leng RP, Brown AJ, Hoyer LL. ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 2004;150:2415-28.
44. Newburg DS, Ashkenazi S, Cleary TG. Human milk contains the Shiga toxin and Shiga-like toxin receptor glycolipid Gb3. J Infect Dis 1992;166:832-6.
45. Newburg DS, Pickering LK, McCluer RH, Cleary TG. Fucosylated oligosaccharides of human milk protect suckling mice from heat-stabile enterotoxin of Escherichia coli. J Infect Dis 1990;162:1075-80.
46. Morrow AL, Ruiz-Palacios GM, Altaye M, Jiang X, Guerrero ML, Meinzen-Derr JK, Farkas T, Chaturvedi P, Pickering LK, Newburg DS. Human milk oligosaccharides are associated with protection against diarrhea in breast-fed infants. J Pediatr 2004;145:297-303.
47. Manzoni P, Rinaldi M, Cattani S, Pugni L, Romeo MG, Messner H, Stolfi I, Decembrino L, Laforgia N, Vagnarelli F, et al. Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birthweight neonates: a randomized trial. JAMA 2009;302:1421-8.
48. Manzoni P, Stolfi I, Messner H, Cattani S, Laforgia N, Romeo MG, Bollani L, Rinaldi M, Gallo E, Quercia M, et al. Bovine lactoferrin prevents invasive fungal infections in very low birth weight infants: a randomized controlled trial. Pediatrics 2012;129:116-23.
49. Underwood MA, Kalanetra KM, Bokulich NA, Mirmiran M, Barile D, Tancredi DJ, German JB, Lebrilla CB, Mills DA. Prebiotic oligosaccharides in premature infants. J Pediatr Gastroenterol Nutr 2014; 58:352-60.