In vivo gut transcriptome responses to Lactobacillus rhamnosus GG and Lactobacillus acidophilus in neonatal gnotobiotic piglets

Gut Microbes

Volumn 5, Issue 2, 2014, Pages

  Kumar, Anand ^a   Vlasova, Anastasia N ^a   Liu, Zhe ^a   Chattha, Kuldeep S ^a   Kandasamy, Sukumar ^a   Esseili, Malak ^a   Zhang, Xiaoli ^b   Rajashekara, Gireesh ^a   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Gnotobiotic pigs; Gut; Lactobacilli; Probiotics; Transcriptome

Indexed keywords

COMPLEMENT COMPONENT C8; COMPLEMENT COMPONENT C9; COMPLEMENTARY DNA; CXCL9 CHEMOKINE; GENOMIC DNA; GLUCAGON LIKE PEPTIDE 2; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 27; INTEGRIN; LYSOZYME; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RNA; SECRETORY COMPONENT; STRESS ACTIVATED PROTEIN KINASE; SURFACTANT PROTEIN D; TRANSCRIPTOME;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; CARBOHYDRATE METABOLISM; COLONY FORMING UNIT; CONTROLLED STUDY; DNA SYNTHESIS; GENE EXPRESSION; GENOME ANALYSIS; GNOTOBIOTICS; IMMUNE RESPONSE; IMMUNOMODULATION; INGENUITY PATHWAY ANALYSIS; INNATE IMMUNITY; INTESTINE FLORA; INTRACELLULAR SIGNALING; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; MICROARRAY ANALYSIS; NONHUMAN; PIGLET; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; ANIMAL; GASTROINTESTINAL TRACT; GENETICS; MICROBIOLOGY; NEWBORN; PHYSIOLOGY; SWINE;

ANIMALS; ANIMALS, NEWBORN; GASTROINTESTINAL TRACT; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; SWINE; TRANSCRIPTOME;

EID: 84899438179     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.27877     Document Type: Article

References (63)

1. Eastham EJ, Lichauco T, Grady MI, Walker WA. Antigenicity of infant formulas: role of immature intestine on protein permeability. J Pediatr 1978; 93: 561-4; PMID: 568172; http://dx. doi. org/10. 1016/S0022-3476(78)80888-9.
2. Axelsson IE, Ivarsson SA, Räihä NC. Protein intake in early infancy: effects on plasma amino acid concentrations, insulin metabolism, and growth. Pediatr Res 1989; 26: 614-7; PMID: 2689986; http://dx. doi. org/10. 1203/00006450-198912000-00020.
3. Chattha KS, Vlasova AN, Kandasamy S, Rajashekara G, Saif LJ. Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J Immunol 2013; 191: 2446-56; PMID: 23918983; http://dx. doi. org/10. 4049/jimmunol. 1300678.
4. de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 2008; 111: 1-66; PMID: 18461293; http://dx. doi. org/10. 1007/10_2008_097.
5. Boirivant M, Strober W. The mechanism of action of probiotics. Curr Opin Gastroenterol 2007; 23: 679-92; PMID: 17906447; http://dx. doi. org/10. 1097/MOG. 0b013e3282f0cffc.
6. Petrof EO. O Probiotics and gastrointestinal diseases: clinical evidence and basic science. Antiinflamm Antiallergy Agents Med Chem 2009; 8: 260-9; PMID: 20890386.
7. Walter J. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 2008; 74: 4985-96; PMID: 18539818; http://dx. doi. org/10. 1128/AEM. 00753-08.
8. Vanderhoof JA, Whitney DB, Antonson DL, Hanner TL, Lupo JV, Young RJ. Lactobacillus GG in the prevention of antibiotic-associated diarrhea in children. J Pediatr 1999; 135: 564-8; PMID: 10547243; http://dx. doi. org/10. 1016/S0022-3476(99)70053-3.
9. Guandalini S, Pensabene L, Zikri MA, Dias JA, Casali LG, Hoekstra H, Kolacek S, Massar K, Micetic-Turk D, Papadopoulou A, et al. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr 2000; 30: 54-60; PMID: 10630440; http://dx. doi. org/10. 1097/00005176-200001000-00018.
10. Szajewska H, Kotowska M, Mrukowicz JZ, Armanska M, Mikołajczyk W. Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants. J Pediatr 2001; 138: 361-5; PMID: 11241043; http://dx. doi. org/10. 1067/mpd. 2001. 111321.
11. Fang SB, Lee HC, Hu JJ, Hou SY, Liu HL, Fang HW. Dose-dependent effect of Lactobacillus rhamnosus on quantitative reduction of faecal rotavirus shedding in children. J Trop Pediatr 2009; 55: 297-301; PMID: 19203988; http://dx. doi. org/10. 1093/tropej/fmp001.
12. Majamaa H, Isolauri E, Saxelin M, Vesikari T. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr 1995; 20: 333-8; PMID: 7608829; http://dx. doi. org/10. 1097/00005176-199504000-00012.
13. Rosenfeldt V, Michaelsen KF, Jakobsen M, Larsen CN, Møller PL, Pedersen P, Tvede M, Weyrehter H, Valerius NH, Paerregaard A. Effect of probiotic Lactobacillus strains in young children hospitalized with acute diarrhea. Pediatr Infect Dis J 2002; 21: 411-6; PMID: 12150178; http://dx. doi. org/10. 1097/00006454-200205000-00012.
14. Yuan-Kun Lee. Rev. ed. of: Handbook of probiotics 2nd ed. 2009; Hoboken, N. J.: John Wiley & Sons. pp. 441-443.
15. Plantinga TS, van Maren WW, van Bergenhenegouwen J, Hameetman M, Nierkens S, Jacobs C, de Jong DJ, Joosten LA, van't Land B, Garssen J, et al. Differential Toll-like receptor recognition and induction of cytokine profile by Bifidobacterium breve and Lactobacillus strains of probiotics. Clin Vaccine Immunol 2011; 18: 621-8; PMID: 21288993; http://dx. doi. org/10. 1128/CVI. 00498-10.
16. Silva M, Jacobus NV, Deneke C, Gorbach SL. Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother 1987; 31: 1231-3; PMID: 3307619; http://dx. doi. org/10. 1128/AAC. 31. 8. 1231.
17. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 2002; 277: 50959-65; PMID: 12393915; http://dx. doi. org/10. 1074/jbc. M207050200.
18. van Baarlen P, Troost F, van der Meer C, Hooiveld G, Boekschoten M, Brummer RJ, Kleerebezem M. Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc Natl Acad Sci U S A 2011; 108(Suppl 1): 4562-9; http://dx. doi. org/10. 1073/pnas. 1000079107; PMID: 20823239.
19. Troost FJ, van Baarlen P, Lindsey P, Kodde A, de Vos WM, Kleerebezem M, Brummer RJ. Identification of the transcriptional response of human intestinal mucosa to Lactobacillus plantarum WCFS1 in vivo. BMC Genomics 2008; 9: 374; PMID: 18681965; http://dx. doi. org/10. 1186/1471-2164-9-374.
20. Zhang W, Azevedo MS, Gonzalez AM, Saif LJ, Van Nguyen T, Wen K, Yousef AE, Yuan L. Influence of probiotic Lactobacilli colonization on neonatal B cell responses in a gnotobiotic pig model of human rotavirus infection and disease. Vet Immunol Immunopathol 2008; 122: 175-81; PMID: 18023882; http://dx. doi. org/10. 1016/j. vetimm. 2007. 10. 003.
21. Wen K, Li G, Zhang W, Azevedo MS, Saif LJ, Liu F, Bui T, Yousef A, Yuan L. Development of γΔ T cell subset responses in gnotobiotic pigs infected with human rotaviruses and colonized with probiotic lactobacilli. Vet Immunol Immunopathol 2011; 141: 267-75; PMID: 21489639; http://dx. doi. org/10. 1016/j. vetimm. 2011. 03. 016.
22. Preidis GA, Saulnier DM, Blutt SE, Mistretta TA, Riehle KP, Major AM, Venable SF, Finegold MJ, Petrosino JF, Conner ME. Versalovic. J. Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine. FASEB 2012; 26: 1960-9; http://dx. doi. org/10. 1096/fj. 10-177980.
23. Meurens F, Summerfield A, Nauwynck H, Saif L, Gerdts V. The pig: a model for human infectious diseases. Trends Microbiol 2012; 20: 50-7; PMID: 22153753; http://dx. doi. org/10. 1016/j. tim. 2011. 11. 002.
24. van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, de Groot PJ, Hooiveld GJ, Brummer RJ, Kleerebezem M. Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A 2009; 106: 2371-6; PMID: 19190178; http://dx. doi. org/10. 1073/pnas. 0809919106.
25. Kleerebezem M, Vaughan EE. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 2009; 63: 269-90; PMID: 19575569; http://dx. doi. org/10. 1146/annurev. micro. 091208. 073341.
26. Ibnou-Zekri N, Blum S, Schiffrin EJ, von der Weid T. Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect Immun 2003; 71: 428-36; PMID: 12496193; http://dx. doi. org/10. 1128/IAI. 71. 1. 428-436. 2003.
27. Belkaid Y, Naik S. Compartmentalized and systemic control of tissue immunity by commensals. Nat Immunol 2013; 14: 646-53; PMID: 23778791; http://dx. doi. org/10. 1038/ni. 2604.
28. Lebeer S, Vanderleyden J, De Keersmaecker SC. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 2008; 72: 728-64; PMID: 19052326; http://dx. doi. org/10. 1128/MMBR. 00017-08.
29. Doherty GJ, McMahon HT. Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu Rev Biophys 2008; 37: 65-95; PMID: 18573073; http://dx. doi. org/10. 1146/annurev. biophys. 37. 032807. 125912.
30. Miner JN, Hong MH, Negro-Vilar A. New and improved glucocorticoid receptor ligands. Expert Opin Investig Drugs 2005; 14: 1527-45; PMID: 16307492; http://dx. doi. org/10. 1517/13543784. 14. 12. 1527.
31. Chan HM, La Thangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci 2001; 114: 2363-73; PMID: 11559745.
32. Legate KR, Montañez E, Kudlacek O, Fässler R. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 2006; 7: 20-31; PMID: 16493410; http://dx. doi. org/10. 1038/nrm1789.
33. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005; 5: 51-63; PMID: 15630415; http://dx. doi. org/10. 1038/nrc1524.
34. Bladh LG, Lidén J, Pazirandeh A, Rafter I, Dahlman-Wright K, Nilsson S, Okret S. Identification of target genes involved in the antiproliferative effect of glucocorticoids reveals a role for nuclear factor-(kappa)B repression. Mol Endocrinol 2005; 19: 632-43; PMID: 15528271; http://dx. doi. org/10. 1210/me. 2004-0294.
35. Harvey CB, Williams GR. Mechanism of thyroid hormone action. Thyroid 2002; 12: 441-6; PMID: 12165104; http://dx. doi. org/10. 1089/105072502760143791.
36. Wan M, Leavens KF, Saleh D, Easton RM, Guertin DA, Peterson TR, Kaestner KH, Sabatini DM, Birnbaum MJ. Postprandial hepatic lipid metabolism requires signaling through Akt2 independent of the transcription factors FoxA2, FoxO1, and SREBP1c. Cell Metab 2011; 14: 516-27; PMID: 21982711; http://dx. doi. org/10. 1016/j. cmet. 2011. 09. 001.
37. Chou JY, Mansfield BC. Mutations in the glucose-6-phosphatase-alpha (G6PC) gene that cause type Ia glycogen storage disease. Hum Mutat 2008; 29: 921-30; PMID: 18449899; http://dx. doi. org/10. 1002/humu. 20772.
38. Wolvers D, Antoine JM, Myllyluoma E, Schrezenmeir J, Szajewska H, Rijkers GT. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of infections by probiotics. J Nutr 2010; 140: 698S-712S; PMID: 20107143; http://dx. doi. org/10. 3945/jn. 109. 113753.
39. Turpin W, Humblot C, Thomas M, Guyot JP. Lactobacilli as multifaceted probiotics with poorly disclosed molecular mechanisms. Int J Food Microbiol 2010; 143: 87-102; http://dx. doi. org/10. 1016/j. ijfoodmicro. 2010. 07. 032; PMID: 20801536.
40. Vendt N, Grünberg H, Tuure T, Malminiemi O, Wuolijoki E, Tillmann V, Sepp E, Korpela R. Growth during the first 6 months of life in infants using formula enriched with Lactobacillus rhamnosus GG: double-blind, randomized trial. J Hum Nutr Diet 2006; 19: 51-8; PMID: 16448475; http://dx. doi. org/10. 1111/j. 1365-277X. 2006. 00660. x.
41. Saran S, Gopalan S, Krishna TP. Use of fermented foods to combat stunting and failure to thrive. Nutrition 2002; 18: 393-6; PMID: 11985943; http://dx. doi. org/10. 1016/S0899-9007(01)00790-0.
42. de Silva DM, Aust SD. Ferritin and ceruloplasmin in oxidative damage: review and recent findings. Can J Physiol Pharmacol 1993; 71: 715-20; PMID: 8313236; http://dx. doi. org/10. 1139/y93-107.
43. Ganz T. Hepcidin and iron regulation, 10 years later. Blood 2011; 117: 4425-33; PMID: 21346250; http://dx. doi. org/10. 1182/blood-2011-01-258467.
44. Wintergerst ES, Maggini S, Hornig DH. Contribution of selected vitamins and trace elements to immune function. Ann Nutr Metab 2007; 51: 301-23; PMID: 17726308; http://dx. doi. org/10. 1159/000107673.
45. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22: 283-307; PMID: 12055347; http://dx. doi. org/10. 1146/annurev. nutr. 22. 011602. 092259.
46. Ataie-Jafari A, Larijani B, Alavi Majd H, Tahbaz F. Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann Nutr Metab 2009; 54: 22-7; PMID: 19229114; http://dx. doi. org/10. 1159/000203284.
47. Wasan KM, Brocks DR, Lee SD, Sachs-Barrable K, Thornton SJ. Impact of lipoproteins on the biological activity and disposition of hydrophobic drugs: implications for drug discovery. Nat Rev Drug Discov 2008; 7: 84-99; PMID: 18079757; http://dx. doi. org/10. 1038/nrd2353.
48. De Preter V, Raemen H, Cloetens L, Houben E, Rutgeerts P, Verbeke K. Effect of dietary intervention with different pre-and probiotics on intestinal bacterial enzyme activities. Eur J Clin Nutr 2008; 62: 225-31; PMID: 17327863; http://dx. doi. org/10. 1038/sj. ejcn. 1602706.
49. Gagné D, Groulx JF, Benoit YD, Basora N, Herring E, Vachon PH, Beaulieu JF. Integrin-linked kinase regulates migration and proliferation of human intestinal cells under a fibronectin-dependent mechanism. J Cell Physiol 2010; 222: 387-400; PMID: 19885839; http://dx. doi. org/10. 1002/jcp. 21963.
50. Kim YB, Choi S, Choi MC, Oh MA, Lee SA, Cho M, Mizuno K, Kim SH, Lee JW. Cell adhesion-dependent cofilin serine 3 phosphorylation by the integrin-linked kinase. c-Src complex. J Biol Chem 2008; 283: 10089-96; PMID: 18252715; http://dx. doi. org/10. 1074/jbc. M708300200.
51. McDonald PC, Fielding AB, Dedhar S. Integrin-linked kinase--essential roles in physiology and cancer biology. J Cell Sci 2008; 121: 3121-32; PMID: 18799788; http://dx. doi. org/10. 1242/jcs. 017996.
52. Markov AG, Veshnyakova A, Fromm M, Amasheh M, Amasheh S. Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine. J Comp Physiol B 2010; 180: 591-8; PMID: 20049600; http://dx. doi. org/10. 1007/s00360-009-0440-7.
53. Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C. Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 2007; 81: 15-27; PMID: 16931602; http://dx. doi. org/10. 1189/jlb. 0306167.
54. Busillo JM, Azzam KM, Cidlowski JA. Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J Biol Chem 2011; 286: 38703-13; PMID: 21940629; http://dx. doi. org/10. 1074/jbc. M111. 275370.
55. Xanthou G, Duchesnes CE, Williams TJ, Pease JE. CCR3 functional responses are regulated by both CXCR3 and its ligands CXCL9, CXCL10 and CXCL11. Eur J Immunol 2003; 33: 2241-50; PMID: 12884299; http://dx. doi. org/10. 1002/eji. 200323787.
56. Chowdhury SR, King DE, Willing BP, Band MR, Beever JE, Lane AB, Loor JJ, Marini JC, Rund LA, Schook LB, et al. Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics 2007; 8: 215; PMID: 17615075; http://dx. doi. org/10. 1186/1471-2164-8-215.
57. El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, Hooiveld G, Levenez F, Doré J, Dekker J, Samsom JN, Nieuwenhuis EE, et al. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol 2012; 5: 567-79; PMID: 22617837; http://dx. doi. org/10. 1038/mi. 2012. 32.
58. El Aidy S, Derrien M, Merrifield CA, Levenez F, Doré J, Boekschoten MV, Dekker J, Holmes E, Zoetendal EG, van Baarlen P, et al. Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon. ISME J 2013; 7: 743-55; http://dx. doi. org/10. 1038/ismej. 2012. 142; PMID: 23178667.
59. Meyer RC, Bohl EH, Kohler EM. E. H. Bohl And E. M. Kohler. Procurement and maintenance of germfree swine for microbiological investigations. Appl Microbiol 1964; 12: 295-300; PMID: 14199016.
60. Rao Y, Lee Y, Jarjoura D, Ruppert AS, Liu CG, Hsu JC, Hagan JP. A comparison of normalization techniques for microRNA microarray data. Stat Appl Genet Mol Biol 2008; 7: e22; PMID: 18673291; http://dx. doi. org/10. 2202/1544-6115. 1287.
61. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-64; PMID: 12925520; http://dx. doi. org/10. 1093/biostatistics/4. 2. 249.
62. Gordon, A., Glazko, G., Qiu, X. & Yakovlev, A. Control of the mean number of false discoveries, Bonferroni and stability of multiple testing. Annals of applied statistics 2007; 1: 179-190; http://dx. doi. org/10. 1214/07-AOAS102.
63. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 2001; 25: 402-8; PMID: 11846609; http://dx. doi. org/10. 1006/meth. 2001. 1262.