Effect of serotype on pneumococcal competition in a mouse colonization model

mBio

Volumn 6, Issue 5, 2015, Pages

  Trzciński, Krzysztof ^a,b,c   Li, Yuan ^a   Weinberger, Daniel M ^a   Thompson, Claudette M ^a   Cordy, Derrick ^a   Bessolo, Andrew ^a   Malley, Richard ^d   Lipsitcha, Marc ^a,b  

^a Department of Immunology and Infectious Diseases ^*  (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATION; CELL SURFACE; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; IMMUNE RESPONSE; IN VITRO STUDY; INTERSPECIFIC COMPETITION; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; TAXONOMIC RANK; ANIMAL; ANIMAL MODEL; BACTERIAL CAPSULE; BACTERIAL LOAD; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROZYGOTE; METABOLISM; MICROBIOLOGY; MIXED INFECTION; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY SYSTEM; STREPTOCOCCUS INFECTION;

ANIMALS; BACTERIAL CAPSULES; BACTERIAL LOAD; CARRIER STATE; COINFECTION; MICE; MODELS, ANIMAL; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY SYSTEM; SEROGROUP; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 84946600336     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00902-15     Document Type: Article

References (49)

1. Bogaert D, de Groot R, Hermans PW. 2004. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 4:144-154. http://dx.doi.org/10.1016/S1473-3099(04)00938-7.
2. Simell B, Auranen K, Käyhty H, Goldblatt D, Dagan R, O’Brien KL, Pneumococcal Carriage Group. 2012. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines 11:841-855. http://dx.doi.org/10.1586/erv.12.53.
3. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, O’Brien KL, Campbell H, Black RE. 2013. Global burden of childhood pneumonia and diarrhoea. Lancet 381:1405-1416. http://dx.doi.org/10.1016/ S0140-6736(13)60222-6.
4. Griffith F. 1927. The significance of pneumococcal types. J Hyg (Lond) 64:129-175.
5. Jansen AGSC, Rodenburg GD, van der Ende A, van Alphen L, Veenhoven RH, Spanjaard L, Sanders EM, Hak E. 2009. Invasive pneumococcal disease among adults: associations among serotypes, disease characteristics, and outcome. Clin Infect Dis 49:e23-e29. http://dx.doi.org/10.1086/600045.
6. Browall S, Norman M, Tångrot J, Galanis I, Sjöström K, Dagerhamn J, Hellberg C, Pathak A, Spadafina T, Sandgren A, Bättig P, Franzén O, Andersson B, Örtqvist Å, Normark S, Henriques-Normark B. 2014. Intraclonal variations among Streptococcus pneumoniae isolates influence the likelihood of invasive disease in children. J Infect Dis 209:377-388. http://dx.doi.org/10.1093/infdis/jit481.
7. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, Collins M, Donohoe K, Harris D, Murphy L, Quail MA, Samuel G, Skovsted IC, Kaltoft MS, Barrell B, Reeves PR, Parkhill J, Spratt BG. 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31. http://dx.doi.org/10.1371/journal.pgen.0020031.
8. Oliver MB, van der Linden MP, Küntzel SA, Saad JS, Nahm MH. 2013. Discovery of Streptococcus pneumoniae serotype 6 variants with glycosyltransferases synthesizing two differing repeating units. J Biol Chem 288: 25976-25985. http://dx.doi.org/10.1074/jbc.M113.480152.
9. Cobey S, Lipsitch M. 2012. Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science 335: 1376-1380. http://dx.doi.org/10.1126/science.1215947.
10. Weinberger DM, Trzciński K, Lu Y-J, Bogaert D, Brandes A, Galagan J, Anderson PW, Malley R, Lipsitch M. 2009. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 5:e1000476. http://dx.doi.org/10.1371/journal.ppat.1000476.
11. Babl FE, Pelton SI, Theodore S, Klein JO. 2001. Constancy of distribution of serogroups of invasive pneumococcal isolates among children: experience during 4 decades. Clin Infect Dis 32:1155-1161. http://dx.doi.org/10.1086/319750.
12. Hausdorff WP, Feikin DR, Klugman KP. 2005. Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 5:83-93. http://dx.doi.org/10.1016/S1473-3099(05)01280-6.
13. Brueggemann AB, Peto TE, Crook DW, Butler JC, Kristinsson KG, Spratt BG. 2004. Temporal and geographic stability of the serogroupspecific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis 190:1203-1211. http://dx.doi.org/10.1086/423820.
14. Hausdorff WP, Bryant J, Paradiso PR, Siber GR. 2000. Which pneumococcal serogroups cause the most invasive disease: implications for conjugate vaccine formulation and use. Part I. Clin Infect Dis 30:100-121. http://dx.doi.org/10.1086/313608.
15. Spijkerman J, van Gils EJM, Veenhoven RH, Hak E, Yzerman F, van der Ende A, Wijmenga-Monsuur AJ, van den Dobbelsteen GPJM, Sanders EAM. 2011. Carriage of Streptococcus pneumoniae 3 years after start of vaccination program, the Netherlands. Emerg Infect Dis 17:584-591. http://dx.doi.org/10.3201/eid1704.101115.
16. Lee GM, Kleinman K, Pelton SI, Hanage W, Huang SS, Lakoma M, Dutta-Linn M, Croucher NJ, Stevenson A, Finkelstein JA. 2014. Impact of 13-valent pneumococcal conjugate vaccination on Streptococcus pneumoniae carriage in young children in Massachusetts. J Pediatr Infect Dis Soc 3:23-32. http://dx.doi.org/10.1093/jpids/pit057.
17. Lipsitch M. 1997. Vaccination against colonizing bacteria with multiple serotypes. Proc Natl Acad Sci U S A 94:6571-6576. http://dx.doi.org/10.1073/pnas.94.12.6571.
18. Lipsitch M. 1999. Bacterial vaccines and serotype replacement: lessons from Haemophilus influenzae and prospects for Streptococcus pneumoniae. Emerg Infect Dis 5:336-345. http://dx.doi.org/10.3201/eid0503.990304.
19. Weinberger DM, Malley R, Lipsitch M. 2011. Serotype replacement in disease after pneumococcal vaccination. Lancet 378:1962-1973. http://dx.doi.org/10.1016/S0140-6736(10)62225-8.
20. Feikin DR, Kagucia EW, Loo JD, Link-Gelles R, Puhan MA, Cherian T, Levine OS, Whitney CG, O’Brien KL, Moore MR. 2013. Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites. PLoS Med 10:e1001517. http://dx.doi.org/10.1371/journal.pmed.1001517.
21. Gundel M, Okura G. 1933. Untersuchungen über das gleichzeitige Vorkommen mehrerer Pneumokokkentypen bei Gesunden und ihre Bedeutung fur die Epidemiologie. Z Hyg 114:678-704. http://dx.doi.org/10.1007/BF02183676.
22. Turner P, Hinds J, Turner C, Jankhot A, Gould K, Bentley SD, Nosten F, Goldblatt D. 2011. Improved detection of nasopharyngeal cocolonization by multiple pneumococcal serotypes by use of latex agglutination or molecular serotyping by microarray. J Clin Microbiol 49:1784-1789. http://dx.doi.org/10.1128/JCM.00157-11.
23. Wyllie AL, Chu MLJN, Schellens MHB, van Engelsdorp Gastelaars J, Jansen MD, van der Ende A, Bogaert D, Sanders EM, Trzciński K. 2014. Streptococcus pneumoniae in saliva of Dutch primary school children. PLoS One 9:e102045. http://dx.doi.org/10.1371/journal.pone.0102045.
24. Andam CP, Hanage WP. 2015. Mechanisms of genome evolution of streptococcus. Infect Genet Evol 33:334-342. http://dx.doi.org/10.1016/j.meegid.2014.11.007.
25. Auranen K, Mehtälä J, Tanskanen A, S Kaltoft M. 2010. Between-strain competition in acquisition and clearance of pneumococcal carriage— epidemiologic evidence from a longitudinal study of day-care children. Am J Epidemiol 171:169-176. http://dx.doi.org/10.1093/aje/kwp351.
26. Erästö P, Hoti F, Granat SM, Mia Z, Mäkelä PH, Auranen K. 2010. Modelling multi-type transmission of pneumococcal carriage in Bangladeshi families. Epidemiol Infect 138:861-872. http://dx.doi.org/10.1017/S0950268809991415.
27. Brugger SD, Frey P, Aebi S, Hinds J, Mühlemann K. 2010. Multiple colonization with S. pneumoniae before and after introduction of the seven-valent conjugated pneumococcal polysaccharide vaccine. PLoS One 5:e11638. http://dx.doi.org/10.1371/journal.pone.0011638.
28. Lipsitch M, Abdullahi O, D’Amour OA, Xie W, Weinberger DM, Tchetgen Tchetgen E, Scott JAG. 2012. Estimating rates of carriage acquisition and clearance and competitive ability for pneumococcal sero-types in Kenya with a Markov transition model. Epidemiology 23: 510-519. http://dx.doi.org/10.1097/EDE.0b013e31824f2f32.
29. Malley R, Weiser JN. 2008. Animal models of pneumococcal colonization, p 59-66. In Siber GR, Klugman KP, Makela HP (ed), Pneumococcal vaccines. ASM Press, Washington, DC.
30. Li Y, Croucher NJ, Thompson CM, Trzciński K, Hanage WP, Lipsitch M. 2015. Identification of pneumococcal colonization determinants in the stringent response pathway facilitated by genomic diversity. BMC Genomics 16:369. http://dx.doi.org/10.1186/s12864-015-1573-6.
31. Trzcinski K, Thompson CM, Lipsitch M. 2003. Construction of otherwise isogenic serotype 6B, 7F, 14, and 19F capsular variants of Streptococcus pneumoniae strain TIGR4. Appl Environ Microbiol 69:7364-7370. http://dx.doi.org/10.1128/AEM.69.12.7364-7370.2003.
32. Trzciński K, Weinberger DM, Thompson CM, Bessolo A, Malley R, Lipsitch M. 2010. 7th Int Symp Pneumococci Pneumococcal Dis, Tel-Aviv, Israel, 14 to 18 March 2010, p 131.
33. van Gils EJM, Veenhoven RH, Hak E, Rodenburg GD, Bogaert D, Ijzerman EPF, Bruin JP, van Alphen L, Sanders EAM. 2009. Effect of reduced-dose schedules with 7-valent pneumococcal conjugate vaccine on nasopharyngeal pneumococcal carriage in children: a randomized controlled trial. JAMA 302:159-167. http://dx.doi.org/10.1001/jama.2009.975.
34. van Hoek AJ, Sheppard CL, Andrews NJ, Waight PA, Slack MPE, Harrison TG, Ladhani SN, Miller E. 2014. Pneumococcal carriage in children and adults two years after introduction of the thirteen valent pneumococcal conjugate vaccine in England. Vaccine 32:4349-4355. http://dx.doi.org/10.1016/j.vaccine.2014.03.017.
35. Lu Y, Gross J, Bogaert D, Finn A, Bagrade L, Zhang Q, Kolls JK, Srivastava A, Lundgren A, Forte S, Thompson CM, Harney KF, Anderson PW, Lipsitch M, Malley R. 2008. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog 4:e1000159. http://dx.doi.org/10.1371/journal.ppat.1000159.
36. Short KR, Reading PC, Wang N, Diavatopoulos DA, Wijburg OL. 2012. Increased nasopharyngeal bacterial titers and local inflammation facilitate transmission of Streptococcus pneumoniae. mBio 3(5):e00255-12. http://dx.doi.org/10.1128/mBio.00255-12.
37. Lipsitch M, Whitney CG, Zell E, Kaijalainen T, Dagan R, Malley R. 2005. Are anticapsular antibodies the primary mechanism of protection against invasive pneumococcal disease? PLoS Med 2:e15. http://dx.doi.org/10.1371/journal.pmed.0020015.
38. Malley R, Lipsitch M, Stack A, Saladino R, Fleisher G, Pelton S, Thompson C, Briles D, Anderson P. 2001. Intranasal immunization with killed unencapsulated whole cells prevents colonization and invasive disease by capsulated pneumococci. Infect Immun 69:4870-4873. http:// dx.doi.org/10.1128/IAI.69.8.4870-4873.2001.
39. Li Y, Thompson CM, Trzciński K, Lipsitch M. 2013. Within-host selection is limited by an effective population of Streptococcus pneumoniae during nasopharyngeal colonization. Infect Immun 81:4534-4543. http://dx.doi.org/10.1128/IAI.00527-13.
40. Zhang Z, Clarke TB, Weiser JN. 2009. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119:1899-1909. http://dx.doi.org/10.1172/JCI36731.
41. Li Y, Weinberger DM, Thompson CM, Trzciński K, Lipsitch M. 2013. Surface charge of Streptococcus pneumoniae predicts serotype distribution. Infect Immun 81:4519-4524. http://dx.doi.org/10.1128/IAI.00724-13.
42. Hathaway LJ, Brugger SD, Morand B, Bangert M, Rotzetter JU, Hauser C, Graber WA, Gore S, Kadioglu A, Mühlemann K. 2012. Capsule type of Streptococcus pneumoniae determines growth phenotype. PLoS Pathog 8:e1002574. http://dx.doi.org/10.1371/journal.ppat.1002574.
43. Lysenko ES, Lijek RS, Brown SP, Weiser JN. 2010. Within-host competition drives selection for the capsule virulence determinant of Streptococcus pneumoniae. Curr Biol 20:1222-1226. http://dx.doi.org/10.1016/j.cub.2010.05.051.
44. Lipsitch M, Dykes JK, Johnson SE, Ades EW, King J, Briles DE, Carlone GM. 2000. Competition among Streptococcus pneumoniae for intranasal colonization in a mouse model. Vaccine 18:2895-2901. http://dx.doi.org/10.1016/S0264-410X(00)00046-3.
45. Sakai F, Chochua S, Satzke C, Dunne EM, Mulholland K, Klugman KP, Vidal JE. 2015. Single-plex quantitative assays for the detection and quantification of most pneumococcal serotypes. PLoS One 10:e0121064. http://dx.doi.org/10.1371/journal.pone.0121064.
46. Davis KM, Nakamura S, Weiser JN. 2011. Nod2 sensing of lysozymedigested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J Clin Invest 121:3666-3676. http://dx.doi.org/10.1172/JCI57761.
47. Malley R, Trzcinski K, Srivastava A, Thompson CM, Anderson PW, Lipsitch M. 2005. CD4_ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc Natl Acad Sci U S A 102: 4848-4853. http://dx.doi.org/10.1073/pnas.0501254102.
48. Wu HY, Virolainen A, Mathews B, King J, Russell MW, Briles DE. 1997. Establishment of a Streptococcus pneumoniae nasopharyngeal colonization model in adult mice. Microb Pathog 23:127-137.
49. Krone CL, Trzciński K, Zborowski T, Sanders EAM, Bogaert D. 2013. Impaired innate mucosal immunity in aged mice permits prolonged Streptococcus pneumoniae colonization. Infect Immun 81:4615-4625. http://dx.doi.org/10.1128/IAI.00618-13.