Cystatin E/M suppresses legumain activity and invasion of human melanoma
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  • 作者:Jon J Briggs (1)
    Mads H Haugen (1)
    Harald T Johansen (2)
    Adam I Riker (3)
    Magnus Abrahamson (4)
    ?ystein Fodstad (1) (5)
    Gunhild M M?landsmo (1)
    Rigmor Solberg (2)
  • 刊名:BMC Cancer
  • 出版年:2010
  • 出版时间:December 2010
  • 年:2010
  • 卷:10
  • 期:1
  • 全文大小:2286KB
  • 参考文献:1. Abrahamson M, Alvarez-Fernandez M, Nathanson CM: Cystatins. / Biochem Soc Symp 2003, 70:179-99.
    2. Henskens YMC, Veerman ECI, Amerongen AVN: Cystatins in health and disease. / Biol Chem Hoppe-Seyler 1996,377(2):71-6. CrossRef
    3. Zeeuwen P: Epidermal differentiation: The role of proteases and their inhibitors. / Eur J Cell Biol 2004,83(11):761-73. CrossRef
    4. Keppler D: Towards novel anti-cancer strategies based on cystatin function. / Cancer Lett 2006,235(2):159-76. CrossRef
    5. Sotiropoulou G, Anisowicz A, Sager R: Identification, cloning, and characterization of cystatin M, a novel cysteine proteinase inhibitor, down-regulated in breast cancer. / J Biol Chem 1997,272(2):903-10. CrossRef
    6. Ni J, Abrahamson M, Zhang M, Fernandez MA, Grubb A, Su J, Yu GL, Li YL, Parmelee D, Xing L, / et al.: Cystatin E is a novel human cysteine proteinase inhibitor with structural resemblance to family 2 cystatins. / J Biol Chem 1997,272(16):10853-0858. CrossRef
    7. Ai LB, Kim WJ, Kim TY, Fields CR, Massoll NA, Robertson KD, Brown KD: Epigenetic silencing of the tumor suppressor cystatin M occurs during breast cancer progression. / Cancer Res 2006,66(16):7899-909. CrossRef
    8. Rivenbark AG, Jones WD, Coleman WB: DNA methylation-dependent silencing of CST6 in human breast cancer cell lines. / Lab Invest 2006,86(12):1233-242. CrossRef
    9. Schagdarsurengin U, Pfeifer GP, Dammann R: Frequent epigenetic inactivation of cystatin M in breast carcinoma. / Oncogene 2007,26(21):3089-094. CrossRef
    10. Kim TY, Zhong S, Fields CR, Kim JH, Robertson KD: Epigenomic profiling reveals novel and frequent targets of aberrant DNA methylation-mediated silencing in malignant glioma. / Cancer Res 2006,66(15):7490-501. CrossRef
    11. Zhong S, Fields CR, Su N, Pan YX, Robertson KD: Pharmacologic inhibition of epigenetic modi. cations, coupled with gene expression profiling, reveals novel targets of aberrant DNA methylation and histone deacetylation in lung cancer. / Oncogene 2007,26(18):2621-634. CrossRef
    12. Shridhar R, Zhang J, Song J, Booth BA, Kevil CG, Sotiropoulou G, Fsloane B, Keppler D: Cystatin M suppresses the malignant phenotype of human MDA-MB-435S cells. / Oncogene 2004,23(12):2206-215. CrossRef
    13. Zhang J, Shridhar R, Dai Q, Song J, Barlow SC, Yin LJ, Sloane BF, Miller FR, Meschonat C, Li BDL, / et al.: Cystatin M: A novel candidate tumor suppressor gene for breast cancer. / Cancer Res 2004,64(19):6957-964. CrossRef
    14. Qiu J, Ai L, Ramachandran C, Yao B, Gopalakrishnan S, Fields CR, Delmas AL, Dyer LM, Melnick SJ, Yachnis AT, / et al.: Invasion suppressor cystatin E/M (CST6): high-level cell type-specific expression in normal brain and epigenetic silencing in gliomas. / Lab Invest 2008,88(9):910-25. CrossRef
    15. Cheng T, Hitomi K, Ishida-Yamamoto A, van Vlijmen-Willems IM, de Jongh GJ, Bergers M, Schalkwijk J, Zeeuwen PL: Novel targets for cystatin M/E: A new route in epidermal differentiation. / J Invest Dermatol 2006, 126:3-. CrossRef
    16. Cheng T, Hitomi K, van Vlijmen-Willems I, de Jongh GJ, Yamamoto K, Nishi K, Watts C, Reinheckel T, Schalkwijk J, Zeeuwen P: Cystatin M/E is a high affinity inhibitor of cathepsin V and cathepsin L by a reactive site that is distinct from the legumain-binding site - A novel clue for the role of cystatin M/E in epidermal cornification. / J Biol Chem 2006,281(23):15893-5899. CrossRef
    17. Alvarez-Fernandez M, Barrett AJ, Gerhartz B, Dando PM, Ni JA, Abrahamson M: Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. / J Biol Chem 1999,274(27):19195-9203. CrossRef
    18. Klose A, Zigrino P, Dennhofer R, Mauch C, Hunzelmann N: Identification and discrimination of extracellularly active cathepsins B and L in high-invasive melanoma cells. / Anal Biochem 2006,353(1):57-2. CrossRef
    19. Gondi CS, Lakka SS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Tung CH, Weissleder R, Rao JS: Adenovirus-mediated expression of antisense urokinase plasminogen activator receptor and antisense cathepsin B inhibits tumor growth, invasion, and angiogenesis in gliomas. / Cancer Res 2004,64(12):4069-077. CrossRef
    20. Lakka SS, Gondi CS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Rao JS: Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. / Oncogene 2004,23(27):4681-689. CrossRef
    21. Yan SQ, Sameni M, Sloane BF: Cathepsin B and human tumor progression. / Biol Chem 1998,379(2):113-23.
    22. Campo E, Munoz J, Miquel R, Palacin A, Cardesa A, Sloane BF, Emmertbuck R: Cathepsin-B expression in colorectal carcinomas correlates with tumor progression and shortened patient survival. / Am J Pathol 1994,145(2):301-09.
    23. Emmert-Buck MR, Roth MJ, Zhuang ZP, Campo E, Rozhin JR, Sloane BF, Liotta LA, Stetlerstevenson WG: Increased gelatinase A (MMP-2) and cathepsin-B activity in invasive tumor regions of human colon-cancer samples. / Am J Pathol 1994,145(6):1285-290.
    24. Sloane BF, Moin K, Krepela E, Rozhin J: Cathepsin-B and its endogenous inhibitors - The role in tumor malignancy. / Cancer Metastasis Rev 1990,9(4):333-52. CrossRef
    25. Frohlich E, Schlagenhauff B, Mohrle M, Weber E, Klessen C, Rassner G: Activity, expression, and transcription rate of the cathepsins B, D, H, and L in cutaneous malignant melanoma. / Cancer 2001,91(5):972-82. CrossRef
    26. Frade R, Rodrigues-Lima F, Huang SY, Xie KP, Guillaume N, Bar-Eli M: Procathepsin-L, a proteinase that cleaves human C3 (the third component of complement), confers high tumorigenic and metastatic properties to human melanoma cells. / Cancer Res 1998,58(13):2733-736.
    27. Szpaderska AM, Frankfater A: An intracellular form of cathepsin B contributes to invasiveness in cancer. / Cancer Res 2001,61(8):3493-500.
    28. Liu C, Sun CZ, Huang HN, Janda K, Edgington T: Overexpression of legumain in tumors is significant for invasion/metastasis and a candidate enzymatic target for prodrug therapy. / Cancer Res 2003,63(11):2957-964.
    29. Murthy RV, Arbman G, Gao JF, Roodman GD, Sun XF: Legumain expression in relation to clinicopathologic and biological variables in colorectal cancer. / Clin Cancer Res 2005,11(6):2293-299. CrossRef
    30. Chen JM, Fortunato M, Stevens RAE, Barrett AJ: Activation of progelatinase A by mammalian legumain, a recently discovered cysteine proteinase. / Biol Chem 2001,382(5):777-83. CrossRef
    31. Riker AI, Enkemann SA, Fodstad O, Liu S, Ren S, Morris C, Xi Y, Howell P, Metge B, Samant RS, / et al.: The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. / BMC Med Genomics 2008, 1:13. CrossRef
    32. Rivoltini L, Barracchini KC, Viggiano V, Kawakami Y, Smith A, Mixon A, Restifo NP, Topalian SL, Simonis TB, Rosenberg SA, / et al.: Quantitative correlation between HLA class-I allele expression and recognition of melanoma-cells by antigen-specific cytotoxic T-lymphocytes. / Cancer Res 1995,55(14):3149-157.
    33. Cormier JN, Panelli MC, Hackett JA, Bettinotti MP, Mixon A, Wunderlich J, Parker LL, Restifo NP, Ferrone S, Marincola FM: Natural variation of the expression of HLA and endogenous antigen modulates ctl recognition in an in vitro melanoma model. / Int J Cancer 1999,80(5):781-90. CrossRef
    34. de Waard-Siebinga I, Blom DJR, Griffioen M, Schrier PI, Hoogendoorn E, Beverstock G, Danen EHJ, Jager MJ: Establishment and characterization of an uveal-melanoma cell-line. / Int J Cancer 1995,62(2):155-61. CrossRef
    35. Rye PD, Norum L, Olsen DR, GarmanVik S, Kaul S, Fodstad O: Brain metastasis model in athymic nude mice using a novel MUC1-secreting human breast-cancer cell line, MA11. / Int J Cancer 1996,68(5):682-87. CrossRef
    36. Wiiger MT, Prydz H: The epidermal growth factor receptor (EGFR) and proline rich tyrosine kinase 2 (PYK2) are involved in tissue factor dependent factor VIIa signalling in HaCaT cells. / Thrombosis and Haemostasis 2004,92(1):13-2.
    37. Bradford MM: Rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding. / Anal Biochem 1976,72(1-):248-54. CrossRef
    38. Olafsson I, Lofberg H, Abrahamson M, Grubb A: Production, characterization and use of monoklonal-antibodies against the major extracellular human cysteine proteinase-inhibitors cystatin-C and kininogen. / Scand J Clin Lab Invest 1988,48(6):573-82. CrossRef
    39. Werle B, Sauckel K, Nathanson CM, Bjarnadottir M, Spiess E, Ebert W, Abrahamson M: Cystatins C, E/M and F in human pleural fluids of patients with neoplastic and inflammatory lung disorders. / Biol Chem 2003,384(2):281-87. CrossRef
    40. Ni J, Fernandez MA, Danielsson L, Chillakuru RA, Zhang JL, Grubb A, Su J, Gentz R, Abrahamson M: Cystatin F is a glycosylated human low molecular weight cysteine proteinase inhibitor. / J Biol Chem 1998,273(38):24797-4804. CrossRef
    41. Hakansson K, Huh C, Grubb A, Karlsson S, Abrahamson M: Mouse and rat cystatin C: Escherichia coli production, characterization and tissue distribution. / Comp Biochem Physiol B-Biochem Mol Biol 1996,114(3):303-11. CrossRef
    42. Freije JP, Balbin M, Abrahamson M, Velasco G, Dalboge H, Grubb A, Lopezotin C: Human cystatin-D - cDNA cloning, characterization of the Escherichia-coli expressed inhibitor, and identification of the native protein in saliva. / J Biol Chem 1993,268(21):15737-5744.
    43. Guesdon JL, Ternynck T, Avrameas S: Use of avidin-biotin interaction in immunoenzymatic techniques. / J Histochem Cytochem 1979,27(8):1131-139.
    44. Chen JM, Dando PM, Rawlings ND, Brown MA, Young NE, Stevens RA, Hewitt E, Watts C, Barrett AJ: Cloning, isolation, and characterization of mammalian legumain, an asparaginyl endopeptidase. / J Biol Chem 1997,272(12):8090-098. CrossRef
    45. Johansen HT, Knight CG, Barrett AJ: Colorimetric and fluorimetric microplate assays for legumain and a staining reaction for detection of the enzyme after electrophoresis. / Anal Biochem 1999,273(2):278-83. CrossRef
    46. Werle B, Ebert W, Klein W, Spiess E: Assessment of cathepsin-L activity by use of the inhibitor CA-074 compared to cathepsin-B activity in human lung tumor-tissue. / Biol Chem Hoppe-Seyler 1995,376(3):157-64. CrossRef
    47. Barrett AJ, Kirschke H: Cathepsin-B, Cathepsin-H, and Cathepsin-L. / Methods Enzymol 1981, 80:535-61. CrossRef
    48. Yamane T, Takeuchi K, Yamamoto Y, Li YH, Fujiwara M, Nishi K, Takahashi S, Ohkubo I: Legumain from bovine kidney: its purification, molecular cloning, immunohistochemical localization and degradation of annexin II and vitamin D-binding protein. / Biochim Biophys Acta 2002,1596(1):108-20. CrossRef
    49. Zeeuwen P, van Vlijmen-Willems I, Jansen BJH, Sotiropoulou G, Curfs JH, Meis J, Janssen JJM, van Ruissen F, Schalkwijk J: Cystatin M/E expression is restricted to differentiated epidermal keratinocytes and sweat glands: a new skin-specific proteinase inhibitor that is a target for cross-linking by transglutaminase. / J Invest Dermatol 2001,116(5):693-01. CrossRef
    50. Zeeuwen P, Van Vlijmen-Willems I, Egami H, Schalkwijk J: Cystatin M/E expression in inflammatory and neoplastic skin disorders. / Br J Dermatol 2002,147(1):87-4. CrossRef
    51. Chen JM, Fortunato M, Barrett AJ: Activation of human prolegumain by cleavage at a C-terminal asparagine residue. / Biochem J 2000, 352:327-34. CrossRef
    52. Maehr R, Hang HC, Mintern JD, Kim YM, Cuvillier A, Nishimura M, Yamada K, Shirahama-Noda K, Hara-Nishimura I, Ploegh HL: Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in mice. / Journal of Immunology 2005,174(11):7066-074.
    53. Vigneswaran N, Wu J, Zacharias W: Upregulation of cystatin M during the progression of oropharyngeal squamous cell carcinoma from primary tumor to metastasis. / Oral Oncol 2003,39(6):559-68. CrossRef
    54. Vigneswaran N, Wu J, Nagaraj N, James R, Zeeuwen P, Zacharias W: Silencing of cystatin M in metastatic oral cancer cell line MDA-686Ln by siRNA increases cysteine proteinases and legumain activities, cell proliferation and in vitro invasion. / Life Sci 2006,78(8):898-07. CrossRef
    55. Hosokawa M, Kashiwaya K, Eguchi H, Ohigashi H, Ishikawa O, Furihata M, Shinomura Y, Imai K, Nakamura Y, Nakagawa H: Over-expression of cysteine proteinase inhibitor cystatin 6 promotes pancreatic cancer growth. / Cancer Sci 2008,99(8):1626-632. CrossRef
    56. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2407/10/17/prepub
  • 作者单位:Jon J Briggs (1)
    Mads H Haugen (1)
    Harald T Johansen (2)
    Adam I Riker (3)
    Magnus Abrahamson (4)
    ?ystein Fodstad (1) (5)
    Gunhild M M?landsmo (1)
    Rigmor Solberg (2)

    1. Department of Tumor Biology, Institute for Cancer Research, Radiumhospitalet, Oslo University Hospital, Oslo, Norway
    2. Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, PO Box 1068, Blindern, N-0316, Oslo, Norway
    3. Ochsner Cancer Institute, Ochsner Medical Center, New Orleans, Louisiana, USA
    4. Department of Laboratory Medicine, Division of Clinical Chemistry & Pharmacology, Lund University, Sweden
    5. Radiumhospitalet Faculty Division, Medical Faculty, University of Oslo, Oslo, Norway
  • ISSN:1471-2407
文摘
Background High activity of cysteine proteases such as legumain and the cathepsins have been shown to facilitate growth and invasion of a variety of tumor types. In breast cancer, several recent studies have indicated that loss of the cysteine protease inhibitor cystatin E/M leads to increased growth and metastasis. Although cystatin E/M is normally expressed in the skin, its role in cysteine protease regulation and progression of malignant melanoma has not been studied. Methods A panel of various non-melanoma and melanoma cell lines was used. Cystatin E/M and C were analyzed in cell media by immunoblotting and ELISA. Legumain, cathepsin B and L were analyzed in cell lysates by immunoblotting and their enzymatic activities were analyzed by peptide substrates. Two melanoma cell lines lacking detectable secretion of cystatin E/M were transfected with a cystatin E/M expression plasmid (pCST6), and migration and invasiveness were studied by a Matrigel invasion assay. Results Cystatin E/M was undetectable in media from all established melanoma cell lines examined, whereas strong immunobands were detected in two of five primary melanoma lines and in two of six lines derived from patients with metastatic disease. Among the four melanoma lines secreting cystatin E/M, the glycosylated form (17 kD) was predominant compared to the non-glycosylated form (14 kD). Legumain, cathepsin B and L were expressed and active in most of the cell lines, although at low levels in the melanomas expressing cystatin E/M. In the melanoma lines where cystatin E/M was secreted, cystatin C was generally absent or expressed at a very low level. When melanoma cells lacking secretion of cystatin E/M were transfected with pCST6, their intracellular legumain activity was significantly inhibited. In contrast, cathepsin B activity was not affected. Furthermore, invasion was suppressed in cystatin E/M over-expressing melanoma cell lines as measured by the transwell Matrigel assay. Conclusions These results suggest that the level of cystatin E/M regulates legumain activity and hence the invasive potential of human melanoma cells.

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