The cysteine protease cathepsin B in cancer

Summary

Of the cysteine proteases, cathepsin B has been most often implicated in tumor progression. Accumulating evidence indicates that the regulation of cathepsin B and other cysteine proteases is under both transcriptional and posttranscriptional control. The elucidation of such control mechanisms may be important for therapeutic strategies aimed at reducing cathepsin B overexpression in tumors and other pathologies. Transcription initiation at more than one initiation site and/or the induction of alternative splicing of mRNA may lead to the production of transcripts that differ in their rate of translation or their stability. Hence, the amount of protein produced may not be proportional to the amount of mRNA observed in tissues. Transcripts lacking exon 3 would encode a truncated procathepsin B, a form predicted to be trafficked to the cytoplasm due to the absence of its signal peptide. Evidence of alterations in trafficking of cathepsin B and distribution of organelles labeling for cathepsin B to more peripheral, basolateral or cell membrane localizations is seen in bladder, breast, colon, prostate and thyroid carcinomas and in gliomas. These may reflect alterations in the cytoskeleton as similar changes in localization of cathepsin B accompany the rearrangement of cytoskeletal elements and the acquisition of an invasive phenotype in MCF-10A breast epithelial cell lines after transfection with oncogenic c-Ha-ras. Alterations in trafficking of cathepsin B and other cysteine proteases may thus be brought about by changes in signal transduction, induced by transfection with an activated oncogene. Signal-transduction pathways as well as the enzymes directly involved in the invasive degradation of basement membranes may therefore both be targets for therapeutic intervention. The results of recent studies suggest that cathepsins B and L are more stable in the extracellular environment than previously believed and so could play a significant extracellular role in invasive cancer.

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References

  1. 1

    San Segundo, B., Chan, S.J. and Steiner, D.F., FEBS Lett., 201 (1986) 251.

    Google Scholar 

  2. 2

    Hamilton, M., Jang, Y.-J., Delgado, M.A., Shim, J.-K., Bruns, K.A., Chiang, C.-P., Fang, -Yu, Parfett, C.J.L., Denhardt, D.T. and Nilsen-Hamilton, R.T., Mol. Reprod. Dev., 30 (1991) 285.

    Google Scholar 

  3. 3

    Petanceska, S., Burke, S., Watson, S.J. and Devi, L., Neuroscience, 59 (1994) 729.

    Google Scholar 

  4. 4

    Uchiyama, Y., Waguri, S., Sato, N., Watanabe, T., Ishido, K. and Kominami, E., Acta Histochem. Cytochem., 27 (1994) 287.

    Google Scholar 

  5. 5

    Aronson, N.N. and Barrett, A.J., Biochem. J., 171 (1978) 759.

    Google Scholar 

  6. 6

    Reyes, V.E., Lu, S. and Humphreys, R.E., J. Immunol., 146 (1991) 3877.

    Google Scholar 

  7. 7

    Bennett, K., Levine, T., Ellis, J.S., Peanasky, R.J., Samloff, I.M., Kay, J. and Chain, B.M., Eur. J. Immunol., 22 (1992) 1519.

    Google Scholar 

  8. 8

    Baici, A., Lang, A., Horler, D., Kissling, R. and Merlin, C., Ann. Rheum. Dis., 54 (1995) 289.

    Google Scholar 

  9. 9

    Nakanishi, H., Tominaga, K., Amano, T., Inoue, T. and Yamamoto, K., Exp. Neurol., 126 (1994) 119.

    Google Scholar 

  10. 10

    Sloane, B.F., Sameni, M., Cao, L., Berquin, I., Rozhin, J., Ziegler, G., Moin, K. and Day, N., In Katunuma, N., Suzuki, K., Travis, J. and Fritz, H. (Eds.) Biological Functions of Proteases and Inhibitors, Japan Scientific Societies Press, Tokyo, Japan, 1994, pp. 131–147.

    Google Scholar 

  11. 11

    Sloane, B.F., Moin, K. and Lah, T., In Pretlow, T.G. and Pretlow, T.P. (Eds.) Biochemical and Molecular Aspects of Selected Cancers, Vol. 2, Academic Press, San Diego, CA, U.S.A., 1994, pp. 411–454.

    Google Scholar 

  12. 12

    Agarwal, S.K., Biochem. Educ., 18 (1990) 67.

    Google Scholar 

  13. 13

    Schwartz, M.K., Clin. Chim. Acta, 237 (1995) 67.

    Google Scholar 

  14. 14

    Barrett, A.J. and Kirschke, H., Methods Enzymol., 80 (1981) 535.

    Google Scholar 

  15. 15

    Velasco, G., Ferrando, A.A., Puente, X.S., Sanchez, L.M. and Lopez-Otin, C., J. Biol. Chem., 269 (1994) 27136.

    Google Scholar 

  16. 16

    Brömme, D. and Okamoto, K., Biol. Chem. Hoppe-Seyler, 376 (1995) 379.

    Google Scholar 

  17. 17

    Dufour, E., Biochimie, 70 (1988) 1335.

    Google Scholar 

  18. 18

    Ishidoh, K., Muno, D., Sato, N. and Kominami, E., J. Biol. Chem., 266 (1991) 16312.

    Google Scholar 

  19. 19

    Berquin, I.M. and Sloane, B.F., Perspect. Drug Discov. Design, 2 (1994) 371.

    Google Scholar 

  20. 20

    Berquin, I.M. and Sloane, B.F., In Suzuki, K. and Bond, J.S. (Eds.) Intracellular Protein Catabolism, Plenum Press, New York, NY, U.S.A., 1995, pp. 281–294.

    Google Scholar 

  21. 21

    Tshushima, H., Ueki, A., Matsuoka, Y., Mihara, H. and Hopsu-Havu, V.K., Int. J. Cancer, 48 (1991) 726.

    Google Scholar 

  22. 22

    Kane, S.E. and Gottesman, M.M., Semin. Cancer Biol., 1 (1990) 127.

    Google Scholar 

  23. 23

    Lemere, C.A., Munger, J.S., Shi, G.-P., Natkin, L., Haass, C., Chapman, H.A. and Selkoe, D.J., Am. J. Pathol., 146 (1995) 848.

    Google Scholar 

  24. 24

    Reddy, V.Y., Zhang, Q.-Y. and Weiss, S.J., Proc. Natl. Acad. Sci. USA, 92 (1995) 3849.

    Google Scholar 

  25. 25

    Keppler, D. and Sloane, B.F., Enzyme Protein, 49 (1996) 94.

    Google Scholar 

  26. 26

    Ren, W.-P. and Sloane, B.F., In Dickson, R.D. and Lippman, M.E. (Eds.) Advances in Cellular and Molecular Biology, Breast Cancer: Mammary Tumor Cell Cycle, Differentiation and Metastasis, Kluwer, Boston, MA, U.S.A., 1996, pp. 325–352.

    Google Scholar 

  27. 27

    Lah, T.T., Buck, M.R., Honn, K.V., Crissman, J.D., Rao, N.C., Liotta, L.A. and Sloane, B.F., Clin. Exp. Metastasis, 7 (1989) 461.

    Google Scholar 

  28. 28

    Buck, M.R., Karustis, D.G., Day, N.A., Honn, K.V. and Sloane, B.F., Biochem. J., 282 (1992) 273.

    Google Scholar 

  29. 29

    Dehrmann, F.M., Coetzer, T.H.T., Pike, R.N. and Dennison, C., Arch. Biochem. Biophys., 324 (1995) 93.

    Google Scholar 

  30. 30

    Dehrmann, F.M., Elliott, E. and Dennison, C., Biol. Chem. Hoppe-Seyler, 377 (1996) 391.

    Google Scholar 

  31. 31

    Kobayashi, H., Schmitt, M., Goretzki, L., Chucholowski, N., Calvete, J., Kramer, M., Gunzler, W.A., Janicke, F. and Graeff, H., J. Biol. Chem., 266 (1991) 5147.

    Google Scholar 

  32. 32

    Kobayashi, H., Ohi, H., Sugimura, M., Shinohara, H., Fujii, T. and Terao, T., Cancer Res., 52 (1992) 3610.

    Google Scholar 

  33. 33

    Kobayashi, H., Moniwa, N., Sugimura, M., Shinohara, H., Ohi, H. and Terao, T., Biochim. Biophys. Acta, 1178 (1993) 55.

    Google Scholar 

  34. 34

    Sinha, A.A., Gleason, D.F., DeLeon, O.F., Wilson, M.J. and Sloane, B.F., Anat. Rec., 235 (1993) 233.

    Google Scholar 

  35. 35

    Sinha, A.A., Wilson, M.J., Gleason, D.F., Reddy, P.K., Sameni, M. and Sloane, B.F., Prostate, 26 (1995) 171.

    Google Scholar 

  36. 36

    Visscher, D.W., Sloane, B.F., Sameni, M., Babiarz, J.W., Jacobson, J. and Crissman, J.D., Mod. Pathol., 7 (1994) 76.

    Google Scholar 

  37. 37

    Emmert-Buck, M.R., Roth, M.J., Zhuang, Z., Campo, E., Rozhin, J., Sloane, B.F., Liotta, L.A. and Stetler-Stevenson, W.G., Am. J. Pathol., 145 (1994) 1285.

    Google Scholar 

  38. 38

    Buck, M.R., Roth, M.J., Zhuang, Z., Campo, E., Rozhin, J., Sloane, B.F., Liotta, L.A. and Stetler-Stevenson, W.G., Proc. Am. Assoc. Cancer Res., 35 (1994) 59.

    Google Scholar 

  39. 39

    Rempel, S.A., Rosenblum, M.L., Mikkelsen, T., Yan, P.S., Ellis, K.D., Golembieski, W.A., Sameni, M., Rozhin, J., Ziegler, G. and Sloane, B.F., Cancer Res., 54 (1994) 6027.

    Google Scholar 

  40. 40

    Campo, E., Munoz, J., Miquel, R., Palacin, A., Cardesa, A., Sloane, B.F. and Emmert-Buck, M., Am. J. Pathol., 145 (1994) 301.

    Google Scholar 

  41. 41

    Werle, B., Ebert, W., Klein, W. and Spiess, E., Anticancer Res., 14 (1994) 1169.

    Google Scholar 

  42. 42

    Campo, E., Munoz, J., Nadal, J., Jares, P., Fernandez, P.L., Pakein, A., Emmert-Buck, M., Sloane, B.F. and Cardesa, A., Lab. Invest., 72 (1995) 58.

    Google Scholar 

  43. 43

    Shuja, S., Sheahan, K. and Murnane, M.J., Int. J. Cancer, 49 (1991) 341.

    Google Scholar 

  44. 44

    Murnane, M.J., Sheahan, K., Ozdemirli, M. and Shuja, S., Cancer Res., 51 (1991) 1137.

    Google Scholar 

  45. 45

    Béchet, D.M., Ferrara, M.J., Mordier, S.B., Roux, M.-P., Deval, C.D. and Obled, A., J. Biol. Chem., 266 (1991) 14104.

    Google Scholar 

  46. 46

    Dong, S.S., Stransky, G.I., Whitaker, C.H., Jordan, S.E., Schlesinger, P.H., Edwards, J.C. and Blair, H.C., Biochim. Biophys. Acta, 1251 (1995) 69.

    Google Scholar 

  47. 47

    Mordier, S.B., Bechet, D.M., Roux, M.P., Obled, A. and Ferrara, M.J., Eur. J. Biochem., 229 (1995) 35.

    Google Scholar 

  48. 48

    Gogos, J.A., Thompson, R., Lowry, W., Sloane, B.F., Weintraub, H. and Horwitz, M., J. Cell Biol., 134 (1996) 837.

    Google Scholar 

  49. 49

    Berquin, I.M., Cao, L., Fong, D. and Sloane, B.F., Gene, 159 (1995) 143.

    Google Scholar 

  50. 50

    Qian, F., Chan, S.J., Achkar, C., Steiner, D.F. and Frankfater, A., Biochem. Biophys. Res. Commun., 202 (1994) 429.

    Google Scholar 

  51. 51

    Sloane, B.F., Moin, K., Sameni, M., Tait, L.R., Rozhin, J. and Ziegler, G., J. Cell Sci., 107 (1994) 373.

    Google Scholar 

  52. 52

    Sameni, M., Elliott, E., Ziegler, G., Fortgens, P.H., Dennison, C. and Sloane, B.F., Pathol. Oncol. Res., 1 (1995) 43.

    Google Scholar 

  53. 53

    Wang, X., Chan, S.J., Eddy, R.L., Byers, M.G., Fukushima, Y., Henry, W.M., Haley, L.L., Steiner, D.F. and Shows, T.B., Cytogenet. Cell Genet., 56 (1988) 710.

    Google Scholar 

  54. 54

    Fong, D., Chan, M.M.-Y., Hsieh, W.-T., Menninger, J.C. and Ward, D.C., Hum. Genet., 89 (1992) 10.

    Google Scholar 

  55. 55

    Gong, Q., Chan, S.J., Bajkowski, A.S., Steiner, D.F. and Frankfater, A., DNA Cell Biol., 12 (1993) 299.

    Google Scholar 

  56. 56

    Gong, Q. and Frankfater, A., FASEB J., 7 (1993) 1208.

    Google Scholar 

  57. 57

    Lah, T.T., Hawley, M., Rock, K.L. and Goldberg, A.L., FEBS Lett., 368 (1995) 85.

    Google Scholar 

  58. 58

    Cao, L., Taggart, R.T., Berquin, I.M., Moin, K., Fong, D. and Sloane, B.F., Gene, 139 (1994) 163.

    Google Scholar 

  59. 59

    Tam, S.W., Cote-Paulino, L.R., Peak, D.A., Sheahan, K. and Murnane, M.J., Gene, 139 (1994) 171.

    Google Scholar 

  60. 60

    Rhaissi, H., Bechet, D. and Ferrara, M., Biochimie, 75 (1993) 899.

    Google Scholar 

  61. 61

    Sloane, B.F., Ahram, M., Sameni, M., Friedman, E. and Moin, K., In Isidoro, C. and Gaudino, G. (Eds.) Physiology and Pathology of Intracellular Protein and Lipid Traffic, Stamperia Ugo Boccassi, Torino, Italy, 1995, pp. 73–77.

    Google Scholar 

  62. 62

    Chan, S.J., San Segundo, B., McCormick, M.B. and Steiner, D.F., Proc. Natl. Acad. Sci. USA, 83 (1986) 7721.

    Google Scholar 

  63. 63

    Mehtani, S., Gong, Q. and Frankfater, A., J. Cell. Biochem., 19B (1995) 17.

    Google Scholar 

  64. 64

    Weiss, R.E., Lui, B.C.S., Ahlering, T.E., Dubeau, L. and Droller, M.J., J. Urol., 144 (1990) 798.

    Google Scholar 

  65. 65

    Mikkelsen, T., Yan, P.-S., Ho, K.-L., Sameni, M., Sloane, B.F. and Rosenblum, M.L., J. Neurosurg., 83 (1995) 285.

    Google Scholar 

  66. 66

    Jiang, L.-W., Maher, V.M., McCormick, J.J. and Schindler, M., J. Biol. Chem., 265 (1990) 4775.

    Google Scholar 

  67. 67

    Bolscher, J.G.M., Van der Bijl, M.M.W., Neefjes, J.J., Hall, A., Smets, L.A. and Ploegh, H.L., EMBO J., 7 (1988) 3361.

    Google Scholar 

  68. 68

    Montcourrier, P., Mangeat, P.H., Salazar, G., Morisset, M., Sahuquet, A. and Rochefort, H., Cancer Res., 50 (1990) 6045.

    Google Scholar 

  69. 69

    Elliott, E., Sameni, M., Dennison, C., Ziegler, G. and Sloane, B.F., Mol. Biol. Cell, 215a (1995) 1245.

    Google Scholar 

  70. 70

    Rochefort, H., Capony, F. and Garcia, M., Cancer Metastasis Rev., 9 (1990) 321.

    Google Scholar 

  71. 71

    Wike-Hooley, J.L., Haveman, J. and Reinhold, H.S., Radiother. Oncol., 2 (1984) 343.

    Google Scholar 

  72. 72

    Rozhin, J., Sameni, M., Ziegler, G. and Sloane, B.F., Cancer Res., 54 (1994) 6517.

    Google Scholar 

  73. 73

    Honn, K.V., Timar, J., Rhozin, J., Bazaz, R., Sameni, M., Ziegler, G. and Sloane, B.F., Exp. Cell Res., 214 (1994) 120.

    Google Scholar 

  74. 74

    Ochieng, J., Basolo, F., Albini, A., Melchiori, A., Watanabe, H., Elliott, J., Raz, A., Parodi, S. and Russo, J., Invasion Metastasis, 11 (1991) 38.

    Google Scholar 

  75. 75

    Basolo, F., Elliot, J., Tait, L., Chen, Q.C., Maloney, T.M., Russo, I.H., Pauley, R., Momiki, S., Caamano, J., Klein-Szanto, A.J.P., Koszalka, M. and Russo, J., Mol. Carcinog., 4 (1991) 25.

    Google Scholar 

  76. 76

    Moin, K., Day, N.A., Sameni, M., Hasnain, S., Hirama, T. and Sloane, B.F., Biochem. J., 285 (1992) 427.

    Google Scholar 

  77. 77

    Halban, P.A. and Irminger, J.-C., Biochem. J., 299 (1994) 1.

    Google Scholar 

  78. 78

    Rowan, A.D., Mason, P., Mach, L. and Mort, J.S., J. Biol. Chem., 267 (1992) 15993.

    Google Scholar 

  79. 79

    Kornfeld, S., Biochem. Soc. Trans., 18 (1990) 367.

    Google Scholar 

  80. 80

    Brown, W.J., Goodhouse, J. and Farquhar, M.G., J. Cell Biol., 103 (1986) 1235.

    Google Scholar 

  81. 81

    Rijnboutt, S., Stoorvogel, W., Geuze, H.J. and Strous, G.J., J. Biol. Chem., 267 (1992) 15665.

    Google Scholar 

  82. 82

    Sleat, D.E., Chen, T.-L., Raska, K. and Lobel, P., Cancer Res., 55 (1995) 3424.

    Google Scholar 

  83. 83

    Ludwig, T., Ovitt, C.E., Bauer, U., Hollinshead, M., Remmler, J., Lobel, P., Ruther, U. and Hoflack, B., EMBO J., 12 (1993) 5225.

    Google Scholar 

  84. 84

    Pohlmann, R., Boeker, M.W.C. and von Figura, K., J. Biol. Chem., 270 (1995) 27318.

    Google Scholar 

  85. 85

    MacDonald, R.G., Pfeffer, S.R., Coussens, L., Tepper, M.A., Brocklebank, C.M., Mole, J.E., Anderson, J.K., Chen, E., Czech, M.P. and Ullrich, A., Science, 239 (1988) 1134.

    Google Scholar 

  86. 86

    Chao, H.H.J., Waheed, A., Pohlmann, R., Hille, A. and von Figura, K., EMBO J., 9 (1990) 3507.

    Google Scholar 

  87. 87

    von Figura, K. and Hasilik, A., Annu. Rev. Biochem., 55 (1986) 167.

    Google Scholar 

  88. 88

    Pagano, M., Dalet-Fumeron, V. and Engler, R., Cancer Lett., 45 (1989) 13.

    Google Scholar 

  89. 89

    Cantor, A.B. and Kornfeld, S., J. Biol. Chem., 267 (1992) 23357.

    Google Scholar 

  90. 90

    Ren, W.-P., Fridman, R., Zabrecky, J.R., Morris, L.D., Day, N.A. and Sloane, B.F., Biochem. J., (1996) in press.

  91. 91

    Tisdale, E.J., Bourne, J.R., Khosravi-Far, R., Der, C.J. and Balch, W.E., J. Cell Biol., 119 (1992) 749.

    Google Scholar 

  92. 92

    Rijnboutt, S., Aerts, H.F.G., Geuze, H.J., Tager, J.M. and Strous, G.J., J. Biol. Chem., 266 (1991) 4862.

    Google Scholar 

  93. 93

    McIntyre, G.F. and Erickson, A.H., J. Biol. Chem., 266 (1991) 15438.

    Google Scholar 

  94. 94

    Authier, F., Mort, J.S., Bell, A.W., Posner, B.I. and Bergernon, J.J.M., J. Biol. Chem., 270 (1995) 15798.

    Google Scholar 

  95. 95

    Khosrafi-Far, R. and Der, C.J., Cancer Metastasis Rev., 13 (1994) 67.

    Google Scholar 

  96. 96

    Kiaris, H. and Spandidos, D.A., Int. J. Oncol., 7 (1995) 413.

    Google Scholar 

  97. 97

    Ichikawa, T., Kyprianou, N. and Issacs, J., Cancer Res., 50 (1990) 6349.

    Google Scholar 

  98. 98

    Cho, K.R. and Vogelstein, B., Cancer (Suppl.), 70 (1992) 1727.

    Google Scholar 

  99. 99

    Inoue, T., Ishida, T., Sugio, K. and Sugimachi, K., Cancer Res., 54 (1994) 6133.

    Google Scholar 

  100. 100

    Sloane, B.F., Nat. Biotechnol., 14 (1996) 826.

    Google Scholar 

  101. 101

    Bar-Sagi, D. and Feramisco, J.R., Science, 233 (1986) 1061.

    Google Scholar 

  102. 102

    Kinch, M.S., Clark, G.J., Dehr, C.J. and Burridge, K., J. Cell Biol., 130 (1995) 461.

    Google Scholar 

  103. 103

    Rodriguez-Viciana, P., Warne, P.H., Dhand, R., Van Haesebroeck, B., Gout, I., Fry, M.J., Waterfield, M.D. and Downward, J., Nature, 370 (1994) 527.

    Google Scholar 

  104. 104

    Feig, L.A. and Schaffhausen, B., Nature, 370 (1994) 508.

    Google Scholar 

  105. 105

    Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H. and Balch, W.E., J. Cell Biol., 130 (1995) 781.

    Google Scholar 

  106. 106

    Davidson, H.W., J. Cell Biol., 130 (1995) 797.

    Google Scholar 

  107. 107

    Ridley, A.J. and Hall, A., Cell, 70 (1992) 389.

    Google Scholar 

  108. 108

    Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D. and Hall, A., Cell, 70 (1992) 401.

    Google Scholar 

  109. 109

    Nobes, C.D. and Hall, A., Cell, 81 (1995) 53.

    Google Scholar 

  110. 110

    Bretcher, A., Annu. Rev. Cell Biol., 7 (1991) 337.

    Google Scholar 

  111. 111

    Bar-Sagi, D., Anticancer Res., 9 (1989) 1427.

    Google Scholar 

  112. 112

    Ridley, A.J., BioEssays, 16 (1995) 321.

    Google Scholar 

  113. 113

    Khosrafi-Far, R., Sloski, P.A., Clark, G.J., Kinch, M.S. and Der, C.J., Mol. Cell. Biol., 15 (1995) 6443.

    Google Scholar 

  114. 114

    Qiu, R.-G., Chen, J., Kirn, D., McCormick, F. and Symons, M., Nature, 374 (1995) 457.

    Google Scholar 

  115. 115

    Qiu, R.-G., Chen, J., Kirn, D., McCormick, F. and Symons, M., Proc. Natl. Acad. Sci. USA, 92 (1995) 11781.

    Google Scholar 

  116. 116

    Prendergast, G.C., Khosrafi-Far, R., Solski, P.A., Kurzawa, H., Lebowitz, P.F. and Der, C.J., Oncogene, 10 (1995) 2289.

    Google Scholar 

  117. 117

    Symons, M., Curr. Opin. Biotechnol., 6 (1995) 668.

    Google Scholar 

  118. 118

    Habets, G.G.M., Scholtes, E.H.M., Zuydgeest, D., Van der Kammen, R.A., Stam, J.C., Berns, A. and Collard, J.G., Cell, 77 (1994) 537.

    Google Scholar 

  119. 119

    Michiels, F., Habets, G.G.M., Stam, J.C., Van der Kammen, R.A. and Collard, J.G., Nature, 375 (1995) 338.

    Google Scholar 

  120. 120

    Huttenlocher, A., Sandborg, R.R. and Horwitz, A.F., Curr. Opin. Cell Biol., 7 (995) 697.

  121. 121

    Baici, A., Knopfel, M. and Keist, R., Invasion Metastasis, 8 (1988) 143.

    Google Scholar 

  122. 122

    Shuja, S. and Murnane, M.J., Int. J. Cancer, 66 (1996) 420.

    Google Scholar 

  123. 123

    Guenette, R.S., Mooibroek, M., Wong, K., Wong, P. and Tenniswood, M., Eur. J. Biochem., 226 (1994) 311.

    Google Scholar 

  124. 124

    Freeman, S.N., Rennie, P.S., Chao, J., Lund, L.R. and Andreasen, P.A., Biochem. J., 269 (1990) 189.

    Google Scholar 

  125. 125

    Sensibar, J.A., Lui, X.X., Patai, B., Alger, B. and Lee, C., Eur. J. Biochem., 226 (1990) 311.

    Google Scholar 

  126. 126

    Lenarcic, B., Krasovec, M., Ritonja, A., Olfsson, I. and Turk, V., FEBS Lett., 280 (1991) 211.

    Google Scholar 

  127. 127

    Hewitt, R.E., Leach, I.H., Powe, D.G., Clark, I.M., Cawston, T.E. and Turner, D.R., Int. J. Cancer, 49 (1991) 666.

    Google Scholar 

  128. 128

    Bursch, W., Gleeson, T.G., Kleine, L. and Tenniswood, M.P., Biochem. Cell Biol., 68 (1990) 1071.

    Google Scholar 

  129. 129

    Pullan, S., Wilson, J., Metcalf, A., Edwards, G.M., Goberdhan, N., Tilly, J., Hickman, J.A., Dive, C. and Streuli, C.H., J. Cell Sci., 109 (1996) 631.

    Google Scholar 

  130. 130

    Tenniswood, M., Guenette, R.S., Lakins, L.I., Mooibroek, M., Wong, P. and Welsh, J., Cancer Metastasis Rev., 11 (1992) 197.

    Google Scholar 

  131. 131

    Delaisse, J.-M., Eeckhout, Y. and Vaes, G., Biochem. Biophys. Res. Commun., 125 (1984) 441.

    Google Scholar 

  132. 132

    Rifkin, B.R., Vernillo, A.T., Kleckner, A.P., Auszmann, J.M., Rosenberg, L.R. and Zimmermann, M., Biochem. Biophys. Res. Commun., 179 (1991) 63.

    Google Scholar 

  133. 133

    Chapman Jr., H.A., Munger, J.S. and Shi, S.P., Am. J. Respir. Crit. Care Med., 150 (1994) 8155.

    Google Scholar 

  134. 134

    Soto, T., Kiyoshima, T., Moroi, R., Nishimura, Y., Himeno, M., Yamomoto, K. and Tanaka, T., Histochemistry, 101 (1994) 33.

    Google Scholar 

  135. 135

    Baici, A. and Lang., A., Cell Tissue Res., 259 (1990) 567.

    Google Scholar 

  136. 136

    Buttle, D.J., Bonner, B.C., Burnett, D. and Barrett, A.J., Biochem. J., 254 (1988) 693.

    Google Scholar 

  137. 137

    Turk, B., Dolenc, I., Zerovnik, E., Turk, D., Gubensek, F. and Turk, V., Biochemistry, 33 (1994) 14800.

    Google Scholar 

  138. 138

    Khan, M.Y. and Ahmad, S., Biochem. Int., 15 (1987) 111.

    Google Scholar 

  139. 139

    Dennison, C., Pike, R.N., Coetzer, T.H.T. and Kirk, K.C., Biol. Chem. Hoppe-Seyler, 373 (1992) 419.

    Google Scholar 

  140. 140

    Willenbrock, F. and Brocklehurst, K., Biochem. J., 227 (1985) 511.

    Google Scholar 

  141. 141

    Khouri, H.E., Plouffe, C., Hasnain, S., Hirama, T., Storer, A.C. and Ménard, R., Biochem. J., 275 (1991) 751.

    Google Scholar 

  142. 142

    Hasnain, S., Hirama, T., Tam, A. and Mort, J.S., J. Biol. Chem., 267 (1992) 4713.

    Google Scholar 

  143. 143

    Navab, R., Mort, J.S. and Brodt, P., Proc. Am. Assoc. Cancer Res., 36 (1995) 102.

    Google Scholar 

  144. 144

    Panchal, R.G., Cusack, E., Cheley, S. and Bayley, H., Nat. Biotechnol., 14 (1996) 352.

    Google Scholar 

  145. 145

    Wagner, A.C.C. and Williams, J.A., Am. J. Physiol., 266 (1994) 1.

    Google Scholar 

  146. 146

    Lerner, E.C., Qian, Y., Blaskovich, M.A., Fossum, R.D., Vogt, A., Sun, J., Cox, A.D., Der, C.J., Hamilton, A.D. and Sebti, S.M., J. Biol. Chem., 270 (1995) 26802.

    Google Scholar 

  147. 147

    Garcia, A.M., Rowell, C., Ackermann, K., Kowalczyk, J.J. and Lewis, M.L., J. Biol. Chem., 268 (1993) 18415.

    Google Scholar 

  148. 148

    Hara, M., Akasaka, K., Akinga, S., Okabe, M., Nakano, H., Gomez, G., Wood, D., Uh, M. and Tamanoi, F., Proc. Natl. Acad. Sci. USA, 90 (1993) 2281.

    Google Scholar 

  149. 149

    Kohl, N.E., Mosser, S.D., deSolms, J., Giuliani, E.A., Pompliano, D.L., Graham, S.L., Smith, R.L., Scolnick, E.M., Oliff, A. and Gibbs, J.B., Science, 260 (1993) 1934.

    Google Scholar 

  150. 150

    Kohl, N.E., Omer, C.A., Conner, M.W., Anthony, N.J., Davide, J.P., deSolms, S., Giuliani, E.A., Gomez, R.P., Graham, S.L., Hamilton, K., Handt, L.K., Hartman, G.D., Koblan, K.S., Kral, A.M., Miller, P.J., Mosser, S.D., O'Neill, T.J., Rands, E., Schaber, M.D., Gibbs, J.B. and Oliff, A., Nat. Med., 1 (1995) 792.

    Google Scholar 

  151. 151

    Tamanoi, F., Trends Biochem. Sci., 18 (1993) 349.

    Google Scholar 

  152. 152

    James, G.L., Goldstein, J.L., Brown, M.S., Rawson, T.E., Somers, T.C., McDowell, R.S., Crowley, C.W., Lucas, B.K., Levinson, A.D. and Marsters, J.C., Science, 260 (1993) 1937.

    Google Scholar 

  153. 153

    Sun, J., Qian, Y., Hamilton, A.D. and Sebti, S.M., Cancer Res., 55 (1995) 4243.

    Google Scholar 

  154. 154

    Gibbs, J.B., Oliff, A. and Kohl, N.E., Cell, 77 (1994) 175.

    Google Scholar 

  155. 155

    Prendergast, G.C., Davide, J.P., deSolms, S.J., Giuliani, E.A., Graham, S.L., Gibbs, J.B., Oliff, A. and Kohl, N.E., Mol. Cell. Biol., 14 (1994) 4193.

    Google Scholar 

  156. 156

    Lebowitz, P.F., Davide, J.P. and Prendergast, G.C., Mol. Cell. Biol., 15 (1995) 6613.

    Google Scholar 

  157. 157

    Adamson, P., Paterson, H.F. and Hall, A., J. Cell Biol., 119 (1992) 617.

    Google Scholar 

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Correspondence to Bonnie F. Sloane.

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Elliott, E., Sloane, B.F. The cysteine protease cathepsin B in cancer. Perspectives in Drug Discovery and Design 6, 12–32 (1996). https://doi.org/10.1007/BF02174043

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Keywords

  • Alternative Splice
  • Thyroid Carcinoma
  • Cysteine Protease
  • Epithelial Cell Line
  • Initiation Site