SpyA, a C3-like ADP-Ribosyltransferase, contributes to virulence in a mouse subcutaneous model of Streptococcus pyogenes infection

Infection and Immunity

Volumn 79, Issue 6, 2011, Pages 2404-2411

  Hoff, Jessica S ^a   DeWald, Mark ^b   Moseley, Steve L ^a   Collins, Carleen M ^a   Voyich, Jovanka M ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GELATINASE A; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; EPITHELIUM CELL; GENE DELETION; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPYA GENE; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; VIM GENE;

ADP RIBOSE TRANSFERASES; ANIMALS; BLOTTING, WESTERN; CHEMOKINE CCL2; CHEMOKINE CXCL1; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; HELA CELLS; HUMANS; MICE; NEUTROPHILS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; VIRULENCE FACTORS;

EID: 79959412072     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01191-10     Document Type: Article

References (68)

1. Aepfelbacher, M., M. Essler, E. Huber, M. Sugai, and P. C. Weber. 1997. Bacterial toxins block endothelial wound repair. Evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler. Thromb. Vasc. Biol. 17:1623-1629.
2. Andreasen, C., and N. H. Carbonetti. 2008. Pertussis toxin inhibits early chemokine production to delay neutrophil recruitment in response to Bordetella pertussis respiratory tract infection in mice. Infect. Immun. 76:5139-5148.
3. Arraj, J. A., and M. G. Marinus. 1983. Phenotypic reversal in dam mutants of Escherichia coli K-12 by a recombinant plasmid containing the dam gene. J. Bacteriol. 153:562-565.
4. Ashbaugh, C. D., H. B. Warren, V. J. Carey, and M. R. Wessels. 1998. Molecular analysis of the role of the group A streptococcal cysteine protease, hyaluronic acid capsule, and M protein in a murine model of human invasive soft-tissue infection. J. Clin. Invest. 102:550-560.
5. Beneš, P., et al. 2006. Role of vimentin in regulation of monocyte/macrophage differentiation. Differentiation 74:265-276.
6. Boyum, A. 1968. Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab Invest. Suppl. 97:77-89.
7. Bricker, A. L., C. Cywes, C. D. Ashbaugh, and M. R. Wessels. 2002. NAD -glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol. Microbiol. 44:257-269.
8. Bunce, C., L. Wheeler, G. Reed, J. Musser, and N. Barg. 1992. Murine model of cutaneous infection with gram-positive cocci. Infect. Immun. 60:2636- 2640.
9. Corda, D., and M. Di Girolamo. 2003. Functional aspects of protein mono-ADP-ribosylation. EMBO J. 22:1953-1958.
10. Coye, L. H., and C. M. Collins. 2004. Identification of SpyA, a novel ADPribosyltransferase of Streptococcus pyogenes. Mol. Microbiol. 54:89-98.
11. Cunningham, M. W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13:470-511.
12. Cywes, C., and M. R. Wessels. 2001. Group A Streptococcus tissue invasion by CD44-mediated cell signalling. Nature 414:648-652.
13. Devalaraja, R. M., et al. 2000. Delayed wound healing in CXCR2 knockout mice. J. Investig. Dermatol. 115:234-244.
14. Domenighini, M., and R. Rappuoli. 1996. Three conserved consensus sequences identify the NAD-binding site of ADP-ribosylating enzymes, expressed by eukaryotes, bacteria and T-even bacteriophages. Mol. Microbiol. 21:667-674.
15. Eckes, B., et al. 2000. Impaired wound healing in embryonic and adult mice lacking vimentin. J. Cell Sci. 113(Pt. 13):2455-2462.
16. Edwards, R. J., et al. 2005. Specific C-terminal cleavage and inactivation of interleukin-8 by invasive disease isolates of Streptococcus pyogenes. J. Infect. Dis. 192:783-790.
17. Fahrer, J., et al. 2010. Selective and specific internalization of clostridial C3 ADP-ribosyltransferases into macrophages and monocytes. Cell Microbiol. 12:233-247.
18. Fritzer, A., et al. 2009. Chemokine degradation by the group A streptococcal serine proteinase ScpC can be reconstituted in vitro and requires two separate domains. Biochem. J. 422:533-542.
19. Gilles, C., et al. 1999. Vimentin contributes to human mammary epithelial cell migration. J. Cell Sci. 112(Pt. 24):4615-4625.
20. Graham, M. R., et al. 2002. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc. Natl. Acad. Sci. U. S. A. 99:13855-13860.
21. Graham, M. R., et al. 2005. Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am. J. Pathol. 166:455-465.
22. Graham, M. R., et al. 2006. Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am. J. Pathol. 169:927-942.
23. Grant, S. G., J. Jessee, F. R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. U. S. A. 87:4645-4649.
24. Greco, R., et al. 1995. Invasion of cultured human cells by Streptococcus pyogenes. Res. Microbiol. 146:551-560.
25. Hamilton, S. M., C. R. Bayer, D. L. Stevens, R. L. Lieber, and A. E. Bryant. 2008. Muscle injury, vimentin expression, and nonsteroidal anti-inflammatory drugs predispose to cryptic group A streptococcal necrotizing infection. J. Infect. Dis. 198:1692-1698.
26. Hass, R., et al. 1990. Differentiation and retrodifferentiation of U937 cells: reversible induction and suppression of intermediate filament protein synthesis. Eur. J. Cell Biol. 51:265-271.
27. Hidalgo-Grass, C., et al. 2006. A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues. EMBO J. 25:4628-4637.
28. Jadoun, J., O. Eyal, and S. Sela. 2002. Role of CsrR, hyaluronic acid, and SpeB in the internalization of Streptococcus pyogenes M type 3 strain by epithelial cells. Infect. Immun. 70:462-469.
29. Johnson, M. R., K. Wang, J. B. Smith, M. J. Heslin, and R. B. Diasio. 2000. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 278:175-184.
30. Klenk, M., et al. 2007. Streptococcus pyogenes serotype-dependent and independent changes in infected HEp-2 epithelial cells. ISME J. 1:678-692.
31. Kline, J. B., and C. M. Collins. 1996. Analysis of the superantigenic activity of mutant and allelic forms of streptococcal pyrogenic exotoxin A. Infect. Immun. 64:861-869.
32. Koch-Nolte, F., P. Reche, F. Haag, and F. Bazan. 2001. ADP-ribosyltransferases: plastic tools for inactivating protein and small molecular weight targets. J. Biotechnol. 92:81-87.
33. Kurupati, P., C. E. Turner, I. Tziona, R. A. Lawrenson, F. M. Alam, M. Nohadani, G. W. Stamp, A. S. Zinkernagel, V. Nizet, R. J. Edwards, and S. Sriskandan. 2010. Chemokine-cleaving Streptococcus pyogenes protease SpyCEP is necessary and sufficient for bacterial dissemination within soft tissues and the respiratory tract. Mol. Microbiol. 76:1387-1397.
34. LaPenta, D., C. Rubens, E. Chi, and P. P. Cleary. 1994. Group A streptococci efficiently invade human respiratory epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 91:12115-12119.
35. Li, X., W. G. Fusco, K. S. Seo, K. W. Bayles, E. E. Mosley, M. A. McGuire, and G. A. Bohach. 2009. Epithelial cell gene expression induced by intracellular Staphylococcus aureus. Int. J. Microbiol. 2009:753278.
36. Low, Q. E. H., et al. 2001. Wound healing in MIP-1alpha-/- and MCP-1-/- mice. Am. J. Pathol. 159:457-463.
37. Madlener, M. 1998. Differential expression of matrix metalloproteinases and their physiological inhibitors in acute murine skin wounds. Arch. Dermatol. Res. 290(Suppl.):S24-S29.
38. Marouni, M. J., and S. Sela. 2004. Fate of Streptococcus pyogenes and epithelial cells following internalization. J. Med. Microbiol. 53:1-7.
39. Medina, E. 2010. Murine model of cutaneous infection with Streptococcus pyogenes. Methods Mol. Biol. 602:395-403.
40. Medina, E., O. Goldmann, A. W. Toppel, and G. S. Chhatwal. 2003. Survival of Streptococcus pyogenes within host phagocytic cells: a pathogenic mechanism for persistence and systemic invasion. J. Infect. Dis. 187:597-603.
41. Medina, E., M. Rohde, and G. S. Chhatwal. 2003. Intracellular survival of Streptococcus pyogenes in polymorphonuclear cells results in increased bacterial virulence. Infect. Immun. 71:5376-5380.
42. Molinari, G., and G. S. Chhatwal. 1998. Invasion and survival of Streptococcus pyogenes in eukaryotic cells correlates with the source of the clinical isolates. J. Infect. Dis. 177:1600-1607.
43. Molinari, G., et al. 2006. Localization of the C3-like ADP-ribosyltransferase from Staphylococcus aureus during bacterial invasion of mammalian cells. Infect. Immun. 74:3673-3677.
44. Mor-Vaknin, N., A. Punturieri, K. Sitwala, and D. M. Markovitz. 2003. Vimentin is secreted by activated macrophages. Nat. Cell Biol. 5:59-63.
45. Moser, B., I. Clark-Lewis, R. Zwahlen, and M. Baggiolini. 1990. Neutrophilactivating properties of the melanoma growth-stimulatory activity. J. Exp. Med. 171:1797-1802.
46. Ortega, S., M. Ittmann, S. H. Tsang, M. Ehrlich, and C. Basilico. 1998. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. U. S. A. 95:5672-5677.
47. Österlund, A., and L. Engstrand. 1995. Intracellular penetration and survival of Streptococcus pyogenes in respiratory epithelial cells in vitro. Acta Otolaryngol. 115:685-688.
48. Österlund, A., R. Popa, T. Nikkilä, A. Scheynius, and L. Engstrand. 1997. Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope 107:640-647.
49. Perez-Casal, J., J. A. Price, E. Maguin, and J. R. Scott. 1993. An M protein with a single C repeat prevents phagocytosis of Streptococcus pyogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes. Mol. Microbiol. 8:809-819.
50. Podbielski, A., et al. 2003. Epidemiology and virulence gene expression of intracellular group A streptococci in tonsils of recurrently infected adults. Int. J. Med. Microbiol. 293:179-190.
51. Rennekampff, H. O., et al. 1997. Role of melanoma growth stimulatory activity (MGSA/gro) on keratinocyte function in wound healing. Arch. Dermatol. Res. 289:204-212.
52. Rius, C., N. Vilaboa, F. Mata, and P. Aller. 1993. Differential modulation of the expression of the intermediate filament proteins vimentin and nuclear lamins A and C by differentiation inducers in human myeloid leukemia (U-937, HL-60) cells. Exp. Cell Res. 208:115-120.
53. Schaffer, B. S., M. H. Grayson, J. M. Wortham, C. B. Kubicek, A. T. Mc-Cleish, S. I. Prajapati, L. D. Nelon, M. M. Brady, I. Jung, T. Hosoyama, L. M. Sarro, M. A. Hanes, B. P. Rubin, J. E. Michalek, C. B. Clifford, A. J. Infante, and C. Keller. 2010. Immune competency of a hairless mouse strain for improved preclinical studies in genetically engineered mice. Mol. Cancer Ther. 9:2354-2364.
54. Schrager, H. M., J. G. Rheinwald, and M. R. Wessels. 1996. Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection. J. Clin. Invest. 98:1954-1958.
55. Shelburne, S. A., III, et al. 2005. Central role of a bacterial two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc. Natl. Acad. Sci. U. S. A. 102:16037-16042.
56. Sin, W. C., X. Q. Chen, T. Leung, and L. Lim. 1998. RhoA-binding kinase alpha translocation is facilitated by the collapse of the vimentin intermediate filament network. Mol. Cell. Biol. 18:6325-6339.
57. Sitkiewicz, I., and J. M. Musser. 2006. Expression microarray and mouse virulence analysis of four conserved two-component gene regulatory systems in group A streptococcus. Infect. Immun. 74:1339-1351.
58. Sumby, P., et al. 2005. Evolutionary origin and emergence of a highly successful clone of serotype M1 group A Streptococcus involved multiple horizontal gene transfer events. J. Infect. Dis. 192:771-782.
59. Sumby, P., A. R. Whitney, E. A. Graviss, F. R. DeLeo, and J. M. Musser. 2006. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2:e5.
60. Thulin, P., et al. 2006. Viable group A streptococci in macrophages during acute soft tissue infection. PLoS Med. 3:0371-0379.
61. Vogelsgesang, M., A. Pautsch, and K. Aktories. 2007. C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins. Naunyn Schmiedebergs Arch. Pharmacol. 374:347-360.
62. Voyich, J. M., et al. 2004. Engagement of the pathogen survival response used by group A Streptococcus to avert destruction by innate host defense. J. Immunol. 173:1194-1201.
63. Voyich, J. M., and F. R. DeLeo. 2002. Host-pathogen interactions: leukocyte phagocytosis and associated sequelae. Methods Cell Sci. 24:79-90.
64. Voyich, J. M., J. M. Musser, and F. R. DeLeo. 2004. Streptococcus pyogenes and human neutrophils: a paradigm for evasion of innate host defense by bacterial pathogens. Microbes Infect. 6:1117-1123.
65. Voyich, J. M., et al. 2003. Genome-wide protective response used by group A Streptococcus to evade destruction by human polymorphonuclear leukocytes. Proc. Natl. Acad. Sci. U. S. A. 100:1996-2001.
66. Yamamoto, T., B. Eckes, C. Mauch, K. Hartmann, and T. Krieg. 2000. Monocyte chemoattractant protein-1 enhances gene expression and synthesis of matrix metalloproteinase-1 in human fibroblasts by an autocrine IL-1 alpha loop. J. Immunol. 164:6174-6179.
67. Yoshimura, T., E. A. Robinson, S. Tanaka, E. Appella, and E. J. Leonard. 1989. Purification and amino acid analysis of two human monocyte chemoattractants produced by phytohemagglutinin-stimulated human blood mononuclear leukocytes. J. Immunol. 142:1956-1962.
68. Zhu, H., M. Liu, P. Sumby, and B. Lei. 2009. The secreted esterase of group A streptococcus is important for invasive skin infection and dissemination in mice. Infect. Immun. 77:5225-5232.