Pglyrp-Regulated gut microflora prevotella falsenii, parabacteroides distasonis and bacteroides eggerthii enhance and alistipes finegoldii attenuates colitis in mice

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Dziarski, Roman ^a   Park, Shin Yong ^a   Kashyap, Des Raj ^a   Dowd, Scot E ^b   Gupta, Dipika ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE NORTHWEST   (United States)

^b MR DNA (Molecular Research LP)   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALISTIPES; ALISTIPES FINEGOLDII; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTEROIDES; BACTEROIDES EGGERTHII; BIOLOGICAL ACTIVITY; BIOLOGICAL THERAPY; COLITIS; CONTROLLED STUDY; FEMALE; GENE SEQUENCE; INNATE IMMUNITY; INTESTINE FLORA; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PARABACTEROIDES DISTASONIS; POPULATION ABUNDANCE; PREVOTELLA; PREVOTELLA FALSENII; PYROSEQUENCING; WILD TYPE; ANIMAL; BACTEROIDETES; BAGG ALBINO MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE PREDISPOSITION; FECES; IMMUNOLOGY; INTESTINE; KNOCKOUT MOUSE; MICROBIOLOGY; PHYSIOLOGY; RIBOTYPING;

CARRIER PROTEIN; CYTOKINE; DEXTRAN SULFATE; PEPTIDOGLYCAN RECOGNITION PROTEIN; PGLYRP1 PROTEIN, MOUSE; PROBIOTIC AGENT;

ANIMALS; BACTEROIDETES; CARRIER PROTEINS; COLITIS; CYTOKINES; DEXTRAN SULFATE; DISEASE SUSCEPTIBILITY; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; IMMUNITY, INNATE; INTESTINES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PREVOTELLA; PROBIOTICS; RIBOTYPING;

EID: 84953775617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146162     Document Type: Article

References (80)

1. Royet J, Gupta D, Dziarski R. Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nature Rev Immunol. 2011; 11: 837-851.
2. Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defenses. Nature Rev Microbiol. 2007; 5: 264-277.
3. Dziarski R, Gupta D. Protein Family Review: The peptidoglycan recognition proteins (PGRPs). Genome Biol. 2006; 7:232.
4. Kang D, Liu G, Lundstrom A, Gelius E, Steiner H. A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc Natl Acad Sci USA. 1998; 95: 10078-10082.
5. Liu C, Xu Z, Gupta D, Dziarski R. Peptidoglycan recognition proteins: A novel family of four human innate immunity pattern recognition molecules. J Biol Chem. 2001; 276: 34686-34694.
6. Lu X, Wang M, Qi J, Wang H, Li X, Gupta D, et al. Peptidoglycan recognition proteins are a new class of human bactericidal proteins. J Biol Chem. 2006; 281: 5895-5907.
7. Li X, Wang S, Wang H, Gupta D. Differential expression of peptidoglycan recognition protein 2 in the skin and liver requires different transcription factors. J Biol Chem. 2006; 281: 20738-20748.
8. Tydell CC, Yuan J, Tran P, Selsted ME. Bovine peptidoglycan recognition protein-S: Antimicrobial activity, localization, secretion and binding properties. J Immunol. 2006; 176: 1154-1162.
9. Wang M, Liu LH, Wang S, Li X, Lu X, Gupta D, et al. Human peptidoglycan recognition proteins require zinc to kill both Gram-positive and Gram-negative bacteria and are synergistic with antibacterial peptides. J Immunol. 2007; 178: 3116-3125.
10. Kashyap DR, Wang M, Liu LH, Boons GJ, Gupta D, Dziarski R. Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nature Med. 2011; 17: 676-683. doi: 10.1038/nm.2357
11. Kashyap DR, Rompca A, Gaballa A, Helmann JD, Chan J, Chang CJ, et al. Peptidoglycan recognition proteins kill bacteria by inducing oxidative, thiol, and metal stress. PLoS Pathogens. 2014; 10: e1004280. doi: 10.1371/journal.ppat.1004280
12. Wang Z-M, Li X, Cocklin RR, Wang M, Wang M, Fukase K, et al. Human peptidoglycan recognition protein-L is an N-Acetylmuramoyl-L-Alanine amidase. J Biol Chem. 2003; 278: 49044-49052.
13. Saha S, Jing X, Park SY, Wang S, Li X, Gupta D, et al. Peptidoglycan Recognition Proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-γ. Cell Host Microbe. 2010; 8: 147-162. doi: 10.1016/j.chom.2010.07.005
14. Jing X, Zulfiqar F, Park SY, Núñez G, Dziarski R, Gupta D. Peptidoglycan recognition protein 3 and Nod2 synergistically protect mice from dextran sodium sulfate-induced colitis. J Immunol. 2014; 193: 3055-3069. doi: 10.4049/jimmunol.1301548
15. Saha S, Qi J, Wang S, Wang M, Li X, Kim Y-G, et al. PGLYRP-2 and Nod2 are both required for peptidoglycan-induced arthritis and local inflammation. Cell Host Microbe. 2009; 5: 137-150. doi: 10.1016/j. chom.2008.12.010
16. Park SY, Gupta D, Hurwich R, Kim CH, Dziarski R. Peptidoglycan recognition protein Pglyrp2 protects mice from psoriasis-like skin inflammation by promoting regulatory T cells and limiting Th17 responses. J Immunol. 2011; 187: 5813-5823. doi: 10.4049/jimmunol.1101068
17. Park SY, Gupta D, Kim CH, Dziarski R. Differential effects of peptidoglycan recognition proteins on experimental atopic and contact dermatitis mediated by Treg and Th17 cells. PLoS One 2011; 6: e24961. doi: 10.1371/journal.pone.0024961
18. Park SY, Jing X, Gupta D, Dziarski R. Peptidoglycan recognition protein 1 enhances experimental asthma by promoting Th2 and Th17 and limiting regulatory T cell and plasmacytoid dendritic cell responses. J Immunol. 2013; 190: 3480-3492. doi: 10.4049/jimmunol.1202675
19. Gowda RN, Redfern R, Frikeche J, Pinglay S, Foster JW, Lema C, et al. Functions of peptidoglycan recognition proteins (Pglyrps) at the ocular surface: bacterial keratitis in gene-Targeted mice deficient in Pglyrp-2,-3 and-4. PLoS One. 2015; 10: e0137129. doi: 10.1371/journal.pone.0137129
20. Read CB, Kuijper JL, Hjorth SA, Heipel MD, Tang X, Fleetwood AJ, et al. Cutting Edge: Identification of neutrophil PGLYRP1 as a ligand for TREM-1. J Immunol. 2015; 194: 1417-1421. doi: 10.4049/jimmunol.1402303
21. Bloom SM, Bijanki VN, Nava GM, Sun L, Malvin NP, Donermeyer DL, et al. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. Cell Host Microbe. 2011; 9: 390-403. doi: 10.1016/j.chom.2011.04.009
22. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011; 145: 745-757. doi: 10.1016/j.cell.2011. 04.022
23. Kang SS, Bloom SM, Norian LA, Geske MJ, Flavell RA, Stappenbeck TS, et al. An antibiotic-responsive mouse model of fulminant ulcerative colitis. PLoS Med. 2008; 5: e41. doi: 10.1371/journal.pmed. 0050041
24. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139: 485-498. doi: 10.1016/j.cell.2009.09.033
25. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010; 330: 1768-73. doi: 10.1126/science.1195568
26. Stepankova R, Powrie F, Kofronova O, Kozakova H, Hudcovic T, Hrncir T, et al. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis. 2007; 13:1202-1211.
27. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 2006; 55: 205-211.
28. Scanlan PD, Shanahan F, O'Mahony C, Marchesi JR. Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease. J Clin Microbiol. 2006; 44: 3980-3988.
29. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007; 104: 13780-13785.
30. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009; 15: 1183-1189. doi: 10.1002/ibd. 20903
31. Willing B, Halfvarson J, Dicksved J, Rosenquist M, Järnerot G, Engstrand L, et al. Twin studies reveal specific imbalances in the mucosa-Associated microbiota of patients with ileal Crohn's disease. Inflamm Bowel Dis. 2009; 15: 653-660. doi: 10.1002/ibd.20783
32. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010; 139: 1844-1854. doi: 10.1053/j.gastro.2010.08.049
33. Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H. Disease phenotype and genotype are associated with shifts in intestinal-Associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011; 17: 179-184. doi: 10.1002/ibd.21339
34. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, et al. A decrease of the butyrateproducing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014; 63: 1275-1283. doi: 10.1136/gutjnl-2013-304833
35. Huttenhower C, Kostic AD, Xavier RJ. Inflammatory bowel disease as a model for translating the microbiome. Immunity. 2014; 40: 843-854. doi: 10.1016/j.immuni.2014.05.013
36. Shanahan F, Quigley EM. Manipulation of the microbiota for treatment of IBS and IBD-challenges and controversies. Gastroenterology. 2014; 146: 1554-1563. doi: 10.1053/j.gastro.2014.01.050
37. Ianiro G, Bibbò S, Scaldaferri F, Gasbarrini A, Cammarota G. Fecal microbiota transplantation in inflammatory bowel disease: beyond the excitement. Medicine (Baltimore). 2014; 93: e97.
38. Colman RJ, Rubin DT. Fecal microbiota transplantation as therapy for inflammatory bowel disease: A systematic review and meta-Analysis. J Crohns Colitis. 2014; 8: 1569-1581. doi: 10.1016/j.crohns. 2014.08.006
39. Mizoguchi A. Animal models of inflammatory bowel disease. Prog Mol Biol Transl Sci. 2012; 105: 263-320. doi: 10.1016/B978-0-12-394596-9.00009-3
40. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007; 131: 33-45.
41. Hashimoto T, Perlot T, Rehman A, Trichereau J, Ishiguro H, Paolino M, et al. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature. 2012; 487: 477-481. doi: 10. 1038/nature11228
42. Zenewicz LA, Yin X, Wang G, Elinav E, Hao L, Zhao L, et al. IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic. J Immunol. 2013; 190: 5306-5312. doi: 10.4049/jimmunol. 1300016
43. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013; 123: 700-711. doi: 10.1172/JCI62236
44. Kullberg MC, Ward JM, Gorelick PL, Caspar P, Hieny S, Cheever A, et al. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12-And gamma interferon-dependent mechanism. Infect Immun. 1998; 66: 5157-5166.
45. Erdman SE, Rao VP, Poutahidis T, Rogers AB, Taylor CL, Jackson EA, et al. Nitric oxide and TNF-α trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci USA. 2009; 106: 1027-1032. doi: 10.1073/pnas.0812347106
46. Chow J, Mazmanian SK. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe. 2010; 7: 265-276. doi: 10.1016/j.chom.2010.03.004
47. Chassaing B, Koren O, Carvalho FA, Ley RE, Gewirtz AT. AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition. Gut. 2014; 63: 1069-1080. doi: 10.1136/gutjnl-2013-304909
48. Yang I, Eibach D, Kops F, Brenneke B, Woltemate S, Schulze J, et al. Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PLoS One. 2013; 8: e70783. doi: 10.1371/journal.pone.0070783
49. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008; 105: 16731-16736. doi: 10.1073/pnas. 0804812105
50. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011; 331: 337-341. doi: 10.1126/science. 1198469
51. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008; 453: 620-625. doi: 10.1038/nature07008
52. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 2010; 107: 12204-12209. doi: 10.1073/pnas. 0909122107
53. Brinkman BM, Becker A, Ayiseh RB, Hildebrand F, Raes J, Huys G, et al. Gut microbiota affects sensitivity to acute DSS-induced colitis independently of host genotype. Inflamm Bowel Dis. 2013; 19: 2560-2567. doi: 10.1097/MIB.0b013e3182a8759a
54. Lucke K, Miehlke S, Jacobs E, Schuppler M. Prevalence of Bacteroides and Prevotella spp. in ulcerative colitis. J Med Microbiol. 2006; 55: 617-624.
55. Larmonier CB, Laubitz D, Hill FM, Shehab KW, Lipinski L, Midura-Kiela MT, et al. Reduced colonic microbial diversity is associated with colitis in NHE3-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2013; 305: G667-G677. doi: 10.1152/ajpgi.00189.2013
56. Zitomersky NL, Atkinson BJ, Franklin SW, Mitchell PD, Snapper SB, Comstock LE, et al. Characterization of adherent Bacteroidales from intestinal biopsies of children and young adults with inflammatory bowel disease. PLoS One. 2013; 8: e63686. doi: 10.1371/journal.pone.0063686
57. De Cruz P, Kang S, Wagner J, Buckley M, Sim WH, Prideaux L, et al. Association between specific mucosa-Associated microbiota in Crohn's disease at the time of resection and subsequent disease recurrence: A pilot study. J Gastroenterol Hepatol. 2015; 30: 268-278. doi: 10.1111/jgh.12694
58. Noor SO, Ridgway K, Scovell L, Kemsley EK, Lund EK, Jamieson C, et al. Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol. 2010; 10: 134. doi: 10.1186/1471-230X-10-134
59. Wright DP, Rosendale DI, Robertson AM. Prevotella enzymes involved in mucin oligosaccharide degradation and evidence for a small operon of genes expressed during growth on mucin. FEMS Microbiol Lett. 2000; 190: 73-79.
60. Tsai HH, Dwarakanath AD, Hart CA, Milton JD, Rhodes JM. Increased faecal mucin sulphatase activity in ulcerative colitis: A potential target for treatment. Gut. 1995; 36: 570-576.
61. Said HS, Suda W, Nakagome S, Chinen H, Oshima K, Kim S, et al. Dysbiosis of salivary microbiota in inflammatory bowel disease and its association with oral immunological biomarkers. DNA Res. 2014; 21: 15-25. doi: 10.1093/dnares/dst037
62. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ. New bacterial species associated with chronic periodontitis. J Dent Res. 2003; 82: 338-344.
63. Kverka M, Zakostelska Z, Klimesova K, Sokol D, Hudcovic T, Hrncir T, et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol. 2011; 163: 250-259. doi: 10.1111/j.1365-2249.2010. 04286.x
64. Comstock LE. Importance of glycans to the host-bacteroides mutualism in the mammalian intestine. Cell Host Microbe. 2009; 5: 522-526. doi: 10.1016/j.chom.2009.05.010
65. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011; 473: 174-180. doi: 10.1038/nature09944
66. Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, et al. Major phenylpropanoidderived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res. 2013; 57: 523-535. doi: 10.1002/mnfr.201200594
67. Zulfiqar F, Hozo I, Rangarajan S, Mariuzza R, Dziarski R, Gupta D. Genetic association of peptidoglycan recognition protein variants with inflammatory bowel disease. PLoS One. 2013; 8: e67393.
68. Rioux JD, Silverberg MS, Daly MJ, Steinhart AH, McLeod RS, Griffiths AM, et al. Genomewide search in Canadian families with inflammatory bowel disease reveals two novel susceptibility loci. Am J Hum Genet. 2000; 66: 1863-1870.
69. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012; 491: 119-124. doi: 10.1038/nature11582
70. Sun C, Mathur P, Dupuis J, Tizard R, Ticho B, Crowell T, et al. Peptidoglycan recognition proteins Pglyrp3 and Pglyrp4 are encoded from the epidermal differentiation complex and are candidate genes for the Psors4 locus on chromosome 1q21. Hum Genet. 2006; 119: 113-125.
71. Kainu K, Kivinen K, Zucchelli M, Suomela S, Kere J, Inerot A, et al. Association of psoriasis to PGLYRP and SPRR genes at PSORS4 locus on 1q shows heterogeneity between Finnish, Swedish and Irish families. Exp Dermatol. 2009; 18: 109-115. doi: 10.1111/j.1600-0625.2008.00769.x
72. Dziarski R, Platt KA, Gelius E, Steiner H, Gupta D. Defect in neutrophil killing and increased susceptibility to infection with non-pathogenic Gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood. 2003; 102: 689-697.
73. Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011; 131: 2026-2032. doi: 10.1038/jid.2011.168
74. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, Ferris MJ. Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS One. 2011; 6: e26732. doi: 10.1371/journal.pone.0026732
75. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72: 5069-5072.
76. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73: 5261-5267.
77. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26: 266-267. doi: 10.1093/bioinformatics/btp636
78. Hamady M, Lozupone C, Knight R. Fast UniFrac: Facilitating high-Throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 2010; 4: 17-27. doi: 10.1038/ismej.2009.97
79. Rautio M, Eerola E, Väisänen-Tunkelrott ML, Molitoris D, Lawson P, Collins MD, et al. Reclassification of Bacteroides putredinis (Weinberg et al., 1937) in a new genus Alistipes gen. nov., as Alistipes putredinis comb. nov., and description of Alistipes finegoldii sp. nov., from human sources. Syst Appl Microbiol. 2003; 26: 182-188.
80. Sakamoto M, Kumada H, Hamada N, Takahashi Y, Okamoto M, Bakir MA, et al. Prevotella falsenii sp. nov., a Prevotella intermedia-like organism isolated from monkey dental plaque. Int J Syst Evol Microbiol. 2009; 59: 319-322. doi: 10.1099/ijs.0.002626-0