Cancer and Metastasis Reviews

, Volume 22, Issue 2–3, pp 271–286 | Cite as

Pericellular cathepsin B and malignant progression

  • Stefanie Roshy
  • Bonnie F. Sloane
  • Kamiar Moin
Article

Abstract

Cathepsin B is a lysosomal cysteine protease in normal cells and tissues. In malignant tumors and premalignant lesions, the expression of cathepsin B is highly upregulated and the enzyme is secreted and becomes associated with the cell surface. Increases in expression are mediated at many levels ranging from gene amplification to increased stability of mRNA and protein. Cathepsin B is synthesized as a preproenzyme and the primary pathways for its normal trafficking to the lysosome utilize mannose 6-phosphate receptors (MPRs). Inactive procathepsin B is processed to active single and double chain forms of cathepsin B in the late endosomes and lysosomes, respectively. Tumor cells secrete procathepsin B and both active forms of cathepsin B. Secretion of procathepsin B occurs principally as a result of increased expression, whereas secretion of active cathepsin B seems to involve active processes that can be induced by a variety of mechanisms. Once secreted procathepsin B binds to the tumor cell surface via p11, the light chain of the annexin II heterotetramer. This binding seems to facilitate conversion of procathepsin B to its active forms. Cathepsin B and the annexin II heterotetramer colocalize in caveolae (lipid raft) fractions isolated from tumor cells. Serine proteases and matrix metalloproteinases also have been found to associate with caveolae and some with the annexin II heterotetramer. Our working hypothesis is that pericellular cathepsin B through its proximity to other proteases in caveolae participates in, perhaps even initiates, a proteolytic cascade on the tumor cell surface.

cysteine proteases lysosomes endosomes cell surface binding proteins secretion 

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References

  1. 1.
    Mort JS, Buttle DJ: Cathepsin B. Int J Biochem Cell Biol 29(5): 715–720, 1997Google Scholar
  2. 2.
    Rozhin J, Robinson D, Stevens MA, Lah TT, Honn KV, Ryan RE, Sloane BF: Properties of a plasma membraneassociated cathepsin B-like cysteine proteinase in metastaticB16 melanoma variants. Cancer Res 47(24 Pt 1): 6620–6628, 1987Google Scholar
  3. 3.
    Sameni M, Elliott E, Ziegler G, Fortgens PH, Dennison C, Sloane BF: Cathepsin B and D are localized at the surface of human breast cancer cells. Pathol Oncol Res 1(1): 43–53, 1995Google Scholar
  4. 4.
    Mach L, Stuwe K, Hagen A, Ballaun C, Glossl J: Proteolytic processing and glycosylation of cathepsin B. The role of the primary structure of the latent precursor and of the carbohydrate moiety for cell-type-specific molecular forms of the enzyme. Biochem J 282(Pt 2): 577–582, 1992Google Scholar
  5. 5.
    Halangk W, Lerch MM, Brandt-Nedelev B, Roth W, Ruthenbuerger M, Reinheckel T, Domschke W, Lippert H, Peters C, Deussing J: Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J Clin Invest 106(6): 773–781, 2000Google Scholar
  6. 6.
    Reinheckel T, Deussing J, Roth W, Peters C: Towards specific functions of lysosomal cysteine peptidases: Phenotypes of mice deficient for cathepsin B or cathepsin L. Biol Chem 382(5): 735–741, 2001Google Scholar
  7. 7.
    Barrett AJ, Kirschke H: Cathepsin B, Cathepsin H, Cathepsin L. Methods Enzymol 80(Pt C): 535–561, 1981Google Scholar
  8. 8.
    Lang A, Horler D, Baici A: The relative importance of cysteine peptidases in osteoarthritis. J Rheumatol 27(8): 1970–1979, 2000Google Scholar
  9. 9.
    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 107(Pt 2): 373–384, 1994Google Scholar
  10. 10.
    Frosch BA, Berquin I, Emmert-Buck MR, Moin K, Sloane BF: Molecular regulation, membrane association and secretion of tumor cathepsin B. Apmis 107(1): 28–37, 1999Google Scholar
  11. 11.
    Baici A, Lang A, Horler D, Kissling R, Merlin C: Cathepsin B in osteoarthritis: Cytochemical and histochemical analysis of human femoral head cartilage. Ann Rheum Dis 54(4): 289–297, 1995Google Scholar
  12. 12.
    Campo E, Munoz J, Miquel R, Palacin A, Cardesa A, Sloane BF, Emmert-Buck MR: Cathepsin B expression in colorectal carcinomas correlates with tumor progression and shortened patient survival. Am J Pathol 145(2): 301–309, 1994Google Scholar
  13. 13.
    Scorilas A, Fotiou S, Tsiambas E, Yotis J, Kotsiandri F, Sameni M, Sloane BF, Talieri M: Determination of cathepsin B expression may offer additional prognostic information for ovarian cancer patients. Biol Chem 383(7/8): 1297–1303, 2002Google Scholar
  14. 14.
    Sinha AA, Gleason DF, Deleon OF, Wilson MJ, Sloane BF: Localization of a biotinylated cathepsin B oligonucleotide probe in human prostate including invasive cells and invasive edges by in situ hybridization. Anat Rec 235(2): 233–240, 1993Google Scholar
  15. 15.
    Demchik LL, Sameni M, Nelson K, Mikkelsen T, Sloane BF: Cathepsin B and glioma invasion. Int J Dev Neurosci 17(5–6): 483–494, 1999Google Scholar
  16. 16.
    Koblinski JE, Dosescu J, Sameni M, Moin K, Clark K, Sloane BF: Interaction of human breast fibroblasts with collagen I increases secretion of procathepsin B. J Biol Chem 277(35): 32220–32227, 2002Google Scholar
  17. 17.
    Yan S, Berquin IM, Troen BR, Sloane BF: Transcription of human cathepsin B is mediated by Sp1 and Ets family factors in glioma. DNA Cell Biol 19(2): 79–91, 2000Google Scholar
  18. 18.
    Naito S, Shimizu S, Matsuu M, Nakashima M, Nakayama T, Yamashita S, Sekine I: Ets-1 upregulates matrix metalloproteinase-1 expression through extracellular matrix adhesion in vascular endothelial cells. Biochem Biophys Res Commun 291(1): 130–138, 2002Google Scholar
  19. 19.
    Delannoy-Courdent A, Mattot V, Fafeur V, Fauquette W, Pollet I, Calmels T, Vercamer C, Boilly B, Vandenbunder B, Desbiens X: The expression of an Ets1 transcription factor lacking its activation domain decreases uPA proteolytic activity and cell motility, and impairs normal tubulogenesis and cancerous scattering in mammary epithelial cells. J Cell Sci 111(Pt 11): 1521–1534, 1998Google Scholar
  20. 20.
    Liu W, Wang G, Yakovlev AG: Identification and functional analysis of the rat caspase-3 gene promoter. J Biol Chem 277(10): 8273–8278, 2002Google Scholar
  21. 21.
    Guo M, Mathieu PA, Linebaugh B, Sloane BF, Reiners JJ Jr: Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factorbeta. A process initiated by the exocytosis of cathepsin B. J Biol Chem 277(17): 14829–14837, 2002Google Scholar
  22. 22.
    Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, Elling F, Leist M, Jaattela M: Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 153(5): 999–1010, 2001Google Scholar
  23. 23.
    Krepela E, Vicar J, Cernoch M: Cathepsin B in human breast tumor tissue and cancer cells. Neoplasma 36(1): 41–52, 1989Google Scholar
  24. 24.
    Lah TT, Calaf G, Kalman E, Shinde BG, Russo J, Jarosz D, Zabrecky J, Somers R, Daskal I: Cathepsins D, B and L in breast carcinoma and in transformed human breast epithelial cells (HBEC). Biol Chem Hoppe Seyler 376(6): 357–363, 1995Google Scholar
  25. 25.
    Murnane MJ, Sheahan K, Ozdemirli M, Shuja S: Stagespecific increases in cathepsin B messenger RNA content in human colorectal carcinoma. Cancer Res 51(4): 1137–1142, 1991Google Scholar
  26. 26.
    Emmert-Buck MR, Roth MJ, Zhuang Z, Campo E, Rozhin J, Sloane BF, Liotta LA, Stetler-Stevenson WG: Increased gelatinase A (MMP-2) and cathepsin B activity in invasive tumor regions of human colon cancer samples. Am J Pathol 145(6): 1285–1290, 1994Google Scholar
  27. 27.
    Sheahan K, Shuja S, Murnane MJ: Cysteine protease activities and tumor development in human colorectal carcinoma. Cancer Res 49(14): 3809–3814, 1989Google Scholar
  28. 28.
    Shuja S, Sheahan K, Murnane MJ: Cysteine endopeptidase activity levels in normal human tissues, colorectal adenomas and carcinomas. Int J Cancer 49(3): 341–346, 1991Google Scholar
  29. 29.
    Hazen LG, Bleeker FE, Lauritzen B, Bahns S, Song J, Jonker A, Van Driel BE, Lyon H, Hansen U, Kohler A, Van Noorden CJ: Comparative localization of cathepsin B protein and activity in colorectal cancer. J Histochem Cytochem 48(10): 1421–1430, 2000Google Scholar
  30. 30.
    Hughes SJ, Glover TW, Zhu XX, Kuick R, Thoraval D, Orringer MB, Beer DG, Hanash S: A novel amplicon at 8p22–23 results in overexpression of cathepsin B in esophageal adenocarcinoma. Proc Natl Acad Sci USA 95(21): 12410–12415, 1998Google Scholar
  31. 31.
    Liu Y, Xiao S, Shi Y, Wang L, Ren W, Sloane BF: Cathepsin B on invasion and metastasis of gastric carcinoma. Chin Med J (Engl) 111(9): 784–788, 1998Google Scholar
  32. 32.
    Ebert W, Knoch H, Werle B, Trefz G, Muley T, Spiess E: Prognostic value of increased lung tumor tissue cathepsin B. Anticancer Res 14(3A): 895–899, 1994Google Scholar
  33. 33.
    Kusunoki T, Nishida S, Nakano T, Funasaka K, Kimoto S, Murata K, Tomura T: Study on cathepsin B activity in human thyroid tumors. Auris Nasus Larynx 22(1): 43–48, 1995Google Scholar
  34. 34.
    Rempel SA, Rosenblum ML, Mikkelsen T, Yan PS, Ellis KD, Golembieski WA, Sameni M, Rozhin J, Ziegler G, Sloane BF: Cathepsin B expression and localization in glioma progression and invasion. Cancer Res 54(23): 6027–6031, 1994Google Scholar
  35. 35.
    Sivaparvathi M, Sawaya R, Wang SW, Rayford A, Yamamoto M, Liotta LA, Nicolson GL, Rao JS: Over-282 Roshy, Sloane and Moin expression and localization of cathepsin B during the progression of human gliomas. Clin Exp Metastasis 13(1): 49–56, 1995Google Scholar
  36. 36.
    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 91(5): 972–982, 2001Google Scholar
  37. 37.
    Kim K, Cai J, Shuja S, Kuo T, Murnane MJ: Presence of activated ras correlates with increased cysteine proteinase activities in human colorectal carcinomas. Int J Cancer 79(4): 324–333, 1998Google Scholar
  38. 38.
    Abdollahi A, Getts LA, Sonoda G, Miller PD, Taguchi T, Godwin AK, Testa JR, Hamilton TC: Genome scanning detects amplification of the cathepsin B gene (CtsB) in transformed rat ovarian surface epithelial cells. J Soc Gynecol Investig 6(1): 32–40, 1999Google Scholar
  39. 39.
    Berquin IM, Cao L, Fong D, Sloane BF: Identification of two new exons and multiple transcription start points in the 5'-untranslated region of the human cathepsin-Bencoding gene. Gene 159(2): 143–149, 1995Google Scholar
  40. 40.
    Wasylyk C, Wasylyk B: Oncogenic conversion alters the transcriptional properties of ets. Cell Growth Differ 3(9): 617–625, 1992Google Scholar
  41. 41.
    Fafeur V, Tulasne D, Queva C, Vercamer C, Dimster V, Mattot V, Stehelin D, Desbiens X, Vandenbunder B: The ETS1 transcription factor is expressed during epithelialmesenchymal transitions in the chick embryo and is activated in scatter factor-stimulated MDCK epithelial cells. Cell Growth Differ 8(6): 655–665, 1997Google Scholar
  42. 42.
    Mehtani S, Gong Q, Panella J, Subbiah S, Peffley DM, Frankfater A: In vivo expression of an alternatively spliced human tumor message that encodes a truncated form of cathepsin B. Subcellular distribution of the truncated enzyme in COS cells. J Biol Chem 273(21): 13236–13244, 1998Google Scholar
  43. 43.
    Berardi S, Lang A, Kostoulas G, Horler D, Vilei EM, Baici A: Alternative messenger RNA splicing and enzyme forms of cathepsin B in human osteoarthritic cartilage and cultured chondrocytes. Arthritis Rheum 44(8): 1819–1831, 2001Google Scholar
  44. 44.
    Berquin IM, Yan S, Katiyar K, Huang L, Sloane BF, Troen BR: Differentiating agents regulate cathepsin B gene expression in HL-60 cells. J Leukoc Biol 66(4): 609–616, 1999Google Scholar
  45. 45.
    Yan Z, Deng X, Chen M, Xu Y, Ahram M, Sloane BF, Friedman E: Oncogenic c-Ki-ras but not oncogenic c-Haras up-regulates CEA expression and disrupts basolateral polarity in colon epithelial cells. J Biol Chem 272(44): 27902–27907, 1997Google Scholar
  46. 46.
    Rozhin J, Sameni M, Ziegler G, Sloane BF: Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res 54(24): 6517–6525, 1994Google Scholar
  47. 47.
    Fearon ER, Vogelstein B: A genetic model for colorectal tumorigenesis. Cell 61(5): 759–767, 1990Google Scholar
  48. 48.
    Marten K, Bremer C, Khazaie K, Sameni M, Sloane B, Tung CH, Weissleder R: Detection of dysplastic intestinal adenomas using enzyme-sensing molecular beacons in mice. Gastroenterology 122(2): 406–414, 2002Google Scholar
  49. 49.
    Hartz PA, Wilson PD: Functional defects in lysosomal enzymes in autosomal dominant polycystic kidney disease (ADPKD): Abnormalities in synthesis, molecular processing, polarity, and secretion. Biochem Mol Med 60(1): 8–26, 1997Google Scholar
  50. 50.
    Wilson PD, Du J, Norman JT: Autocrine, endocrine and paracrine regulation of growth abnormalities in autosomal dominant polycystic kidney disease. Eur J Cell Biol 61(1): 131–138, 1993Google Scholar
  51. 51.
    Du J, Wilson PD: Abnormal polarization of EGF receptors and autocrine stimulation of cyst epithelial growth in human ADPKD. Am J Physiol 269(2 Pt 1): C487-C495, 1995Google Scholar
  52. 52.
    Wilson PD, Burrow CR: Autosomal dominant polycystic kidney disease: Cellular and molecular mechanisms of cyst formation. Adv Nephrol Necker Hosp 21: 125–142, 1992Google Scholar
  53. 53.
    Carone FA, Nakamura S, Schumacher BS, Punyarit P, Bauer KD: Cyst-derived cells do not exhibit accelerated growth or features of transformed cells in vitro. Kidney Int 35(6): 1351–1357, 1989Google Scholar
  54. 54.
    Capony F, Rougeot C, Montcourrier P, Cavailles V, Salazar G, Rochefort H: Increased secretion, altered processing, and glycosylation of pro-cathepsin D in human mammary cancer cells. Cancer Res 49(14): 3904–3909, 1989Google Scholar
  55. 55.
    Matteoni R, Kreis TE: Translocation and clustering of endosomes and lysosomes depends on microtubules. J Cell Biol 105(3): 1253–1265, 1987Google Scholar
  56. 56.
    Nishimura Y, Sameni M, Sloane BF: Malignant transformation alters intracellular trafficking of lysosomal cathepsin D in human breast epithelial cells. Pathol Oncol Res 4(4): 283–296, 1998Google Scholar
  57. 57.
    Milisav I: Dynein and dynein-related genes. Cell Motil Cytoskeleton 39(4): 261–272, 1998Google Scholar
  58. 58.
    Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, Hirokawa N: Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol 141(1): 51–59, 1998Google Scholar
  59. 59.
    Quintyne NJ, Gill SR, Eckley DM, Crego CL, Compton DA, Schroer TA: Dynactin is required for microtubule anchoring at centrosomes. J Cell Biol 147(2): 321–334, 1999Google Scholar
  60. 60.
    Bi GQ, Morris RL, Liao G, Alderton JM, Scholey JM, Steinhardt RA: Kinesin-and myosin-driven steps of vesicle recruitment for Ca2+-regulated exocytosis. J Cell Biol 138(5): 999–1008, 1997Google Scholar
  61. 61.
    Kamal A, Goldstein LS: Principles of cargo attachment to cytoplasmic motor proteins. Curr Opin Cell Biol 14(1): 63–68, 2002Google Scholar
  62. 62.
    Nakata T, Hirokawa N: Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J Cell Biol 131(4): 1039–1053, 1995Google Scholar
  63. 63.
    Stearns ME, Wang M: Regulation of kinesin expression and type IV collagenase secretion in invasive human prostate PC-3 tumor sublines. Cancer Res 51(21): 5866–5875, 1991Google Scholar
  64. 64.
    Santama N, Krijnse-Locker J, Griffiths G, Noda Y, Hirokawa N, Dotti CG: KIF2beta, a new kinesin superfamily protein in non-neuronal cells, is associated with Pericellular cathepsin B and malignant progression 283 lysosomes and may be implicated in their centrifugal translocation. Embo J 17(20): 5855–5867, 1998Google Scholar
  65. 65.
    Montcourrier P, Mangeat PH, Salazar G, Morisset M, Sahuquet A, Rochefort H: Cathepsin D in breast cancer cells can digest extracellular matrix in large acidic vesicles. Cancer Res 50(18): 6045–6054, 1990Google Scholar
  66. 66.
    Ludwig T, Ovitt CE, Bauer U, Hollinshead M, Remmler J, Lobel P, Ruther U, Hoflack B: Targeted disruption of the mouse cation-dependent mannose 6-phosphate receptor results in partial missorting of multiple lysosomal enzymes. Embo J 12(13): 5225–5235, 1993Google Scholar
  67. 67.
    Braulke T, Mach L, Hoflack B, Glossl J: Biosynthesis and endocytosis of lysosomal enzymes in human colon carcinoma SW 1116 cells: Impaired internalization of plasma membrane-associated cation-independent mannose 6-phosphate receptor. Arch Biochem Biophys 298(1): 176–181, 1992Google Scholar
  68. 68.
    Kuliawat R, Klumperman J, Ludwig T, Arvan P: Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic beta-cells. J Cell Biol 137(3): 595–608, 1997Google Scholar
  69. 69.
    Lorenzo K, Ton P, Clark JL, Coulibaly S, Mach L: Invasive properties of murine squamous carcinoma cells: secretion of matrix-degrading cathepsins is attributable to a deficiency in the mannose 6-phosphate/insulin-like growth factor II receptor. Cancer Res 60(15): 4070–4076, 2000Google Scholar
  70. 70.
    Kuliawat R, Arvan P: Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic beta-cells. J Cell Biol 126(1): 77–86, 1994Google Scholar
  71. 71.
    De Stefanis D, Demoz M, Dragonetti A, Houri JJ, Ogier-Denis E, Codogno P, Baccino FM, Isidoro C: Differentiation-induced changes in the content, secretion, and subcellular distribution of lysosomal cathepsins in the human colon cancer HT-29 cell line. Cell Tissue Res 289(1): 109–117, 1997Google Scholar
  72. 72.
    Laurent-Matha V, Farnoud MR, Lucas A, Rougeot C, Garcia M, Rochefort H: Endocytosis of pro-cathepsin D into breast cancer cells is mostly independent of mannose-6-phosphate receptors. J Cell Sci 111(Pt 17): 2539–2549, 1998Google Scholar
  73. 73.
    McIntyre GF, Erickson AH: Procathepsins L and D are membrane-bound in acidic microsomal vesicles. J Biol Chem 266(23): 15438–15445, 1991Google Scholar
  74. 74.
    McIntyre GF, Erickson AH: The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. Proc Natl Acad Sci USA 90(22): 10588–10592, 1993Google Scholar
  75. 75.
    McIntyre GF, Godbold GD, Erickson AH: The pHdependent membrane association of procathepsin L is mediated by a 9-residue sequence within the propeptide. J Biol Chem 269(1): 567–572, 1994Google Scholar
  76. 76.
    Ahn K, Yeyeodu S, Collette J, Madden V, Arthur J, Li L, Erickson AH: An alternate targeting pathway for procathepsin L in mouse fibroblasts. Traffic 3(2): 147–159, 2002Google Scholar
  77. 77.
    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 264(1): 100–109, 1999Google Scholar
  78. 78.
    Turner MD, Arvan P: Protein trafficfrom the secretory pathway to the endosomal system in pancreatic beta-cells. J Biol Chem 275(19): 14025–14030, 2000Google Scholar
  79. 79.
    Heuser J: Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J Cell Biol 108(3): 855–864, 1989Google Scholar
  80. 80.
    Rodriguez A, Samoff E, Rioult MG, Chung A, Andrews NW: Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol 134(2): 349–362, 1996Google Scholar
  81. 81.
    Tardieux I, Webster P, Ravesloot J, Boron W, Lunn JA, Heuser JE, Andrews NW: Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 71(7): 1117–1130, 1992Google Scholar
  82. 82.
    Gerasimenko JV, Gerasimenko OV, Petersen OH: Membrane repair: Ca(2+)-elicited lysosomal exocytosis. Curr Biol 11(23): R971-R974, 2001Google Scholar
  83. 83.
    Ulbricht B, Henny H, Horstmann H, Spring H, Faigle W, Spiess E: Influence of 12(S)-hydroxyeicosatetraenoic acid (12(S)-HETE) on the localization of cathepsin B and cathepsin L in human lung tumor cells. Eur J Cell Biol 74(3): 294–301, 1997Google Scholar
  84. 84.
    Lemaire R, Huet G, Zerimech F, Grard G, Fontaine C, Duquesnoy B, Flipo RM: Selective induction of the secretion of cathepsins B and L by cytokines in synovial fibroblast-like cells. Br J Rheumatol 36(7): 735–743, 1997Google Scholar
  85. 85.
    Balaji KN, Schaschke N, Machleidt W, Catalfamo M, Henkart PA: Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J Exp Med 196(4): 493–503, 2002Google Scholar
  86. 86.
    Brix K, Lemansky P, Herzog V: Evidence for extracellularly acting cathepsins mediating thyroid hormone liberation in thyroid epithelial cells. Endocrinology 137(5): 1963–1974, 1996Google Scholar
  87. 87.
    Linke M, Jordans S, Mach L, Herzog V, Brix K: Thyroid stimulating hormone upregulates secretion of cathepsin B from thyroid epithelial cells. Biol Chem 383(5): 773–784, 2002Google Scholar
  88. 88.
    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 83(8): 2483–2487, 1986Google Scholar
  89. 89.
    Warwas M, Haczynska H, Gerber J, Nowak M: Cathepsin B-like activity as a serum tumor marker in ovarian carcinoma. Eur J Clin Chem Clin Biochem 35(4): 301–304, 1997Google Scholar
  90. 90.
    Sinha AA, Jamuar MP, Wilson MJ, Rozhin J, Sloane BF: Plasma membrane association of cathepsin B in human prostate cancer: Biochemical and immunogold electron microscopic analysis. Prostate 49(3): 172–184, 2001Google Scholar
  91. 91.
    Cao L, Taggart RT, Berquin IM, Moin K, Fong D, Sloane BF: Human gastric adenocarcinoma cathepsin B: Isolation and sequencing of full-length cDNAs and polymorphisms of the gene. Gene 139(2): 163–169, 1994Google Scholar
  92. 92.
    Moin K, Day NA, Sameni M, Hasnain S, Hirama T, Sloane BF: Human tumor cathepsin B. Comparison with normal liver cathepsin B. Biochem J 285(Pt 2): 427–434, 1992Google Scholar
  93. 93.
    Moin K, Cao L, Day NA, Koblinski JE, Sloane BF: Tumor cell membrane cathepsin B. Biol Chem 379(8–9): 1093–1099, 1998Google Scholar
  94. 94.
    Almeida PC, Nantes IL, Chagas JR, Rizzi CC, Faljoni-Alario A, Carmona E, Juliano L, Nader HB, Tersariol IL: Cathepsin B activity regulation. Heparin-like glycosaminogylcans protect human cathepsin B from alkaline pHinduced inactivation. J Biol Chem 276(2): 944–951, 2001Google Scholar
  95. 95.
    Arkona C, Wiederanders B: Expression, subcellular distribution and plasma membrane binding of cathepsin B and gelatinases in bone metastatictissue. Biol Chem 377(11): 695–702, 1996Google Scholar
  96. 96.
    Mai J, Finley RL Jr, Waisman DM, Sloane BF: Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J Biol Chem 275(17): 12806–12812, 2000Google Scholar
  97. 97.
    Schafer BW, Heizmann CW: The S100 family of EF-hand calcium-binding proteins: Functions and pathology. Trends Biochem Sci 21(4): 134–140, 1996Google Scholar
  98. 98.
    Thiel C, Osborn M, Gerke V: The tight association of the tyrosine kinase substrate annexin II with the submembranous cytoskeleton depends on intact p11-and Ca(2+)-binding sites. J Cell Sci 103(Pt 3): 733–742, 1992Google Scholar
  99. 99.
    Vishwanatha JK, Chiang Y, Kumble KD, Hollingsworth MA, Pour PM: Enhanced expression of annexin II in human pancreatic carcinoma cells and primary pancreatic cancers. Carcinogenesis 14(12): 2575–2579, 1993Google Scholar
  100. 100.
    Kumble KD, Hirota M, Pour PM, Vishwanatha JK: Enhanced levels of annexins in pancreatic carcinoma cells of Syrian hamsters and their intrapancreatic allografts. Cancer Res 52(1): 163–167, 1992Google Scholar
  101. 101.
    Cole SP, Pinkoski MJ, Bhardwaj G, Deeley RG: Elevated expression of annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line. Br J Cancer 65(4): 498–502, 1992Google Scholar
  102. 102.
    Reeves SA, Chavez-Kappel C, Davis R, Rosenblum M, Israel MA: Developmental regulation of annexin II (Lipocortin 2) in human brain and expression in high grade glioma. Cancer Res 52(24): 6871–6876, 1992Google Scholar
  103. 103.
    Roseman BJ, Bollen A, Hsu J, Lamborn K, Israel MA: Annexin II marks astrocytic brain tumors of high histologicgrade. Oncol Res 6(12): 561–567, 1994Google Scholar
  104. 104.
    Chiang Y, Davis RG, Vishwanatha JK: Altered expression of annexin II in human B-cell lymphoma cell lines. Biochim Biophys Acta 1313(3): 295–301, 1996Google Scholar
  105. 105.
    Yeatman TJ, Updyke TV, Kaetzel MA, Dedman JR, Nicolson GL: Expression of annexins on the surfaces of non-metastaticand metastatic human and rodent tumor cells. Clin Exp Metastasis 11(1): 37–44, 1993Google Scholar
  106. 106.
    Kassam G, Manro A, Braat CE, Louie P, Fitzpatrick SL, Waisman DM: Characterization of the heparin binding properties of annexin II tetramer. J Biol Chem 272(24): 15093–15100, 1997Google Scholar
  107. 107.
    Wirl G, Schwartz-Albiez R: Collagen-binding proteins of mammary epithelial cells are related to Ca2(+)-and phospholipid-binding annexins. J Cell Physiol 144(3): 511–522, 1990Google Scholar
  108. 108.
    Chung CY, Erickson HP: Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol 126(2): 539–548, 1994Google Scholar
  109. 109.
    Kassam G, Choi KS, Ghuman J, Kang HM, Fitzpatrick SL, Zackson T, Zackson S, Toba M, Shinomiya A, Waisman DM: The role of annexin II tetramer in the activation of plasminogen. J Biol Chem 273(8): 4790–4799, 1998Google Scholar
  110. 110.
    Hajjar KA, Jacovina AT, Chacko J: An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. J Biol Chem 269(33): 21191–21197, 1994Google Scholar
  111. 111.
    Sargiacomo M, Sudol M, Tang Z, Lisanti MP: Signal transducing molecules and glycosyl-phosphatidylinositollinked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 122(4): 789–807, 1993Google Scholar
  112. 112.
    Harder T, Gerke V: The annexin II2p11(2) complex is the major protein component of the triton X-100-insoluble low-density fraction prepared from MDCK cells in the presence of Ca2+. Biochim Biophys Acta 1223(3): 375–382, 1994Google Scholar
  113. 113.
    Lipardi C, Mora R, Colomer V, Paladino S, Nitsch L, Rodriguez-Boulan E, Zurzolo C: Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J Cell Biol 140(3): 617–626, 1998Google Scholar
  114. 114.
    Rajjayabun PH, Garg S, Durkan GC, Charlton R, Robinson MC, Mellon JK: Caveolin-1 expression is associated with high-grade bladder cancer. Urology 58(5): 811–814, 2001Google Scholar
  115. 115.
    Yang G, Truong LD, Timme TL, Ren C, Wheeler TM, Park SH, Nasu Y, Bangma CH, Kattan MW, Scardino PT, Thompson TC: Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res 4(8): 1873–1880, 1998Google Scholar
  116. 116.
    Fine SW, Lisanti MP, Galbiati F, Li M: Elevated expression of caveolin-1 in adenocarcinoma of the colon. Am J Clin Pathol 115(5): 719–724, 2001Google Scholar
  117. 117.
    Yang G, Truong LD, Wheeler TM, Thompson TC: Caveolin-1 expression in clinically confined human prostate cancer: A novel prognostic marker. Cancer Res 59(22): 5719–5723, 1999Google Scholar
  118. 118.
    Stahl A, Mueller BM: The urokinase-type plasminogen activator receptor, a GPI-linked protein, is localized in caveolae. J Cell Biol 129(2): 335–344, 1995Google Scholar
  119. 119.
    Annabi B, Lachambre M, Bousquet-Gagnon N, Page M, Gingras D, Beliveau R: Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem J 353(Pt 3): 547–553, 2001Google Scholar
  120. 120.
    Puyraimond A, Fridman R, Lemesle M, Arbeille B, Menashi S: MMP-2 colocalizes with caveolae on the surface of endothelial cells. Exp Cell Res 262(1): 28–36, 2001Google Scholar
  121. 121.
    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 282(Pt 1): 273–278, 1992Google Scholar
  122. 122.
    Visscher DW, Sloane BF, Sameni M, Babiarz JW, Jacobson J, Crissman JD: Clinicopathologic significance Pericellular cathepsin B and malignant progression 285 of cathepsin B immunostaining in transitional neoplasia. Mod Pathol 7(1): 76–81, 1994Google Scholar
  123. 123.
    Khan A, Krishna M, Baker SP, Malhothra R, Banner BF: Cathepsin B expression and its correlation with tumorassociated laminin and tumor progression in gastric cancer. Arch Pathol Lab Med 122(2): 172–177, 1998Google Scholar
  124. 124.
    Sukoh N, Abe S, Ogura S, Isobe H, Takekawa H, Inoue K, Kawakami Y: Immunohistochemical study of cathepsin B. Prognostic significance in human lung cancer. Cancer 74(1): 46–51, 1994Google Scholar
  125. 125.
    Higashiyama M, Doi O, Kodama K, Yokouchi H, Tateishi R: Cathepsin B expression in tumor cells and laminin distribution in pulmonary adenocarcinoma. J Clin Pathol 46(1): 18–22, 1993Google Scholar
  126. 126.
    Sameni M, Dosescu J, Sloane BF: Imaging proteolysis by living human glioma cells. Biol Chem 382(5): 785–788, 2001Google Scholar
  127. 127.
    Sameni M, Moin K, Sloane BF: Imaging proteolysis by living human breast cancer cells. Neoplasia 2(6): 496–504, 2000Google Scholar
  128. 128.
    Mai J, Waisman DM, Sloane BF: Cell surface complex of cathepsin B/annexin II tetramer in malignant progression. Biochim Biophys Acta 1477(1–2): 215–230, 2000Google Scholar
  129. 129.
    Gong Q, Chan SJ, Bajkowski AS, Steiner DF, Frankfater A: Characterization of the cathepsin B gene and multiple mRNAs in human tissues: evidence for alternative splicing of cathepsin B pre-mRNA. DNA Cell Biol 12(4): 299–309, 1993Google Scholar
  130. 130.
    Felbor U, Kessler B, Mothes W, Goebel HH, Ploegh HL., Bronson RT, Olsen BR: Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc Natl Acad Sci USA 99(12): 7883–7888, 2002Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Stefanie Roshy
    • 1
  • Bonnie F. Sloane
    • 1
    • 2
    • 3
  • Kamiar Moin
    • 2
    • 3
  1. 1.Program in Cancer Biology, Barbara Ann Karmanos Cancer InstituteWayne State UniversityDetroitUSA
  2. 2.Proteases and Cancer Program, Barbara Ann Karmanos Cancer InstituteWayne State UniversityDetroit
  3. 3.Department of Pharmacology, Barbara Ann Karmanos Cancer InstituteWayne State UniversityDetroitUSA

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