ModM DNA methyltransferase methylome analysis reveals a potential role for Moraxella catarrhalis phasevarions in otitis media

FASEB Journal

Volumn 28, Issue 12, 2014, Pages 5197-5207

  Blakeway, Luke V ^a   Power, Peter M ^a   Jen, Freda E C ^a   Worboys, Sam R ^a   Boitano, Matthew ^b   Clark, Tyson A ^b   Korlach, Jonas ^b   Bakaletz, Lauren O ^c   Jennings, Michael P ^a   Peak, Ian R ^a   Seib, Kate L ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b PACIFIC BIOSCIENCES   (United States)

^c THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

Epigenetic regulation; Middle ear infection; Phase variation; Single molecule, real time genome sequencing; SMRT

Indexed keywords

DNA METHYLTRANSFERASE; MODM DNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; PRIMER DNA;

ALLELE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA METHYLATION; ENZYME ANALYSIS; GENE EXPRESSION; GENE SEQUENCE; GENOME; HOST RESISTANCE; HUMAN; MIDDLE EAR EFFUSION; MORAXELLA CATARRHALIS; MUTATION RATE; NASOPHARYNX; NONHUMAN; OPEN READING FRAME; OTITIS MEDIA; PATHOGENESIS; PHASE VARIABLE REGULON; PROTEIN EXPRESSION; PROTEOMICS; REGULON; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MORAXELLACEAE INFECTION; PATHOGENICITY; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

MORAXELLA CATARRHALIS;

AMINO ACID SEQUENCE; DNA MODIFICATION METHYLASES; DNA PRIMERS; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MORAXELLA (BRANHAMELLA) CATARRHALIS; MORAXELLACEAE INFECTIONS; OTITIS MEDIA; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84919773076     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-256578     Document Type: Article

References (49)

1. Vergison, A. (2008) Microbiology of otitis media: a moving target. Vaccine 26(Suppl. 7), G5-G10
2. Murphy, T. F., and Parameswaran, G. I. (2009) Moraxella catarrhalis, a human respiratory tract pathogen. Clin. Infect. Dis. 49, 124-131
3. Post, J. C., Preston, R. A., Aul, J. J., Larkins-Pettigrew, M., Rydquist-White, J., Anderson, K. W., Wadowsky, R. M., Reagan, D. R., Walker, E. S., Kingsley, L. A., Magit, A. E., and Ehrlich, G. D. (1995) Molecular analysis of bacterial pathogens in otitis media with effusion. JAMA 273, 1598-1604
4. Mackenzie, G. A., Leach, A. J., Carapetis, J. R., Fisher, J., and Morris, P. S. (2010) Epidemiology of nasopharyngeal carriage of respiratory bacterial pathogens in children and adults: crosssectional surveys in a population with high rates of pneumococcal disease. BMC Infect. Dis. 10, 304
5. Faden, H., Duffy, L., Wasielewski, R., Wolf, J., Krystofik, D., and Tung, Y. (1997) Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J. Infect. Dis. 175, 1440-1445
6. Revai, K., Mamidi, D., and Chonmaitree, T. (2008) Association of nasopharyngeal bacterial colonization during upper respiratory tract infection and the development of acute otitis media. Clin. Infect. Dis. 46, e34-e37
7. Faden, H., Harabuchi, Y., and Hong, J. J. (1994) Epidemiology of Moraxella catarrhalis in children during the first 2 years of life: relationship to otitis media. J. Infect. Dis. 169, 1312-1317
8. American Academy of Pediatrics Subcommittee on Management of Acute OM. (2004) Diagnosis and management of acute otitis media. Pediatrics 113, 1451-1465
9. Freid, V. M., Makuc, D. M., and Rooks, R. N. (1998) Ambulatory health care visits by children: principal diagnosis and place of visit. Vital Health Stat. Series 13, 1-23
10. Gonzales, R., Malone, D. C., Maselli, J. H., and Sande, M. A. (2001) Excessive antibiotic use for acute respiratory infections in the United States. Clin. Infect. Dis. 33, 757-762
11. Sethi, S., and Murphy, T. F. (2008) Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N. Engl. J. Med. 359, 2355-2365
12. Murphy, T. F., Brauer, A. L., Grant, B. J., and Sethi, S. (2005) Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. Am. J. Respir. Crit. Care Med. 172, 195-199
13. Mannino, D. M., and Buist, A. S. (2007) Global burden of COPD: risk factors, prevalence, and future trends. Lancet 370, 765-773
14. Revai, K., McCormick, D. P., Patel, J., Grady, J. J., Saeed, K., and Chonmaitree, T. (2006) Effect of pneumococcal conjugate vaccine on nasopharyngeal bacterial colonization during acute otitis media. Pediatrics 117, 1823-1829
15. Moxon, R., Bayliss, C., and Hood, D. (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 40, 307-333
16. Srikhanta, Y. N., Fox, K. L., and Jennings, M. P. (2010) The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol. 8, 196-206
17. Srikhanta, Y. N., Maguire, T. L., Stacey, K. J., Grimmond, S. M., and Jennings, M. P. (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc. Natl. Acad. Sci. U. S. A. 102, 5547-5551
18. Fox, K. L., Dowideit, S. J., Erwin, A. L., Srikhanta, Y. N., Smith, A. L., and Jennings, M. P. (2007) Haemophilus influenzae phasevarions have evolved from type III DNA restriction systems into epigenetic regulators of gene expression. Nucleic Acids Res. 35, 5242-5252
19. Srikhanta, Y. N., Dowideit, S. J., Edwards, J. L., Falsetta, M. L., Wu, H. J., Harrison, O. B., Fox, K. L., Seib, K. L., Maguire, T. L., Wang, A. H., Maiden, M. C., Grimmond, S. M., Apicella, M. A., and Jennings, M. P. (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog 5, e1000400
20. Seib, K. L., Pigozzi, E., Muzzi, A., Gawthorne, J. A., Delany, I., Jennings, M. P., and Rappuoli, R. (2011) A novel epigenetic regulator associated with the hypervirulent Neisseria meningitidis clonal complex 41/44. FASEB J. 25, 3622-3633
21. Srikhanta, Y. N., Gorrell, R. J., Steen, J. A., Gawthorne, J. A., Kwok, T., Grimmond, S. M., Robins-Browne, R. M., and Jennings, M. P. (2011) Phasevarion mediated epigenetic gene regulation in Helicobacter pylori. PLoS One 6, e27569
22. Gawthorne, J. A., Beatson, S. A., Srikhanta, Y. N., Fox, K. L., and Jennings, M. P. (2012) Origin of the diversity in DNA recognition domains in phasevarion associated modA genes of pathogenic Neisseria and Haemophilus influenzae. PLoS One 7, e32337
23. Wion, D., and Casadesus, J. (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol. 4, 183-192
24. Seib, K. L., Peak, I. R., and Jennings, M. P. (2002) Phase variable restriction-modification systems in Moraxella catarrhalis. FEMS Immunol. Med. Microbiol. 32, 159-165
25. Wu, H. J., Seib, K. L., Srikhanta, Y. N., Edwards, J., Kidd, S. P., Maguire, T. L., Hamilton, A., Pan, K. T., Hsiao, H. H., Yao, C. W., Grimmond, S. M., Apicella, M. A., McEwan, A. G., Wang, A. H., and Jennings, M. P. (2010) Manganese regulation of virulence factors and oxidative stress resistance in Neisseria gonorrhoeae. J. Proteomics 73, 899-916
26. Seib, K. L., Oriente, F., Adu-Bobie, J., Montanari, P., Ferlicca, F., Giuliani, M. M., Rappuoli, R., Pizza, M., and Delany, I. (2010) Influence of serogroup B meningococcal vaccine antigens on growth and survival of the meningococcus in vitro and in ex vivo and in vivo models of infection. Vaccine 28, 2416-2427
27. Clark, T. A., Murray, I. A., Morgan, R. D., Kislyuk, A. O., Spittle, K. E., Boitano, M., Fomenkov, A., Roberts, R. J., and Korlach, J. (2012) Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res. 40, e29
28. Song, X., Bandow, J., Sherman, J., Baker, J. D., Brown, P. W., McDowell, M. T., and Molloy, M. P. (2008) iTRAQ experimental design for plasma biomarker discovery. J. Proteome Res. 7, 2952-2958
29. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protocols 1, 2856-2860
30. Roberts, R. J., Vincze, T., Posfai, J., and Macelis, D. (2010) REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res. 38, D234-D236
31. Murphy, T. F. (2009) Vaccine development for Moraxella catarrhalis: rationale, approaches and challenges. Expert Rev. Vaccines 8, 655-658
32. Bootsma, H. J., van Dijk, H., Vauterin, P., Verhoef, J., and Mooi, F. R. (2000) Genesis of BRO β-lactamase-producing Moraxella catarrhalis: evidence for transformation-mediated horizontal transfer. Mol. Microbiol. 36, 93-104
33. Murphy, T. F. (1996) Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60, 267-279
34. Bakaletz, L. O. (2010) Immunopathogenesis of polymicrobial otitis media. J. Leukoc. Biol. 87, 213-222
35. Lafontaine, E. R., Wagner, N. J., and Hansen, E. J. (2001) Expression of the Moraxella catarrhalis UspA1 protein undergoes phase variation and is regulated at the transcriptional level. J. Bacteriol. 183, 1540-1551
36. Wang, W., Pearson, M. M., Attia, A. S., Blick, R. J., and Hansen, E. J. (2007) A UspA2H-negative variant of Moraxella catarrhalis strain O46E has a deletion in a homopolymeric nucleotide repeat common to uspA2H genes. Infect. Immun. 75, 2035-2045
37. Mollenkvist, A., Nordstrom, T., Hallden, C., Christensen, J. J., Forsgren, A., and Riesbeck, K. (2003) The Moraxella catarrhalis immunoglobulin D-binding protein MID has conserved sequences and is regulated by a mechanism corresponding to phase variation. J. Bacteriol. 185, 2285-2295
38. Jen, F. E., Seib, K. L., and Jennings, M. P. (2014) Phasevarions mediate epigenetic regulation of antimicrobial susceptibility in Neisseria meningitidis. Antimicrob Agents Chemother 58, 4219-4221
39. Hoopman, T. C., Liu, W., Joslin, S. N., Pybus, C., Sedillo, J. L., Labandeira-Rey, M., Laurence, C. A., Wang, W., Richardson, J. A., Bakaletz, L. O., and Hansen, E. J. (2012) Use of the chinchilla model for nasopharyngeal colonization to study gene expression by Moraxella catarrhalis. Infect. Immun. 80, 982-995
40. De Vries, S. P., Eleveld, M. J., Hermans, P. W., and Bootsma, H. J. (2013) Characterization of the molecular interplay between Moraxella catarrhalis and human respiratory tract epithelial cells. PLoS One 8, e72193
41. Hoopman, T. C., Liu, W., Joslin, S. N., Pybus, C., Brautigam, C. A., and Hansen, E. J. (2011) Identification of gene products involved in the oxidative stress response of Moraxella catarrhalis. Infect. Immun. 79, 745-755
42. Wang, W., Reitzer, L., Rasko, D. A., Pearson, M. M., Blick, R. J., Laurence, C., and Hansen, E. J. (2007) Metabolic analysis of Moraxella catarrhalis and the effect of selected in vitro growth conditions on global gene expression. Infect. Immun. 75, 4959-4971
43. Wang, W., Joslin, S. N., Pybus, C., Evans, A. S., Lichaa, F., Brautigam, C. A., and Hansen, E. J. (2014) Identification of an outer membrane lipoprotein involved in nasopharyngeal colonization by Moraxella catarrhalis in an animal model. Infect Immun 82, 2287-2299
44. Murray, I. A., Clark, T. A., Morgan, R. D., Boitano, M., Anton, B. P., Luong, K., Fomenkov, A., Turner, S. W., Korlach, J., and Roberts, R. J. (2012) The methylomes of six bacteria. Nucleic Acids Res. 40, 11450-11462
45. Krebes, J., Morgan, R. D., Bunk, B., Sproer, C., Luong, K., Parusel, R., Anton, B. P., Konig, C., Josenhans, C., Overmann, J., Roberts, R. J., Korlach, J., and Suerbaum, S. (2014) The complex methylome of the human gastric pathogen Helicobacter pylori. Nucleic Acids Res. 42, 2415-2432
46. Juni, E., and Bovre, K. (2007) Family II. Moraxellaceae. In Bergey's Manual of Systematic Bacteriology, Vol. 2: The Proteobacteria, Part B: The Gammaproteobacteria (Garrity, G., Brenner, D. J., Krieg, N. R., and Staley, J. R., eds), Springer, New York
47. Davie, J. J., Earl, J., de Vries, S. P., Ahmed, A., Hu, F. Z., Bootsma, H. J., Stol, K., Hermans, P. W., Wadowsky, R. M., Ehrlich, G. D., Hays, J. P., and Campagnari, A. A. (2011) Comparative analysis and supragenome modeling of twelve Moraxella catarrhalis clinical isolates. BMC Genomics 12, 70
48. De Vries, S. P., van Hijum, S. A., Schueler, W., Riesbeck, K., Hays, J. P., Hermans, P. W., and Bootsma, H. J. (2010) Genome analysis of Moraxella catarrhalis strain BBH18, [corrected] a human respiratory tract pathogen. J. Bacteriol. 192, 3574-3583
49. Zomer, A., de Vries, S. P., Riesbeck, K., Meinke, A. L., Hermans, P. W., and Bootsma, H. J. (2012) Genome sequence of Moraxella catarrhalis RH4, an isolate of seroresistant lineage. J. Bacteriol. 194, 6969