Characterization and in vitro properties of oral lactobacilli in breastfed infants

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Romani Vestman, Nelly ^a   Timby, Niklas ^a   Holgerson, Pernilla Lif ^a   Kressirer, Christine A ^b,c   Claesson, Rolf ^a   Domellöf, Magnus ^a   Öhman, Carina ^a   Tanner, Anne Cr ^b,c   Hernell, Olle ^a   Johansson, Ingegerd ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b FORSYTH INSTITUTE   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Adhesion; Breastfed infants; Gp340; Growth; L.gasseri; Lactobacillus

Indexed keywords

BACTERIAL RNA; HYDROXYAPATITE; MUCIN 7; PROBIOTIC AGENT; RNA 16S; SEMPER MAGDROPPAR; UNCLASSIFIED DRUG;

ACTINOMYCES NAESLUNDII; ALVEOLAR RIDGE; ARTICLE; ARTIFICIAL MILK; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM ISOLATE; BIRTH WEIGHT; BREAST FEEDING; BREAST MILK; CANDIDA ALBICANS; CHILD DEVELOPMENT; CHILD GROWTH; EPITHELIUM CELL; FUSOBACTERIUM NUCLEATUM; GENE SEQUENCE; GROWTH INHIBITION; HUMAN; IN VITRO STUDY; INFANT; LACTOBACILLUS; LACTOBACILLUS GASSERI; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MEDICAL RECORD; MICROBIOLOGICAL EXAMINATION; MOUTH CAVITY; MOUTH FLORA; NONHUMAN; SALIVA ANALYSIS; STREPTOCOCCUS MUTANS; STREPTOCOCCUS SOBRINUS;

ADULT; ANTIBIOSIS; BACTERIAL LOAD; BREAST FEEDING; DNA, BACTERIAL; DNA, RIBOSOMAL; FEMALE; HUMANS; INFANT; INFANT FORMULA; INFANT, NEWBORN; LACTOBACILLUS; MALE; MOUTH; PROBIOTICS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SALIVA; SEQUENCE ANALYSIS, DNA;

EID: 84882783682     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-193     Document Type: Article

References (59)

1. The normal Lactobacillus flora of healthy human rectal and oral mucosa. Ahrne S, Nobaek S, Jeppsson B, Adlerberth I, Wold AE, Molin G, J Appl Microbiol 1998 85 88 94 10.1046/j.1365-2672.1998.00480.x 9721659
2. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Preidis GA, Versalovic J, Gastroenterology 2009 136 2015 2031 10.1053/j.gastro.2009.01.072 19462507
3. The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits. Tsai YT, Cheng PC, Pan TM, Appl Microbiol Biotechnol 2012 96 853 862 10.1007/s00253-012-4407-3 23001058
4. Food and Agriculture Organization/World health Organization (FAO/WHO), Guidelines for the evaluation of probiotics in food: report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food Ontario, Canada 2002
5. Recent advances in the role of probiotics in human inflammation and gut health. Rupa P, Mine Y, J Agric Food Chem 2012 60 8249 8256 10.1021/jf301903t
6. Probiotics during weaning reduce the incidence of eczema. West CE, Hammarström ML, Hernell O, Pediatr Allergy Immunol 2009 20 430 437 10.1111/j.1399-3038.2009.00745.x 19298231
7. Species and strain specificity of Lactobacillus probiotics effect on weight regulation. Million M, Raoult D, Microb Pathog 2013 55 52 54 23332210
8. Bacterial specificity in the etiology of dental caries. Van Houte J, Int Dent J 1980 30 305 7005104
9. Bacteria of dental caries in primary and permanent teeth in children and young adults. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, Leys EJ, Paster BJ, J Clin Microbiol 2008 46 1407 1417 10.1128/JCM.01410-07 18216213
10. Probiotics and oral health. Haukioja A, Eur J Dent 2010 4 348 355 20613927
11. Lactobacillus-mediated interference of mutans streptococci in caries-free vs. caries-active subjects. Simark-Mattsson C, Emilson CG, Hakansson EG, Jacobsson C, Roos K, Holm S, Eur J Oral Sci 2007 115 308 314 10.1111/j.1600-0722.2007.00458.x 17697171
12. Microbial risk markers for childhood caries in pediatricians' offices. Kanasi E, Johansson I, Lu SC, Kressin NR, Nunn ME, Kent R Jr, Tanner AC, J Dent Res 2010 89 378 383 10.1177/0022034509360010 20164496
13. Oral microbial profile discriminates breast-fed from formula-fed infants. Holgerson PL, Vestman NR, Claesson R, Ohman C, Domellof M, Tanner AC, Hernell O, Johansson I, J Pediatr Gastroenterol Nutr 2013 56 127 136 10.1097/MPG.0b013e31826f2bc6 22955450
14. Colonization with mutans streptococci and lactobacilli and the caries experience of children after the age of five. Straetemans MM, van Loveren C, de Soet JJ, de Graaff J, ten Cate JM, J Dent Res 1998 77 1851 1855 10.1177/00220345980770101301 9786642
15. Human milk is a source of lactic acid bacteria for the infant gut. Martin R, Langa S, Reviriego C, Jiminez E, Marin ML, Xaus J, Fernandez L, Rodriguez JM, J Pediatr 2003 143 754 758 10.1016/j.jpeds.2003.09.028 14657823
16. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Solis G, de Los Reyes-Gavilan CG, Fernandez N, Margolles A, Gueimonde M, Anaerobe 2010 16 307 310 10.1016/j.anaerobe.2010.02.004 20176122
17. Bioactive properties of milk proteins with particular focus on anticariogenesis. Aimutis WR, J Nutr 2004 134 989 995
18. Human milk compounds inhibiting adhesion of mutans streptococci to host ligand-coated hydroxyapatite in vitro. Danielsson Niemi L, Hernell O, Johansson I, Caries Res 2009 43 171 178 10.1159/000213888 19390191
19. Effects of human milk on adhesion of Streptococcus mutans to saliva-coated hydroxyapatite in vitro. Wernersson J, Danielsson Niemi L, Einarson S, Hernell O, Johansson I, Caries Res 2006 40 412 417 10.1159/000094287 16946610
20. Human milk composition: nutrients and bioactive factors. Ballard O, Morrow AL, Pediatr Clin North Am 2013 60 49 74 10.1016/j.pcl.2012.10.002 23178060
21. Proteomic characterization of human milk fat globule membrane proteins during a 12 month lactation period. Liao Y, Alvarado R, Phinney B, Lonnerdal B, J Proteome Res 2011 10 3530 3541 10.1021/pr200149t 21714549
22. Milk fat globule membrane components-a proteomic approach. Cavaletto M, Giuffrida MG, Conti A, Adv Exp Med Biol 2008 606 129 141 10.1007/978-0-387- 74087-4-4 18183927
23. Use of proteomic methodology for the characterization of human milk fat globular membrane proteins. Charlwood J, Hanrahan S, Tyldesley R, Langridge J, Dwek M, Camilleri P, Anal Biochem 2002 301 314 324 10.1006/abio.2001.5498 11814302
24. Bioactive proteins in breast milk. Lonnerdal B, J Paediatr Child Health 2013 49 Suppl 1 1 7 23517111
25. Characterization of Lactobacillus reuteri interaction with milk fat globule membrane components in dairy products. Brisson G, Payken HF, Sharpe JP, Jimenez-Flores R, J Agric Food Chem 2010 58 5612 5619 10.1021/jf904381s 20377223
26. Antimicrobial properties of milkfat globule membrane fractions. Clare DA, Zheng Z, Hassan HM, Swaisgood HE, Catignani GL, J Food Prot 2008 71 126 133 18236672
27. Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N, J Clin Microbiol 2004 42 3128 3136 10.1128/JCM.42.7.3128-3136.2004 15243071
28. Simplified method for collection of pure submandibular saliva in large volumes. Truelove EL, Bixler D, Merritt AD, J Dent Res 1967 46 1400 1403 10.1177/00220345670460064301 5234911
29. Human salivary acidic proline-rich proteins and statherin promote the attachment of Actinomyces viscosus LY7 to apatitic surfaces. Gibbons RJ, Hay DI, Infect Immun 1988 56 439 445 2892794
30. Actinomyces naeslundii genospecies 1 and 2 express different binding specificities to N-acetyl-beta-D-galactosamine, whereas Actinomyces odontolyticus expresses a different binding specificity in colonizing the human mouth. Hallberg K, Hammarstrom KJ, Falsen E, Dahlen G, Gibbons RJ, Hay DI, Stromberg N, Oral Microbiol Immunol 1998 13 327 336 10.1111/j.1399-302X.1998. tb00687.x 9872107
31. Studies of Lewis antigens and H. pylori adhesion in CHO cell lines engineered to express Lewis b determinants. Lofling J, Diswall M, Eriksson S, Boren T, Breimer ME, Holgersson J, Glycobiology 2008 18 494 501 10.1093/glycob/cwn030 18400963
32. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Boren T, Falk P, Roth KA, Larson G, Normark S, Science 1993 262 1892 1895 10.1126/science.8018146 8018146
33. Probiotic bacteria affect the composition of salivary pellicle and streptococcal adhesion in vitro. Haukioja A, Loimaranta V, Tenovuo J, Oral Microbiol Immunol 2008 23 336 343 10.1111/j.1399-302X.2008.00435.x 18582334
34. Variant size- and glycoforms of the scavenger receptor cysteine-rich protein gp-340 with differential bacterial aggregation. Eriksson C, Frangsmyr L, Danielsson Niemi L, Loimaranta V, Holmskov U, Bergman T, Leffler H, Jenkinson HF, Stromberg N, Glycoconj J 2007 24 131 142 10.1007/s10719-006-9020-1 17243023
35. Macromolecular organization of saliva: identification of 'insoluble' MUC5B assemblies and non-mucin proteins in the gel phase. Wickström C, Christersson C, Davies J, Carlstedt I, Biochem J 2000 351 421 10.1042/0264-6021:3510421 11023828
36. Body-composition assessment in infancy: air-displacement plethysmography compared with a reference 4-compartment model. Ellis KJ, Yao M, Shypailo RJ, Urlando A, Wong WW, Heird WC, Am J Clin Nutr 2007 85 90 95 17209182
37. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S, Helm K, Klarczyk M, Schopfer H, Bockler HM, Wells J, J Pediatr Gastroenterol Nutr 2005 40 36 42 10.1097/00005176-200501000- 00007 15625424
38. OPLS discriminant analysis: combining the strengths of PLSDA and SIMCA classification. Bylesjö M, Rantalainen M, Cloarec O, Nicholson JK, Holmes E, Trygg J, Journal of Chemometrics 2006 20 341 351 10.1002/cem.1006
39. Sjöström M, Wold S, Söderström B, PLS discriminant plots Amsterdam: Elsevier 1986
40. Therapeutic modulation of microbiota-host metabolic interactions. Holmes E, Kinross J, Gibson GR, Burcelin R, Jia W, Pettersson S, Nicholson JK, Sci Trans Med 2012 4 137rv6 10.1126/scitranslmed.3004244
41. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. Holscher HD, Faust KL, Czerkies LA, Litov R, Ziegler EE, Lessin H, Hatch T, Sun S, Tappenden KA, JPEN J Parenter Enteral Nutr 2012 36 Suppl 1 95S 105S 22237884
42. Mode of birth delivery affects oral microbiota in infants. Lif Holgerson P, Harnevik L, Hernell O, Tanner AC, Johansson I, J Dent Res 2011 90 1183 1188 10.1177/0022034511418973 21828355
43. Lactobacilli in the intestinal microbiota of Swedish infants. Ahrne S, Lonnermark E, Wold AE, Aberg N, Hesselmar B, Saalman R, Strannegard IL, Molin G, Adlerberth I, Microbes and infection / Institut Pasteur 2005 7 1256 1262 10.1016/j.micinf.2005.04.011 16002310
44. Screening for lactobacilli with probiotic properties in the infant gut microbiota. Kirtzalidou E, Pramateftaki P, Kotsou M, Kyriacou A, Anaerobe 2011 17 440 443 10.1016/j.anaerobe.2011.05.007 21621627
45. Use of the DNA sequence of variable regions of the 16S rRNA gene for rapid and accurate identification of bacteria in the Lactobacillus acidophilus complex. Kullen MJ, Sanozky-Dawes RB, Crowell DC, Klaenhammer TR, J Appl Microbiol 2000 89 511 516 10.1046/j.1365-2672.2000.01146.x 11021584
46. Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. Chauviere G, Coconnier MH, Kerneis S, Fourniat J, Servin AL, J Gen Microbiol 1992 138 1689 1696 10.1099/00221287-138-8-1689 1527509
47. Evaluation of adhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Kotzamanidis C, Kourelis A, Litopoulou-Tzanetaki E, Tzanetakis N, Yiangou M, Int J Food Microbiol 2010 140 154 163 10.1016/j.ijfoodmicro.2010.04.004 20452079
48. In vitro evaluation of Lactobacillus gasseri strains of infant origin on adhesion and aggregation of specific pathogens. Ferreira CL, Grzeskowiak L, Collado MC, Salminen S, J Food Prot 2011 74 1482 1487 10.4315/0362-028X.JFP-11- 074 21902917
49. Characterization of Lactobacillus gasseri isolates from a breast-fed infant. Rodrigues Da Cunha L, Fortes Ferreira CL, Durmaz E, Goh YJ, Sanozky-Dawes R, Klaenhammer T, Gut microbes 2012 3 15 24 10.4161/gmic.19489 22555546
50. Effects of gassericins A and T, bacteriocins produced by Lactobacillus gasseri, with glycine on custard cream preservation. Arakawa K, Kawai Y, Iioka H, Tanioka M, Nishimura J, Kitazawa H, Tsurumi K, Saito T, J Dairy Sci 2009 92 2365 2372 10.3168/jds.2008-1240 19447968
51. Isolation and characterization of a highly hydrophobic new bacteriocin (gassericin A) from Lactobacillus gasseri LA39. Kawai Y, Saito T, Toba T, Samant SK, Itoh T, Biosci Biotechnol Biochem 1994 58 1218 1221 10.1271/bbb.58.1218 7765246
52. Survival of yogurt-containing organisms and Lactobacillus gasseri (ADH) and their effect on bacterial enzyme activity in the gastrointestinal tract of healthy and hypochlorhydric elderly subjects. Pedrosa MC, Golner BB, Goldin BR, Barakat S, Dallal GE, Russell RM, Am J Clin Nutr 1995 61 353 359 7840074
53. Role of Toll-like receptors in the development of immunotolerance mediated by probiotics. Gomez-Llorente C, Munoz S, Gil A, Proc Nutr Soc 2010 69 381 389 10.1017/S0029665110001527 20416121
54. Identification of a high-molecular-mass Lactobacillus epithelium adhesin (LEA) of Lactobacillus crispatus ST1 that binds to stratified squamous epithelium. Edelman SM, Lehti TA, Kainulainen V, Antikainen J, Kylvaja R, Baumann M, Westerlund-Wikstrom B, Korhonen TK, Microbiology 2012 158 1713 1722 10.1099/mic.0.057216-0 22516222
55. An Adhesin-Like Protein, Lam29, from Lactobacillus mucosae ME-340 Binds to Histone H3 and Blood Group Antigens in Human Colonic Mucus. Watanabe M, Kinoshita H, Huang IN, Eguchi K, Tsurumi T, Kawai Y, Kitazawa H, Kimura K, Taketomo N, Kikuchi D, et al. Biosci Biotechnol Biochem 2012 76 1655 1660 10.1271/bbb.120150 22972326
56. Lactobacillus adhesion to mucus. Van Tassell ML, Miller MJ, Nutrients 2011 3 613 636 10.3390/nu3050613 22254114
57. Glutamine synthetase and glucose-6-phosphate isomerase are adhesive moonlighting proteins of Lactobacillus crispatus released by epithelial cathelicidin LL-37. Kainulainen V, Loimaranta V, Pekkala A, Edelman S, Antikainen J, Kylvaja R, Laaksonen M, Laakkonen L, Finne J, Korhonen TK, J Bacteriol 2012 194 2509 2519 10.1128/JB.06704-11 22389474
58. Cathelicidin antimicrobial peptides are expressed in salivary glands and saliva. Murakami M, Ohtake T, Dorschner RA, Gallo RL, J Dent Res 2002 81 845 850 10.1177/154405910208101210 12454100
59. Proteins in whole saliva during the first year of infancy. Ruhl S, Rayment SA, Schmalz G, Hiller KA, Troxler RF, J Dent Res 2005 84 29 34 10.1177/154405910508400104 15615871