Nuclear cathepsin L activity is required for cell cycle progression of colorectal carcinoma cells

Biochimie

Volumn 122, Issue , 2016, Pages 208-218

  Tamhane, Tripti ^a   Lllukkumbura, Rukshala ^a   Lu, Shiying ^a   Maelandsmo, Gunhild M ^b   Haugen, Mads H ^a,b   Brix, Klaudia ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Colorectal carcinoma; cysteine cathepsins; Trafficking

Indexed keywords

CATHEPSIN L; CYSTATIN B; GREEN FLUORESCENT PROTEIN;

ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CELL CYCLE PROGRESSION; CELL FRACTIONATION; CELL NUCLEUS; CELL SYNCHRONIZATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HCT116 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN FUNCTION; S PHASE CELL CYCLE CHECKPOINT; TISSUE MICROARRAY; ANIMAL; CACO-2 CELL LINE; CELL CYCLE; CELL CYCLE S PHASE; CELL LINE; COLORECTAL TUMOR; CONFOCAL MICROSCOPY; CYTOLOGY; ENDOSOME; ENZYMOLOGY; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; HCT 116 CELL LINE; INTESTINE; LYSOSOME; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CACO-2 CELLS; CATHEPSIN L; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; COLORECTAL NEOPLASMS; ENDOSOMES; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HCT116 CELLS; HUMANS; IMMUNOBLOTTING; INTESTINES; LYSOSOMES; MICROSCOPY, CONFOCAL; S PHASE;

EID: 84957846249     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.09.003     Document Type: Article

References (63)

1. V. Turk, B. Turk, and D. Turk Lysosomal cysteine proteases: facts and opportunities EMBO J. 20 17 2001 4629 4633 10.1093/emboj/20.17.4629
2. K. Brix, A. Dunkhorst, K. Mayer, and S. Jordans Cysteine cathepsins: cellular roadmap to different functions Biochimie 90 2 2008 194 207 10.1016/j.biochi.2007.07.024
3. S. Dauth, M. Arampatzidou, M. Rehders, D.M.T. Yu, D. Fuehrer, and K. Brix Thyroid cathepsin K - roles in physiology and thyroid diseases Clin. Rev. Bone Miner. Metab. 9 2 2011 94 106 10.1007/s12018-011-9093-7
4. V. Turk, V. Stoka, O. Vasiljeva, M. Renko, T. Sun, B. Turk, and D. Turk Cysteine cathepsins: from structure, function and regulation to new frontiers Biochim. Biophys. Acta 1824 1 2012 68 88 10.1016/j.bbapap.2011.10.002
5. K. Brix, C.J. Scott, and M.M.S. Heck Compartmentalization of proteolysis K. Brix, W. Stocker, Proteases: Structure and Function 2013 Springer-Verlag Wien 85 125 http://dx.doi.org/10.1007/978-3-7091-0885-7-3
6. K. Brix, J. McInnes, A. Al-Hashimi, M. Rehders, T. Tamhane, and M.H. Haugen Proteolysis mediated by cysteine cathepsins and legumain-recent advances and cell biological challenges Protoplasma 252 3 2015 755 774 10.1007/s00709-014-0730-0
7. T. Tamhane, M. Arampatzidou, V. Gerganova, M. Tacke, R. Illukkumbura, S. Dauth, N. Schaschke, C. Peters, T. Reinheckel, and K. Brix The activity and localization patterns of cathepsins B and X in cells of the mouse gastrointestinal tract differ along its length Biol. Chem. 395 10 2014 1201 1219 10.1515/hsz-2014-0151
8. K. Mayer, S. Schwartz, M.J. Lentze, J.C. Klaff, and K. Brix Localization of intestinal cathepsins: implications of their actions during post-operative ileus B. Vollmar, XLI Congress of the European Society for Surgical Research 2006 Medimond International Proceedings Rostock, Germany 63 66
9. K. Mayer, M.E. Iolyeva, U. Meyer-Grahle, and K. Brix Intestine-specific expression of green fluorescent protein-tagged cathepsin B: proof-of-principle experiments Biol. Chem. 389 8 2008 1085 1096 10.1515/BC.2008.112
10. A. Vreemann, H. Qu, K. Mayer, L.B. Andersen, M.I. Stefana, S. Wehner, M. Lysson, A.M. Farcas, C. Peters, T. Reinheckel, J. Kalff, and K. Brix Cathepsin B release from rodent intestine mucosa due to mechanical injury results in extracellular matrix damage in early post-traumatic phases Biol. Chem. 390 5-6 2009 481 492 10.1515/BC.2009.055
11. M. Arampatzidou, A. Schutte, G.C. Hansson, P. Saftig, and K. Brix Effects of cathepsin K deficiency on intercellular junction proteins, luminal mucus layers, and extracellular matrix constituents in the mouse colon Biol. Chem. 393 12 2012 1391 1403 10.1515/hsz-2012-0204
12. M.M. Mohamed, and B.F. Sloane Cysteine cathepsins: multifunctional enzymes in cancer Nat. Rev. Cancer 6 10 2006 764 775 10.1038/nrc1949
13. J.A. Joyce, and J.W. Pollard Microenvironmental regulation of metastasis Nat. Rev. Cancer 9 4 2009 239 252 10.1038/nrc2618
14. S. Sullivan, M. Tosetto, D. Kevans, A. Coss, L. Wang, D. O'Donoghue, J. Hyland, K. Sheahan, H. Mulcahy, and J. O'Sullivan Localization of nuclear cathepsin L and its association with disease progression and poor outcome in colorectal cancer Int. J. Cancer 125 1 2009 54 61 10.1002/ijc.24275
15. T. Reinheckel, C. Peters, A. Kruger, B. Turk, and O. Vasiljeva Differential impact of cysteine cathepsins on genetic mouse models of de novo carcinogenesis: cathepsin B as emerging therapeutic target Front. Pharmacol. 3 2012 133 10.3389/fphar.2012.00133
16. B.F. Sloane, K. List, B. Fingleton, and L. Matrisian Proteases in cancer: significance for invasion and metastasis K. Brix, W. Stocker, Proteases: Structure and Function 2013 Springer-Verlag Wien 491 550 http://dx.doi.org/10.1007/978-3-7091-0885-7-15
17. O. Vasiljeva, T. Reinheckel, C. Peters, D. Turk, V. Turk, and B. Turk Emerging roles of cysteine cathepsins in disease and their potential as drug targets Curr. Pharm. Des. 13 4 2007 387 403 http://dx.doi.org/10.2174/138161207780162962
18. O. Vasiljeva, and B. Turk Dual contrasting roles of cysteine cathepsins in cancer progression: apoptosis versus tumour invasion Biochimie 90 2 2008 380 386 10.1016/j.biochi.2007.10.004
19. S. Tedelind, S. Jordans, H. Resemann, G. Blum, M. Bogyo, D. Fuhrer, and K. Brix Cathepsin B trafficking in thyroid carcinoma cells Thyroid. Res. 4 Suppl. 1 2011 S2 10.1186/1756-6614-4-S1-S2
20. A. Gopinathan, G.M. Denicola, K.K. Frese, N. Cook, F.A. Karreth, J. Mayerle, M.M. Lerch, T. Reinheckel, and D.A. Tuveson Cathepsin B promotes the progression of pancreatic ductal adenocarcinoma in mice Gut 61 6 2012 877 884 10.1136/gutjnl-2011-300850
21. B. Goulet, A. Baruch, N.S. Moon, M. Poirier, L.L. Sansregret, A. Erickson, M. Bogyo, and A. Nepveu A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor Mol. Cell 14 2 2004 207 219 http://dx.doi.org/10.1016/S1097-2765(04)00209-6
22. E.M. Duncan, T.L. Muratore-Schroeder, R.G. Cook, B.A. Garcia, J. Shabanowitz, D.F. Hunt, and C.D. Allis Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation Cell 135 2 2008 284 294 10.1016/j.cell.2008.09.055
23. S. Tedelind, K. Poliakova, A. Valeta, R. Hunegnaw, E.L. Yemanaberhan, N. Heldin, J. Kurebayashi, E. Weber, N. Kopitar-Jerala, B. Turk, M. Bogyo, and K. Brix Nuclear cysteine cathepsin variants in thyroid carcinoma cells Biol. Chem. 391 8 2010 923 935 10.1515/BC.2010.109
24. M.H. Haugen, H.T. Johansen, S.J. Pettersen, R. Solberg, K. Brix, K. Flatmark, and G.M. Maelandsmo Nuclear legumain activity in colorectal cancer PLoS One 8 1 2013 e52980 10.1371/journal.pone.0052980
25. T. Tamhane, B.K. Wolters, R. Illukkumbura, G.M. Maelandsmo, M.H. Haugen, and K. Brix Construction of a plasmid coding for green fluorescent protein-tagged cathepsin L and data on expression in colorectal carcinoma cells Data Brief 2015 (submitted for publication)
26. M. Linke, V. Herzog, and K. Brix Trafficking of lysosomal cathepsin B-green fluorescent protein to the surface of thyroid epithelial cells involves the endosomal/lysosomal compartment J. Cell Sci. 115 Pt 24 2002 4877 4889 http://dx.doi.org/10.1242/jcs.00184
27. M. Rehders, B.B. Grosshauser, A. Smarandache, A. Sadhukhan, U. Mirastschijski, J. Kempf, M. Dunne, K. Slenzka, and K. Brix Effects of lunar and mars dust simulants on HaCaT keratinocytes and CHO-K1 fibroblasts Adv. Space Res. 47 7 2011 1200 1213 10.1016/j.asr.2010.11.033
28. E. Shaw, S. Mohanty, A. Colic, V. Stoka, and V. Turk The affinity-labelling of cathepsin S with peptidyl diazomethyl ketones. Comparison with the inhibition of cathepsin L and calpain FEBS Lett. 334 3 1993 340 342 http://dx.doi.org/10.1016/0014-5793(93)80707-2
29. M. Arampatzidou, M. Rehders, S. Dauth, D.M. Yu, S. Tedelind, and K. Brix Imaging of protease functions-current guide to spotting cysteine cathepsins in classical and novel scenes of action in mammalian epithelial cells and tissues Ital. J. Anat. Embryol. 116 1 2011 1 19 http://dx.doi.org/10.13128/IJAE-9633
30. L. Kamentsky, T.R. Jones, A. Fraser, M.A. Bray, D.J. Logan, K.L. Madden, V. Ljosa, C. Rueden, K.W. Eliceiri, and A.E. Carpenter Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software Bioinformatics 27 8 2011 1179 1180 10.1093/bioinformatics/btr095
31. K. Brix, P. Lemansky, and V. Herzog Evidence for extracellularly acting cathepsins mediating thyroid hormone liberation in thyroid epithelial cells Endocrinology 137 5 1996 1963 1974 10.1210/endo.137.5.8612537
32. A.J. Barrett Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates Biochem. J. 187 3 1980 909 912 http://dx.doi.org/10.1042/bj1870909
33. K. Mayer, A. Vreemann, H. Qu, and K. Brix Release of endo-lysosomal cathepsins B, D, and L from IEC6 cells in a cell culture model mimicking intestinal manipulation Biol. Chem. 390 5-6 2009 471 480 10.1515/BC.2009.047
34. D. Bromme, Z. Li, M. Barnes, and E. Mehler Human cathepsin V functional expression, tissue distribution, electrostatic surface potential, enzymatic characterization, and chromosomal localization Biochemistry 38 8 1999 2377 2385 10.1021/bi982175f
35. R. Itoh, S. Kawamoto, W. Adachi, S. Kinoshita, and K. Okubo Genomic organization and chromosomal localization of the human cathepsin L2 gene DNA Res. 6 2 1999 137 140 http://dx.doi.org/10.1093/dnares/6.2.137
36. R.N. Pike, T.H. Coetzer, and C. Dennison Proteolytically active complexes of cathepsin L and a cysteine proteinase inhibitor; purification and demonstration of their formation in vitro Arch. Biochem. Biophys. 294 2 1992 623 629 http://dx.doi.org/10.1016/0003-9861(92)90734-E
37. B. Lenarcic, I. Krizaj, P. Zunec, and V. Turk Differences in specificity for the interactions of stefins A, B and D with cysteine proteinases FEBS Lett. 395 2-3 1996 113 118 http://dx.doi.org/10.1016/0014-5793(96)00984-2
38. M. Abrahamson, M. Alvarez-Fernandez, and C.M. Nathanson Cystatins Biochem. Soc. Symp. 70 2003 179 199
39. S. Magister, and J. Kos Cystatins in immune system J. Cancer 4 1 2013 45 56 10.7150/jca.5044
40. K. Menzel, M. Hausmann, F. Obermeier, K. Schreiter, N. Dunger, F. Bataille, W. Falk, J. Scholmerich, H. Herfarth, and G. Rogler Cathepsins B, L and D in inflammatory bowel disease macrophages and potential therapeutic effects of cathepsin inhibition in vivo Clin. Exp. Immunol. 146 1 2006 169 180 10.1111/j.1365-2249.2006.03188.x
41. S. Ceru, S. Konjar, K. Maher, U. Repnik, I. Krizaj, M. Bencina, M. Renko, A. Nepveu, E. Zerovnik, B. Turk, and N. Kopitar-Jerala Stefin B interacts with histones and cathepsin L in the nucleus J. Biol. Chem. 285 13 2010 10078 10086 10.1074/jbc.M109.034793
42. J.S. Mort, A.D. Recklies, and A.R. Poole Extracellular presence of the lysosomal proteinase cathepsin B in rheumatoid synovium and its activity at neutral pH Arthritis Rheum. 27 5 1984 509 515 http://dx.doi.org/10.1002/art.1780270505
43. D. Turk, M. Podobnik, T. Popovic, N. Katunuma, W. Bode, R. Huber, and V. Turk Crystal structure of cathepsin B inhibited with CA030 at 2.0-A resolution: a basis for the design of specific epoxysuccinyl inhibitors Biochemistry 34 14 1995 4791 4797 http://dx.doi.org/10.1021/bi00014a037
44. F.M. Dehrmann, T.H. Coetzer, R.N. Pike, and C. Dennison Mature cathepsin L is substantially active in the ionic milieu of the extracellular medium Arch. Biochem. Biophys. 324 1 1995 93 98 10.1006/abbi.1995.9924 http://dx.doi.org/10.1016/S1357-2725(96)00152-5
45. J.S. Mort, and D.J. Buttle Cathepsin B Int. J. Biochem. Cell Biol. 29 5 1997 715 720 http://dx.doi.org/10.1016/S1357-2725(96)00152-5
46. B. Turk, I. Dolenc, B. Lenarcic, I. Krizaj, V. Turk, J.G. Bieth, and I. Bjork Acidic pH as a physiological regulator of human cathepsin L activity Eur. J. Biochem. 259 3 1999 926 932 http://dx.doi.org/10.1046/j.1432-1327.1999.00145.x
47. S. Jordans, S. Jenko-Kokalj, N.M. Kuhl, S. Tedelind, W. Sendt, D. Bromme, D. Turk, and K. Brix Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions BMC Biochem. 10 2009 23 10.1186/1471-2091-10-23
48. P.C. Ong, S. McGowan, M.C. Pearce, J.A. Irving, W.T. Kan, S.A. Grigoryev, B. Turk, G.A. Silverman, K. Brix, S.P. Bottomley, J.C. Whisstock, and R.N. Pike DNA accelerates the inhibition of human cathepsin V by serpins J. Biol. Chem. 282 51 2007 36980 36986 10.1074/jbc.M706991200
49. Y.A. Bulynko, L.C. Hsing, R.W. Mason, D.J. Tremethick, and S.A. Grigoryev Cathepsin L stabilizes the histone modification landscape on the Y chromosome and pericentromeric heterochromatin Mol. Cell Biol. 26 11 2006 4172 4184 10.1128/MCB.00135-06
50. B. Goulet, M. Truscott, and A. Nepveu A novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L Biol. Chem. 387 9 2006 1285 1293 10.1515/BC.2006.159
51. J. Dennemarker, T. Lohmuller, J. Mayerle, M. Tacke, M.M. Lerch, L.M. Coussens, C. Peters, and T. Reinheckel Deficiency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis Oncogene 29 11 2010 1611 1621 10.1038/onc.2009.466
52. F. Benavides, C. Perez, J. Blando, O. Contreras, J. Shen, L.M. Coussens, S.M. Fischer, D.F. Kusewitt, J. DiGiovanni, and C.J. Conti Protective role of cathepsin L in mouse skin carcinogenesis Mol. Carcinog. 51 4 2012 352 361 10.1002/mc.20792
53. V. Gocheva, W. Zeng, D. Ke, D. Klimstra, T. Reinheckel, C. Peters, D. Hanahan, and J.A. Joyce Distinct roles for cysteine cathepsin genes in multistage tumorigenesis Genes Dev. 20 5 2006 543 556 10.1101/gad.1407406
54. V. Morin, A. Sanchez, K. Quinones, J.G. Huidobro, C. Iribarren, P. Bustos, M. Puchi, A.M. Geneviere, and M. Imschenetzky Cathepsin L inhibitor I blocks mitotic chromosomes decondensation during cleavage cell cycles of sea urchin embryos J. Cell Physiol. 216 3 2008 790 795 10.1002/jcp.21459
55. V. Morin, A. Sanchez-Rubio, A. Aze, C. Iribarren, C. Fayet, Y. Desdevises, J. Garcia-Huidobro, M. Imschenetzky, M. Puchi, and A.M. Geneviere The protease degrading sperm histones post-fertilization in sea urchin eggs is a nuclear cathepsin L that is further required for embryo development PLoS One 7 11 2012 e46850 10.1371/journal.pone.0046850
56. K. Muntener, R. Zwicky, G. Csucs, J. Rohrer, and A. Baici Exon skipping of cathepsin B: mitochondrial targeting of a lysosomal peptidase provokes cell death J. Biol. Chem. 279 39 2004 41012 41017 10.1074/jbc.M405333200
57. F. Bestvater, C. Dallner, and E. Spiess The C-terminal subunit of artificially truncated human cathepsin B mediates its nuclear targeting and contributes to cell viability BMC Cell Biol. 6 1 2005 16 10.1186/1471-2121-6-16
58. M. Tholen, L.E. Hillebrand, S. Tholen, O. Sedelmeier, S.J. Arnold, and T. Reinheckel Out-of-frame start codons prevent translation of truncated nucleo-cytosolic cathepsin L in vivo Nat. Commun. 5 2014 4931 10.1038/ncomms5931
59. C.J. Luke, S.C. Pak, Y.S. Askew, T.L. Naviglia, D.J. Askew, S.M. Nobar, A.C. Vetica, O.S. Long, S.C. Watkins, D.B. Stolz, R.J. Barstead, G.L. Moulder, D. Bromme, and G.A. Silverman An intracellular serpin regulates necrosis by inhibiting the induction and sequelae of lysosomal injury Cell 130 6 2007 1108 1119 10.1016/j.cell.2007.07.013
60. S.A. Grigoryev, and C.L. Woodcock Chromatin structure in granulocytes. A link between tight compaction and accumulation of a heterochromatin-associated protein (MENT) J. Biol. Chem. 273 5 1998 3082 3089 http://dx.doi.org/10.1074/jbc.273.5.3082
61. J.A. Irving, S.S. Shushanov, R.N. Pike, E.Y. Popova, D. Bromme, T.H. Coetzer, S.P. Bottomley, I.A. Boulynko, S.A. Grigoryev, and J.C. Whisstock Inhibitory activity of a heterochromatin-associated serpin (MENT) against papain-like cysteine proteinases affects chromatin structure and blocks cell proliferation J. Biol. Chem. 277 15 2002 13192 13201 10.1074/jbc.M108460200
62. H. Nishitani, Y. Shiomi, H. Iida, M. Michishita, T. Takami, and T. Tsurimoto CDK inhibitor p21 is degraded by a proliferating cell nuclear antigen-coupled Cul4-DDB1Cdt2 pathway during S phase and after UV irradiation J. Biol. Chem. 283 43 2008 29045 29052 10.1074/jbc.M806045200
63. T. Sperka, J. Wang, and K.L. Rudolph DNA damage checkpoints in stem cells, ageing and cancer Nat. Rev. Mol. Cell Biol. 13 9 2012 579 590 10.1038/nrm3420