Cathepsin B facilitates autophagy-mediated apoptosis in SPARC overexpressed primitive neuroectodermal tumor cells

Cell Death and Differentiation

Volumn 17, Issue 10, 2010, Pages 1529-1539

  Bhoopathi, P ^a   Chetty, C ^a   Gujrati, M ^a   Dinh, D H ^a   Rao, J S ^a   Lakka, S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

apoptosis; autophagy; Bid; cathepsin B; PNET; SPARC

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 3; CASPASE 8; CATHEPSIN B; CATHEPSIN B INHIBITOR; COMPLEMENTARY DNA; CYTOCHROME C; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; OSTEONECTIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME RELEASE; GENE OVEREXPRESSION; MOUSE; NEUROECTODERM TUMOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASE 3; CATHEPSIN B; CYTOCHROMES C; HUMANS; MICE; MICE, NUDE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; NEUROECTODERMAL TUMORS, PRIMITIVE; OSTEONECTIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 77956668302     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2010.28     Document Type: Article

References (49)

1. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290: 1717-1721.
2. Xue L, Fletcher GC, Tolkovsky AM. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 1999; 14: 180-198.
3. Espert L, Denizot M, Grimaldo M, Robert-Hebmann V, Gay B, Varbanov M et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006; 116: 2162-2172.
4. Katayama M, Kawaguchi T, Berger MS, Pieper RO. DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ 2007; 14: 548-558.
5. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
6. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10: 51-64.
7. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005; 120: 237-248.
8. Jin S, DiPaola RS, Mathew R, White E. Metabolic catastrophe as a means to cancer cell death. J Cell Sci 2007; 120: 379-383.
9. DiPaola RS, Dvorzhinski D, Thalasila A, Garikapaty V, Doram D, May M et al. Therapeutic starvation and autophagy in prostate cancer: a new paradigm for targeting metabolism in cancer therapy. Prostate 2008; 68: 1743-1752.
10. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res 2009; 15: 5308-5316.
11. Yiu GK, Chan WY, Ng SW, Chan PS, Cheung KK, Berkowitz RS et al. SPARC (secreted protein acidic and rich in cysteine) induces apoptosis in ovarian cancer cells. Am J Pathol 2001; 159: 609-622.
12. Puolakkainen PA, Brekken RA, Muneer S, Sage EH. Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis. Mol Cancer Res 2004; 2: 215-224.
13. DiMartino JF, Lacayo NJ, Varadi M, Li L, Saraiya C, Ravindranath Y et al. Low or absent SPARC expression in acute myeloid leukemia with MLL rearrangements is associated with sensitivity to growth inhibition by exogenous SPARC protein. Leukemia 2006; 20: 426-432.
14. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
15. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 2001; 61: 439-444.
16. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004; 36: 2491-2502.
17. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-5728.
18. Yousefi S, Perozzo R,SchmidI, Ziemiecki A,SchaffnerT,ScapozzaLet al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-1132.
19. Seglen PO, Gordon PB. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 1982; 79: 1889-1892.
20. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001; 2: 589-598.
21. Salvesen GS. A lysosomal protease enters the death scene. J Clin Invest 2001; 107: 21-22.
22. Guicciardi ME, Miyoshi H, Bronk SF, Gores GJ. Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am J Pathol 2001; 159: 2045-2054.
23. Cirman T, Oresic K, Mazovec GD, Turk V, Reed JC, Myers RM et al. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 2004; 279: 3578-3587.
24. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94: 481-490.
25. Ding Q, Grammer JR, Nelson MA, Guan JL, Stewart Jr JE, Gladson CL. p27Kip1 and cyclin D1 are necessary for focal adhesion kinase regulation of cell cycle progression in glioblastoma cells propagated in vitro and in vivo in the scid mouse brain. J Biol Chem 2005; 280: 6802-6815.
26. Gorski SM, Chittaranjan S, Pleasance ED, Freeman JD, Anderson CL, Varhol RJ et al. A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 2003; 13: 358-363.
27. Herman-Antosiewicz A, Johnson DE, Singh SV. Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res 2006; 66: 5828-5835.
28. Kanzawa T, Ito H, Kondo Y, Kondo S. Current and future gene therapy for malignant gliomas. J Biomed Biotechnol 2003; 2003: 25-34.
29. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117: 2805-2812.
30. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3: 452-460.
31. Scott RC, Juhasz G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 2007; 17: 1-11.
32. Yu L, Lenardo MJ, Baehrecke EH. Autophagy and caspases: a new cell death program. Cell Cycle 2004; 3: 1124-1126.
33. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112: 1809-1820.
34. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-1075.
35. Chen Y, Millan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008; 15: 171-182.
36. Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C et al. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest 2000; 106: 1127-1137.
37. Werneburg NW, Guicciardi ME, Bronk SF, Gores GJ. Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent. Am J Physiol Gastrointest Liver Physiol 2002; 283: G947-G956.
38. Tang MJ, Tai IT. A novel interaction between procaspase 8 and SPARC enhances apoptosis and potentiates chemotherapy sensitivity in colorectal cancers. J Biol Chem 2007; 282: 34457-34467.
39. Lotem J, Peled-Kamar M, Groner Y, Sachs L. Cellular oxidative stress and the control of apoptosis by wild-type p53, cytotoxic compounds, and cytokines. Proc Natl Acad Sci USA 1996; 93: 9166-9171.
40. Hill IE, Preston E, Monette R, MacManus JP. A comparison of cathepsin B processing and distribution during neuronal death in rats following global ischemia or decapitation necrosis. Brain Res 1997; 751: 206-216.
41. Turk B, Stoka V,Rozman-PungercarJ, Cirman T, Droga-Mazovec G, Oresic K et al. Apoptotic pathways: involvement of lysosomal proteases. Biol Chem 2002; 383: 1035-1044.
42. Williams MS, Henkart PA. Apoptotic cell death induced by intracellular proteolysis. J Immunol 1994; 153: 4247-4255.
43. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, DeVos K, Totty N et al. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett 1998; 438: 150-158.
44. Mohan PM, Barve M, Chatterjee A, Hosur RV. pH driven conformational dynamics and dimer-to-monomer transition in DLC8. Protein Sci 2006; 15: 335-342.
45. Bhoopathi P, Chetty C, Kunigal S, Vanamala SK, Rao JS, Lakka SS. Blockade of tumor growth due to matrix metalloproteinase-9 inhibition is mediated by sequential activation of beta1-integrin, ERK, and NF-kappaB. J Biol Chem 2008; 283: 1545-1552.
46. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159.
47. Healy E, Dempsey M, Lally C, Ryan MP. Apoptosis and necrosis: mechanisms of cell death induced by cyclosporine A in a renal proximal tubular cell line. Kidney Int 1998; 54: 1955-1966.
48. Ha SD, Martins A, Khazaie K, Han J, Chan BM, Kim SO. Cathepsin B is involved in the trafficking of TNF-alpha-containing vesicles to the plasma membrane in macrophages. J Immunol 2008; 181: 690-697.
49. Lal S, Lacroix M, Tofilon P, Fuller GN, Sawaya R, Lang FF. An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg 2000; 92: 326-333.