Lessons from mother: Long-term impact of antibodies in breast milk on the gut microbiota and intestinal immune system of breastfed offspring

Gut Microbes

Volumn 5, Issue 5, 2014, Pages 663-668

  Rogier, Eric W ^a,c   Frantz, Aubrey L ^a,d   Bruno, Maria E C ^a   Wedlund, Leia ^a   Cohen, Donald A ^a   Stromberg, Arnold J ^b   Kaetzel, Charlotte S ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Breastfeeding; Gene expression; Gut microbiota; Inflammatory bowel disease; Intestinal epithelial cells; Polymeric immunoglobulin receptor; Secretory IgA

Indexed keywords

MATERNAL ANTIBODY; SECRETORY IMMUNOGLOBULIN; ANTIBODY;

ADAPTIVE IMMUNITY; ARTICLE; BREAST MILK; COMAMONADACEAE; COMMENSAL; GENE EXPRESSION; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; INTESTINE MUCOSA PERMEABILITY; MOTHER CHILD RELATION; NONHUMAN; OCHROBACTRUM ANTHROPI; SUCKLING ANIMAL; WEANING; ANIMAL; ANIMAL MODEL; BREAST FEEDING; GASTROINTESTINAL TRACT; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; MILK; MOUSE; MUCOSAL IMMUNITY;

BACTERIA (MICROORGANISMS); MUS;

ANIMALS; ANTIBODIES; BREAST FEEDING; GASTROINTESTINAL TRACT; IMMUNITY, MUCOSAL; MICE; MICROBIOTA; MILK; MODELS, ANIMAL;

EID: 84922032682     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/19490976.2014.969984     Document Type: Article

References (32)

1. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107:11971-5; PMID:20566857; http://dx.doi.org/ 10.1073/pnas.1002601107
2. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012; 489:220-30; PMID:22972295; http://dx.doi.org/10.1038/nature 11550
3. Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology 2010; 156:3329-41; PMID:20864478; http://dx.doi.org/ 10.1099/mic.0.043224-0
4. Fallani M, Amarri S, Uusijarvi A, Adam R, Khanna S, Aguilera M, Gil A, Vieites JM, Norin E, Young D, et al. Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology 2011; 157:1385-92; PMID:21330436; http://dx.doi.org/10.1099/mic.0.042143-0
5. Tsuji H, Oozeer R, Matsuda K, Matsuki T, Ohta T, Nomoto K, Tanaka R, Kawashima M, Kawashima K, Nagata S, et al. Molecular monitoring of the development of intestinal microbiota in Japanese infants. Benef Microbes 2012; 3:113-25; PMID:22683836; http://dx. doi.org/10.3920/BM2011.0038
6. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS ONE 2012; 7:e36957; PMID:22606315; http://dx.doi.org/10.1371/journal. pone.0036957
7. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can Med Assoc J 2013; 185:385-94; PMID:23401405; http://dx.doi.org/10.1503/cmaj. 121189
8. Fan W, Huo G, Li X, Yang L, Duan C, Wang T, Chen J. Diversity of the intestinal microbiota in different patterns of feeding infants by Illumina high-throughput sequencing. World J Microbiol Biotechnol 2013; 29:2365-72; PMID:23793940; http://dx.doi.org/ 10.1007/s11274-013-1404-3
9. Gomez-Llorente C, Plaza-Diaz J, Aguilera M, Munoz- Quezada S, Bermudez-Brito M, Peso-Echarri P, Martinez- Silla R, Vasallo-Morillas MI, Campana-Martin L, Vives-Pinera I, et al. Three main factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr 2013; 57:461-6; PMID:23752082; http://dx.doi.org/10.1097/MPG. 0b013e31829d519a
10. Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, Molgaard C, Michaelsen KF, Licht TR. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 2014; 80:2889-900; PMID:24584251; http://dx.doi. org/10.1128/AEM.00342-14
11. Kaetzel CS. Cooperativity among secretory IgA, the polymeric immunoglobulin receptor, and the gut microbiota promotes host-microbial mutualism. Immunol Lett 2014;10; S0165-2478:00100-X; PMID:24877874; http:// dx.doi.org/10.1016/j.imlet.2014.05.008
12. Kaetzel CS. The polymeric immunoglobulin receptor. eLS 2013; http://dx.doi.org/10.1002/9780470015902. a0024237
13. Wilson E, Butcher EC. CCL28 controls immunoglobulin (Ig)A plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J Exp Med 2004; 200:805-9; PMID:15381732; http://dx.doi.org/10.1084/jem.20041069
14. Brandtzaeg P. The mucosal immune system and its integration with the mammary glands. J Pediatr 2010; 156:S8-15; PMID:20105666; http://dx.doi.org/ 10.1016/j.jpeds.2009.11.014
15. Rogier EW, Frantz AL, Bruno MEC, Wedlund L, Cohen DA, Stromberg AJ, Kaetzel CS. Secretory antibodies in breast milk promote long-term intestinal homeostasis by regulating the gut microbiota and host gene expression. Proc Natl Acad Sci USA 2014; 111:3074-9.
16. Lonnerdal B. Bioactive proteins in human milk: mechanisms of action. J Pediatr 2010; 156:S26-30; PMID:20105661; http://dx.doi.org/10.1016/j.jpeds. 2009.11.017
17. Hettinga K, van VH, de VS, Boeren S, van HT, van AJ, Vervoort J. The host defense proteome of human and bovine milk. PLoS ONE 2011; 6:e19433; PMID:21556375; http://dx.doi.org/10.1371/journal. pone.0019433
18. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol 2012; 12:9-23; PMID:22158411; http://dx.doi.org/10.1038/ nri3112
19. Johansen FE, Pekna M, Norderhaug IN, Haneberg B, Hietala MA, Krajci P, Betsholtz C, Brandtzaeg P. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptorsecretory component-deficient mice. J Exp Med 1999; 190:915-22; PMID:10510081; http://dx.doi.org/10.1084/jem.190.7.915
20. Stiakaki E, Galanakis E, Samonis G, Christidou A,Maraka S, Tselentis Y, KalmantiM.Ochrobactrumanthropi bacteremia in pediatric oncology patients. Pediatr Infect Dis J 2002; 21:72-4; PMID:11791106; http://dx.doi.org/ 10.1097/00006454-200201000-00018
21. Duran R, Vatansever U, Acunas B, Basaran UN. Ochrobactrum anthropi bacteremia in a preterm infant with meconium peritonitis. Int J Infect Dis 2009; 13: e61-3; PMID:18842433; http://dx.doi.org/10.1016/j. ijid.2008.06.027
22. Naik C, Kulkarni H, Darabi A, Bhanot N. Ochrobactrum anthropi: a rare cause of pneumonia. J Infect Chemother 2013; 19:162-5; PMID:22669505; http://dx. doi.org/10.1007/s10156-012-0436-1
23. Saulnier DM, Riehle K, Mistretta TA, Diaz MA,Mandal D,Raza S,Weidler EM,Qin X, Coarfa C, MilosavljevicA, et al. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 2011; 141:1782-91; PMID:21741921; http://dx.doi.org/ 10.1053/j.gastro.2011.06.072
24. TannockGW, LawleyB, MunroK, Lay C,Taylor C,Daynes C, Baladjay L, Mcleod R, Thompson-Fawcett M. Comprehensive analysis of the bacterial content of stool from patients with chronic pouchitis, normal pouches, or familial adenomatous polyposis pouches. Inflamm Bowel Dis 2012; 18:925-34; PMID:22114001; http://dx.doi.org/ 10.1002/ibd.21936
25. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 2010; 10:131-44; PMID:20098461; http://dx.doi.org/10.1038/nri2707
26. Rogier EW, Frantz AL, Bruno MEC, Kaetzel CS. Secretory IgA is concentrated in the outer layer of intestinal mucus along with gut bacteria. Pathogens 2014; 3:390-403; PMID:24710095; http://dx.doi.org/ 10.3390/pathogens3020390
27. van der Waaij LA, Limburg PC, Mesander G, van der WD. In vivo IgA coating of anaerobic bacteria in human faeces. Gut 1996; 38:348-54; PMID:8675085; http://dx.doi.org/10.1136/gut.38.3.348
28. Rol N, Favre L, Benyacoub J, Corthesy B. The role of secretory immunoglobulin A in the natural sensing of commensal bacteria by mouse Peyer's patch dendritic cells. J Biol Chem 2012; 287:40074-82; PMID:23027876; http://dx.doi.org/10.1074/jbc. M112.405001
29. Frantz AL, Rogier EW, Weber CR, Shen L, Cohen DA, Fenton LA, Bruno ME, Kaetzel CS. Targeted deletion of MyD88 in intestinal epithelial cells results in compromised antibacterial immunity associated with downregulation of polymeric immunoglobulin receptor, mucin-2, and antibacterial peptides. Mucosal Immunol 2012; 5:501-12; PMID:22491177; http://dx.doi.org/ 10.1038/mi.2012.23
30. von Mutius E., Schmid S. The PASTURE project: EU support for the improvement of knowledge about risk factors and preventive factors for atopy in Europe. Allergy 2006; 61:407-13; PMID:16512801; http://dx. doi.org/10.1111/j.1398-9995.2006.01009.x
31. Orivuori L, Loss G, Roduit C, Dalphin JC, Depner M, Genuneit J, Lauener R, Pekkanen J, Pfefferle P, Riedler J, et al. Soluble immunoglobulin A in breast milk is inversely associated with atopic dermatitis at early age: the PASTURE cohort study. Clin Exp Allergy 2014; 44:102-12; PMID:24102779; http://dx.doi.org/ 10.1111/cea.12199
32. Colaizy TT. Donor human milk for preterm infants: what it is, what it can do, and what still needs to be learned. Clin Perinatol 2014; 41:437- 50; PMID:24873842; http://dx.doi.org/10.1016/j. clp.2014.02.003