Contribution of eukaryotic-type serine/threonine kinase to stress response and virulence of Streptococcus suis

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Zhu, Haodan ^a,b   Zhou, Junming ^a,b   Ni, Yanxiu ^a,b   Yu, Zhengyu ^a,b   Mao, Aihua ^a,b   Hu, Yiyi ^a,b   Wang, Wei ^a,b   Zhang, Xuehan ^a,b   Wen, Libin ^a,b   Li, Bin ^a,b   Wang, Xiaomin ^a,b   Yu, Yang ^a,b   Lv, Lixin ^a,b   Guo, Rongli ^a,b   Lu, Chengping ^c   He, Kongwang ^a,b  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b YANGZHOU UNIVERSITY   (China)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SERINE THREONINE KINASE; BACTERIAL PROTEIN; VIRULENCE FACTOR;

ACID TOLERANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; DELETION MUTANT; ENVIRONMENTAL STRESS; GENE EXPRESSION; HEP 2 CELL; HIGH TEMPERATURE; MOUSE; MUTANT RAT STRAIN; NONHUMAN; OSMOLARITY; OSMOTIC STRESS; OXIDATIVE STRESS; PH; PIGLET; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROTYPE; STREPTOCOCCUS SUIS; STRESS; TEMPERATURE STRESS; WILD TYPE; ANIMAL; BACTERIAL GENOME; BACTERIUM ADHERENCE; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MORTALITY; MUTATION; PATHOGENICITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; STREPTOCOCCUS INFECTION; SWINE; ULTRASTRUCTURE; VIRULENCE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; MICE; MUTATION; PROTEIN-SERINE-THREONINE KINASES; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS SUIS; STRESS, PHYSIOLOGICAL; SWINE; VIRULENCE; VIRULENCE FACTORS;

EID: 84898618028     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091971     Document Type: Article

References (59)

1. Ohlsen K, Donat S (2010) The impact of serine/threonine phosphorylation in Staphylococcus aureus. Int J Med Microbiol 300:137-141.
2. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183-215.
3. Munoz-Dorado J, Inouye S, Inouye M (1991) A gene encoding a protein serine/threonine kinase is required for normal d (Pubitemid 121001513)
4. Tran LS, Szabo L, Ponyi T, Orosz L, Sik T, et al. (1999) Phage abortive infection of Bacillus licheniformis ATCC 9800; identification of the abiBL11 gene and localisation and sequencing of its promoter region. Appl Microbiol Biotechnol 52:845-852.
5. Jin H, Pancholi V (2006) Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in Streptococcus pyogenes: their biological functions and substrate identification. J Mol Biol 357:1351-1372.
6. Rajagopal L, Clancy A, Rubens CE (2003) A eukaryotic type serine/threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J Biol Chem 278:14429-14441. (Pubitemid 36799996)
7. Echenique J, Kadioglu A, Romao S, Andrew PW, Trombe MC (2004) Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect Immun 72:2434-2437. (Pubitemid 38419967)
8. Hussain H, Branny P, Allan E (2006) A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J Bacteriol 188:1628-1632. (Pubitemid 43228697)
9. Av-Gay Y, Everett M (2000) The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol 8:238-244. (Pubitemid 30236245)
10. Kristich CJ, Wells CL, Dunny GM (2007) A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc Natl Acad Sci U S A 104:3508-3513. (Pubitemid 46364189)
11. Misra SK, Milohanic E, Ake F, Mijakovic I, Deutscher J, et al. (2011) Analysis of the serine/threonine/tyrosine phosphoproteome of the pathogenic bacterium Listeria monocytogenes reveals phosphorylated proteins related to virulence. Proteomics 11:4155-4165.
12. Madec E, Laszkiewicz A, Iwanicki A, Obuchowski M, Seror S (2002) Characterization of a membrane-linked Ser/Thr protein kinase in Bacillus subtilis, implicated in developmental processes. Mol Microbiol 46:571-586. (Pubitemid 35340965)
13. Beltramini AM, Mukhopadhyay CD, Pancholi V (2009) Modulation of cell wall structure and antimicrobial susceptibility by a Staphylococcus aureus eukaryotelike serine/threonine kinase and phosphatase. Infect Immun 77:1406-1416.
14. Rajagopal L, Vo A, Silvestroni A, Rubens CE (2005) Regulation of purine biosynthesis by a eukaryotic-type kinase in Streptococcus agalactiae. Mol Microbiol 56:1329-1346. (Pubitemid 40756014)
15. Saskova L, Novakova L, Basler M, Branny P (2007) Eukaryotic-type serine/threonine protein kinase StkP is a global regulator of gene expression in Streptococcus pneumoniae. J Bacteriol 189:4168-4179. (Pubitemid 46847365)
16. Burnside K, Rajagopal L (2011) Aspects of eukaryotic-like signaling in Grampositive cocci: a focus on virulence. Future Microbiol 6:747-761.
17. Donat S, Streker K, Schirmeister T, Rakette S, Stehle T, et al. (2009) Transcriptome and functional analysis of the eukaryotic-type serine/threonine kinase PknB in Staphylococcus aureus. J Bacteriol 191:4056-4069.
18. Banu LD, Conrads G, Rehrauer H, Hussain H, Allan E, et al. (2010) The Streptococcus mutans serine/threonine kinase, PknB, regulates competence development, bacteriocin production, and cell wall metabolism. Infect Immun 78:2209-2220.
19. Jang J, Stella A, Boudou F, Levillain F, Darthuy E, et al. (2010) Functional characterization of the Mycobacterium tuberculosis serine/threonine kinase PknJ. Microbiology 156:1619-1631.
20. Gopalaswamy R, Narayanan S, Chen B, Jacobs WR, Av-Gay Y (2009) The serine/threonine protein kinase PknI controls the growth of Mycobacterium tuberculosis upon infection. FEMS Microbiol Lett 295:23-29.
21. Wiley DJ, Nordfeldth R, Rosenzweig J, Da Fonseca CJ, Gustin R, et al. (2006) The Ser/Thr kinase activity of the Yersinia protein kinase A (YpkA) is necessary for full virulence in the mouse, mollifying phagocytes, and disrupting the eukaryotic cytoskeleton. Microb Pathog 40:234-243. (Pubitemid 44275106)
22. Debarbouille M, Dramsi S, Dussurget O, Nahori MA, Vaganay E, et al. (2009) Characterization of a serine/threonine kinase involved in virulence of Staphylococcus aureus. J Bacteriol 191:4070-4081.
23. Gottschalk M, Segura M (2000) The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet Microbiol 76:259-272.
24. Hill JE, Gottschalk M, Brousseau R, Harel J, Hemmingsen SM, et al. (2005) Biochemical analysis, cpn60 and 16S rDNA sequence data indicate that Streptococcus suis serotypes 32 and 34, isolated from pigs, are Streptococcus orisratti. Vet Microbiol 107:63-69. (Pubitemid 40417530)
25. Segura M, Gottschalk M, Olivier M (2004) Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infect Immun 72:5322-5330. (Pubitemid 39223420)
26. Chabot-Roy G, Willson P, Segura M, Lacouture S, Gottschalk M (2006) Phagocytosis and killing of Streptococcus suis by porcine neutrophils. Microb Pathog 41:21-32. (Pubitemid 44088586)
27. Baums CG, Kaim U, Fulde M, Ramachandran G, Goethe R, et al. (2006) Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74:6154-6162. (Pubitemid 44657394)
28. Jacobs AA, Loeffen PL, Van Den Berg AJ, Storm PK (1994) Identification, purification, and characterization of a thiol-activated hemolysin (suilysin) of Streptococcus suis. Infect Immun 62:1742-1748. (Pubitemid 24136972)
29. De Greeff A, Buys H, Verhaar R, Dijkstra J, Van Alphen L, et al. (2002) Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infect Immun 70:1319-1325. (Pubitemid 34163407)
30. Zhang XH, He KW, Duan ZT, Zhou JM, Yu ZY, et al. (2009) Identification and characterization of inosine 5-monophosphate dehydrogenase in Streptococcus suis type 2. Microb Pathog 47:267-273.
31. 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.
32. Li M, Wang C, Feng Y, Pan X, Cheng G, et al. (2008) SalK/SalR, a twocomponent signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. PLoS One 3:e2080.
33. Li J, Tan C, Zhou Y, Fu S, Hu L, et al. The two-component regulatory system CiaRH contributes to the virulence of Streptococcus suis 2. Vet Microbiol 148:99-104.
34. Pan X, Ge J, Li M, Wu B, Wang C, et al. (2009) The orphan response regulator CovR: a globally negative modulator of virulence in Streptococcus suis serotype 2. J Bacteriol 191:2601-2612.
35. Ho Dang Trung N, Le Thi Phuong T, Wolbers M, Nguyen Van Minh H, Nguyen Thanh V, et al. (2012) Aetiologies of Central Nervous System Infection in Viet Nam: A Prospective Provincial Hospital-Based Descriptive Surveillance Study. PLoS One 7:e37825.
36. Fittipaldi N, Segura M, Grenier D, Gottschalk M (2012) Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol 7:259-279.
37. Charland N, Nizet V, Rubens CE, Kim KS, Lacouture S, et al. (2000) Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells. Infect Immun 68:637-643. (Pubitemid 30056517)
38. Rajagopal L, Vo A, Silvestroni A, Rubens CE (2006) Regulation of cytotoxin expression by converging eukaryotic-type and two-component signalling mechanisms in Streptococcus agalactiae. Mol Microbiol 62:941-957. (Pubitemid 44655310)
39. Zhu H, Huang D, Zhang W, Wu Z, Lu Y, et al. (2011) The novel virulencerelated gene stp of Streptococcus suis serotype 9 strain contributes to a significant reduction in mouse mortality. Microb Pathog 51:442-453.
40. Takamatsu D, Osaki M, Sekizaki T (2001) Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid 46:140-148. (Pubitemid 32980676)
41. Takamatsu D, Osaki M, Sekizaki T (2001) Construction and characterization of Streptococcus suis-Escherichia coli shuttle cloning vectors. Plasmid 45:101-113. (Pubitemid 32221956)
42. Vanier G, Segura M, Friedl P, Lacouture S, Gottschalk M (2004) Invasion of porcine brain microvascular endothelial cells by Streptococcus suis serotype 2. Infect Immun 72:1441-1449. (Pubitemid 38263766)
43. Lapointe L, D'Allaire S, Lebrun A, Lacouture S, Gottschalk M (2002) Antibody response to an autogenous vaccine and serologic profile for Streptococcus suis capsular type 1/2. Can J Vet Res 66:8-14. (Pubitemid 34173143)
44. Bonifait L, De La Cruz Dominguez-Punaro M, Vaillancourt K, Bart C, Slater J, et al. (2010) The cell envelope subtilisin-like proteinase is a virulence determinant for Streptococcus suis. BMC Microbiol 10:42.
45. Dominguez-Punaro MC, Segura M, Plante MM, Lacouture S, Rivest S, et al. (2007) Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol 179:1842-1854.
46. Reed LJ (1938) A simple method of estimating fifty per cent endpoints. American Journal of Epidemiology 27:493.
47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25:402-408. (Pubitemid 34164012)
48. Bork P, Brown NP, Hegyi H, Schultz J (1996) The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci 5:1421-1425. (Pubitemid 26239449)
49. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
50. Winterhoff N, Goethe R, Gruening P, Rohde M, Kalisz H, et al. (2002) Identification and characterization of two temperature-induced surface-associated proteins of Streptococcus suis with high homologies to members of the Arginine Deiminase system of Streptococcus pyogenes. J Bacteriol 184:6768-6776. (Pubitemid 36356111)
51. Garibaldi M, Rodriguez-Ortega MJ, Mandanici F, Cardaci A, Midiri A, et al. (2010) Immunoprotective activities of a Streptococcus suis pilus subunit in murine models of infection. Vaccine 28:3609-3616.
52. Brassard J, Gottschalk M, Quessy S (2004) Cloning and purification of the Streptococcus suis serotype 2 glyceraldehyde-3-phosphate dehydrogenase and its involvement as an adhesin. Vet Microbiol 102:87-94. (Pubitemid 39037377)
53. Tang Y, Zhang X, Wu W, Lu Z, Fang W (2012) Inactivation of the sodA gene of Streptococcus suis type 2 encoding superoxide dismutase leads to reduced virulence to mice. Vet Microbiol 158:360-366.
54. Bugrysheva J, Froehlich BJ, Freiberg JA, Scott JR (2011) Serine/Threonine Protein Kinase Stk Is Required for Virulence, Stress Response, and Penicillin Tolerance in Streptococcus pyogenes. Infect Immun 79:4201-4209.
55. Osaki M, Arcondeguy T, Bastide A, Touriol C, Prats H, et al. (2009) The StkP/PhpP signaling couple in Streptococcus pneumoniae: cellular organization and physiological characterization. J Bacteriol 191:4943-4950.
56. Lalonde M, Segura M, Lacouture S, Gottschalk M (2000) Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology 146(Pt 8):1913-1921. (Pubitemid 30639266)
57. Yeats C, Finn RD, Bateman A (2002) The PASTA domain: a beta-lactambinding domain. Trends Biochem Sci 27:438.
58. Wu T, Zhao Z, Zhang L, Ma H, Lu K, et al. (2011) Trigger factor of Streptococcus suis is involved in stress tolerance and virulence. Microb Pathog 51:69-76.
59. Liu M, Hanks TS, Zhang J, McClure MJ, Siemsen DW, et al. (2006) Defects in ex vivo and in vivo growth and sensitivity to osmotic stress of group A Streptococcus caused by interruption of response regulator gene vicR. Microbiology 152:967-978.