1887

Abstract

Matrix metalloproteinases (MMPs) degrade extracellular matrix. They are involved in cellular proliferation, migration, angiogenesis, invasion and metastasis. MT-1 MMP, a membrane-bound MMP, is expressed in carcinomas of the uterine cervix . This type of cancer is associated with human papillomavirus (HPV) infection. Here it was shown that keratinocytes transformed with HPV16 or HPV18 , and HPV-positive cervical carcinoma cell lines, constitutively expressed MT-1 MMP. Expression of the E7 protein from the mucosal and cutaneous high-risk types HPV16 and HPV8, but not from the cutaneous low-risk type HPV1, was sufficient to induce MT-1 MMP expression in primary human keratinocytes and HaCaT cells. As a consequence, MMP-2 was activated. MT-1 MMP expression might play a role in the HPV life cycle by promoting proliferation of host cells and might contribute to their invasive phenotype during malignant progression.

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2005-05-01
2020-08-10
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References

  1. Aaronson S. A., Rubin J. S., Finch P. W., Wong J., Marchese C., Falco J., Taylor W. G., Kraus M. H. 1990; Growth factor-regulated pathways in epithelial cell proliferation. Am Rev Respir Dis 142:S7–S10 [CrossRef]
    [Google Scholar]
  2. Azzam H. S., Arand G., Lippman M. E., Thompson E. W. 1993; Association of MMP-2 activation potential with metastatic progression in human breast cancer cell lines independent of MMP-2 production. J Natl Cancer Inst 85:1758–1764 [CrossRef]
    [Google Scholar]
  3. Balbin M., Fueyo A., Tester A. M., Pendas A. M., Pitiot A. S., Astudillo A., Overall C. M., Shapiro S. D., Lopez-Otin C. 2003; Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 35:252–257 [CrossRef]
    [Google Scholar]
  4. Boukamp P., Petrussevska R. T., Breitkreutz D., Hornung J., Markham A., Fusenig N. E. 1988; Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761–771 [CrossRef]
    [Google Scholar]
  5. Brummer O., Bohmer G., Hollwitz B., Flemming P., Petry K. U., Kuhnle H. 2002; MMP-1 and MMP-2 in the cervix uteri in different steps of malignant transformation – an immunohistochemical study. Gynecol Oncol 84:222–227 [CrossRef]
    [Google Scholar]
  6. Butler G. S., Butler M. J., Atkinson S. J. 7 other authors 1998; The TIMP2 membrane type 1 metalloproteinase “receptor” regulates the concentration and efficient activation of progelatinase A. A kinetic study. J Biol Chem 273:871–880 [CrossRef]
    [Google Scholar]
  7. Chattopadhyay N., Mitra A., Frei E., Chatterjee A. 2001; Human cervical tumor cell (SiHa) surface α v β 3 integrin receptor has associated matrix metalloproteinase (MMP-2) activity. J Cancer Res Clin Oncol 127:653–658 [CrossRef]
    [Google Scholar]
  8. Coussens L. M., Tinkle C. L., Hanahan D., Werb Z. 2000; MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103:481–490 [CrossRef]
    [Google Scholar]
  9. Davidson B., Goldberg I., Kopolovic J., Lerner-Geva L., Gotlieb W. H., Ben-Baruch G., Reich R. 1999; MMP-2 and TIMP-2 expression correlates with poor prognosis in cervical carcinoma – a clinicopathologic study using immunohistochemistry and mRNA in situ hybridization. Gynecol Oncol 73:372–382 [CrossRef]
    [Google Scholar]
  10. Dobbs S. P., Hewett P. W., Johnson I. R., Carmichael J., Murray J. C. 1997; Angiogenesis is associated with vascular endothelial growth factor expression in cervical intraepithelial neoplasia. Br J Cancer 76:1410–1415 [CrossRef]
    [Google Scholar]
  11. Durst M., Dzarlieva-Petrusevska R. T., Boukamp P., Fusenig N. E., Gissmann L. 1987; Molecular and cytogenetic analysis of immortalized human primary keratinocytes obtained after transfection with human papillomavirus type 16 DNA. Oncogene 1:251–256
    [Google Scholar]
  12. Feltkamp M. C., Broer R., di Summa F. M. 7 other authors 2003; Seroreactivity to epidermodysplasia verruciformis-related human papillomavirus types is associated with nonmelanoma skin cancer. Cancer Res 63:2695–2700
    [Google Scholar]
  13. Fuchs P. G., Pfister H. 1996; Papillomaviruses in epidermodysplasia verruciformis. In Papillomavirus Reviews: Current Research on Papillomaviruses pp  253–262 Edited by Lacey C. Leeds: Leeds University Press;
    [Google Scholar]
  14. Gaiotto M. A., Focchi J., Ribalta J. L., Stavale J. N., Baracat E. C., Lima G. R., Guerreiro da Silva I. D. 2004; Comparative study of MMP-2 (matrix metalloproteinase 2) immune expression in normal uterine cervix, intraepithelial neoplasias, and squamous cells cervical carcinoma. Am J Obstet Gynecol 190:1278–1282 [CrossRef]
    [Google Scholar]
  15. Gilles C., Polette M., Piette J., Munaut C., Thompson E. W., Birembaut P., Foidart J. M. 1996; High level of MT-MMP expression is associated with invasiveness of cervical cancer cells. Int J Cancer 65:209–213 [CrossRef]
    [Google Scholar]
  16. Goldberg G. I., Marmer B. L., Grant G. A., Eisen A. Z., Wilhelm S., He C. S. 1989; Human 72-kilodalton type IV collagenase forms a complex with a tissue inhibitor of metalloproteases designated TIMP-2. Proc Natl Acad Sci U S A 86:8207–8211 [CrossRef]
    [Google Scholar]
  17. Guidi A. J., Abu-Jawdeh G., Berse B., Jackman R. W., Tognazzi K., Dvorak H. F., Brown L. F. 1995; Vascular permeability factor (vascular endothelial growth factor) expression and angiogenesis in cervical neoplasia. J Natl Cancer Inst 87:1237–1245 [CrossRef]
    [Google Scholar]
  18. Hernandez-Barrantes S., Bernardo M., Toth M., Fridman R. 2002; Regulation of membrane type-matrix metalloproteinases. Semin Cancer Biol 12:131–138 [CrossRef]
    [Google Scholar]
  19. Howes K. A., Ransom N., Papermaster D. S., Lasudry J. G., Albert D. M., Windle J. J. 1994; Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53 [published erratum appears in Genes Dev 8, 1738, 1994]. . Genes Dev 8, 1300–1310 [CrossRef]
    [Google Scholar]
  20. Iftner T., Bierfelder S., Csapo Z., Pfister H. 1988; Involvement of human papillomavirus type 8 genes E6 and E7 in transformation and replication. J Virol 62:3655–3661
    [Google Scholar]
  21. Itoh Y., Takamura A., Ito N., Maru Y., Sato H., Suenaga N., Aoki T., Seiki M. 2001; Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J 20:4782–4793 [CrossRef]
    [Google Scholar]
  22. Kabsch K., Alonso A. 2002; The human papillomavirus type 16 E5 protein impairs TRAIL- and FasL-mediated apoptosis in HaCaT cells by different mechanisms. J Virol 76:12162–12172 [CrossRef]
    [Google Scholar]
  23. Kajita M., Itoh Y., Chiba T., Mori H., Okada A., Kinoh H., Seiki M. 2001; Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 153:893–904 [CrossRef]
    [Google Scholar]
  24. Koshikawa N., Giannelli G., Cirulli V., Miyazaki K., Quaranta V. 2000; Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148:615–624 [CrossRef]
    [Google Scholar]
  25. Lara-Pezzi E., Gomez-Gaviro M. V., Galvez B. G., Mira E., Iniguez M. A., Fresno M., Martinez A. C., Arroyo A. G., Lopez-Cabrera M. 2002; The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression. J Clin Invest 110:1831–1838 [CrossRef]
    [Google Scholar]
  26. Lehman T. A., Modali R., Boukamp P. 7 other authors 1993; p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 14:833–839 [CrossRef]
    [Google Scholar]
  27. Liotta L. A., Tryggvason K., Garbisa S., Hart I., Foltz C. M., Shafie S. 1980; Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67–68 [CrossRef]
    [Google Scholar]
  28. Magal S. S., Jackman A., Pei X. F., Schlegel R., Sherman L. 1998; Induction of apoptosis in human keratinocytes containing mutated p53 alleles and its inhibition by both the E6 and E7 oncoproteins. Int J Cancer 75:96–104 [CrossRef]
    [Google Scholar]
  29. Masini C., Fuchs P. G., Gabrielli F. 11 other authors 2003; Evidence for the association of human papillomavirus infection and cutaneous squamous cell carcinoma in immunocompetent individuals. Arch Dermatol 139:890–894
    [Google Scholar]
  30. Matthews K., Leong C. M., Baxter L., Inglis E., Yun K., Backstrom B. T., Doorbar J., Hibma M. 2003; Depletion of Langerhans cells in human papillomavirus type 16-infected skin is associated with E6-mediated down regulation of E-cadherin. J Virol 77:8378–8385 [CrossRef]
    [Google Scholar]
  31. Mitra A., Chakrabarti J., Chattopadhyay N., Chatterjee A. 2003; Membrane-associated MMP-2 in human cervical cancer. J Environ Pathol Toxicol Oncol 22:93–100
    [Google Scholar]
  32. Nuovo G. J., MacConnell P. B., Simsir A., Valea F., French D. L. 1995; Correlation of the in situ detection of polymerase chain reaction-amplified metalloproteinase complementary DNAs and their inhibitors with prognosis in cervical carcinoma. Cancer Res 55:267–275
    [Google Scholar]
  33. Obermair A., Bancher-Todesca D., Bilgi S., Kaider A., Kohlberger P., Mullauer-Ertl S., Leodolter S., Gitsch G. 1997; Correlation of vascular endothelial growth factor expression and microvessel density in cervical intraepithelial neoplasia. J Natl Cancer Inst 89:1212–1217 [CrossRef]
    [Google Scholar]
  34. Okada A., Bellocq J. P., Rouyer N., Chenard M. P., Rio M. C., Chambon P., Basset P. 1995; Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc Natl Acad Sci U S A 92:2730–2734 [CrossRef]
    [Google Scholar]
  35. Pei D., Weiss S. J. 1995; Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375:244–247 [CrossRef]
    [Google Scholar]
  36. Remacle-Bonnet M. M., Garrouste F. L., Pommier G. J. 1997; Surface-bound plasmin induces selective proteolysis of insulin-like-growth-factor (IGF)-binding protein-4 (IGFBP-4) and promotes autocrine IGF-II bio-availability in human colon-carcinoma cells. Int J Cancer 72:835–843 [CrossRef]
    [Google Scholar]
  37. Ries C., Petrides P. E. 1995; Cytokine regulation of matrix metalloproteinase activity and its regulatory dysfunction in disease. Biol Chem Hoppe-Seyler 376:345–355
    [Google Scholar]
  38. Sabeh F., Ota I., Holmbeck K. 10 other authors 2004; Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167:769–781 [CrossRef]
    [Google Scholar]
  39. Sato H., Takino T., Okada Y., Cao J., Shinagawa A., Yamamoto E., Seiki M. 1994; A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370:61–65 [CrossRef]
    [Google Scholar]
  40. Sato H., Takino T., Kinoshita T., Imai K., Okada Y., Stetler Stevenson W. G., Seiki M. 1996; Cell surface binding and activation of gelatinase A induced by expression of membrane-type-1-matrix metalloproteinase (MT1-MMP. FEBS Lett 385:238–240 [CrossRef]
    [Google Scholar]
  41. Seiki M., Mori H., Kajita M., Uekita T., Itoh Y. 2003; Membrane-type 1 matrix metalloproteinase and cell migration. Biochem Soc Symp 70:253–262
    [Google Scholar]
  42. Sheu B.-C., Lien H.-C., Ho H.-N., Lin H.-H., Chow S.-N., Huang S.-C., Hsu S.-M. 2003; Increased expression and activation of gelatinolytic matrix metalloproteinases is associated with the progression and recurrence of human cervical cancer. Cancer Res 63:6537–6542
    [Google Scholar]
  43. Smith-McCune K., Zhu Y. H., Hanahan D., Arbeit J. 1997; Cross-species comparison of angiogenesis during the premalignant stages of squamous carcinogenesis in the human cervix and K14-HPV16 transgenic mice. Cancer Res 57:1294–1300
    [Google Scholar]
  44. Smola-Hess S., Schnitzler R., Hadaschik D., Smola H., Mauch C., Krieg T., Pfister H. 2001; CD40L induces matrix-metalloproteinase-9 but not tissue inhibitor of metalloproteinases-1 in cervical carcinoma cells: imbalance between NF- κ B and STAT3 activation. Exp Cell Res 267:205–215 [CrossRef]
    [Google Scholar]
  45. Sounni N. E., Devy L., Hajitou A. 7 other authors 2002; MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J 16:555–564 [CrossRef]
    [Google Scholar]
  46. Sternlicht M. D., Werb Z. 2001; How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516 [CrossRef]
    [Google Scholar]
  47. Strongin A. Y., Collier I., Bannikov G., Marmer B. L., Grant G. A., Goldberg G. I. 1995; Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270:5331–5338 [CrossRef]
    [Google Scholar]
  48. Tam E. M., Morrison C. J., Wu Y. I., Stack M. S., Overall C. M. 2004; Membrane protease proteomics: isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates. Proc Natl Acad Sci U S A 101:6917–6922 [CrossRef]
    [Google Scholar]
  49. Thathiah A., Carson D. D. 2004; MT1-MMP mediates MUC1 shedding independently of TACE/ADAM17. Biochem J 382:363–373 [CrossRef]
    [Google Scholar]
  50. Walboomers J. M., Jacobs M. V., Manos M. M. 7 other authors 1999; Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12–19 [CrossRef]
    [Google Scholar]
  51. zur Hausen H. 2002; Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350 [CrossRef]
    [Google Scholar]
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