Melanoma heterogeneity: Differential, invasive, metastatic properties and profiles of cathepsin B, D and L activities in subclones of the B16F10-NEX2 cell line

Melanoma Research

Volumn 14, Issue 5, 2004, Pages 333-344

  Freitas, Zenilda F O ^a   Rodrigues, Elaine G ^a   Oliveira, Vitor ^a   Carmona, Adriana K ^a   Travassos, Luiz R ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

B16F10 melanoma; Cathepsins; Clones; Metastasis; Tissue invasion

Indexed keywords

CATHEPSIN B; CATHEPSIN D; CATHEPSIN L; CHAGASIN; CYSTEINE PROTEINASE INHIBITOR; MATRIGEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INVASION; CELL CLONING; CELL GROWTH; CELL ISOLATION; CELL LINE; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; GENETIC HETEROGENEITY; INCUBATION TIME; LUNG; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SURVIVAL; TRYPANOSOMA CRUZI; TUMOR CELL LINE; TUMOR GROWTH;

ANIMALS; ANTIGENS, NEOPLASM; CATHEPSIN B; CATHEPSINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SEPARATION; CELL SURVIVAL; COLLAGEN; CYSTEINE ENDOPEPTIDASES; DRUG COMBINATIONS; FLOW CYTOMETRY; HYDROGEN-ION CONCENTRATION; LAMININ; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; PEPTIDE HYDROLASES; PROTEOGLYCANS; RNA, MESSENGER; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 7244248965     PISSN: 09608931     EISSN: None     Source Type: Journal    
DOI: 10.1097/00008390-200410000-00002     Document Type: Article

References (85)

1. Balch CM, Soong SJ, Gershenwald JE, Thompson JF, Reinigen DS, Cascinelli N, et al. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer Melanoma Staging. J Clin Oncol 2001; 19:3622-3624.
2. Heppner GH, Dexter DL, DeNucci T, Miller FR, Calabresi P. Heterogeneity in drug sensitivity among tumor cell subpopulations of a single mouse mammary tumor. Cancer Res 1978; 38:3758-3763.
3. Ferrone S, Marincola FM. Loss of HLA class I antigens by melanoma cells: molecular mechanisms, functional significance and clinical relevance. Immunol Today 1995; 16:487-494.
4. Buck CA. Adhesion mechanisms controlling cell-cell and cell-matrix interactions during the metastatic process. In: Mendelsohn J, Howley PM, Israel MA, Liotta LA (editors): Molecular Basis of Cancer. Philadelphia, PA: W. B. Saunders Company; 1995. pp. 172-205.
5. Stracke ML, Liotta LA. Molecular mechanisms of tumor cell metastasis. In: Mendelsohn J, Howley PM, Israel MA Liotta LA (editors): Molecular Basis of Cancer. Philadelphia, PA: W. B. Saunders Company; 1995. pp. 233-250.
6. Welch DR, Krizman DB, Nicolson GL. Multiple phenotypic divergence of mammary adenocarcinoma cell clones. I. In vitro and in vivo properties. Clin Exp Metastasis 1984; 2:333-355.
7. Welch DR, Evans DP, Tomasovic SP, Milas L, Nicolson GL. Multiple phenotypic divergence of mammary adenocarcinoma cell clones. II. Sensitivity to radiation, hyperthermia and FUdR. Clin Exp Metastasis 1984; 2:357-371.
8. Jacob K, Bosserhoff AK, Wach F, Knuchel R, Klein EC, Hein R, et al. Characterization of selected strongly and weakly invasive sublines of a primary human melanoma cell line and isolation of subtractive cDNA clones. Int J Cancer 1995; 60:668-675.
9. Poste G, Doll J, Fidler IJ. Interactions among clonal subpopulations affect stability of the metastatic phenotype in polyclonal populations of B16 melanoma cells. Proc Natl Acad Sci USA 1981; 78:6226-6230.
10. Fidler IJ. Biological behaviour of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975; 35:218-224.
11. Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977; 197:893-895.
12. Fidler IJ. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res 1978; 38:2651-2660.
13. Duffy MJ. The role of proteolytic enzymes in cancer invasion and metastasis. Clin Exp Metastasis 1992; 10:145-155.
14. Mignati P, Rifkin DB. Biology and biochemistry of proteinases in tumor invasion. Physiol Rev 1993; 73:161-195.
15. Kolkhorst V, Sturzebecher J, Wiederanders B. Inhibition of tumor cell invasion by protease inhibitors: correlation with the protease profile. J Clin Cancer Res Clin Oncol 1998; 124:598-606.
16. Schmitt M, Janicke F, Graeff F. Tumor-associated proteases. Fibrinolysis 1992; 6(Suppl. 4):3-26.
17. Kageshita T, Yoshii A, Kimura T, Maruo K, Ono T, Himeno M, et al. Biochemical and immunohistochemical analysis of cathepsin B, H, L and D in human melanotic tumors. Arch Dermatol Res 1995; 287:266-272.
18. Budihna M, Strojan P, Smid L, Skrk J, Vrhovec I, Zupevc A, et al. Prognostic value of cathepsin B, H, L, D and their endogenous inhibitors stefins A and B in head and neck carcinoma. Biol Chem 1996; 377:385-390.
19. Kos J, Stabuc B, Schweiger A, Krasovec M, Cimerman N, Kopitar-Jerala N, et al. Cathepsins B, H and L and their inhibitors stefin A and cystatin C in sera of melanoma patients. Clin Cancer Res 1997; 3:181-182.
20. Tao K, Li J, Warner J, MacLeod K, Miller FR, Sahagian GG. Multiple lysosomal trafficking phenotypes in metastatic mouse mammary tumor cell lines. Int J Oncol 2001; 19:1333-1339.
21. Sever N, Filipic M, Brzin J, Lah TT. Effect of cysteine proteinase inhibitors on murine melanoma cell invasion in vitro. Biol Chem 2002; 383:839-842.
22. Qian F, Bajkowski AS, Steiner DF, Chan S-J, Frankfater A. Expression of five cathepsins in murine melanomas of varying metastatic potential and normal tissues. Cancer Res 1989; 49:4870-4875.
23. Krepela E, Kasafirek E, Novak K, Viklicky J. Increased cathepsin B activity in human lung tumors. Neoplasma 1990; 37:61-70.
24. Qian F, Chan SJ, Gong QM, Bajkowski AS, Steiner DF, Frankfater A. The expression of cathepsin B and other lysosomal proteinases in normal tissues and tumors. Biomed Biochim Acta 1991; 50:531-540.
25. Sukoh N, Abe S, Ogura S, Isobe H, Takekawa H, Inoue K, et al. Immunohistochemical study of cathepsin B. Prognostic significance in human lung cancer. Cancer (Phila.) 1994; 74:46-51.
26. Budihna M, Skrk J, Zakotnik B, Gabrijelcic D, Lindtner J. Prognostic value of total cathepsin B in invasive ductal carcinoma of the breast. Eur J Cancer 1995; 31:661-664.
27. Thomssen C, Schmitt M, Goretzki L, Oppelt P, Pache L, Dettmar P, et al. Prognostic value of cysteine proteases cathepsin B and cathepsin L in human breast cancer. Clin Cancer Res 1995; 1:741-746.
28. Hughes SJ, Glover TW, Zhu XX, Kuick R, Thoraval D, Orringer MB, et al. A novel amplicon 8p22-23 results in overexpression of cathepsin B in esophageal adenocarcinoma. Proc Natl Acad Sci USA 1998; 95:12410-12415.
29. Khan A, Krishna M, Baker SP, Malhothra R, Banner BF. Cathepsin B expression and its correlation with tumor-associated laminin and tumor progression in gastric cancer. Arch Pathol Lab Med 1998; 122:172-177.
30. Yan S, Sameni M, Sloane BF. Cathepsin B and human tumor progression. Biol Chem 1998; 379:113-123.
31. Werle B, Lotterle H, Schanzenbacher U, Lah TT, Kalman E, Kayser K, et al. Immunochemical analysis of cathepsin B in lung tumors; an independent prognostic factor for squamous cell carcinoma patients. Br J Cancer 1999; 81:510-519.
32. Lah TT, Cercek M, Blejec A, Kos J, Gorodetsky E, Somers R, et al. Cathepsin B, a prognostic indicator in lymph node-negative breast carcinoma patients: comparison with cathepsin D, cathepsin L, and other clinical indicators. Clin Cancer Res 2000; 6:578-584.
33. Podgorski I, Sloane BF. Cathepsin B and its role(s) in cancer progression. Biochem Soc Symp 2003; 70:263-276.
34. Poole AR, Tiltman KJ, Recklies AD, Stoker TA. Differences in secretion of the proteinase cathepsin B at the edges of human breast carcinomas and fibroadenomas. Nature 1978; 273:545-547.
35. Recklies AD, Mort JS, Poole AR. Secretion of a thiol proteinase from mouse mammary carcinomas and its characterization. Cancer Res 1982; 42:1026-1032.
36. Achkar C, Gong Q, Frankfater A, Bajkowski AS. Differences in the targeting and secretion of cathepsin B and L by Balb/3T3 fibroblasts and Moloney murine sarcoma virus transformed Balb/3T3 fibroblasts. J Biol Chem 1990; 265:13650-13654.
37. Linebaugh BE, Sameni M, Day NA, Sloane BF, Keppler D. Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur J Biochem 1999; 264:100-109.
38. Sloane BF, Moin K, Sameni M, Tait LR, Rozhin J, Ziegler G. Membrane association of cathepsin B can be induced by transfection of human breast epithelial cells with c-Ha-ras oncogene. J Cell Sci 1994; 107:373-384.
39. Erdel M, Treftz G, Spiess E, Habermaas S, Spring H, Lah T, et al. Localization of cathepsin B in two human cancer cell lines. J Histochem Cytochem 1990; 38:1313-1315.
40. Spiess E, Bruning A, Gack S, Ulbricht B, Spring H, Treftz G, et al. Cathepsin B activity in human lung tumor cell lines: ultrastructural localization, pH sensitivity and inhibitor status at the cellular level. J Histochem Cytochem 1994; 42:917-921.
41. Sameni M, Elliott E, Ziegler G, Fortgens PH, Dennison C, Sloane BF. Cathepsins B and D are localized at the surface of human breast cancer cells. Pathol Oncol Res 1995; 1:43-53.
42. Arkona C, Wiederanders B. Expression, subcellular distribution and plasma membrane binding of cathepsin B and gelatinases in bone metastatic tissue. Biol Chem 1996; 377:695-702.
43. Frosch BA, Berquin I, Emmert-Bluck MR, Moin K, Sloane BF. Molecular regulation, membrane association and secretion of tumor cathepsin B. APMIS 1999; 107:28-37.
44. Mai J, Finley Jr RL, Waisman DM, Sloane BF. Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J Biol Chem 2000; 275:12806-12812.
45. Almeida PC, Nantes IL, Chagas JR, Rizzi CC, Faljoni-Alario A, Carmona E, et al. Cathepsin B activity regulation. Heparin-like glycosaminoglycans protect human cathepsin B from alkaline pH-induced inactivation. J Biol Chem 2001; 276:944-951.
46. Guinec N, Pagano M, Dalet-Fumeron V, Engler R. In vitro digestion of intact bovine lens capsules by four human lysosomal cysteine-proteinases. Biol Chem Hoppe-Seyler 1990; 371(Suppl.):239-254.
47. Maciewicz RA, Wotton SF, Etherington DJ, Duance VC. Susceptibility of the cartilage collagens types II, IX and XI to degradation by the cysteine proteinases, cathepsins B and L. FEBS Lett 1990; 269:189-193.
48. Buck MR, Karustis DG, Day NA, Honn KV, Sloane BF. Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumor tissues. Biochem J 1992; 282:273-277.
49. Guinec N, Dalet-Fumeron V, Pagano M. In vitro study of basement membrane degradation by the cysteine proteinases, cathepsin B, B-like and L. Digestion of collagen IV, lamir in, fibronectin, and release of gelatinase activities from basement membrene fibronectin. Biol Chem Hoppe-Seyler 1993; 374:1135-1146.
50. Creamers LB, Hoeben KA, Jansen DC, Buttle DJ, Beertsen W, Everts V. Participation of intracellular cysteine proteinases, in particular cathepsin B, in degradation of collagen in periosteal tissue explants. Matrix Biol 1997; 16:575-584.
51. Szpaderska AM, Frankfater A. An intracellular form of cathepsin B contributes to invasiveness in cancer. Cancer Res 2001; 61:3493-3500.
52. Premzl A, Zavasnik-Bergant V, Turk V, Kos J. Intracellular and extracellular cathepsin B facilitate invasion of MCF-10AneoTcell through reconstituted extracellular matrix in vitro. Exp Cell Res 2003; 283:206-214.
53. Murphy G, Ward R, Gavrilovic J, Atkinson S. Physiological mechanism for metalloproteinase activation. Matrix 1992; 1(Suppl.):224-230.
54. Kobayashi H, Moniwa N, Sugimura M, Shinohara H, Ohi H, Terao T. Effects of membrane-associated cathepsin B on the activation of receptor-bound prourokinase and subsequent invasion of reconstituted basement membranes. Biochim Biophys Acta 1993; 1178:55-62.
55. Murphy G, Gavrilovic J. Proteolysis and cell migration: creating a path? Curr Opin Cell Biol 1999; 11:614-6511.
56. Hill PA, Buttle DJ, Jones SJ, Boyde A, Murata M, Reynolds JJ. Inhibition of bone resorption by selective inactivators of cysteine proteinases. J Cell Biochem 1994; 56:118-130.
57. Rochefort H. Cathepsin D in breast cancer: a tissue marker associated with metastasis. Eur J Cancer 1992; 28:1780-1783.
58. Kos J, Smid A, Krasovec M, Svetic B, Lenarcic B, Vrhovec I, et al. Lysosomal proteases cathepsins D, B, H and L and their inhibitors stefins A and B in head and neck cancer. Biol Chem Hoppe-Seyler 1995; 376:401-405.
59. Strojan P, Budihna M, Smid L, Vrhovec I, Skrk J. Cathepsin D in tissue and serum of patients with squamous cell carcinoma of the head and neck. Cancer Lett 1998; 130:49-56.
60. Podhajcer OL, Bover L, Bravo AI, Ledda MF, Kairiyama C, Calb I, et al. Expression of cathepsin D in primary and metastatic human melanoma and dysplastic nevi. J Invest Dermatol 1995; 104:340-344.
61. Frohlich E, Schlagenhauff B, Mohile M, Weber E, Klessen C, Rassner G. Activity, expression, and transcription rate of cathepsins B, D, H and L in cutaneous malignant melanoma. Cancer 2001; 91:972-982.
62. Capony F, Rougeot C, Mountcounier P, Cavailles V, Salazar G, Rochefort H. Increased secretion, altered processing and glycosylation of procathepsin D in mammary carcinoma cells. Cancer Res 1989; 48:3904-3909.
63. Arao J, Fukui H, Ono Y, Ueda Y, Chiba T, Fujimori T. Immunohistochemical localization of cathepsin D in colorectal tumors. Dis Colon Rectum 2000; 43:396-401.
64. Kashida H, Kawamata H, Ichikawa K, Morita K, Imura J, Fujimori T. Intracytoplasmic localization of cathepsin D reflects the invasive potential of gastric carcinoma. J Gastroenterol 2001; 36:809-815.
65. Juliano L, Chagas JR, Hirata IY, Carmona E, Sucupira M, Oliveira ES, et al. A selective assay for endo-oligopeptidase A based on the cleavage of fluorogenic substrate structurally related to enkephalin. Biochem Biophys Res Commun 1990; 173:647-652.
66. Chagas JR, Juliano L, Prado ES. Intramolecularly quenched fluorogenic tetrapeptide substrates for tissue and plasma kallikreins. Anal Biochem 1991; 192:419-425.
67. Oliveira V, Ferro ES, Gomes MD, Oshiro MEM, Almeida PC, Juliano MA, et al. Characterization of thiol-, aspartyl- and thiol-metallo-peptidase activities in Madim-Darby canine kidney cells. J Cell Biochem 2000; 76:478-488.
68. Timpl R, Bruckner P, Fietzek P. Characterization of pepsin fragments of basement membrane collagen obtained from a mouse tumor. Eur J Biochem 1979; 95:255-263.
69. Laurie GW, Leblond CP, Martin GR. Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes. J Cell Biol 1982; 95:340-344.
70. Monteiro ACS, Abrahamson M, Lima APCA, Santos MAV, Scharfstein J. Identification, characterization and localization of chagasin, a tight-binding cysteine protease inhibitor in Trypanosoma cruzi. J Cell Sci 2001; 114:3933-3942.
71. Nowell PC. Biology of the disease: cancer, chromosomes and genetics. Lab Invest 1992; 66:407-417.
72. Rao UNM, Jones MW, Finkelstein SD. Genotypic analysis of primary and metastatic cutaneous melanoma. Cancer Gen Cytogen 2003; 140:37-44.
73. Nakayama T, Taback B, Turner R, Morton DL, Hoon DS. Molecular clonality of in-transit melanoma metastasis. Am J Pathol 2001; 158:1371-1378.
74. Takata M, Morita R, Takehara K. Clonal heterogeneity in sporadic melanomas as revealed by loss-of-heterozygosity analysis. Int J Cancer 2000; 85:492-497.
75. Rodrigues EG, Travassos LR. Endogenous accumulation of IFN-gamma in IFN-gamma-R (-/-) mice increases resistance to B16F10-Nex2 murine melanoma: a model for direct IFN-gamma anti-tumor cytotoxicity in vitro and in vivo. Cytokines Cell Mol Ther 2002; 7:107-116.
76. Hart IR, Birch M, Marshall JF. Cell adhesion receptor expression during melanoma progression and metastasis. Cancer Metast Rev 1991; 10:115-128.
77. Navab R, Mort JS, Brodt P. Inhibition of carcinoma cell invasion and liver metastases formation by the cysteine proteinase inhibitor E-64. Clin Exp Metastasis 1997; 15:121-129.
78. Leto G, Pizzolanti G, Tumminello FM, Gebbia N. Effects of E-64 (cysteine-proteinase inhibitor) and pepstatin (aspartyl-proteinase inhibitor) on metastasis formation in mice with mammary and ovarian tumors. In vivo 1994; 8:231-236.
79. Corticchiato O, Cajot JF, Abrahamson M, Chan SJ, Keppler D, Sordat B. Cystatin C and cathepsin B in human colon carcinoma: expression by cell lines and matrix degradation. Int J Cancer 1992; 52:645-652.
80. Qian F, Chan SJ, Achkar C, Steiner DF, Frankfater A. Transcriptional regulation of cathepsin B expression in B16 melanomas of varying metastatic potential. Biochem Biophys Res Commun 1994; 207:429-436.
81. Keppler D, Sameni M, Moin K, Mikkelsen T, Diglio CA, Sloane BF. Tumor progression and angiogenesis: cathepsin B & Co. Biochem Cell Biol 1996; 74:799-810.
82. Yanamandra N, Gumidyala KV, Waldron KG, Gujrati M, Olivero WC, Dinh DH, et al. Blockade of cathepsin B expression in human glioblastoma cells is associated with suppression of angiogenesis. Oncogene 2004; 23:2224-2230.
83. Sloane BF, Rozhin J, Johnson K, Taylor H, Crissman JD, Honn KV. Cathepsin B: association with plasma membrane in metastatic tumors. Proc Natl Acad Sci USA 1986; 83:2483-2487.
84. Berquin IM, Sloane BF. Cathepsin B expression in human tumors. Adv Exp Med Biol 1996; 389:281-294.
85. Nakao H, Kurita Y, Tsuboi R, Takamori K, Ogawa H. Differences in induction of lysosomal protease activity by protease inhibitors in 816 melanoma cell lines. Int J Biochem 1989; 21:139-142.