Pneumococcal neuraminidase A (NanA) promotes biofilm formation and synergizes with influenza A virus in nasal colonization and middle ear infection

Infection and Immunity

Volumn 85, Issue 4, 2017, Pages

  Wren, John T ^a   Blevins, Lance K ^a   Pang, Bing ^a   Roy, Ankita Basu ^a,b   Oliver, Melissa B ^a,b   Reimche, Jennifer L ^a   Wozniak, Jessie E ^a   Alexander Miller, Martha A ^a   Swords, W Edward ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Biofilms; Neuraminidase; Otitis media; Streptococcus pneumoniae

Indexed keywords

BACTERIAL ENZYME; PNEUMOCOCCAL NEURAMINIDASE A; SIALIDASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIABILITY; BACTERIUM ADHERENCE; BIOFILM; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; IN VITRO STUDY; INFLUENZA A; MIXED INFECTION; MOUSE; NONHUMAN; NOSE; OTITIS MEDIA; PATHOGENESIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; ANIMAL; DISEASE MODEL; ENZYME ACTIVATION; GENETICS; INFLUENZA A VIRUS; METABOLISM; MICROBIOLOGY; NOSE MUCOSA; PHYSIOLOGY; STREPTOCOCCUS PNEUMONIAE; SYMBIOSIS; VIROLOGY;

ANIMALS; BACTERIAL ADHESION; BIOFILMS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; INFLUENZA A VIRUS; MICE; NASAL MUCOSA; NEURAMINIDASE; OTITIS MEDIA; STREPTOCOCCUS PNEUMONIAE; SYMBIOSIS;

EID: 85016211494     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01044-16     Document Type: Article

References (62)

1. Adegbola RA, Obaro SK, Biney E, Greenwood BM. 2001. Evaluation of Binax now Streptococcus pneumoniae urinary antigen test in children in a community with a high carriage rate of pneumococcus. Pediatr Infect Dis J 20:718-719. https://doi.org/10.1097/00006454-200107000-00018.
2. Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S, Wanjiru E, Jomo J, Musyimi R, Lipsitch M, Scott JA. 2012. Rates of acquisition and clearance of pneumococcal serotypes in the nasopharynges of children in Kilifi District, Kenya. J Infect Dis 206:1020-1029. https://doi.org/10.1093/infdis/jis447.
3. Bogaert D, De Groot R, Hermans PW. 2004. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 4:144-154. https://doi.org/10.1016/S1473-3099(04)00938-7.
4. Casey JR, Adlowitz DG, Pichichero ME. 2010. New patterns in the otopathogens causing acute otitis media six to eight years after introduction of pneumococcal conjugate vaccine. Pediatr Infect Dis J 29: 304-309. https://doi.org/10.1097/INF.0b013e3181c1bc48.
5. Monasta L, Ronfani L, Marchetti F, Montico M, Vecchi Brumatti L, Bavcar A, Grasso D, Barbiero C, Tamburlini G. 2012. Burden of disease caused by otitis media: systematic review and global estimates. PLoS One 7:e36226. https://doi.org/10.1371/journal.pone.0036226.
6. Chonmaitree T, Revai K, Grady JJ, Clos A, Patel JA, Nair S, Fan J, Henrickson KJ. 2008. Viral upper respiratory tract infection and otitis media complication in young children. Clin Infect Dis 46:815-823. https://doi.org/10.1086/528685.
7. Ruohola A, Pettigrew MM, Lindholm L, Jalava J, Raisanen KS, Vainionpaa R, Waris M, Tahtinen PA, Laine MK, Lahti E, Ruuskanen O, Huovinen P. 2013 Bacterial and viral interactions within the nasopharynx contribute to the risk of acute otitis media. J Infect 66:247-254. https://doi.org/10.1016/j.jinf.2012.12.002.
8. Diavatopoulos DA, Short KR, Price JT, Wilksch JJ, Brown LE, Briles DE, Strugnell RA, Wijburg OL. 2010. Influenza A virus facilitates Streptococcus pneumoniae transmission and disease. FASEB J 24:1789-1798. https://doi.org/10.1096/fj.09-146779.
9. McCullers JA, McAuley JL, Browall S, Iverson AR, Boyd KL, Henriques Normark B. 2010. Influenza enhances susceptibility to natural acquisition of and disease due to Streptococcus pneumoniae in ferrets. J Infect Dis 202:1287-1295. https://doi.org/10.1086/656333.
10. Short KR, Reading PC, Brown LE, Pedersen J, Gilbertson B, Job ER, Edenborough KM, Habets MN, Zomer A, Hermans PW, Diavatopoulos DA, Wijburg OL. 2013. Influenza-induced inflammation drives pneumococcal otitis media. Infect Immun 81:645-652. https://doi.org/10.1128/IAI.01278-12.
11. Wadowsky RM, Mietzner SM, Skoner DP, Doyle WJ, Fireman P. 1995. Effect of experimental influenza A virus infection on isolation of Streptococcus pneumoniae and other aerobic bacteria from the oropharynges of allergic and nonallergic adult subjects. Infect Immun 63:1153-1157.
12. Wren JT, Blevins LK, Pang B, King LB, Perez AC, Murrah KA, Reimche JL, Alexander-Miller MA, Swords WE. 2014. Influenza A virus alters pneumococcal nasal colonization and middle ear infection independently of phase variation. Infect Immun 82:4802-4812. https://doi.org/10.1128/IAI.01856-14.
13. Blevins LK, Wren JT, Holbrook BC, Hayward SL, Swords WE, Parks GD, Alexander-Miller MA. 2014. Coinfection with Streptococcus pneumoniae negatively modulates the size and composition of the ongoing influenza-specific CD8(+) T cell response. J Immunol 193:5076-5087. https://doi.org/10.4049/jimmunol.1400529.
14. Lewis AL, Lewis WG. 2012. Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14:1174-1182. https://doi.org/10.1111/j.1462-5822.2012.01807.x.
15. Peltola VT, McCullers JA. 2004. Respiratory viruses predisposing to bacterial infections: role of neuraminidase. Pediatr Infect Dis J 23:S87-S97. https://doi.org/10.1097/01.inf.0000108197.81270.35.
16. Kamali A, Holodniy M. 2013. Influenza treatment and prophylaxis with neuraminidase inhibitors: a review. Infect Drug Resist 6:187-198. https://doi.org/10.2147/IDR.S36601.
17. McCullers JA, Bartmess KC. 2003. Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J Infect Dis 187:1000-1009. https://doi.org/10.1086/368163.
18. Siegel SJ, Roche AM, Weiser JN. 2014. Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe 16:55-67. https://doi.org/10.1016/j.chom.2014.06.005.
19. Nita-Lazar M, Banerjee A, Feng C, Amin MN, Frieman MB, Chen WH, Cross AS, Wang LX, Vasta GR. 2015. Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. Mol Immunol 65:1-16. https://doi.org/10.1016/j.molimm.2014.12.010.
20. Berry AM, Lock RA, Paton JC. 1996. Cloning and characterization of nanB, a second Streptococcus pneumoniae neuraminidase gene, and purification of the NanB enzyme from recombinant Escherichia coli. J Bacteriol 178:4854-4860. https://doi.org/10.1128/jb.178.16.4854-4860.1996.
21. Kelly RT, Farmer S, Greiff D. 1967. Neuraminidase activities of clinical isolates of Diplococcus pneumoniae. J Bacteriol 94:272-273.
22. King SJ, Hippe KR, Gould JM, Bae D, Peterson S, Cline RT, Fasching C, Janoff EN, Weiser JN. 2004. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol 54:159-171. https://doi.org/10.1111/j.1365-2958.2004.04252.x.
23. King SJ, Whatmore AM, Dowson CG. 2005. NanA, a neuraminidase from Streptococcus pneumoniae, shows high levels of sequence diversity, at least in part through recombination with Streptococcus oralis. J Bacteriol 187:5376-5386. https://doi.org/10.1128/JB.187.15.5376-5386.2005.
24. Manco S, Hernon F, Yesilkaya H, Paton JC, Andrew PW, Kadioglu A. 2006. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun 74: 4014-4020. https://doi.org/10.1128/IAI.01237-05.
25. Jedrzejas MJ. 2001. Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev 65:187-207. https://doi.org/10.1128/MMBR.65.2.187-207.2001.
26. Tong HH, Liu X, Chen Y, James M, Demaria T. 2002. Effect of neuraminidase on receptor-mediated adherence of Streptococcus pneumoniae to chinchilla tracheal epithelium. Acta Otolaryngol 122:413-419. https://doi.org/10.1080/00016480260000111.
27. Dalia AB, Standish AJ, Weiser JN. 2010. Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun 78:2108-2116. https://doi.org/10.1128/IAI.01125-09.
28. Burnaugh AM, Frantz LJ, King SJ. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190:221-230. https://doi.org/10.1128/JB.01251-07.
29. Trappetti C, Kadioglu A, Carter M, Hayre J, Iannelli F, Pozzi G, Andrew PW, Oggioni MR. 2009. Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis 199:1497-1505. https://doi.org/10.1086/598483.
30. Brittan JL, Buckeridge TJ, Finn A, Kadioglu A, Jenkinson HF. 2012. Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae. Mol Oral Microbiol 27:270-283. https://doi.org/10.1111/j.2041-1014.2012.00658.x.
31. Parker D, Soong G, Planet P, Brower J, Ratner AJ, Prince A. 2009. The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect Immun 77:3722-3730. https://doi.org/10.1128/IAI.00228-09.
32. Soong G, Muir A, Gomez MI, Waks J, Reddy B, Planet P, Singh PK, Kaneko Y, Wolfgang MC, Hsiao YS, Tong L, Prince A. 2006. Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest 116:2297-2305. https://doi.org/10.1172/JCI27920.
33. Roy S, Honma K, Douglas CW, Sharma A, Stafford GP. 2011. Role of sialidase in glycoprotein utilization by Tannerella forsythia. Microbiology 157:3195-3202. https://doi.org/10.1099/mic.0.052498-0.
34. Tong HH, Blue LE, James MA, DeMaria TF. 2000. Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase-deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect Immun 68:921-924. https://doi.org/10.1128/IAI.68.2.921-924.2000.
35. Berry AM, Paton JC. 2000. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun 68:133-140. https://doi.org/10.1128/IAI.68.1.133-140.2000.
36. LeMessurier KS, Ogunniyi AD, Paton JC. 2006. Differential expression of key pneumococcal virulence genes in vivo. Microbiology 152:305-311. https://doi.org/10.1099/mic.0.28438-0.
37. Oggioni MR, Trappetti C, Kadioglu A, Cassone M, Iannelli F, Ricci S, Andrew PW, Pozzi G. 2006. Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol Microbiol 61:1196-1210. https://doi.org/10.1111/j.1365-2958.2006.05310.x.
38. Kadioglu A, Weiser JN, Paton JC, Andrew PW. 2008. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6:288-301. https://doi.org/10.1038/nrmicro1871.
39. Xu G, Potter JA, Russell RJ, Oggioni MR, Andrew PW, Taylor GL. 2008. Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J Mol Biol 384:436-449. https://doi.org/10.1016/j.jmb.2008.09.032.
40. Marks LR, Parameswaran GI, Hakansson AP. 2012. Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo. Infect Immun 80:2744-2760. https://doi.org/10.1128/IAI.00488-12.
41. Reid SD, Hong W, Dew KE, Winn DR, Pang B, Watt J, Glover DT, Hollingshead SK, Swords WE. 2009. Streptococcus pneumoniae forms surfaceattached communities in the middle ear of experimentally infected chinchillas. J Infect Dis 199:786-794. https://doi.org/10.1086/597042.
42. Perez AC, Pang B, King LB, Tan L, Murrah KA, Reimche JL, Wren JT, Richardson SH, Ghandi U, Swords WE. 2014. Residence of Streptococcus pneumoniae and Moraxella catarrhalis within polymicrobial biofilm promotes antibiotic resistance and bacterial persistence in vivo. Pathog Dis 70:280-288. https://doi.org/10.1111/2049-632X.12129.
43. Walther E, Richter M, Xu Z, Kramer C, von Grafenstein S, Kirchmair J, Grienke U, Rollinger JM, Liedl KR, Slevogt H, Sauerbrei A, Saluz HP, Pfister W, Schmidtke M. 2014. Antipneumococcal activity of neuraminidase inhibiting artocarpin. Int J Med Microbiol 305:289-297. https://doi.org/10.1016/j.ijmm.2014.12.004.
44. Weiser JN, Austrian R, Sreenivasan PK, Masure HR. 1994. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun 62:2582-2589.
45. Marom T, Nokso-Koivisto J, Chonmaitree T. 2012. Viral-bacterial interactions in acute otitis media. Curr Allergy Asthma Rep 12:551-558. https://doi.org/10.1007/s11882-012-0303-2.
46. Tong HH, Grants I, Liu X, DeMaria TF. 2002. Comparison of alteration of cell surface carbohydrates of the chinchilla tubotympanum and colonial opacity phenotype of Streptococcus pneumoniae during experimental pneumococcal otitis media with or without an antecedent influenza A virus infection. Infect Immun 70:4292-4301. https://doi.org/10.1128/IAI.70.8.4292-4301.2002.
47. King SJ, Hippe KR, Weiser JN. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol 59:961-974. https://doi.org/10.1111/j.1365-2958.2005.04984.x.
48. King QO, Lei B, Harmsen AG. 2009. Pneumococcal surface protein A contributes to secondary Streptococcus pneumoniae infection after influenza virus infection. J Infect Dis 200:537-545. https://doi.org/10.1086/600871.
49. Kato K, Takegawa Y, Ralston KS, Gilchrist CA, Hamano S, Petri WA, Jr, Shinohara Y. 2013. Sialic acid-dependent attachment of mucins from three mouse strains to Entamoeba histolytica. Biochem Biophys Res Commun 436:252-258. https://doi.org/10.1016/j.bbrc.2013.05.085.
50. Tong HH, James M, Grants I, Liu X, Shi G, DeMaria TF. 2001. Comparison of structural changes of cell surface carbohydrates in the eustachian tube epithelium of chinchillas infected with a Streptococcus pneumoniae neuraminidase-deficient mutant or its isogenic parent strain. Microb Pathog 31:309-317. https://doi.org/10.1006/mpat.2001.0473.
51. LaMarco KL, Diven WF, Glew RH, Doyle WJ, Cantekin EI. 1984. Neuraminidase activity in middle ear effusions. Ann Otol Rhinol Laryngol 93(Pt 1):76-84.
52. Uchiyama S, Carlin AF, Khosravi A, Weiman S, Banerjee A, Quach D, Hightower G, Mitchell TJ, Doran KS, Nizet V. 2009. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med 206:1845-1852. https://doi.org/10.1084/jem.20090386.
53. Limoli DH, Sladek JA, Fuller LA, Singh AK, King SJ. 2011. BgaA acts as an adhesin to mediate attachment of some pneumococcal strains to human epithelial cells. Microbiology 157:2369-2381. https://doi.org/10.1099/mic.0.045609-0.
54. Nishikawa T, Shimizu K, Tanaka T, Kuroda K, Takayama T, Yamamoto T, Hanada N, Hamada Y. 2012. Bacterial neuraminidase rescues influenza virus replication from inhibition by a neuraminidase inhibitor. PLoS One 7:e45371. https://doi.org/10.1371/journal.pone.0045371.
55. Li C, Kurniyati Hu B, Bian J, Sun J, Zhang W, Liu J, Pan Y, Li C. 2012. Abrogation of neuraminidase reduces biofilm formation, capsule biosynthesis, and virulence of Porphyromonas gingivalis. Infect Immun 80: 3-13. https://doi.org/10.1128/IAI.05773-11.
56. Andersson B, Dahmen J, Frejd T, Leffler H, Magnusson G, Noori G, Eden CS. 1983. Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells. J Exp Med 158:559-570. https://doi.org/10.1084/jem.158.2.559.
57. Briles DE, Crain MJ, Gray BM, Forman C, Yother J. 1992. Strong association between capsular type and virulence for mice among human isolates of Streptococcus pneumoniae. Infect Immun 60:111-116.
58. Coats MT, Murphy T, Paton JC, Gray B, Briles DE. 2011. Exposure of Thomsen-Friedenreich antigen in Streptococcus pneumoniae infection is dependent on pneumococcal neuraminidase A. Microb Pathog 50: 343-349. https://doi.org/10.1016/j.micpath.2011.02.010.
59. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, García-Sastre A. 2010. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc Natl Acad Sci U S A 107:11531-11536. https://doi.org/10.1073/pnas.0914994107.
60. Aminoff D. 1961. Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids. Biochem J 81:384-392. https://doi.org/10.1042/bj0810384.
61. Skoza L, Mohos S. 1976. Stable thiobarbituric acid chromophore with dimethyl sulphoxide. Application to sialic acid assay in analytical de-Oacetylation. Biochem J 159:457-462.
62. Warren L. 1959. The thiobarbituric acid assay of sialic acids. J Biol Chem 234:1971-1975.