Salmonella Degrades the Host Glycocalyx Leading to Altered Infection and Glycan Remodeling

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Arabyan, Narine ^a   Park, Dayoung ^a   Foutouhi, Soraya ^a   Weis, Allison M ^a   Huang, Bihua C ^a   Williams, Cynthia C ^a   Desai, Prerak ^a,d   Shah, Jigna ^a,e   Jeannotte, Richard ^a,b   Kong, Nguyet ^a   Lebrilla, Carlito B ^a,c   Weimer, Bart C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD DE TARAPACÁ   (Chile)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ZOETIS   (United States)

^e MPI RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOSIDASE; POLYSACCHARIDE; VIRULENCE FACTOR;

CACO-2 CELL LINE; CELL LINE; CHEMISTRY; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GLYCOCALYX; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN DEGRADATION; SALMONELLA ENTERICA SEROVAR TYPHI;

BACTERIAL PROTEINS; CACO-2 CELLS; CELL LINE; GENE DELETION; GENE EXPRESSION REGULATION; GLYCOCALYX; GLYCOSIDE HYDROLASES; HOST-PATHOGEN INTERACTIONS; HUMANS; IN VITRO TECHNIQUES; INTESTINAL MUCOSA; POLYSACCHARIDES; PROTEOLYSIS; SALMONELLA TYPHI; VIRULENCE FACTORS;

EID: 84978114987     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29525     Document Type: Article

References (62)

1. Moran, A. P., Gupta, A. & Joshi, L. Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60, 1412-1425, doi: 10.1136/gut.2010.212704 (2011)
2. McGuckin, M. A., Linden, S. K., Sutton, P. & Florin, T. H. Mucin dynamics and enteric pathogens. Nature reviews. Microbiology 9, 265-278, doi: 10.1038/nrmicro2538 (2011)
3. Varki, A. Evolutionary forces shaping the Golgi glycosylation machinery: why cell surface glycans are universal to living cells. Cold Spring Harbor perspectives in biology 3, doi: 10.1101/cshperspect.a005462 (2011)
4. Imai, M. & Kawaoka, Y. The role of receptor binding specificity in interspecies transmission of influenza viruses. Current opinion in virology 2, 160-167, doi: 10.1016/j.coviro.2012.03.003 (2012)
5. de Graaf, M. & Fouchier, R. A. Role of receptor binding specificity in influenza A virus transmission and pathogenesis. The EMBO journal 33, 823-841, doi: 10.1002/embj.201387442 (2014)
6. Bry, L., Falk, P. G. & Gordon, J. L. Genetic engineering of carbohydrate biosynthetic pathways in transgenic mice demonstrates cell cycle-associated regulation of glycoconjugate production in small intestinal epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 93, 1161-1166 (1996)
7. Hooper, L. V., Xu, J., Falk, P. G., Midtvedt, T. & Gordon, J. I. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proceedings of the National Academy of Sciences of the United States of America 96, 9833-9838 (1999)
8. Huang, Y. L., Chassard, C., Hausmann, M., von Itzstein, M. & Hennet, T. Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat Commun 6, 8141, doi: 10.1038/ncomms9141 (2015)
9. Ng, K. M. et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502, 96-99, doi: 10.1038/nature12503 (2013)
10. Pickard, J. M. & Chervonsky, A. V. Intestinal fucose as a mediator of host-microbe symbiosis. J Immunol 194, 5588-5593, doi: 10.4049/jimmunol.1500395 (2015)
11. Tailford, L. E., Crost, E. H., Kavanaugh, D. & Juge, N. Mucin glycan foraging in the human gut microbiome. Front Genet 6, 81, doi: 10.3389/fgene.2015.00081 (2015)
12. Bergstrom, K. S. & Xia, L. Mucin-type O-glycans and their roles in intestinal homeostasis. Glycobiology 23, 1026-1037, doi: 10.1093/ glycob/cwt045 (2013)
13. El Kaoutari, A., Armougom, F., Gordon, J. I., Raoult, D. & Henrissat, B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nature reviews. Microbiology 11, 497-504, doi: 10.1038/nrmicro3050 (2013)
14. Marcobal, A., Southwick, A. M., Earle, K. A. & Sonnenburg, J. L. A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 23, 1038-1046, doi: 10.1093/glycob/cwt040 (2013)
15. Johansson, M. E. et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proceedings of the National Academy of Sciences of the United States of America 105, 15064-15069, doi: 10.1073/pnas.0803124105 (2008)
16. Cantarel, B. L. et al. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic acids research 37, D233-238, doi: 10.1093/nar/gkn663 (2009)
17. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic acids research 42, D490-495, doi: 10.1093/nar/gkt1178 (2014)
18. Eilam, O. et al. Glycan degradation (GlyDeR) analysis predicts mammalian gut microbiota abundance and host diet-specific adaptations. mBio 5, doi: 10.1128/mBio.01526-14 (2014)
19. Lim, J. S. et al. Caveolae-mediated entry of Salmonella typhimurium into senescent nonphagocytotic host cells. Aging cell 9, 243-251, doi: 10.1111/j.1474-9726.2010.00554.x (2010)
20. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences of the United States of America 97, 6640-6645, doi: 10.1073/pnas.120163297 (2000)
21. Dos Santos, P. C., Fang, Z., Mason, S. W., Setubal, J. C. & Dixon, R. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC genomics 13, 162, doi: 10.1186/1471-2164-13-162 (2012)
22. Smith, A. C. et al. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. The Journal of cell biology 176, 263-268, doi: 10.1083/jcb.200611056 (2007)
23. Chu, C. S. et al. Profile of native N-linked glycan structures from human serum using high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. Proteomics 9, 1939-1951, doi: 10.1002/pmic.200800249 (2009)
24. Kronewitter, S. R. et al. The development of retrosynthetic glycan libraries to profile and classify the human serum N-linked glycome. Proteomics 9, 2986-2994, doi: 10.1002/pmic.200800760 (2009)
25. Pickard, J. M. et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514, 638-641, doi: 10.1038/nature13823 (2014)
26. Kirmiz, C. et al. A serum glycomics approach to breast cancer biomarkers. Molecular & cellular proteomics: MCP 6, 43-55, doi: 10.1074/mcp.M600171-MCP200 (2007)
27. Bishop, J. R. & Gagneux, P. Evolution of carbohydrate antigens-microbial forces shaping host glycomes? Glycobiology 17, 23R-34R, doi: 10.1093/glycob/cwm005 (2007)
28. An, H. J., Kronewitter, S. R., de Leoz, M. L. & Lebrilla, C. B. Glycomics and disease markers. Current opinion in chemical biology 13, 601-607, doi: 10.1016/j.cbpa.2009.08.015 (2009)
29. Lebrilla, C. B. & An, H. J. The prospects of glycan biomarkers for the diagnosis of diseases. Molecular bioSystems 5, 17-20, doi: 10.1039/b811781k (2009)
30. Jacobsen, A., Hendriksen, R. S., Aaresturp, F. M., Ussery, D. W. & Friis, C. The Salmonella enterica pan-genome. Microbial ecology 62, 487-504, doi: 10.1007/s00248-011-9880-1 (2011)
31. Gordienko, E. N., Kazanov, M. D. & Gelfand, M. S. Evolution of pan-genomes of Escherichia coli, Shigella spp., and Salmonella enterica. Journal of bacteriology 195, 2786-2792, doi: 10.1128/JB.02285-12 (2013)
32. Lai, Y. Y. et al. [A comparative study of fluorescence in situ hybridization versus conventional cytogenetics in the detection of clonal aberrations in myelodysplastic syndrome]. Zhonghua Yi Xue Za Zhi 93, 3175-3179 (2013)
33. He, X., Mishchuk, D. O., Shah, J., Weimer, B. C. & Slupsky, C. M. Cross-talk between E. coli strains and a human colorectal adenocarcinoma-derived cell line. Scientific reports 3, 3416, doi: 10.1038/srep03416 (2013)
34. Shah, J., Desai, P. T., Chen, D., Stevens, J. R. & Weimer, B. C. Preadaptation to cold stress in Salmonella enterica serovar Typhimurium increases survival during subsequent acid stress exposure. Applied and environmental microbiology 79, 7281-7289, doi: 10.1128/ AEM.02621-13 (2013)
35. Shah, J., Desai, P. T. & Weimer, B. C. Genetic mechanisms underlying the pathogenicity of cold-stressed Salmonella enterica serovar typhimurium in cultured intestinal epithelial cells. Applied and environmental microbiology 80, 6943-6953, doi: 10.1128/ AEM.01994-14 (2014)
36. Ferruzza, S., Rossi, C., Scarino, M. L. & Sambuy, Y. A protocol for differentiation of human intestinal Caco-2 cells in asymmetric serum-containing medium. Toxicology in vitro: an international journal published in association with BIBRA 26, 1252-1255, doi: 10.1016/j.tiv.2012.01.008 (2012)
37. Sambuy, Y. et al. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell biology and toxicology 21, 1-26, doi: 10.1007/s10565-005-0085-6 (2005)
38. Ludeke, C. H., Kong, N., Weimer, B. C., Fischer, M. & Jones, J. L. Complete Genome Sequences of a Clinical Isolate and an Environmental Isolate of Vibrio parahaemolyticus. Genome Announc 3, doi: 10.1128/genomeA.00216-15 (2015)
39. Jeannotte, R et al. Optimization of Covaris Settings for Shearing Bacterial Genomic DNA by Focused Ultrasonication and Analysis Using Agilent 2200 TapeStation (2014)
40. Jeannotte, R et al. High-Throughput Analysis of Foodborne Bacterial Genomic DNA Using Agilent 2200 TapeStation and Genomic DNA ScreenTape System (2014)
41. Kong, N. et al. Integrating the DNA Integrity Number (DIN) to Assess Genomic DNA (gDNA) Quality Control Using the Agilent 2200 TapeStation System (2014)
42. Kong, N et al. Quality Control of High-Throughput Library Construction Pipeline for KAPA HTP Library Using an Agilent 2200 TapeStation (2014)
43. Kong, N., Ng, W., Kelly, L & Weimer, B. C. Quality Control of Library Construction Pipeline for PacBio SMRTbell 10 kb Library Using an Agilent 2200 TapeStation System (2015)
44. Kong, N., Ng, W., Lee, V., Kelly, L & Weimer, B. C. Production and Analysis of High Molecular Weight Genomic DNA for NGS Pipelines Using Agilent DNA Extraction Kit (p/n 200600) (2013)
45. Kong, N et al. Automated Library Construction Using KAPA Library Preparation Kits on the Agilent NGS Workstation Yields High-Quality Libraries for Whole-Genome Sequencing on the Illumina Platform (2014)
46. Kong, N et al. Automation of PacBio SMRTbell 10 kb Template Preparation on an Agilent NGS Workstation (2014)
47. Miller, B. et al. A novel, single tube enzymatic fragmentation and library construction method enables fast turnaround times and improved data qulaity for microbial whole-genome sequencing (2015)
48. Simpson, J. T. et al. ABySS: A parallel assembler for short read sequence data. Genome Res 19, 1117-1123, doi: 10.1101/ Gr.089532.108 (2009)
49. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068-2069, doi: 10.1093/Bioinformatics/Btu153 (2014)
50. Auch, A. F., von Jan, M., Klenk, H. P. & Goker, M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2, 117-134, doi: 10.4056/Sigs.531120 (2010)
51. Meier-Kolthoff, J. P., Auch, A. F., Klenk, H. P. & Goker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. Bmc Bioinformatics 14, doi: 10.1186/1471-2105-14-60 (2013)
52. Darling, A. C., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14, 1394-1403, doi: 10.1101/gr.2289704 (2004)
53. Darling, A. E., Mau, B. & Perna, N. T. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PloS one 5, e11147, doi: 10.1371/journal.pone.0011147 (2010)
54. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research 32, 1792-1797, doi: 10.1093/nar/gkh340 (2004)
55. Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649, doi: 10.1093/bioinformatics/bts199 (2012)
56. Elsinghorst, E. A. Measurement of invasion by gentamicin resistance. Methods in enzymology 236, 405-420 (1994)
57. Desai, P. T., Walsh, M. K. & Weimer, B. C. Solid-phase capture of pathogenic bacteria by using gangliosides and detection with realtime PCR. Applied and environmental microbiology 74, 2254-2258, doi: 10.1128/AEM.02601-07 (2008)
58. Ganesan, B., Dobrowolski, P. & Weimer, B. C. Identification of the leucine-to-2-methylbutyric acid catabolic pathway of Lactococcus lactis. Applied and environmental microbiology 72, 4264-4273, doi: 10.1128/AEM.00448-06 (2006)
59. Xie, Y., Chou, L. S., Cutler, A. & Weimer, B. DNA Macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Applied and environmental microbiology 70, 6738-6747, doi: 10.1128/AEM.70.11.6738-6747.2004 (2004)
60. Marcobal, A. et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell host & microbe 10, 507-514, doi: 10.1016/j.chom.2011.10.007 (2011)
61. Tusher, V. G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 98, 5116-5121, doi: 10.1073/pnas.091062498 (2001)
62. Champine, P. J., Michaelson, J., Weimer, B. C., Welch, D. R. & DeWald, D. B. Microarray analysis reveals potential mechanisms of BRMS1-mediated metastasis suppression. Clinical & experimental metastasis 24, 551-565, doi: 10.1007/s10585-007-9092-8 (2007)