Defining the role of pneumococcal neuraminidases and o-glycosidase in pneumococcal haemolytic uraemic syndrome

Journal of Medical Microbiology

Volumn 65, Issue 9, 2016, Pages 975-984

  Singh, Anirudh K ^a   Osman, Amin S ^a   Woodiga, Shireen A ^a   White, Peter ^a,b   Mahan, John D ^a,b   King, Samantha J ^a,b  

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

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; ENG PROTEIN; GLYCOSIDASE; HOST FACTOR; NANC PROTEIN; SIALIDASE; T ANTIGEN; UNCLASSIFIED DRUG; THOMSEN-FRIEDENREICH ANTIGEN; TUMOR ANTIGEN;

ADULT; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; BLOOD SAMPLING; CHILD; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE SEQUENCE; GENOMICS; HEMOLYTIC UREMIC SYNDROME; HUMAN; PATHOGENESIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; SCHOOL CHILD; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; TAIWAN; UNITED STATES; AGED; ENZYMOLOGY; FEMALE; HOST PATHOGEN INTERACTION; INFANT; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; NEWBORN; PATHOPHYSIOLOGY; PRESCHOOL CHILD; PROTEIN PROCESSING;

ADULT; AGED; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; BACTERIAL PROTEINS; CHILD, PRESCHOOL; FEMALE; GLYCOSIDE HYDROLASES; HEMOLYTIC-UREMIC SYNDROME; HOST-PATHOGEN INTERACTIONS; HUMANS; INFANT; INFANT, NEWBORN; MALE; MIDDLE AGED; NEURAMINIDASE; PNEUMOCOCCAL INFECTIONS; PROTEIN PROCESSING, POST-TRANSLATIONAL; STREPTOCOCCUS PNEUMONIAE; UNITED STATES;

EID: 84989822451     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.000322     Document Type: Article

References (63)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.
2. Ault, B. H. (2000). Factor H and the pathogenesis of renal diseases. Pediatr Nephrol 14, 1045–1053.
3. Banerjee, R., Hersh, A. L., Newland, J., Beekmann, S. E., Polgreen, P. M., Bender, J., Shaw, J., Copelovitch, L., Kaplan, B. S. & other authors (2011). Streptococcus pneumoniae-associated hemolytic uremic syndrome among children in North America. Pediatr Infect Dis J 30, 736–739.
4. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S. & other authors (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19, 455–477.
5. Bender, J. M., Ampofo, K., Byington, C. L., Grinsell, M., Korgenski, K., Daly, J. A., Mason, E. O. & Pavia, A. T. (2010). Epidemiology of Streptococcus pneumoniae-induced hemolytic uremic syndrome in Utah children. Pediatr Infect Dis J 29, 712–716.
6. Berry, A. M., Lock, R. A. & Paton, J. C. (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.
7. Bhavanandan, V. P., Umemoto, J. & Davidson, E. A. (1976). Characterization of an endo-alpha-N-acetyl galactosaminidase from Diplococcus pneu-moniae. Biochem Biophys Res Commun 70, 738–745.
8. Brandt, J., Wong, C., Mihm, S., Roberts, J., Smith, J., Brewer, E., Thiagarajan, R. & Warady, B. (2002). Invasive pneumococcal disease and hemolytic uremic syndrome. Pediatrics 110, 371–376.
9. Bray, J., Lemieux, R. U. & McPherson, T. A. (1981). Use of a synthetic hapten in the demonstration of the Thomsen-Friedenreich (T) antigen on neuraminidase-treated human red blood cells and lymphocytes. J Immunol 126, 1966–1969.
10. Cabrera, G. R., Fortenberry, J. D., Warshaw, B. L., Chambliss, C. R., Butler, J. C. & Cooperstone, B. G. (1998). Hemolytic uremic syndrome associated with invasive Streptococcus pneumoniae infection. Pediatrics 101, 699–703.
11. Caines, M. E., Zhu, H., Vuckovic, M., Willis, L. M., Withers, S. G., Wakarchuk, W. W. & Strynadka, N. C. (2008). The structural basis for T-antigen hydrolysis by Streptococcus pneumoniae: a target for structure-based vaccine design. J Biol Chem 283, 31279–31283.
12. C amara, M., Boulnois, G. J., Andrew, P. W. & Mitchell, T. J. (1994). A neuraminidase from Streptococcus pneumoniae has the features of a surface protein. Infect Immun 62, 3688–3695.
13. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V. & Henrissat, B. (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37, D233–238.
14. Chen, S. Y., Wu, C. Y., Tsai, I. J., Tsau, Y. K. & Su, Y. T. (2011). Nonenter-opathic hemolytic uremic syndrome: the experience of a medical center. Pediatr Neonatol 52, 73–77.
15. Coats, M. T., Murphy, T., Paton, J. C., Gray, B. & Briles, D. E. (2011). Exposure of Thomsen-Friedenreich antigen in Streptococcus pneumoniae infection is dependent on pneumococcal neuraminidase A. Microb Pathog 50, 343–349.
16. Cochran, J. B., Panzarino, V. M., Maes, L. Y. & Tecklenburg, F. W. (2004). Pneumococcus-induced T-antigen activation in hemolytic uremic syndrome and anemia. Pediatr Nephrol 19, 317–321.
17. Constantinescu, A. R., Bitzan, M., Weiss, L. S., Christen, E., Kaplan, B. S., Cnaan, A. & Trachtman, H. (2004). Non-enteropathic hemolytic uremic syndrome: causes and short-term course. Am J Kidney Dis 43, 976–982.
18. Copelovitch, L. & Kaplan, B. S. (2008). Streptococcus pneumoniae-associated hemolytic uremic syndrome. Pediatr Nephrol 23, 1951–1956.
19. Copelovitch, L. & Kaplan, B. S. (2010). Streptococcus pneumoniae-associated hemolytic uremic syndrome: classification and the emergence of sero-type 19A. Pediatrics 125, e174–182.
20. Crookston, K. P., Reiner, A. P., Cooper, L. J., Sacher, R. A., Blajchman, M. A. & Heddle, N. M. (2000). RBC T activation and hemoly-sis: implications for pediatric transfusion management. Transfusion 40, 801–812.
21. Darling, A. C., Mau, B., Blattner, F. R. & Perna, N. T. (2004). Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14, 1394–1403.
22. Eber, S. W., Polster, H., Quentin, S. H., Rumpf, K. W. & Lynen, R. (1993). Hemolytic-uremic syndrome in pneumococcal meningitis and infection. Importance of T-transformation. Monatsschr Kinderheilkd 141, 219–222.
23. Enright, M. C. & Spratt, B. G. (1998). A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144, 3049–3060.
24. Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P. & Spratt, B. G. (2004). eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186, 1518–1530.
25. Geary, D. F. (2007). Hemolytic uremic syndrome and Streptococcus pneu-moniae: improving our understanding. J Pediatr 151, 113–114.
26. Giefing, C., Meinke, A. L., Hanner, M., Henics, T., Bui, M. D., Gelbmann, D., Lundberg, U., Senn, B. M., Schunn, M. & other authors (2008). Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J Exp Med 205, 117–131.
27. Giefing, C., Jelencsics, K. E., Gelbmann, D., Senn, B. M. & Nagy, E. (2010). The pneumococcal eukaryotic-type serine/threonine protein kinase StkP co-localizes with the cell division apparatus and interacts with FtsZ in vitro. Microbiology 156, 1697–1707.
28. Gilbert, R. D., Nagra, A. & Haq, M. R. (2013). Does dysregulated complement activation contribute to haemolytic uraemic syndrome secondary to Streptococcus pneumoniae? Med Hypotheses 81, 400–403.
29. Gut, H., King, S. J. & Walsh, M. A. (2008). Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett 582, 3348–3352.
30. Hsiao, H. J., Wu, C. T., Huang, J. L., Chiu, C. H., Huang, Y. C., Lin, J. J., Huang, I. A., Chan, O. W., Chou, I. J. & Hsia, S. H. (2015). Clinical features and outcomes of invasive pneumococcal disease in a pediatric intensive care unit. BMC Pediatr 15, 85.
31. Huang, D. T., Chi, H., Lee, H. C., Chiu, N. C. & Huang, F. Y. (2006). T-antigen activation for prediction of pneumococcus-induced hemolytic uremic syndrome and hemolytic anemia. Pediatr Infect Dis J 25, 608–610.
32. Imai, S., Ito, Y., Ishida, T., Hirai, T., Ito, I., Yoshimura, K., Maekawa, K., Takakura, S., Niimi, A. & other authors (2011). Distribution and clonal relationship of cell surface virulence genes among Streptococcus pneumoniae isolates in Japan. Clin Microbiol Infect 17, 1409–1414.
33. Janapatla, R. P., Hsu, M. H., Hsieh, Y. C., Lee, H. Y., Lin, T. Y. & Chiu, C. H. (2013). Necrotizing pneumonia caused by nanC-carrying serotypes is associated with pneumococcal haemolytic uraemic syndrome in children. Clin Microbiol Infect 19, 480–486.
34. Johnston, J. W. (2009). Example of use of taqman real-time RT-PCR to analyze bacterial gene transcript levels: Haemophilus influenzae. Curr Protoc Microbiol Chapter 1, Unit 1D.
35. Kim, Y. D., Prakash, U., Weber, G. F. & Hargie, M. (1979). Nature of human serum blood group T antibodies. Immunol Commun 8, 397–406.
36. King, S. J., Hippe, K. R., Gould, J. M., Bae, D., Peterson, S., Cline, R. T., Fasching, C., Janoff, E. N. & Weiser, J. N. (2004). Phase variable desialy-lation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol 54, 159–171.
37. King, S. J., Whatmore, A. M. & Dowson, C. G. (2005). NanA, a neuramin-idase from Streptococcus pneumoniae, shows high levels of sequence diversity, at least in part through recombination with Streptococcus oralis. J Bacteriol 187, 5376–5386.
38. King, S. J. (2010). Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 25, 15–24.
39. Klein, P. J., Bulla, M., Newman, R. A., Müller, P., Uhlenbruck, G., Schaefer, H. E., Krüger, G. & Fisher, R. (1977). Thomsen-Friedenreich antigen in haemolytic-uraemic syndrome. Lancet 2, 1024–1025.
40. Lacks, S. & Hotchkiss, R. D. (1960). A study of the genetic material determining an enzyme in Pneumococcus. Biochim Biophys Acta 39, 508–518.
41. Lee, C. S., Chen, M. J., Chiou, Y. H., Shen, C. F., Wu, C. Y. & Chiou, Y. Y. (2012). Invasive pneumococcal pneumonia is the major cause of paediatric haemolytic-uraemic syndrome in Taiwan. Nephrology 17, 48–52.
42. Linke, C. M., Woodiga, S. A., Meyers, D. J., Buckwalter, C. M., Salhi, H. E. & King, S. J. (2013). The ABC transporter encoded at the pneumococcal fructooligosaccharide utilization locus determines the ability to utilize long- and short-chain fructooligosaccharides. J Bacteriol 195, 1031–1041.
43. Marion, C., Limoli, D. H., Bobulsky, G. S., Abraham, J. L., Burnaugh, A. M. & King, S. J. (2009). Identification of a pneumococcal glycosidase that modifies O-linked glycans. Infect Immun 77, 1389–1396.
44. Martin, B., Humbert, O., Camara, M., Guenzi, E., Walker, J., Mitchell, T., Andrew, P., Prudhomme, M., Alloing, G. & other authors. (1992). A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 20, 3479–3483.
45. McGraw, M. E., Lendon, M., Stevens, R. F., Postlethwaite, R. J. & Taylor, C. M. (1989). Haemolytic uraemic syndrome and the Thomsen Friedenreich antigen. Pediatr Nephrol 3, 135–139.
46. Nathanson, S. & Deschênes, G. (2001). Prognosis of Streptococcus pneu-moniae-induced hemolytic uremic syndrome. Pediatr Nephrol 16, 362–365.
47. Pareja-Tobes, P., Manrique, M., Pareja-Tobes, E., Pareja, E. & Tobes, R. (2012). BG7: a new approach for bacterial genome annotation designed for next generation sequencing data. PLoS One 7, e49239.
48. Pettigrew, M. M., Fennie, K. P., York, M. P., Daniels, J. & Ghaffar, F. (2006). Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect Immun 74, 3360–3365.
49. Poulsen, M. P. E. Polyagglutinability and T transformation (Engl Summary). Disseration. University of Copenhagen, Copenhagen, Denmark, p. 186.
50. Smith, A., Johnston, C., Inverarity, D., Slack, M., Paterson, G. K., Diggle, M. & Mitchell, T. (2013). Investigating the role of pneumococcal neuraminidase A activity in isolates from pneumococcal haemolytic urae-mic syndrome. J Med Microbiol 62, 1735–1742.
51. Solovyev, V. & Saloamov, A. (2011). Automatic annotation of microbial genomes and metagenomic sequences. In Metagenomics and Its Applications in Agriculture, Biomedicine and Environmental Studies, pp. 66–78. Edited by R. Li. Hauppauge: Nova Science.
52. Springer, G. F. & Tegtmeyer, H. (1981). Origin of anti-Thomsen-Frie-denreich (T) and Tn agglutinins in man and in White Leghorn chicks. Br J Haematol 47, 453–460.
53. Szil agyi, Á., Györke, Z., Bereczki, C., Kelen, K., Tóth-Heyn, P., Tulassay, T., Reusz, G. S., Szabó, A. J. & Proh aszka, Z. (2015). The use of a rapid fluorogenic neuraminidase assay to differentiate acute Streptococcus pneumoniae-associated hemolytic uremic syndrome (HUS) from other forms of HUS. Clin Chem Lab Med 53, e117–119.
54. Szil agyi, A., Kiss, N., Bereczki, C., T alosi, G., R acz, K., Túri, S., Györke, Z., Simon, E., Horv ath, E. & other authors (2013). The role of complement in Streptococcus pneumoniae-associated haemolytic uraemic syndrome. Nephrol Dial Transplant 28, 2237–2245.
55. Tettelin, H. & Hollingshead, S. K. (2004). Comparative genomics of Streptococcus pneumoniae: intra-strain diversity and genome plasticity. In The Pneumococcus, pp. 15–29. Edited by E. Tuomanen, T. J. Mitchell, D. A. Morrison & B. G. Spratt. Washington, D.C.: ASM Press.
56. Trappetti, C., Kadioglu, A., Carter, M., Hayre, J., Iannelli, F., Pozzi, G., Andrew, P. W. & Oggioni, M. R. (2009). Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis 199, 1497–1505.
57. Treangen, T. J., Ondov, B. D., Koren, S. & Phillippy, A. M. (2014). The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15, 524.
58. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, RESEARCH0034.
59. Waters, A. M., Kerecuk, L., Luk, D., Haq, M. R., Fitzpatrick, M. M., Gilbert, R. D., Inward, C., Jones, C., Pichon, B. & other authors (2007). Hemolytic uremic syndrome associated with invasive pneumococcal disease: the United Kingdom experience. J Pediatr 151, 140–144.
60. Whatmore, A. M., Barcus, V. A. & Dowson, C. G. (1999). Genetic diversity of the streptococcal competence (com) gene locus. J Bacteriol 181, 3144–3154.
61. Willis, L. M., Zhang, R., Reid, A., Withers, S. G. & Wakarchuk, W. W. (2009). Mechanistic investigation of the endo-alpha-N-acetylgalactosa-minidase from Streptococcus pneumoniae R6. Biochemistry 48, 10334–10341.
62. Xu, G., Potter, J. A., Russell, R. J., Oggioni, M. R., Andrew, P. W. & Taylor, G. L. (2008). Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J Mol Biol 384, 436–449.
63. Xu, G., Kiefel, M. J., Wilson, J. C., Andrew, P. W., Oggioni, M. R. & Taylor, G. L. (2011). Three Streptococcus pneumoniae sialidases: three different products. J Am Chem Soc 133, 1718–1721.