1887

Abstract

The high incidence of multiple wart formation and skin cancer in organ-transplant recipients, as well as the question of an involvement of papillomaviruses in a variety of human cancers, require a model system for papillomavirus infections in immunocompetent animals. Such an model is represented by the multimammate rat , which is infected with papillomavirus (MnPV). MnPV primarily induces benign skin tumours, such as papillomas and keratoacanthomas. Here, the incidence of MnPV infections in different skin areas and various organs is described. hybridization showed that hair follicle cells were positive for viral DNA and that the amount of MnPV in normal skin may be considered a predictor for the development of skin tumours. MnPV infection is not restricted to the skin, but can also be detected in inner organs. As the blood and the lymphatic system were temporarily also found to be virus-positive, a haematogenic propagation of MnPV can be assumed. However, MnPV is apparently not transmitted through the germ line, as fetuses and newborns lack viral DNA, despite infection of their mothers. In conclusion, is not only useful to study papillomavirus-induced skin carcinogenesis, but may also serve as a model to identify additional, still unknown target cells of papillomavirus infections and the potential pathological impact.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82955-0
2007-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/10/2670.html?itemId=/content/journal/jgv/10.1099/vir.0.82955-0&mimeType=html&fmt=ahah

References

  1. Akgül B., Cooke J. C., Storey A. 2006; HPV-associated skin disease. J Pathol 208:165–175 [CrossRef]
    [Google Scholar]
  2. Amtmann E., Wayss K. 1987; The Papovaviridae . In The Mastomys natalensis Papillomavirus . pp 187–198 Edited by Salzman N. P., Howley P. M. New York: Plenum Press;
  3. Amtmann E., Volm M., Wayss K. 1984; Tumour induction in the rodent Mastomys natalensis by activation of endogenous papilloma virus genomes. Nature 308:291–292 [CrossRef]
    [Google Scholar]
  4. Bouwes Bavinck J. N., Feltkamp M., Struijk L., ter Schegget J. 2001; Human papillomavirus infection and skin cancer risk in organ transplant recipients. J Investig Dermatol Symp Proc 6:207–211 [CrossRef]
    [Google Scholar]
  5. Caldeira S., Zehbe I., Accardi R., Malanchi I., Dong W., Giarre M., de Villiers E. M., Filotico R., Boukamp P., Tommasino M. 2003; The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J Virol 77:2195–2206 [CrossRef]
    [Google Scholar]
  6. Cason J., Mant C. A. 2005; High-risk mucosal human papillomavirus infections during infancy & childhood. J Clin Virol 32 (Suppl. 1):S52–S58 [CrossRef]
    [Google Scholar]
  7. de Villiers E. M., Fauquet C., Broker T. R., Bernard H. U., zur Hausen H. 2004; Classification of papillomaviruses. Virology 324:17–27 [CrossRef]
    [Google Scholar]
  8. Doan T., Herd K., Street M., Bryson G., Fernando G., Lambert P., Tindle R. 1999; Human papillomavirus type 16 E7 oncoprotein expressed in peripheral epithelium tolerizes E7-directed cytotoxic T-lymphocyte precursors restricted through human (and mouse) major histocompatibility complex class I alleles. J Virol 73:6166–6170
    [Google Scholar]
  9. Dong W., Kloz U., Accardi R., Caldeira S., Tong W. M., Wang Z. Q., Jansen L., Dürst M., Sylla B. S. other authors 2005; Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38. J Virol 79:14899–14908 [CrossRef]
    [Google Scholar]
  10. Doorbar J. 2005; The papillomavirus life cycle. J Clin Virol 32 (Suppl. 1):S7–S15
    [Google Scholar]
  11. Forslund O., Lindelof B., Hradil E., Nordin P., Stenquist B., Kirnbauer R., Slupetzky K., Dillner J. 2004; High prevalence of cutaneous human papillomavirus DNA on the top of skin tumors but not in “stripped” biopsies from the same tumors. J Invest Dermatol 123:388–394 [CrossRef]
    [Google Scholar]
  12. Haag A., Wayss K., Rommelaere J., Cornelis J. J. 2000; Experimentally induced infection with autonomous parvoviruses, minute virus of mice and H-1, in the African multimammate mouse ( Mastomys coucha ). Comp Med 50:613–621
    [Google Scholar]
  13. Harwood C. A., Proby C. M. 2002; Human papillomaviruses and non-melanoma skin cancer. Curr Opin Infect Dis 15:101–114 [CrossRef]
    [Google Scholar]
  14. Helfrich I., Chen M., Schmidt R., Fürstenberger G., Kopp-Schneider A., Trick D., Gröne H. J., zur Hausen H., Rösl F. 2004; Increased incidence of squamous cell carcinomas in Mastomys natalensis papillomavirus E6 transgenic mice during two-stage skin carcinogenesis. J Virol 78:4797–4805 [CrossRef]
    [Google Scholar]
  15. Hoffmann R., Hirt B., Bechtold V., Beard P., Raj K. 2006; Different modes of human papillomavirus DNA replication during maintenance. J Virol 80:4431–4439 [CrossRef]
    [Google Scholar]
  16. Ito M., Liu Y., Yang Z., Nguyen J., Liang F., Morris R. J., Cotsarelis G. 2005; Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11:1351–1354 [CrossRef]
    [Google Scholar]
  17. Karagas M. R., Nelson H. H., Sehr P., Waterboer T., Stukel T. A., Andrew A., Green A. C., Bavinck J. N., Perry A. other authors 2006; Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin. J Natl Cancer Inst 98:389–395 [CrossRef]
    [Google Scholar]
  18. Kendall T. L., Byerley D. J., Dean R. 1991; Isolation of DNA from blood. Anal Biochem 195:74–76 [CrossRef]
    [Google Scholar]
  19. Kim K., Angeletti P. C., Hassebroek E. C., Lambert P. F. 2005; Identification of cis-acting elements that mediate the replication and maintenance of human papillomavirus type 16 genomes in Saccharomyces cerevisiae . J Virol 79:5933–5942 [CrossRef]
    [Google Scholar]
  20. Majewski S., Jablonska S. 2002; Do epidermodysplasia verruciformis human papillomaviruses contribute to malignant and benign epidermal proliferations?. Arch Dermatol 138:649–654
    [Google Scholar]
  21. McNicol A. M., Farquharson M. A. 1997; In situ hybridization and its diagnostic applications in pathology. J Pathol 182:250–261 [CrossRef]
    [Google Scholar]
  22. Medeiros L. R., Ethur A. B., Hilgert J. B., Zanini R. R., Berwanger O., Bozzetti M. C., Mylius L. C. 2005; Vertical transmission of the human papillomavirus: a systematic quantitative review. Cad Saude Publica 21:1006–1015
    [Google Scholar]
  23. Middleton K., Peh W., Southern S., Griffin H., Sotlar K., Nakahara T., El Sherif A., Morris L., Seth R. other authors 2003; Organization of human papillomavirus productive cycle during neoplastic progression provides a basis for selection of diagnostic markers. J Virol 77:10186–10201 [CrossRef]
    [Google Scholar]
  24. Millar S. E. 2002; Molecular mechanisms regulating hair follicle development. J Invest Dermatol 118:216–225 [CrossRef]
    [Google Scholar]
  25. Müller H., Gissmann L. 1978; Mastomys natalensis papilloma virus (MnPV), the causative agent of epithelial proliferations: characterization of the virus particle. J Gen Virol 41:315–323 [CrossRef]
    [Google Scholar]
  26. Nafz J. 2007; Mastomys coucha: a natural animal model for papillomavirus-induced skin carcinogenesis . PhD thesis University of Heidelberg; Germany:
  27. Peh W. L., Middleton K., Christensen N., Nicholls P., Egawa K., Sotlar K., Brandsma J., Percival A., Lewis J. other authors 2002; Life cycle heterogeneity in animal models of human papillomavirus-associated disease. J Virol 76:10401–10416 [CrossRef]
    [Google Scholar]
  28. Pfister H. 2003; Chapter 8: human papillomavirus and skin cancer. J Natl Cancer Inst Monogr 31:52–56
    [Google Scholar]
  29. Reubi J. C., Waser B., Horisberger U., Halter F., Soroka C. J., Kumar R. R., Goldenring J. R., Modlin I. M. 1992; Identification of somatostatin and gastrin receptors on enterochromaffin-like cells from Mastomys gastric tumors. Endocrinology 131:166–172
    [Google Scholar]
  30. Rickert C. H., Paulus W. 2001; Tumors of the choroid plexus. Microsc Res Tech 52:104–111 [CrossRef]
    [Google Scholar]
  31. Rudolph R. L., Muller H., Reinacher M., Thiel W. 1981; Morphology of experimentally induced so-called keratoacanthomas and squamous cell carcinomas in 2 inbred-lines of Mastomys natalensis . J Comp Pathol 91:123–134 [CrossRef]
    [Google Scholar]
  32. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  33. Schäfer K. 2006; Die humorale Immunantwort auf Papillomvirusinfektionen im Tiermodell Mastomys coucha und Herstellung virus-ähnlicher Partikeln . Diploma thesis University of Heidelberg; Germany: (in German
  34. Schaper I. D., Marcuzzi G. P., Weissenborn S. J., Kasper H. U., Dries V., Smyth N., Fuchs P., Pfister H. 2005; Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res 65:1394–1400 [CrossRef]
    [Google Scholar]
  35. Schmitt A., Rochat A., Zeltner R., Borenstein L., Barrandon Y., Wettstein F. O., Iftner T. 1996; The primary target cells of the high-risk cottontail rabbit papillomavirus colocalize with hair follicle stem cells. J Virol 70:1912–1922
    [Google Scholar]
  36. Siegsmund M., Wayss K., Amtmann E. 1991; Activation of latent papillomavirus genomes by chronic mechanical irritation. J Gen Virol 72:2787–2789 [CrossRef]
    [Google Scholar]
  37. Smith E. M., Ritchie J. M., Yankowitz J., Swarnavel S., Wang D., Haugen T. H., Turek L. P. 2004; Human papillomavirus prevalence and types in newborns and parents: concordance and modes of transmission. Sex Transm Dis 31:57–62 [CrossRef]
    [Google Scholar]
  38. Stockfleth E., Ulrich C., Meyer T., Arndt R., Christophers E. 2001; Skin diseases following organ transplantation--risk factors and new therapeutic approaches. Transplant Proc 33:1848–1853 [CrossRef]
    [Google Scholar]
  39. Storey A. 2002; Papillomaviruses: death-defying acts in skin cancer. Trends Mol Med 8:417–421 [CrossRef]
    [Google Scholar]
  40. Tan C. H., Tachezy R., van Ranst M., Chan S. Y., Bernard H. U., Burk R. D. 1994; The Mastomys natalensis papillomavirus: nucleotide sequence, genome organization, and phylogenetic relationship of a rodent papillomavirus involved in tumorigenesis of cutaneous epithelia. Virology 198:534–541 [CrossRef]
    [Google Scholar]
  41. Thomas M., Banks L. 1999; Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types. J Gen Virol 80:1513–1517
    [Google Scholar]
  42. Wayss K., Reyes-Mayes D., Volm M. 1981; Chemical carcinogenesis by the two-stage protocol in the skin Mastomys natalensis (Muridae) using topical initiation with 7,12-dimethylbenz(a)anthracene and topical promotion with 12–0-tetradecanoylphorbol-13-acetate. Virchows Arch B Cell Pathol Incl Mol Pathol 38:13–21 [CrossRef]
    [Google Scholar]
  43. zur Hausen H. 2000; Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 92:690–698 [CrossRef]
    [Google Scholar]
  44. zur Hausen H. 2002; Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82955-0
Loading
/content/journal/jgv/10.1099/vir.0.82955-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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