1887

Abstract

Considerable progress has been made in understanding the roles of in inflammation and gastric cancer; however, far less is known about the roles of enterohepatic species (EHS) in carcinogenesis and their zoonotic or pathogenic potential. We determined the prevalence of EHS infection in a cohort of geriatric rhesus monkeys in which intestinal adenocarcinoma (IAC) is common and investigated the association between EHS infection and IAC. The cohort consisted of 36 animals, 14 of which (age 26–35 years) had IAC. Of the 36 rhesus, 35 (97 %) were positive for EHS using PCR or bacterial isolation from faeces, colonic or tumour tissues. Only a single rhesus, which had IAC, was negative for EHS by all detection methods. The EHS identified by 16S rRNA sequencing in this study were from three taxa: (previously rhesus monkey taxon 1), sp. rhesus monkey taxon 2, previously described from strain MIT 99-5507, and sp. rhesus monkey taxon 4, related to . Thirteen of 14 monkeys with IAC were positive for either (7/13, 54 %), EHS rhesus monkey taxon 4 (4/13, 31 %) or a mixture of the two EHS (2/13, 15 %). These results indicate that EHS are prevalent among aged rhesus macaques with IAC. Using genus-specific florescent hybridization, EHS were detected on the surface of colonic epithelia of infected monkeys. All isolates, including , effectively adhered to, invaded, and significantly induced proinflammatory genes, including , , α and , while downregulating genes involved in the function of inflammasomes, particularly β and in the human colonic T84 cell line (<0.0001). These results suggest that EHS may represent an aetiological agent mediating diarrhoea, chronic inflammation, and possibly intestinal cancer in non-human primates, and may play a role in similar disease syndromes in humans. Downregulation of inflammasome function may represent an EHS strategy for long-term persistence in the host and play a role in inducing pathological changes in the host’s lower bowel.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.072462-0
2014-07-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/7/1004.html?itemId=/content/journal/jmm/10.1099/jmm.0.072462-0&mimeType=html&fmt=ahah

References

  1. Avenaud P., Marais A., Monteiro L., Le Bail B., Bioulac Sage P., Balabaud C., Mégraud F. 2000; Detection of Helicobacter species in the liver of patients with and without primary liver carcinoma. Cancer 89:1431–1439 [View Article][PubMed]
    [Google Scholar]
  2. Bornschein J., Kandulski A., Selgrad M., Malfertheiner P. 2010; From gastric inflammation to gastric cancer. Dig Dis 28:609–614 [View Article][PubMed]
    [Google Scholar]
  3. Bridgeford E. C., Marini R. P., Feng Y., Parry N. M., Rickman B., Fox J. G. 2008; Gastric Helicobacter species as a cause of feline gastric lymphoma: a viable hypothesis. Vet Immunol Immunopathol 123:106–113 [View Article][PubMed]
    [Google Scholar]
  4. Burman W. J., Cohn D. L., Reves R. R., Wilson M. L. 1995; Multifocal cellulitis and monoarticular arthritis as manifestations of Helicobacter cinaedi bacteremia. Clin Infect Dis 20:564–570 [View Article][PubMed]
    [Google Scholar]
  5. Burnens A. P., Stanley J., Morgenstern R., Nicolet J. 1994; Gastroenteritis associated with Helicobacter pullorum. Lancet 344:1569–1570 [View Article][PubMed]
    [Google Scholar]
  6. Cahill R. J., Foltz C. J., Fox J. G., Dangler C. A., Powrie F., Schauer D. B. 1997; Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect Immun 65:3126–3131[PubMed]
    [Google Scholar]
  7. Candido J., Hagemann T. 2013; Cancer-related inflammation. J Clin Immunol 33:Suppl 179–84 [View Article][PubMed]
    [Google Scholar]
  8. Carvalho F. A., Nalbantoglu I., Aitken J. D., Uchiyama R., Su Y., Doho G. H., Vijay-Kumar M., Gewirtz A. T. 2012; Cytosolic flagellin receptor NLRC4 protects mice against mucosal and systemic challenges. Mucosal Immunol 5:288–298 [View Article][PubMed]
    [Google Scholar]
  9. Ceelen L., Decostere A., Verschraegen G., Ducatelle R., Haesebrouck F. 2005; Prevalence of Helicobacter pullorum among patients with gastrointestinal disease and clinically healthy persons. J Clin Microbiol 43:2984–2986 [View Article][PubMed]
    [Google Scholar]
  10. Chan V., Crocetti G., Grehan M., Zhang L., Danon S., Lee A., Mitchell H. 2005; Visualization of Helicobacter species within the murine cecal mucosa using specific fluorescence in situ hybridization. Helicobacter 10:114–124 [View Article][PubMed]
    [Google Scholar]
  11. Chichlowski M., Sharp J. M., Vanderford D. A., Myles M. H., Hale L. P. 2008; Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice. Comp Med 58:534–541[PubMed]
    [Google Scholar]
  12. Chien C. C., Taylor N. S., Ge Z., Schauer D. B., Young V. B., Fox J. G. 2000; Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp.. J Med Microbiol 49:525–534[PubMed]
    [Google Scholar]
  13. Chin E. Y., Dangler C. A., Fox J. G., Schauer D. B. 2000; Helicobacter hepaticus infection triggers inflammatory bowel disease in T cell receptor αβ mutant mice. Comp Med 50:586–594[PubMed]
    [Google Scholar]
  14. Cimolai N., Gill M. J., Jones A., Flores B., Stamm W. E., Laurie W., Madden B., Shahrabadi M. S. 1987; Campylobacter cinaedi” bacteremia: case report and laboratory findings. J Clin Microbiol 25:942–943[PubMed]
    [Google Scholar]
  15. Cortes-Bratti X., Chaves-Olarte E., Lagergård T., Thelestam M. 1999; The cytolethal distending toxin from the chancroid bacterium Haemophilus ducreyi induces cell-cycle arrest in the G2 phase. J Clin Invest 103:107–115 [View Article][PubMed]
    [Google Scholar]
  16. Dewhirst F. E., Shen Z., Scimeca M. S., Stokes L. N., Boumenna T., Chen T., Paster B. J., Fox J. G. 2005; Discordant 16S and 23S rRNA gene phylogenies for the genus Helicobacter: implications for phylogenetic inference and systematics. J Bacteriol 187:6106–6118 [View Article][PubMed]
    [Google Scholar]
  17. Eiró N., Vizoso F. J. 2012; Inflammation and cancer. World J Gastrointest Surg 4:62–72 [View Article][PubMed]
    [Google Scholar]
  18. Elinav E., Strowig T., Kau A. L., Henao-Mejia J., Thaiss C. A., Booth C. J., Peaper D. R., Bertin J., Eisenbarth S. C.& other authors ( 2011; NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145:745–757 [View Article][PubMed]
    [Google Scholar]
  19. Erdman S. E., Poutahidis T., Tomczak M., Rogers A. B., Cormier K., Plank B., Horwitz B. H., Fox J. G. 2003; CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 162:691–702 [View Article][PubMed]
    [Google Scholar]
  20. Erdman S. E., Rao V. P., Poutahidis T., Rogers A. B., Taylor C. L., Jackson E. A., Ge Z., Lee C. W., Schauer D. B.& other authors ( 2009; Nitric oxide and TNF-α trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci U S A 106:1027–1032 [View Article][PubMed]
    [Google Scholar]
  21. Fernandez K. R., Hansen L. M., Vandamme P., Beaman B. L., Solnick J. V. 2002; Captive rhesus monkeys (Macaca mulatta) are commonly infected with Helicobacter cinaedi. J Clin Microbiol 40:1908–1912 [View Article][PubMed]
    [Google Scholar]
  22. Flores B. M., Fennell C. L., Kuller L., Bronsdon M. A., Morton W. R., Stamm W. E. 1990; Experimental infection of pig-tailed macaques (Macaca nemestrina) with Campylobacter cinaedi and Campylobacter fennelliae. Infect Immun 58:3947–3953[PubMed]
    [Google Scholar]
  23. Foley J. E., Solnick J. V., Lapointe J. M., Jang S., Pedersen N. C. 1998; Identification of a novel enteric Helicobacter species in a kitten with severe diarrhea. J Clin Microbiol 36:908–912[PubMed]
    [Google Scholar]
  24. Foley J. E., Marks S. L., Munson L., Melli A., Dewhirst F. E., Yu S., Shen Z., Fox J. G. 1999; Isolation of Helicobacter canis from a colony of Bengal cats with endemic diarrhea. J Clin Microbiol 37:3271–3275[PubMed]
    [Google Scholar]
  25. Foltz C. J., Fox J. G., Cahill R., Murphy J. C., Yan L., Shames B., Schauer D. B. 1998; Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus. Helicobacter 3:69–78 [View Article][PubMed]
    [Google Scholar]
  26. Fox J. G. 2002; The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50:273–283 [View Article][PubMed]
    [Google Scholar]
  27. Fox J. G., Li X., Yan L., Cahill R. J., Hurley R., Lewis R., Murphy J. C. 1996a; Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of Helicobacter-induced carcinogenesis. Infect Immun 64:1548–1558[PubMed]
    [Google Scholar]
  28. Fox J. G., Yan L., Shames B., Campbell J., Murphy J. C., Li X. 1996b; Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus. Infect Immun 64:3673–3681[PubMed]
    [Google Scholar]
  29. Fox J. G., Gorelick P. L., Kullberg M. C., Ge Z., Dewhirst F. E., Ward J. M. 1999; A novel urease-negative Helicobacter species associated with colitis and typhlitis in IL-10-deficient mice. Infect Immun 67:1757–1762[PubMed]
    [Google Scholar]
  30. Fox J. G., Chien C. C., Dewhirst F. E., Paster B. J., Shen Z., Melito P. L., Woodward D. L., Rodgers F. G. 2000; Helicobacter canadensis sp. nov. isolated from humans with diarrhea as an example of an emerging pathogen. J Clin Microbiol 38:2546–2549[PubMed]
    [Google Scholar]
  31. Fox J. G., Handt L., Sheppard B. J., Xu S., Dewhirst F. E., Motzel S., Klein H. 2001a; Isolation of Helicobacter cinaedi from the colon, liver, and mesenteric lymph node of a rhesus monkey with chronic colitis and hepatitis. J Clin Microbiol 39:1580–1585 [View Article][PubMed]
    [Google Scholar]
  32. Fox J. G., Handt L., Xu S., Shen Z., Dewhirst F. E., Paster B. J., Dangler C. A., Lodge K., Motzel S., Klein H. 2001b; Novel Helicobacter species isolated from rhesus monkeys with chronic idiopathic colitis. J Med Microbiol 50:421–429[PubMed]
    [Google Scholar]
  33. Fox J. G., Shen Z., Xu S., Feng Y., Dangler C. A., Dewhirst F. E., Paster B. J., Cullen J. M. 2002; Helicobacter marmotae sp. nov. isolated from livers of woodchucks and intestines of cats. J Clin Microbiol 40:2513–2519 [View Article][PubMed]
    [Google Scholar]
  34. Fox J. G., Boutin S. R., Handt L. K., Taylor N. S., Xu S., Rickman B., Marini R. P., Dewhirst F. E., Paster B. J.& other authors ( 2007; Isolation and characterization of a novel helicobacter species, “Helicobacter macacae,” from rhesus monkeys with and without chronic idiopathic colitis. J Clin Microbiol 45:4061–4063 [View Article][PubMed]
    [Google Scholar]
  35. Fox J. G., Ge Z., Whary M. T., Erdman S. E., Horwitz B. H. 2011; Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol 4:22–30 [View Article][PubMed]
    [Google Scholar]
  36. García A., Zeng Y., Muthupalani S., Ge Z., Potter A., Mobley M. W., Boussahmain C., Feng Y., Wishnok J. S., Fox J. G. 2011; Helicobacter hepaticus-induced liver tumor promotion is associated with increased serum bile acid and a persistent microbial-induced immune response. Cancer Res 71:2529–2540 [View Article][PubMed]
    [Google Scholar]
  37. Ge Z., Feng Y., Muthupalani S., Eurell L. L., Taylor N. S., Whary M. T., Fox J. G. 2011; Coinfection with enterohepatic Helicobacter species can ameliorate or promote Helicobacter pylori-induced gastric pathology in C57BL/6 mice. Infect Immun 79:3861–3871 [View Article][PubMed]
    [Google Scholar]
  38. Goldman C. G., Mitchell H. M. 2010; Helicobacter spp. other than Helicobacter pylori. Helicobacter 15:Suppl 169–75 [View Article][PubMed]
    [Google Scholar]
  39. Grivennikov S. I., Karin M. 2010; Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 20:65–71 [View Article][PubMed]
    [Google Scholar]
  40. Grivennikov S. I., Greten F. R., Karin M. 2010; Immunity, inflammation, and cancer. Cell 140:883–899 [View Article][PubMed]
    [Google Scholar]
  41. Haggerty T. D., Perry S., Sanchez L., Perez-Perez G., Parsonnet J. 2005; Significance of transiently positive enzyme-linked immunosorbent assay results in detection of Helicobacter pylori in stool samples from children. J Clin Microbiol 43:2220–2223 [View Article][PubMed]
    [Google Scholar]
  42. Hansen R., Thomson J. M., Fox J. G., El-Omar E. M., Hold G. L. 2011; Could Helicobacter organisms cause inflammatory bowel disease?. FEMS Immunol Med Microbiol 61:1–14 [View Article][PubMed]
    [Google Scholar]
  43. Hsueh P. R., Teng L. J., Hung C. C., Chen Y. C., Yang P. C., Ho S. W., Luh K. T. 1999; Septic shock due to Helicobacter fennelliae in a non-human immunodeficiency virus-infected heterosexual patient. J Clin Microbiol 37:2084–2086[PubMed]
    [Google Scholar]
  44. Huber S., Gagliani N., Zenewicz L. A., Huber F. J., Bosurgi L., Hu B., Hedl M., Zhang W., O’Connor W. Jr& other authors ( 2012; IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491:259–263 [View Article][PubMed]
    [Google Scholar]
  45. Hung C. C., Hsueh P. R., Chen M. Y., Teng L. J., Chen Y. C., Luh K. T., Chuang C. Y. 1997; Bacteremia caused by Helicobacter cinaedi in an AIDS patients. J Formos Med Assoc 96:558–560[PubMed]
    [Google Scholar]
  46. Kempster S. L., Belteki G., Forhead A. J., Fowden A. L., Catalano R. D., Lam B. Y., McFarlane I., Charnock-Jones D. S., Smith G. C. 2011; Developmental control of the Nlrp6 inflammasome and a substrate, IL-18, in mammalian intestine. Am J Physiol Gastrointest Liver Physiol 300:G253–G263 [View Article][PubMed]
    [Google Scholar]
  47. Kitamura T., Kawamura Y., Ohkusu K., Masaki T., Iwashita H., Sawa T., Fujii S., Okamoto T., Akaike T. 2007; Helicobacter cinaedi cellulitis and bacteremia in immunocompetent hosts after orthopedic surgery. J Clin Microbiol 45:31–38 [View Article][PubMed]
    [Google Scholar]
  48. Lamkanfi M., Dixit V. M. 2011; Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 187:597–602 [View Article][PubMed]
    [Google Scholar]
  49. Lapin B. A., Yakovleva L. A. 2014; Spontaneous and experimental malignancies in non-human primates. J Med Primatol 43:100–110 [View Article][PubMed]
    [Google Scholar]
  50. Lertpiriyapong K., Gamazon E. R., Feng Y., Park D. S., Pang J., Botka G., Graffam M. E., Ge Z., Fox J. G. 2012; Campylobacter jejuni type VI secretion system: roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. PLoS ONE 7:e42842 [View Article][PubMed]
    [Google Scholar]
  51. Maggio-Price L., Treuting P., Zeng W., Tsang M., Bielefeldt-Ohmann H., Iritani B. M. 2006; Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res 66:828–838 [View Article][PubMed]
    [Google Scholar]
  52. Mangerich A., Knutson C. G., Parry N. M., Muthupalani S., Ye W., Prestwich E., Cui L., McFaline J. L., Mobley M.& other authors ( 2012; Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci U S A 109:E1820–E1829 [View Article][PubMed]
    [Google Scholar]
  53. Marini R. P., Muthupalani S., Shen Z., Buckley E. M., Alvarado C., Taylor N. S., Dewhirst F. E., Whary M. T., Patterson M. M., Fox J. G. 2010; Persistent infection of rhesus monkeys with ‘Helicobacter macacae’ and its isolation from an animal with intestinal adenocarcinoma. J Med Microbiol 59:961–969 [View Article][PubMed]
    [Google Scholar]
  54. Master S. S., Rampini S. K., Davis A. S., Keller C., Ehlers S., Springer B., Timmins G. S., Sander P., Deretic V. 2008; Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 3:224–232 [View Article][PubMed]
    [Google Scholar]
  55. Melito P. L., Munro C., Chipman P. R., Woodward D. L., Booth T. F., Rodgers F. G. 2001; Helicobacter winghamensis sp. nov., a novel Helicobacter sp. isolated from patients with gastroenteritis. J Clin Microbiol 39:2412–2417 [View Article][PubMed]
    [Google Scholar]
  56. Oyama K., Khan S., Okamoto T., Fujii S., Ono K., Matsunaga T., Yoshitake J., Sawa T., Tomida J.& other authors ( 2012; Identification of and screening for human Helicobacter cinaedi infections and carriers via nested PCR. J Clin Microbiol 50:3893–3900 [View Article][PubMed]
    [Google Scholar]
  57. Pereira M. S., Morgantetti G. F., Massis L. M., Horta C. V., Hori J. I., Zamboni D. S. 2011; Activation of NLRC4 by flagellated bacteria triggers caspase-1-dependent and -independent responses to restrict Legionella pneumophila replication in macrophages and in vivo. J Immunol 187:6447–6455 [View Article][PubMed]
    [Google Scholar]
  58. Proietti F. A., Carneiro-Proietti A. B., Catalan-Soares B. C., Murphy E. L. 2005; Global epidemiology of HTLV-I infection and associated diseases. Oncogene 24:6058–6068 [View Article][PubMed]
    [Google Scholar]
  59. Ranatunga D. C., Ramakrishnan A., Uprety P., Wang F., Zhang H., Margolick J. B., Brayton C., Bream J. H. 2012; A protective role for human IL-10-expressing CD4+ T cells in colitis. J Immunol 189:1243–1252 [View Article][PubMed]
    [Google Scholar]
  60. Rathinam V. A., Vanaja S. K., Fitzgerald K. A. 2012; Regulation of inflammasome signaling. Nat Immunol 13:333–342 [View Article][PubMed]
    [Google Scholar]
  61. Rodriguez N. A., Garcia K. D., Fortman J. D., Hewett T. A., Bunte R. M., Bennett B. T. 2002; Clinical and histopathological evaluation of 13 cases of adenocarcinoma in aged rhesus macaques (Macaca mulatta). J Med Primatol 31:74–83 [View Article][PubMed]
    [Google Scholar]
  62. Russell R. G., Sarmiento J. I., Fox J., Panigrahi P. 1990; Evidence of reinfection with multiple strains of Campylobacter jejuni and Campylobacter coli in Macaca nemestrina housed under hyperendemic conditions. Infect Immun 58:2149–2155[PubMed]
    [Google Scholar]
  63. Saunders K. E., Shen Z., Dewhirst F. E., Paster B. J., Dangler C. A., Fox J. G. 1999; Novel intestinal Helicobacter species isolated from cotton-top tamarins (Saguinus oedipus) with chronic colitis. J Clin Microbiol 37:146–151[PubMed]
    [Google Scholar]
  64. Shen Z., Feng Y., Rogers A. B., Rickman B., Whary M. T., Xu S., Clapp K. M., Boutin S. R., Fox J. G. 2009; Cytolethal distending toxin promotes Helicobacter cinaedi-associated typhlocolitis in interleukin-10-deficient mice. Infect Immun 77:2508–2516 [View Article][PubMed]
    [Google Scholar]
  65. Sugai M., Kawamoto T., Pérès S. Y., Ueno Y., Komatsuzawa H., Fujiwara T., Kurihara H., Suginaka H., Oswald E. 1998; The cell cycle-specific growth-inhibitory factor produced by Actinobacillus actinomycetemcomitans is a cytolethal distending toxin. Infect Immun 66:5008–5019[PubMed]
    [Google Scholar]
  66. Taylor N. S., Ge Z., Shen Z., Dewhirst F. E., Fox J. G. 2003; Cytolethal distending toxin: a potential virulence factor for Helicobacter cinaedi. J Infect Dis 188:1892–1897 [View Article][PubMed]
    [Google Scholar]
  67. Thomson J. M., Hansen R., Berry S. H., Hope M. E., Murray G. I., Mukhopadhya I., McLean M. H., Shen Z., Fox J. G.& other authors ( 2011; Enterohepatic Helicobacter in ulcerative colitis: potential pathogenic entities?. PLoS ONE 6:e17184 [View Article][PubMed]
    [Google Scholar]
  68. Uno H., Alsum P., Zimbric M. L., Houser W. D., Thomson J. A., Kemnitz J. W. 1998; Colon cancer in aged captive rhesus monkeys (Macaca mulatta). Am J Primatol 44:19–27 [View Article][PubMed]
    [Google Scholar]
  69. Valverde C. R., Tarara R. P., Griffey S. M., Roberts J. A. 2000; Spontaneous intestinal adenocarcinoma in geriatric macaques (Macaca sp.). Comp Med 50:540–544[PubMed]
    [Google Scholar]
  70. Whary M. T., Danon S. J., Feng Y., Ge Z., Sundina N., Ng V., Taylor N. S., Rogers A. B., Fox J. G. 2006; Rapid onset of ulcerative typhlocolitis in B6.129P2-IL10tm1Cgn (IL-10−/−) mice infected with Helicobacter trogontum is associated with decreased colonization by altered Schaedler’s flora. Infect Immun 74:6615–6623 [View Article][PubMed]
    [Google Scholar]
  71. Young V. B., Chien C. C., Knox K. A., Taylor N. S., Schauer D. B., Fox J. G. 2000a; Cytolethal distending toxin in avian and human isolates of Helicobacter pullorum. J Infect Dis 182:620–623 [View Article][PubMed]
    [Google Scholar]
  72. Young V. B., Knox K. A., Schauer D. B. 2000b; Cytolethal distending toxin sequence and activity in the enterohepatic pathogen Helicobacter hepaticus. Infect Immun 68:184–191 [View Article][PubMed]
    [Google Scholar]
  73. Zaki M. H., Boyd K. L., Vogel P., Kastan M. B., Lamkanfi M., Kanneganti T. D. 2010; The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32:379–391 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.072462-0
Loading
/content/journal/jmm/10.1099/jmm.0.072462-0
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