1887

Abstract

Strangles caused by the host adapted Lancefield group C subspecies ( equi) is a frequently diagnosed infectious disease of horses worldwide. Critical to the global success of is its ability to establish persistent infections within the guttural pouches of recovered apparently healthy horses that can result in transmission to in-contact animals. Recent research has identified key events in the genome, which occurred during its evolution from an ancestral strain of subspecies , that may enhance its ability to evade host innate immune responses and rapidly multiply in the tonsillar complex and draining lymph nodes. This review discusses the role of these genetic events on the evolution and emergence of this important host-restricted pathogen.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.028233-0
2011-09-01
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/jmm/60/9/1231.html?itemId=/content/journal/jmm/10.1099/jmm.0.028233-0&mimeType=html&fmt=ahah

References

  1. Abbot E. L., Smith W. D., Siou G. P., Chiriboga C., Smith R. J., Wilson J. A., Hirst B. H., Kehoe M. A. 2007; Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol 9:1822–1833 [View Article][PubMed]
    [Google Scholar]
  2. Anzai T., Sheoran A. S., Kuwamoto Y., Kondo T., Wada R., Inoue T., Timoney J. F. 1999a; Streptococcus equi but not Streptococcus zooepidemicus produces potent mitogenic responses from equine peripheral blood mononuclear cells. Vet Immunol Immunopathol 67:235–246 [View Article][PubMed]
    [Google Scholar]
  3. Anzai T., Timoney J. F., Kuwamoto Y., Fujita Y., Wada R., Inoue T. 1999b; In vivo pathogenicity and resistance to phagocytosis of Streptococcus equi strains with different levels of capsule expression. Vet Microbiol 67:277–286 [View Article][PubMed]
    [Google Scholar]
  4. Artiushin S. C., Timoney J. F., Sheoran A. S., Muthupalani S. K. 2002; Characterization and immunogenicity of pyrogenic mitogens SePE-H and SePE-I of Streptococcus equi . Microb Pathog 32:71–85 [View Article][PubMed]
    [Google Scholar]
  5. Bannister M. F., Benson C. E., Sweeney C. R. 1985; Rapid species identification of group C streptococci isolated from horses. J Clin Microbiol 21:524–526[PubMed]
    [Google Scholar]
  6. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D. A., Horvath P. 2007; CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712 [View Article][PubMed]
    [Google Scholar]
  7. Bearden S. W., Fetherston J. D., Perry R. D. 1997; Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis . Infect Immun 65:1659–1668[PubMed]
    [Google Scholar]
  8. Beres S. B., Sesso R., Pinto S. W., Hoe N. P., Porcella S. F., Deleo F. R., Musser J. M. 2008; Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: new information about an old disease. PLoS ONE 3:e3026 [View Article][PubMed]
    [Google Scholar]
  9. Blank L. M., Hugenholtz P., Nielsen L. K. 2008; Evolution of the hyaluronic acid synthesis (has) operon in Streptococcus zooepidemicus and other pathogenic streptococci. J Mol Evol 67:13–22 [View Article][PubMed]
    [Google Scholar]
  10. Bobrov A. G., Geoffroy V. A., Perry R. D. 2002; Yersiniabactin production requires the thioesterase domain of HMWP2 and YbtD, a putative phosphopantetheinylate transferase. Infect Immun 70:4204–4214 [View Article][PubMed]
    [Google Scholar]
  11. Boschwitz J. S., Timoney J. F. 1994; Inhibition of C3 deposition on Streptococcus equi subsp. equi by M protein: a mechanism for survival in equine blood. Infect Immun 62:3515–3520[PubMed]
    [Google Scholar]
  12. Breiman R. F., Silverblatt F. J. 1986; Systemic Streptococcus equi infection in a horse handler – a case of human strangles. West J Med 145:385–386[PubMed]
    [Google Scholar]
  13. Brown J. S., Holden D. W. 2002; Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect 4:1149–1156 [View Article][PubMed]
    [Google Scholar]
  14. Brüssow H., Canchaya C., Hardt W. D. 2004; Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602 [View Article][PubMed]
    [Google Scholar]
  15. Chanter N., Talbot N. C., Newton J. R., Hewson D., Verheyen K. 2000; Streptococcus equi with truncated M-proteins isolated from outwardly healthy horses. Microbiology 146:1361–1369[PubMed]
    [Google Scholar]
  16. Dellabona P., Peccoud J., Kappler J., Marrack P., Benoist C., Mathis D. 1990; Superantigens interact with MHC class II molecules outside of the antigen groove. Cell 62:1115–1121 [View Article][PubMed]
    [Google Scholar]
  17. Edwards R. J., Taylor G. W., Ferguson M., Murray S., Rendell N., Wrigley A., Bai Z., Boyle J., Finney S. 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 [View Article][PubMed]
    [Google Scholar]
  18. Eichenbaum Z., Muller E., Morse S. A., Scott J. R. 1996; Acquisition of iron from host proteins by the group A streptococcus . Infect Immun 64:5428–5429[PubMed]
    [Google Scholar]
  19. Flanagan J., Collin N., Timoney J., Mitchell T., Mumford J. A., Chanter N. 1998; Characterization of the haemolytic activity of Streptococcus equi . Microb Pathog 24:211–221 [View Article][PubMed]
    [Google Scholar]
  20. Flock M., Jacobsson K., Frykberg L., Hirst T. R., Franklin A., Guss B., Flock J. I. 2004; Recombinant Streptococcus equi proteins protect mice in challenge experiments and induce immune response in horses. Infect Immun 72:3228–3236 [View Article][PubMed]
    [Google Scholar]
  21. Flock M., Karlström A., Lannergård J., Guss B., Flock J. I. 2006; Protective effect of vaccination with recombinant proteins from Streptococcus equi subspecies equi in a strangles model in the mouse. Vaccine 24:4144–4151 [View Article][PubMed]
    [Google Scholar]
  22. Fontaine M. C., Lee J. J., Kehoe M. A. 2003; Combined contributions of streptolysin O and streptolysin S to virulence of serotype M5 Streptococcus pyogenes strain Manfredo. Infect Immun 71:3857–3865 [View Article][PubMed]
    [Google Scholar]
  23. Guss B., Flock M., Frykberg L., Waller A. S., Robinson C., Smith K. C., Flock J. I. 2009; Getting to grips with strangles: an effective multi-component recombinant vaccine for the protection of horses from Streptococcus equi infection. PLoS Pathog 5:e1000584 [View Article][PubMed]
    [Google Scholar]
  24. Hanks T. S., Liu M., McClure M. J., Lei B. 2005; ABC transporter FtsABCD of Streptococcus pyogenes mediates uptake of ferric ferrichrome. BMC Microbiol 5:62 [View Article][PubMed]
    [Google Scholar]
  25. Heather Z., Holden M. T., Steward K. F., Parkhill J., Song L., Challis G. L., Robinson C., Davis-Poynter N., Waller A. S. 2008; A novel streptococcal integrative conjugative element involved in iron acquisition. Mol Microbiol 70:1274–1292 [View Article][PubMed]
    [Google Scholar]
  26. Holden M. T., Heather Z., Paillot R., Steward K. F., Webb K., Ainslie F., Jourdan T., Bason N. C., Holroyd N. E. et al. 2009; Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 5:e1000346 [View Article][PubMed]
    [Google Scholar]
  27. Hulting G., Flock M., Frykberg L., Lannergård J., Flock J. I., Guss B. 2009; Two novel IgG endopeptidases of Streptococcus equi . FEMS Microbiol Lett 298:44–50 [View Article][PubMed]
    [Google Scholar]
  28. Ivens P. A., Matthews D., Webb K., Newton J. R., Steward K., Waller A. S., Robinson C., Slater J. D. 2011; Molecular characterisation of ‘strangles’ outbreaks in the UK: the use of M-protein typing of Streptococcus equi ssp. equi . Equine Vet J 43:359–364[PubMed] [CrossRef]
    [Google Scholar]
  29. Jacobs A. A., Goovaerts D., Nuijten P. J., Theelen R. P., Hartford O. M., Foster T. J. 2000; Investigations towards an efficacious and safe strangles vaccine: submucosal vaccination with a live attenuated Streptococcus equi . Vet Rec 147:563–567 [View Article][PubMed]
    [Google Scholar]
  30. Janulczyk R., Pallon J., Björck L. 1999; Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34:596–606 [View Article][PubMed]
    [Google Scholar]
  31. Jorm L. R., Love D. N., Bailey G. D., McKay G. M., Briscoe D. A. 1994; Genetic structure of populations of β-haemolytic Lancefield group C streptococci from horses and their association with disease. Res Vet Sci 57:292–299 [View Article][PubMed]
    [Google Scholar]
  32. Kelly C., Bugg M., Robinson C., Mitchell Z., Davis-Poynter N., Newton J. R., Jolley K. A., Maiden M. C., Waller A. S. 2006; Sequence variation of the SeM gene of Streptococcus equi allows discrimination of the source of strangles outbreaks. J Clin Microbiol 44:480–486 [View Article][PubMed]
    [Google Scholar]
  33. Kotb M., Norrby-Teglund A., McGeer A., El-Sherbini H., Dorak M. T., Khurshid A., Green K., Peeples J., Wade J. et al. 2002; An immunogenetic and molecular basis for differences in outcomes of invasive group A streptococcal infections. Nat Med 8:1398–1404[PubMed] [CrossRef]
    [Google Scholar]
  34. Kurupati P., Turner C. E., Tziona I., Lawrenson R. A., Alam F. M., Nohadani M., Stamp G. W., Zinkernagel A. S., Nizet V. et al. 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 [View Article][PubMed]
    [Google Scholar]
  35. Ladlow J., Scase T., Waller A. 2006; Canine strangles case reveals a new host susceptible to infection with Streptococcus equi . J Clin Microbiol 44:2664–2665 [View Article][PubMed]
    [Google Scholar]
  36. Lannergård J., Guss B. 2006; IdeE, an IgG-endopeptidase of Streptococcus equi ssp. equi . FEMS Microbiol Lett 262:230–235 [View Article][PubMed]
    [Google Scholar]
  37. Lannergård J., Frykberg L., Guss B. 2003; CNE, a collagen-binding protein of Streptococcus equi . FEMS Microbiol Lett 222:69–74 [View Article][PubMed]
    [Google Scholar]
  38. Lei B., DeLeo F. R., Hoe N. P., Graham M. R., Mackie S. M., Cole R. L., Liu M., Hill H. R., Low D. E. et al. 2001; Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 7:1298–1305 [View Article][PubMed]
    [Google Scholar]
  39. Lewis M. J., Meehan M., Owen P., Woof J. M. 2008; A common theme in interaction of bacterial immunoglobulin-binding proteins with immunoglobulins illustrated in the equine system. J Biol Chem 283:17615–17623 [View Article][PubMed]
    [Google Scholar]
  40. Li H., Llera A., Malchiodi E. L., Mariuzza R. A. 1999; The structural basis of T cell activation by superantigens. Annu Rev Immunol 17:435–466 [View Article][PubMed]
    [Google Scholar]
  41. Lidén A., Van Wieringen T., Lannergård J., Kassner A., Heinegård D., Reed R. K., Guss B., Rubin K. 2008; A secreted collagen- and fibronectin-binding streptococcal protein modulates cell-mediated collagen gel contraction and interstitial fluid pressure. J Biol Chem 283:1234–1242 [View Article][PubMed]
    [Google Scholar]
  42. Lindmark H., Nilsson M., Guss B. 2001; Comparison of the fibronectin-binding protein FNE from Streptococcus equi subspecies equi with FNZ from S. equi subspecies zooepidemicus reveals a major and conserved difference. Infect Immun 69:3159–3163 [View Article][PubMed]
    [Google Scholar]
  43. Lindsay A. M., Zhang M., Mitchell Z., Holden M. T., Waller A. S., Sutcliffe I. C., Black G. W. 2009; The Streptococcus equi prophage-encoded protein SEQ2045 is a hyaluronan-specific hyaluronate lyase that is produced during equine infection. Microbiology 155:443–449 [View Article][PubMed]
    [Google Scholar]
  44. Liu M., Lei B. 2010; IgG Endopeptidase SeMac does not inhibit opsonophagocytosis of Streptococcus equi subspecies equi by horse polymorphonuclear leukocytes. Open Microbiol J 4:20–25 [View Article][PubMed]
    [Google Scholar]
  45. Llewelyn M., Cohen J. 2002; Superantigens: microbial agents that corrupt immunity. Lancet Infect Dis 2:156–162 [View Article][PubMed]
    [Google Scholar]
  46. Llewelyn M., Sriskandan S., Peakman M., Ambrozak D. R., Douek D. C., Kwok W. W., Cohen J., Altmann D. M. 2004; HLA class II polymorphisms determine responses to bacterial superantigens. J Immunol 172:1719–1726[PubMed] [CrossRef]
    [Google Scholar]
  47. Meehan M., Nowlan P., Owen P. 1998; Affinity purification and characterization of a fibrinogen-binding protein complex which protects mice against lethal challenge with Streptococcus equi subsp. equi . Microbiology 144:993–1003 [View Article][PubMed]
    [Google Scholar]
  48. Meehan M., Muldowney D. A., Watkins N. J., Owen P. 2000; Localization and characterization of the ligand-binding domain of the fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi . Microbiology 146:1187–1194[PubMed]
    [Google Scholar]
  49. Meehan M., Lynagh Y., Woods C., Owen P. 2001; The fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi additionally binds IgG and contributes to virulence in a mouse model. Microbiology 147:3311–3322[PubMed]
    [Google Scholar]
  50. Meehan M., Lewis M. J., Byrne C., O’Hare D., Woof J. M., Owen P. 2009; Localization of the equine IgG-binding domain in the fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi . Microbiology 155:2583–2592 [View Article][PubMed]
    [Google Scholar]
  51. Meehan M., Burke F. M., Macken S., Owen P. 2010; Characterization of the haem-uptake system of the equine pathogen Streptococcus equi subsp. equi . Microbiology 156:1824–1835 [View Article][PubMed]
    [Google Scholar]
  52. Newton J. R., Wood J. L., Dunn K. A., DeBrauwere M. N., Chanter N. 1997; Naturally occurring persistent and asymptomatic infection of the guttural pouches of horses with Streptococcus equi . Vet Rec 140:84–90 [View Article][PubMed]
    [Google Scholar]
  53. Newton J. R., Verheyen K., Talbot N. C., Timoney J. F., Wood J. L., Lakhani K. H., Chanter N. 2000; Control of strangles outbreaks by isolation of guttural pouch carriers identified using PCR and culture of Streptococcus equi . Equine Vet J 32:515–526 [View Article][PubMed]
    [Google Scholar]
  54. Nygaard T. K., Liu M., McClure M. J., Lei B. 2006; Identification and characterization of the heme-binding proteins SeShp and SeHtsA of Streptococcus equi subspecies equi . BMC Microbiol 6:82 [View Article][PubMed]
    [Google Scholar]
  55. Paillot R., Darby A. C., Robinson C., Wright N. L., Steward K. F., Anderson E., Webb K., Holden M. T., Efstratiou A. et al. 2010a; Identification of three novel superantigen-encoding genes in Streptococcus equi subsp. zooepidemicus, szeF, szeN, and szeP . Infect Immun 78:4817–4827 [View Article][PubMed]
    [Google Scholar]
  56. Paillot R., Robinson C., Steward K., Wright N., Jourdan T., Butcher N., Heather Z., Waller A. S. 2010b; Contribution of each of four superantigens to Streptococcus equi-induced mitogenicity, gamma interferon synthesis, and immunity. Infect Immun 78:1728–1739 [View Article][PubMed]
    [Google Scholar]
  57. Pointon J. A., Smith W. D., Saalbach G., Crow A., Kehoe M. A., Banfield M. J. 2010; A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J Biol Chem 285:33858–33866 [View Article][PubMed]
    [Google Scholar]
  58. Pritchard D. G., Lin B., Willingham T. R., Baker J. R. 1994; Characterization of the group B streptococcal hyaluronate lyase. Arch Biochem Biophys 315:431–437 [View Article][PubMed]
    [Google Scholar]
  59. Proft T., Fraser J. D. 2003; Bacterial superantigens. Clin Exp Immunol 133:299–306 [View Article][PubMed]
    [Google Scholar]
  60. Proft T., Webb P. D., Handley V., Fraser J. D. 2003; Two novel superantigens found in both group A and group C streptococcus. Infect Immun 71:1361–1369 [View Article][PubMed]
    [Google Scholar]
  61. Seedorf H., Fricke W. F., Veith B., Brüggemann H., Liesegang H., Strittmatter A., Miethke M., Buckel W., Hinderberger J. et al. 2008; The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci U S A 105:2128–2133 [View Article][PubMed]
    [Google Scholar]
  62. Shelburne S. A. III, Keith D., Horstmann N., Sumby P., Davenport M. T., Graviss E. A., Brennan R. G., Musser J. M. 2008; A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus . Proc Natl Acad Sci U S A 105:1698–1703 [View Article][PubMed]
    [Google Scholar]
  63. Sheoran A. S., Artiushin S., Timoney J. F. 2002; Nasal mucosal immunogenicity for the horse of a SeM peptide of Streptococcus equi genetically coupled to cholera toxin. Vaccine 20:1653–1659 [View Article][PubMed]
    [Google Scholar]
  64. Sitkiewicz I., Nagiec M. J., Sumby P., Butler S. D., Cywes-Bentley C., Musser J. M. 2006; Emergence of a bacterial clone with enhanced virulence by acquisition of a phage encoding a secreted phospholipase A2 . Proc Natl Acad Sci U S A 103:16009–16014 [View Article][PubMed]
    [Google Scholar]
  65. Sorek R., Kunin V., Hugenholtz P. 2008; CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181–186 [View Article][PubMed]
    [Google Scholar]
  66. Spanier J. G., Timoney J. F. 1977; Bacteriophages of Streptococcus equi . J Gen Virol 35:369–375 [View Article][PubMed]
    [Google Scholar]
  67. Sriskandan S., Faulkner L., Hopkins P. 2007; Streptococcus pyogenes: insight into the function of the streptococcal superantigens. Int J Biochem Cell Biol 39:12–19 [View Article][PubMed]
    [Google Scholar]
  68. Swierczynski A., Ton-That H. 2006; Type III pilus of corynebacteria: pilus length is determined by the level of its major pilin subunit. J Bacteriol 188:6318–6325 [View Article][PubMed]
    [Google Scholar]
  69. Timoney J. F. 1993; Strangles. Vet Clin North Am Equine Pract 9:365–374[PubMed]
    [Google Scholar]
  70. Timoney J. F., Kumar P. 2008; Early pathogenesis of equine Streptococcus equi infection (strangles). Equine Vet J 40:637–642 [View Article][PubMed]
    [Google Scholar]
  71. Timoney J. F., Artiushin S. C., Boschwitz J. S. 1997; Comparison of the sequences and functions of Streptococcus equi M-like proteins SeM and SzPSe. Infect Immun 65:3600–3605[PubMed]
    [Google Scholar]
  72. Timoney J. F., Yang J., Liu J., Merant C. 2008; IdeE reduces the bactericidal activity of equine neutrophils for Streptococcus equi . Vet Immunol Immunopathol 122:76–82 [View Article][PubMed]
    [Google Scholar]
  73. Timoney J. F., DeNegri R., Sheoran A., Forster N. 2010; Affects of N-terminal variation in the SeM protein of Streptococcus equi on antibody and fibrinogen binding. Vaccine 28:1522–1527 [View Article][PubMed]
    [Google Scholar]
  74. Tiwari R., Timoney J. F. 2009; Streptococcus equi bacteriophage SeP9 binds to group C carbohydrate but is not infective for the closely related S. zooepidemicus . Vet Microbiol 135:304–307 [View Article][PubMed]
    [Google Scholar]
  75. Tiwari R., Qin A., Artiushin S., Timoney J. F. 2007; Se18.9, an anti-phagocytic factor H binding protein of Streptococcus equi . Vet Microbiol 121:105–115 [View Article][PubMed]
    [Google Scholar]
  76. Turner C. E., Kurupati P., Wiles S., Edwards R. J., Sriskandan S. 2009; Impact of immunization against SpyCEP during invasive disease with two streptococcal species: Streptococcus pyogenes and Streptococcus equi . Vaccine 27:4923–4929 [View Article][PubMed]
    [Google Scholar]
  77. Verheyen K., Newton J. R., Talbot N. C., De Brauwere M. N., Chanter N. 2000; Elimination of guttural pouch infection and inflammation in asymptomatic carriers of Streptococcus equi . Equine Vet J 32:527–532 [View Article][PubMed]
    [Google Scholar]
  78. Von Pawel-Rammingen U., Johansson B. P., Björck L. 2002; IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J 21:1607–1615 [View Article][PubMed]
    [Google Scholar]
  79. Wade C. M., Giulotto E., Sigurdsson S., Zoli M., Gnerre S., Imsland F., Lear T. L., Adelson D. L., Bailey E. et al. 2009; Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865–867 [View Article][PubMed]
    [Google Scholar]
  80. Wandersman C., Delepelaire P. 2004; Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647 [View Article][PubMed]
    [Google Scholar]
  81. Wannamaker L. W. 1983; Streptococcal toxins. Rev Infect Dis 5:Suppl. 4S723–S732 [View Article][PubMed]
    [Google Scholar]
  82. Webb K., Jolley K. A., Mitchell Z., Robinson C., Newton J. R., Maiden M. C., Waller A. 2008; Development of an unambiguous and discriminatory multilocus sequence typing scheme for the Streptococcus zooepidemicus group. Microbiology 154:3016–3024 [View Article][PubMed]
    [Google Scholar]
  83. Woolcock J. B. 1974; The capsule of Streptococcus equi . J Gen Microbiol 85:372–375[PubMed] [CrossRef]
    [Google Scholar]
  84. Wooldridge K. G., Williams P. H. 1993; Iron uptake mechanisms of pathogenic bacteria. FEMS Microbiol Rev 12:325–348 [View Article][PubMed]
    [Google Scholar]
  85. Zhu H., Liu M., Lei B. 2008; The surface protein Shr of Streptococcus pyogenes binds heme and transfers it to the streptococcal heme-binding protein Shp. BMC Microbiol 8:15 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.028233-0
Loading
/content/journal/jmm/10.1099/jmm.0.028233-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error