Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression

Infection and Immunity

Volumn 82, Issue 6, 2014, Pages 2615-2625

  Wang, Zhaofei ^a   Guo, Changming ^a   Xu, Yannan ^a   Liu, Guangjin ^a   Lu, Chengping ^a   Liu, Yongjie ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CYTOKINE; HYALURONIC ACID; HYALURONIDASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; HYALURONOGLUCOSAMINIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BLOOD; BRAIN; CARBON SOURCE; CELL SURVIVAL; CONTROLLED STUDY; ENERGY RESOURCE; EXPERIMENTAL INFECTION; FEMALE; GRAM POSITIVE BACTERIUM; INFLAMMATION; LD 50; MACROPHAGE; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; STREPTOCOCCUS AGALACTIAE; WILD TYPE; ZEBRA FISH; ANALYSIS OF VARIANCE; ANIMAL; BACTERIAL COUNT; BAGG ALBINO MOUSE; CELL CULTURE; DISEASE MODEL; FISH DISEASE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; STREPTOCOCCUS INFECTION;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CELLS, CULTURED; COLONY COUNT, MICROBIAL; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; FISH DISEASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; HYALURONOGLUCOSAMINIDASE; MACROPHAGES; MICE; MICE, INBRED BALB C; SPLEEN; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE; ZEBRAFISH;

EID: 84900450813     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00022-14     Document Type: Article

References (59)

1. Rajagopal L. 2009. Understanding the regulation of group B streptococcal virulence factors. Future Microbiol. 4:201-221. http://dx.doi.org/10.2217/17460913.4.2.201.
2. Chaiwarith R, Jullaket W, Bunchoo M, Nuntachit N, Sirisanthana T, Supparatpinyo K. 2011. Streptococcus agalactiae in adults at Chiang Mai University Hospital: a retrospective study. BMC Infect. Dis. 11:149. http://dx.doi.org/10.1186/1471-2334-11-149.
3. Keefe GP. 1997. Streptococcus agalactiae mastitis: a review. Can. Vet. J. 38:429-437.
4. Richards VP, Lang P, Bitar PD, Lefebure T, Schukken YH, Zadoks RN, Stanhope MJ. 2011. Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae. Infect. Genet. Evol. 11:1263-1275. http://dx.doi.org/10.1016/j.meegid.2011.04.019.
5. Pridgeon JW, Klesius PH. 2011. Development and efficacy of a novobiocin-resistant Streptococcus iniae as a novel vaccine in Nile tilapia (Oreochromis niloticus). Vaccine 29:5986-5993. http://dx.doi.org/10.1016/j.vaccine.2011.06.036.
6. Ferguson HW, Morales JA, Ostland VE. 1994. Streptococcosis in aquarium fish. Dis. Aquat. Organ. 19:1-6. http://dx.doi.org/10.3354/dao019001.
7. Evans JJ, Klesius PH, Shoemaker CA. 2004. Efficacy of Streptococcus agalactiae (group B) vaccine in tilapia (Oreochromis niloticus) by intraperitoneal and bath immersion administration. Vaccine 22:3769-3773. http://dx.doi.org/10.1016/j.vaccine.2004.03.012.
8. Cornacchione P, Scaringi L, Fettucciari K, Rosati E, Sabatini R, Orefici G, von Hunolstein C, Modesti A, Modica A, Minelli F, Marconi P. 1998. Group B streptococci persist inside macrophages. Immunology 93:86-95. http://dx.doi.org/10.1046/j.1365-2567.1998.00402.x.
9. Valenti-Weigand P, Benkel P, Rohde M, Chhatwal GS. 1996. Entry and intracellular survival of group B streptococci in J774 macrophages. Infect. Immun. 64:2467-2473.
10. Kaplan EL, Chhatwal GS, Rohde M. 2006. Reduced ability of penicillin to eradicate ingested group A streptococci from epithelial cells: clinical and pathogenetic implications. Clin. Infect. Dis. 43:1398-1406. http://dx.doi.org/10.1086/508773.
11. Lemire P, Houde M, Lecours MP, Fittipaldi N, Segura M. 2012. Role of capsular polysaccharide in group B Streptococcus interactions with dendritic cells. Microbes Infect. 14:1064-1076. http://dx.doi.org/10.1016/j.micinf.2012.05.015.
12. Liu GY, Doran KS, Lawrence T, Turkson N, Puliti M, Tissi L, Nizet V. 2004. Sword and shield: linked group B streptococcal beta-hemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc. Natl. Acad. Sci. U. S. A. 101:14491-14496. http://dx.doi.org/10.1073/pnas.0406143101.
13. Cumley NJ, Smith LM, Anthony M, May RC. 2012. The CovS/CovR acid response regulator is required for intracellular survival of group B Streptococcus in macrophages. Infect. Immun. 80:1650-1661. http://dx.doi.org/10.1128/IAI.05443-11.
14. Guo C, Chen R, Kalhoro DH, Wang Z, Liu G, Liu LUCY. 2014. Identification of genes preferentially expressed by highly virulent piscine Streptococcus agalactiae upon interaction with macrophages. PLoS One 9:e87980. http://dx.doi.org/10.1371/journal.pone.0087980.
15. Pritchard DG, Lin B, Willingham TR, Baker JR. 1994. Characterization of the group B streptococcal hyaluronate lyase. Arch. Biochem. Biophys. 315:431-437. http://dx.doi.org/10.1006/abbi.1994.1521.
16. Hynes WL, Walton SL. 2000. Hyaluronidases of Gram-positive bacteria. FEMS Microbiol. Lett. 183:201-207. http://dx.doi.org/10.1111/j.1574-6968.2000.tb08958.x.
17. Calvinho LF, Almeida RA, Oliver SP. 1998. Potential virulence factors of Streptococcus dysgalactiae associated with bovine mastitis. Vet. Microbiol. 61:93-110. http://dx.doi.org/10.1016/S0378-1135(98)00172-2.
18. Matthews KR, Rejman JJ, Turner JD, Oliver SP. 1994. Proliferation of a bovine mammary epithelial-cell line in the presence of bacterial virulence factors. J. Dairy Sci. 77:2959-2964. http://dx.doi.org/10.3168/jds.S0022-0302(94)77237-4.
19. Berry AM, Lock RA, Thomas SM, Rajan DP, Hansman D, Paton JC. 1994. Cloning and nucleotide sequence of the Streptococcus pneumoniae hyaluronidase gene and purification of the enzyme from recombinant Escherichia coli. Infect. Immun. 62:1101-1108.
20. Starr CR, Engleberg NC. 2006. Role of hyaluronidase in subcutaneous spread and growth of group A streptococcus. Infect. Immun. 74:40-48. http://dx.doi.org/10.1128/IAI.74.1.40-48.2006.
21. Campo GM, Avenoso A, D'Ascola A, Scuruchi M, Prestipino V, Calatroni A, Campo S. 2012. Hyaluronan in part mediates IL-1beta-induced inflammation in mouse chondrocytes by up-regulating CD44 receptors. Gene 494:24-35. http://dx.doi.org/10.1016/j.gene.2011.11.064.
22. Turley EA, Noble PW, Bourguignon LY. 2002. Signaling properties of hyaluronan receptors. J. Biol. Chem. 277:4589-4592. http://dx.doi.org/10.1074/jbc.R100038200.
23. Pure E, Cuff CA. 2001.Acrucial role for CD44 in inflammation. Trends Mol. Med. 7:213-221. http://dx.doi.org/10.1016/S1471-4914(01)01963-3.
24. Noble PW, Lake FR, Henson PM, Riches DW. 1993. Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-alpha-dependent mechanism in murine macrophages. J. Clin. Invest. 91:2368-2377. http://dx.doi.org/10.1172/JCI 116469.
25. Harada H, Takahashi M. 2007. CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and-2. J. Biol. Chem. 282:5597-5607. http://dx.doi.org/10.1074/jbc.M608358200.
26. Lepperdinger G, Strobl B, Kreil G. 1998. HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity. J. Biol. Chem. 273:22466-22470. http://dx.doi.org/10.1074/jbc.273.35.22466.
27. Liu G, Zhang W, Lu C. 2012. Complete genome sequence of Streptococcus agalactiae GD201008-001, isolated in China from tilapia with meningoencephalitis. J. Bacteriol. 194:6653. http://dx.doi.org/10.1128/JB.01788-12.
28. Takamatsu D, Osaki M, Sekizaki T. 2001. Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid 46:140-148. http://dx.doi.org/10.1006/plas.2001.1532.
29. Takamatsu D, Osaki M, Sekizaki T. 2001. Construction and characterization of Streptococcus suis-Escherichia coli shuttle cloning vectors. Plasmid 45:101-113. http://dx.doi.org/10.1006/plas.2000.1510.
30. Ju CX, Gu HW, Lu CP. 2012. Characterization and functional analysis of atl, a novel gene encoding autolysin in Streptococcus suis. J. Bacteriol. 194: 1464-1473. http://dx.doi.org/10.1128/JB.06231-11.
31. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
32. Smith RF, Willett NP. 1968. Rapid plate method for screening hyaluronidase and chondroitin sulfatase-producing microorganisms. Appl. Microbiol. 16:1434-1436.
33. Kloosterman TG, Bijlsma JJ, Kok J, Kuipers OP. 2006. To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae. Microbiology 152:351-359. http://dx.doi.org/10.1099/mic.0.28521-0.
34. Patterson H, Saralahti A, Parikka M, Dramsi S, Trieu-Cuot P, Poyart C, Rounioja S, Ramet M. 2012. Adult zebrafish model of bacterial meningitis in Streptococcus agalactiae infection. Dev. Comp. Immunol. 38:447-455. http://dx.doi.org/10.1016/j.dci.2012.07.007.
35. Stanic M. 1963. A simplification of the estimation of the 50 percent endpoints according to the Reed and Muench method. Pathol. Microbiol. (Basel) 26:298-302. (In German.)
36. Marion C, Stewart JM, Tazi MF, Burnaugh AM, Linke CM, Woodiga SA, King SJ. 2012. Streptococcus pneumoniae can utilize multiple sources of hyaluronic acid for growth. Infect. Immun. 80:1390-1398. http://dx.doi.org/10.1128/IAI.05756-11.
37. McHugh SL, Newton CA, Yamamoto Y, Klein TW, Friedman H. 2000. Tumor necrosis factor induces resistance of macrophages to Legionella pneumophila infection. Proc. Soc. Exp. Biol. Med. 224:191-196. http://dx.doi.org/10.1046/j.1525-1373.2000.22420.x.
38. Girish KS, Kemparaju K. 2007. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci. 80:1921-1943. http://dx.doi.org/10.1016/j.lfs.2007.02.037.
39. Li S, Jedrzejas MJ. 2001. Hyaluronan binding and degradation by Streptococcus agalactiae hyaluronate lyase. J. Biol. Chem. 276:41407-41416. http://dx.doi.org/10.1074/jbc.M106634200.
40. Sagar A, Klemm C, Hartjes L, Mauerer S, van Zandbergen G, Spellerberg B. 2013. The β-hemolysin and intracellular survival of Streptococcus agalactiae in human macrophages. PLoS One 8:e60160. http://dx.doi.org/10.1371/journal.pone.0060160.
41. Sendi P, Johansson L, Dahesh S, Van Sorge NM, Darenberg J, Norgren M, Sjolin J, Nizet V, Norrby-Teglund A. 2009. Bacterial phenotype variants in group B streptococcal toxic shock syndrome. Emerg. Infect. Dis. 15:223-232. http://dx.doi.org/10.3201/eid1502.080990.
42. Costagliola C, DelPrete A, Winkler NR, Carpineto P, Ciancaglini M, Piccolomini R, Mastropasqua L. 1996. The ability of bacteria to use Na-hyaluronate as a nutrient. Acta Ophthalmol. Scand. 74:566-568.
43. Lowe BA, Miller JD, Neely MN. 2007. Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 75:1255-1264. http://dx.doi.org/10.1128/IAI.01484-06.
44. Neely MN, Pfeifer JD, Caparon M. 2002. Streptococcus-zebrafish model of bacterial pathogenesis. Infect. Immun. 70:3904-3914. http://dx.doi.org/10.1128/IAI.70.7.3904-3914.2002.
45. Kostyukova NN, Volkova MO, Ivanova VV, Kvetnaya AS. 1995. A study of pathogenic factors of Streptococcus pneumoniae strains causing meningitis. FEMS Immunol. Med. Microbiol. 10:133-137. http://dx.doi.org/10.1111/j.1574-695X.1995.tb00022.x.
46. Zwijnenburg PJ, van der Poll T, Florquin S, van Deventer SJ, Roord JJ, van Furth AM. 2001. Experimental pneumococcal meningitis in mice: a model of intranasal infection. J. Infect. Dis. 183:1143-1146. http://dx.doi.org/10.1086/319271.
47. Vallejo JG, Baker CJ, Edwards MS. 1996. Roles of the bacterial cell wall and capsule in induction of tumor necrosis factor alpha by type III group B streptococci. Infect. Immun. 64:5042-5046.
48. McCoy-Simandle K, Stewart CR, Dao J, DebRoy S, Rossier O, Bryce PJ, Cianciotto NP. 2011. Legionella pneumophila type II secretion dampens the cytokine response of infected macrophages and epithelia. Infect. Immun. 79:1984-1997. http://dx.doi.org/10.1128/IAI.01077-10.
49. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M. 2005. IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 434:1138-1143. http://dx.doi.org/10.1038/nature03491.
50. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449:819-826. http://dx.doi.org/10.1038/nature06246.
51. Sims JE, Smith DE. 2010. The IL-1 family: regulators of immunity. Nat. Rev. Immunol. 10:89-102. http://dx.doi.org/10.1038/nri2691.
52. Costa A, Gupta R, Signorino G, Malara A, Cardile F, Biondo C, Midiri A, Galbo R, Trieu-Cuot P, Papasergi S, Teti G, Henneke P, Mancuso G, Golenbock DT, Beninati C. 2012. Activation of the NLRP3 inflammasome by group B streptococci. J. Immunol. 188:1953-1960. http://dx.doi.org/10.4049/jimmunol.1102543.
53. Vossenkamper A, Marches O, Fairclough PD, Warnes G, Stagg AJ, Lindsay JO, Evans PC, le Luong A, Croft NM, Naik S, Frankel G, MacDonald TT. 2010. Inhibition of NF-kappaB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. J. Immunol. 185: 4118-4127. http://dx.doi.org/10.4049/jimmunol.1000500.
54. Lamy MC, Zouine M, Fert J, Vergassola M, Couve E, Pellegrini E, Glaser P, Kunst F, Msadek T, Trieu-Cuot P, Poyart C. 2004. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence. Mol. Microbiol. 54:1250-1268. http://dx.doi.org/10.1111/j.1365-2958.2004.04365.x.
55. Patras KA, Wang NY, Fletcher EM, Cavaco CK, Jimenez A, Garg M, Fierer J, Sheen TR, Rajagopal L, Doran KS. 2013. Group B Streptococcus CovR regulation modulates host immune signalling pathways to promote vaginal colonization. Cell. Microbiol. 15:1154-1167. http://dx.doi.org/10.1111/cmi.12105.
56. Fan H, Williams DL, Zingarelli B, Breuel KF, Teti G, Tempel GE, Spicher K, Boulay G, Birnbaumer L, Halushka PV, Cook JA. 2007. Differential regulation of lipopolysaccharide and Gram-positive bacteria induced cytokine and chemokine production in macrophages by Galpha( i) proteins. Immunology 122:116-123. http://dx.doi.org/10.1111/j.1365-2567.2007.02619.x.
57. Kurtz SL, Foreman O, Bosio CM, Anver MR, Elkins KL. 2013. Interleukin-6 is essential for primary resistance to Francisella tularensis live vaccine strain infection. Infect. Immun. 81:585-597. http://dx.doi.org/10.1128/IAI.01249-12.
58. Buckner MMC, Antunes LCM, Gill N, Russell SL, Shames SR, Finlay BB. 2013. 15-Deoxy-Δ 12,14-prostaglandin J2 inhibits macrophage colonization by Salmonella enterica serovar Typhimurium. PLoS One 8:e69759. http://dx.doi.org/10.1371/journal.pone.0069759.
59. Schett G. 2011. Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur. J. Clin. Invest. 41:1361-1366. http://dx.doi.org/10.1111/j.1365-2362.2011.02545.x.