1887

Journal of General Virology header logo

Volume 97, Issue 7

Novel bat adenoviruses with an extremely large E3 gene Free

Abstract

Bats carry diverse RNA viruses, some of which are responsible for human diseases. Compared to bat-borne RNA viruses, relatively little information is known regarding bat-borne DNA viruses. In this study, we isolated and characterized three novel bat adenoviruses (BtAdV WIV9–11) from . Their genomes, which are highly similar to each other but distinct from those of previously sequenced adenoviruses (AdVs), are 37 545, 37 566 and 38 073 bp in size, respectively. An unusually large E3 gene was identified in their genomes. Phylogenetic and taxonomic analyses suggested that these isolates represent a distinct species of the genus . Cell susceptibility assays revealed a broad cell tropism for these isolates, indicating that they have a potentially wide host range. Our results expand the understanding of genetic diversity of bat AdVs.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bat adenovirus , long E3 gene and mastadenovirus
© 2016 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000470
2016-07-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/7/1625.html?itemId=/content/journal/jgv/10.1099/jgv.0.000470&mimeType=html&fmt=ahah

References

  1. Anthony S. J., Epstein J. H., Murray K. A., Navarrete-Macias I., Zambrana-Torrelio C. M., Solovyov A., Ojeda-Flores R., Arrigo N. C., Islam A. et al. 2013; A strategy to estimate unknown viral diversity in mammals. MBio 4:e0059800513 [View Article][PubMed]
     [Google Scholar]
  2. Appel M., Bistner S. I., Menegus M., Albert D. A., Carmichael L. E. 1973; Pathogenicity of low-virulence strains of two canine adenovirus types. Am J Vet Res 34:543–550[PubMed]
     [Google Scholar]
  3. Bahr U., Schöndorf E., Handermann M., Darai G. 2003; Molecular anatomy of Tupaia (tree shrew) adenovirus genome; evolution of viral genes and viral phylogeny. Virus Genes 27:29–48[PubMed] [CrossRef]
     [Google Scholar]
  4. Baker K. S., Leggett R. M., Bexfield N. H., Alston M., Daly G., Todd S., Tachedjian M., Holmes C. E., Crameri S. et al. 2013; Metagenomic study of the viruses of african straw-coloured fruit bats: Detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 441:95–106 [CrossRef]
     [Google Scholar]
  5. Benkö M., Harrach B. 2003; Molecular evolution of adenoviruses. Curr Top Microbiol Immunol 272:3–35[PubMed]
     [Google Scholar]
  6. Burgert H. G., Kvist S. 1985; An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell 41:987–997 [View Article][PubMed]
     [Google Scholar]
  7. Burgert H. G., Maryanski J. L., Kvist S. 1987; "E3/19K" protein of adenovirus type 2 inhibits lysis of cytolytic T lymphocytes by blocking cell-surface expression of histocompatibility class I antigens. Proc Natl Acad Sci U S A 84:1356–1360[PubMed] [CrossRef]
     [Google Scholar]
  8. Casas I., Vazquez-Moron S., Juste J., Falcon A., Aznar C., Ibanez C., Pozo F., Ruiz G., Berciano J. M. et al. 2010 Adenovirus groups in western Palaearctic bats in Spain GenBank Accession No: JX065117 to JX065129
    [Google Scholar]
  9. Chen L. H., Wu Z. Q., Hu Y. F., Yang F., Yang J., Jin Q. 2012; [Genetic diversity of adenoviruses in bats of China]. Bing Du Xue Bao 28:403–408[PubMed]
     [Google Scholar]
  10. Chua K. B., Bellini W. J., Rota P. A., Harcourt B. H., Tamin A., Lam S. K., Ksiazek T. G., Rollin P. E., Zaki S. R. et al. 2000; Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432–1435 [View Article][PubMed]
     [Google Scholar]
  11. Corman V. M., Baldwin H. J., Tateno A. F., Zerbinati R. M., Annan A., Owusu M., Nkrumah E. E., Maganga G. D., Oppong S., other authors. 2015; Evidence for an ancestral association of human coronavirus 229E with Bats. J Virol 89:11858–11870 [View Article][PubMed]
     [Google Scholar]
  12. Crameri G., Todd S., Grimley S., McEachern J. A., Marsh G. A., Smith C., Tachedjian M., De Jong C., Virtue E. R. et al. 2009; Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One 4:e8266 [View Article][PubMed]
     [Google Scholar]
  13. Dán A., Ruzsics Z., Russell W. C., Benkö M., Harrach B. 1998; Analysis of the hexon gene sequence of bovine adenovirus type 4 provides further support for a new adenovirus genus (Atadenovirus). J Gen Virol 79:1453–1460 [View Article][PubMed]
     [Google Scholar]
  14. Davison A. J., Wright K. M., Harrach B. 2000; DNA sequence of frog adenovirus. J Gen Virol 81:2431–2439 [View Article][PubMed]
     [Google Scholar]
  15. Davison A. J., Benko M., Harrach B. 2003; Genetic content and evolution of adenoviruses. J Gen Virol 84:2895–2908 [View Article][PubMed]
     [Google Scholar]
  16. De Jong J. C., Wermenbol A. G., Verweij-Uijterwaal M. W., Slaterus K. W., Wertheim-Van Dillen P., Van Doornum G. J., Khoo S. H., Hierholzer J. C. 1999; Adenoviruses from human immunodeficiency virus-infected individuals, including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D, respectively. J Clin Microbiol 37:3940–3945[PubMed]
     [Google Scholar]
  17. DeBey B. M., Lehmkuhl H. D., Chard-Bergstrom C., Hobbs L. A. 2001; Ovine adenovirus serotype 7-associated mortality in lambs in the United States. Vet Pathol 38:644–648 [View Article][PubMed]
     [Google Scholar]
  18. Deryckere F., Burgert H. G. 1996; Early region 3 of adenovirus type 19 (subgroup D) encodes an hla-binding protein distinct from that of subgroups B and C. J Virol 70:2832–2841[PubMed]
     [Google Scholar]
  19. Echavarría M. 2008; Adenoviruses in immunocompromised hosts. Clin Microbiol Rev 21:704–715 [View Article][PubMed]
     [Google Scholar]
  20. Elsing A., Burgert H. G. 1998; The adenovirus E3/10.4K-14.5K proteins down-modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc Natl Acad Sci U S A 95:10072–10077 [View Article][PubMed]
     [Google Scholar]
  21. Farkas S. L., Harrach B., Benko M. 2008; Completion of the genome analysis of snake adenovirus type 1, a representative of the reptilian lineage within the novel genus atadenovirus. Virus Res 132:132–139 [View Article][PubMed]
     [Google Scholar]
  22. Fessler S. P., Delgado-Lopez F., Horwitz M. S. 2004; Mechanisms of E3 modulation of immune and inflammatory responses. Curr Top Microbiol Immunol 273:113–135 [View Article][PubMed]
     [Google Scholar]
  23. Frazer K. A., Pachter L., Poliakov A., Rubin E. M., Dubchak I. 2004; VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279 [View Article][PubMed]
     [Google Scholar]
  24. Frohman M. A., Dush M. K., Martin G. R. 1988; Rapid production of full-length cDNAS from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A 85:8998–9002 [View Article][PubMed]
     [Google Scholar]
  25. Ge X. Y., Li J. L., Yang X. L., Chmura A. A., Zhu G., Epstein J. H., Mazet J. K., Hu B., Zhang W. et al. 2013; Isolation and characterization of a bat sars-like coronavirus that uses the ACE2 receptor. Nat New Biol 503:535–538 [CrossRef]
     [Google Scholar]
  26. Geisbert T. W., Bailey M., Hensley L., Asiedu C., Geisbert J., Stanley D., Honko A., Johnson J., Mulangu S., other authors. 2011; Recombinant adenovirus serotype 26 (Ad26) and Ad35 vaccine vectors bypass immunity to Ad5 and protect nonhuman primates against ebolavirus challenge. J Virol 85:4222–4233 [View Article][PubMed]
     [Google Scholar]
  27. Ghebremedhin B. 2014; Human adenovirus: Viral pathogen with increasing importance. Eur J Microbiol Immunol (Bp) 4:26–33 [View Article]
     [Google Scholar]
  28. Gooding L. R., Elmore L. W., Tollefson A. E., Brady H. A., Wold W. S. 1988; A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. Cell 53:341–346 [View Article][PubMed]
     [Google Scholar]
  29. Harrach B., Benkö M., Both G. W., Brown M., Davison A. J., Echavarría M., Hess M., Jones M. S., Kajon A. et al. 2011; Family Adenoviridae. In Virus Taxonomy Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses pp. 125–141 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. San Diego: Elsevier;
     [Google Scholar]
  30. Hemmi S., Vidovszky M. Z., Ruminska J., Ramelli S., Decurtins W., Greber U. F., Harrach B. 2011; Genomic and phylogenetic analyses of murine adenovirus 2. Virus Res 160:128–135 [View Article][PubMed]
     [Google Scholar]
  31. Hess M., Blöcker H., Brandt P., Blocker H. 1997; The complete nucleotide sequence of the egg drop syndrome virus: An intermediate between mastadenoviruses and aviadenoviruses. Virology 238:145–156 [View Article]
     [Google Scholar]
  32. Hofmayer S., Madisch I., Darr S., Rehren F., Heim A. 2009; Unique sequence features of the human adenovirus 31 complete genomic sequence are conserved in clinical isolates. BMC Genomics 10:557 [View Article]
     [Google Scholar]
  33. Horton T. M., Ranheim T. S., Aquino L., Kusher D. I., Saha S. K., Ware C. F., Wold W. S., Gooding L. R. 1991; Adenovirus E3 14.7K protein functions in the absence of other adenovirus proteins to protect transfected cells from tumor necrosis factor cytolysis. J Virol 65:2629–2639[PubMed]
     [Google Scholar]
  34. Hoşnut F. Ö., Özçay F., Malbora B., Hızlı S., Özbek N. 2014; Severe adenovirus infection associated with hemophagocytic lymphohistiocytosis. Turk J Haematol 31:103–105 [View Article][PubMed]
     [Google Scholar]
  35. Ishiko H., Shimada Y., Konno T., Hayashi A., Ohguchi T., Tagawa Y., Aoki K., Ohno S., Yamazaki S. 2008; Novel human adenovirus causing nosocomial epidemic keratoconjunctivitis. J Clin Microbiol 46:2002–2008 [View Article][PubMed]
     [Google Scholar]
  36. Jones M. S., Harrach B., Ganac R. D., Gozum M. M., Dela Cruz W. P., Riedel B., Pan C., Delwart E. L., Schnurr D. P. 2007; New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81:5978–5984 [View Article][PubMed]
     [Google Scholar]
  37. Käll L., Krogh A., Sonnhammer E. L. 2004; A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036 [View Article][PubMed]
     [Google Scholar]
  38. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S. et al. 2012; Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649 [View Article][PubMed]
     [Google Scholar]
  39. Kelley L. A., Mezulis S., Yates C. M., Wass M. N., Sternberg M. J. 2015; The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858 [View Article][PubMed]
     [Google Scholar]
  40. Kohl C., Vidovszky M. Z., Mühldorfer K., Dabrowski P. W., Radonić A., Nitsche A., Wibbelt G., Kurth A., Harrach B. 2012; Genome analysis of bat adenovirus 2: Indications of interspecies transmission. J Virol 86:1888–1892 [View Article][PubMed]
     [Google Scholar]
  41. Kovács E. R., Benko M. 2009; Confirmation of a novel siadenovirus species detected in raptors: Partial sequence and phylogenetic analysis. Virus Res 140:64–70 [View Article][PubMed]
     [Google Scholar]
  42. Kovács E. R., Jánoska M., Dán A., Harrach B., Benko M. 2010; Recognition and partial genome characterization by non-specific DNA amplification and PCR of a new siadenovirus species in a sample originating from Parus major, a great tit. J Virol Methods 163:262–268 [View Article][PubMed]
     [Google Scholar]
  43. Kovács G. M., LaPatra S. E., D'Halluin J. C., Benko M. 2003; Phylogenetic analysis of the hexon and protease genes of a fish adenovirus isolated from white sturgeon (Acipenser transmontanus) supports the proposal for a new adenovirus genus. Virus Res 98:27–34[PubMed] [CrossRef]
     [Google Scholar]
  44. Kremer E. J., Boutin S., Chillon M., Danos O. 2000; Canine adenovirus vectors: An alternative for adenovirus-mediated gene transfer. J Virol 74:505–512[PubMed] [CrossRef]
     [Google Scholar]
  45. Ledgerwood J. E., DeZure A. D., Stanley D. A., Novik L., Enama M. E., Berkowitz N. M., Hu Z., Joshi G., Ploquin A. et al. 2014; Chimpanzee adenovirus vector ebola vaccine - preliminary report. N Engl J Med [View Article][PubMed]
     [Google Scholar]
  46. Leroy E. M., Kumulungui B., Pourrut X., Rouquet P., Hassanin A., Yaba P., Délicat A., Paweska J. T., Gonzalez J. J. et al. 2005; Fruit bats as reservoirs of Ebola virus. Nat New Biol 438:575–576 [CrossRef]
     [Google Scholar]
  47. Lewis P. F., Schmidt M. A., Lu X., Erdman D. D., Campbell M., Thomas A., Cieslak P. R., Grenz L. D., Tsaknardis L. et al. 2009; A community-based outbreak of severe respiratory illness caused by human adenovirus serotype 14. J Infect Dis 199:1427–1434 [View Article][PubMed]
     [Google Scholar]
  48. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J. H., Wang H., Crameri G., Hu Z. et al. 2005; Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–679 [View Article][PubMed]
     [Google Scholar]
  49. Li Y., Ge X., Zhang H., Zhou P., Zhu Y., Zhang Y., Yuan J., Wang L. F., Shi Z. 2010; Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol 84:3889–3897 [View Article][PubMed]
     [Google Scholar]
  50. Lima F. E., Cibulski S. P., Elesbao F., Carnieli Junior P., Batista H. B., Roehe P. M., Franco A. C. 2013; First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes 47:378–381 [View Article][PubMed]
     [Google Scholar]
  51. Liu L., Qian Y., Zhang Y., Deng J., Jia L., Dong H. 2014; Adenoviruses associated with acute diarrhea in children in Beijing, China. PLoS One 9:e88791 [View Article][PubMed]
     [Google Scholar]
  52. Maeda K., Hondo E., Terakawa J., Kiso Y., Nakaichi N., Endoh D., Sakai K., Morikawa S., Mizutani T. 2008; Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg Infect Dis 14:347–349 [View Article][PubMed]
     [Google Scholar]
  53. McSharry B. P., Burgert H. G., Owen D. P., Stanton R. J., Prod'homme V., Sester M., Koebernick K., Groh V., Spies T. et al. 2008; Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol 82:4585–4594 [View Article][PubMed]
     [Google Scholar]
  54. Nicklin S. A., Wu E., Nemerow G. R., Baker A. H. 2005; The influence of adenovirus fiber structure and function on vector development for gene therapy. Mol Ther 12:384–393 [View Article][PubMed]
     [Google Scholar]
  55. Parcell B. J., McIntyre P. G., Yirrell D. L., Fraser A., Quinn M., Templeton K., Christie S., Romanes F. 2015; Prison and community outbreak of severe respiratory infection due to adenovirus type 14p1 in Tayside, UK. J Public Health (Oxf) 37:64–69 [View Article][PubMed]
     [Google Scholar]
  56. Pauly M., Hoppe E., Mugisha L., Petrzelkova K., Akoua-Koffi C., Couacy-Hymann E., Anoh A. E., Mossoun A., Schubert G. et al. 2014; High prevalence and diversity of species D adenoviruses (HAdV-D) in human populations of four Sub-Saharan countries. Virol J 11:25 [View Article][PubMed]
     [Google Scholar]
  57. Raut C. G., Yadav P. D., Towner J. S., Amman B. R., Erickson B. R., Cannon D. L., Sivaram A., Basu A., Nichol S. T. et al. 2012; Isolation of a novel adenovirus from Rousettus leschenaultii bats from India. Intervirology 55:488–490 [View Article][PubMed]
     [Google Scholar]
  58. Reed L. J., Muench H. 1938; A simple method of estimating fifty percent endpoints. Am J Epidemiol 27:493–497
     [Google Scholar]
  59. Roberts D. M., Nanda A., Havenga M. J. E., Abbink P., Lynch D. M., Ewald B. A., Liu J., Thorner A. R., Swanson P. E. et al. 2006; Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nat New Biol 441:239–243 [CrossRef]
     [Google Scholar]
  60. Rocholl C., Gerber K., Daly J., Pavia A. T., Byington C. L. 2004; Adenoviral infections in children: the impact of rapid diagnosis. Pediatrics 113:e5156 [View Article][PubMed]
     [Google Scholar]
  61. Roy S., Clawson D. S., Adam V. S., Medina A., Wilson J. M. 2011; Construction of gene transfer vectors based on simian adenovirus 7. J Gen Virol 92:1749–1753 [View Article][PubMed]
     [Google Scholar]
  62. Ryan M. A., Gray G. C., Smith B., McKeehan J. A., Hawksworth A. W., Malasig M. D. 2002; Large epidemic of respiratory illness due to adenovirus types 7 and 3 in healthy young adults. Clin Infect Dis 34:577–582 [View Article][PubMed]
     [Google Scholar]
  63. San Martín C., Burnett. R. M. 2003; Structural studies on adenoviruses. Curr Top Microbiol Immunol 272:57–94[PubMed]
     [Google Scholar]
  64. Sharma A., Li X., Bangari D. S., Mittal S. K. 2009; Adenovirus receptors and their implications in gene delivery. Virus Res 143:184–194 [View Article][PubMed]
     [Google Scholar]
  65. Shisler J., Yang C., Walter B., Ware C. F., Gooding L. R. 1997; The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J Virol 71:8299–8306[PubMed]
     [Google Scholar]
  66. Simmons N. B. 2005; Order Chiroptera. In Mammal Species of the World: A taxonomic and geographic reference pp. 312–529 Edited by Wilson D. E., Reeder D. M. Maryland: Johns Hopkins University Press;
     [Google Scholar]
  67. Sonntag M., Mühldorfer K., Speck S., Wibbelt G., Kurth A. 2009; New adenovirus in bats, Germany. Emerg Infect Dis 15:2052–2055 [View Article][PubMed]
     [Google Scholar]
  68. Stewart A. R., Tollefson A. E., Krajcsi P., Yei S. P., Wold W. S. 1995; The adenovirus E3 10.4K and 14.5K proteins, which function to prevent cytolysis by tumor necrosis factor and to down-regulate the epidermal growth factor receptor, are localized in the plasma membrane. J Virol 69:172–181[PubMed]
     [Google Scholar]
  69. Swango L. J., Wooding W. L. Jr, Binn L. N. 1970; A comparison of the pathogenesis and antigenicity of infectious canine hepatitis virus and the A26-61 virus strain (toronto). J Am Vet Med Assoc 156:1687–1696[PubMed]
     [Google Scholar]
  70. Thomas M. A., Lichtenstein D. L., Krajcsi P., Wold W. S. 2007; A real-time PCR method to rapidly titer adenovirus stocks. Methods Mol Med 130:185–192[PubMed]
     [Google Scholar]
  71. Uchino J., Curiel D. T., Ugai H. 2014; Species D human adenovirus type 9 exhibits better virus-spread ability for antitumor efficacy among alternative serotypes. PLoS One 9:e87342 [View Article][PubMed]
     [Google Scholar]
  72. Ursu K., Harrach B., Matiz K., Benko M. 2004; DNA sequencing and analysis of the right-hand part of the genome of the unique bovine adenovirus type 10. J Gen Virol 85:593–601 [View Article][PubMed]
     [Google Scholar]
  73. Vidovszky M., Kohl C., Boldogh S., Görföl T., Wibbelt G., Kurth A., Harrach B. 2015; Random sampling of the Central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses. Acta Vet Hung 63:508–525 [View Article][PubMed]
     [Google Scholar]
  74. Wang L. F., Walker P. J., Poon L. L. 2011; Mass extinctions, biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses?. Curr Opin Virol 1:649–657 [View Article][PubMed]
     [Google Scholar]
  75. Wellehan J. F., Johnson A. J., Harrach B., Benkö M., Pessier A. P., Johnson C. M., Garner M. M., Childress A., Jacobson E. R. 2004; Detection and analysis of six lizard adenoviruses by consensus primer PCR provides further evidence of a reptilian origin for the atadenoviruses. J Virol 78:13366–13369 [View Article][PubMed]
     [Google Scholar]
  76. Windheim M., Southcombe J. H., Kremmer E., Chaplin L., Urlaub D., Falk C. S., Claus M., Mihm J., Braithwaite M. et al. 2013; A unique secreted adenovirus E3 protein binds to the leukocyte common antigen CD45 and modulates leukocyte functions. Proc Natl Acad Sci U S A 110:E4884E4893 [View Article][PubMed]
     [Google Scholar]
  77. Wu L., Zhou P., Ge X., Wang L. F., Baker M. L., Shi Z. 2013; Deep RNA sequencing reveals complex transcriptional landscape of a bat adenovirus. J Virol 87:503–511 [View Article][PubMed]
     [Google Scholar]
  78. Ye W., Liu R., Pan C., Jiang W., Zhang L., Guan Z., Wu J., Ying X., Li L. 2014; Multicenter randomized phase 2 clinical trial of a recombinant human endostatin adenovirus in patients with advanced head and neck carcinoma. Mol Ther 22:1221–1229 [View Article][PubMed]
     [Google Scholar]
  79. Yang X. L., Tan B., Wang B., Li W., Wang N., Luo C. M., Wang M. N., Zhang W., Li B. et al. 2015; Isolation and identification of bat viruses closely related to human, porcine and mink orthoreoviruses. J Gen Virol 96:3525–3531 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000470
Loading
Novel bat adenoviruses with an extremely large E3 gene
J. Gen. Virol. 97, 1625 (2016); https://doi.org/10.1099/jgv.0.000470
/content/journal/jgv/10.1099/jgv.0.000470
/content/journal/jgv/10.1099/jgv.0.000470
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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