Browse > Article
http://dx.doi.org/10.1007/s10059-009-0079-y

The Heat Shock Protein 27 (Hsp27) Operates Predominantly by Blocking the Mitochondrial-Independent/Extrinsic Pathway of Cellular Apoptosis  

Tan, Cheau Yih (Department of Bioengineering, Hanyang University)
Ban, Hongseok (Department of Bioengineering, Hanyang University)
Kim, Young-Hee (Department of Bioengineering, Hanyang University)
Lee, Sang-Kyung (Department of Bioengineering, Hanyang University)
Publication Information
Molecules and Cells / v.27, no.5, 2009 , pp. 533-538 More about this Journal
Abstract
Heat shock protein 27 (Hsp27) is a molecular chaperone protein which regulates cell apoptosis by interacting directly with the caspase activation components in the apoptotic pathways. With the assistance of the Tat protein transduction domain we directly delivered the Hsp27 into the myocardial cell line, H9c2 and demonstrate that this protein can reverse hypoxia-induced apoptosis of cells. In order to characterize the contribution of Hsp27 in blocking the two major apoptotic pathways operational within cells, we exposed H9c2 cells to staurosporine and cobalt chloride, agents that induce mitochondria-dependent (intrinsic) and -independent (extrinsic) pathways of apoptosis in cells respectively. The Tat-Hsp27 fusion protein showed a greater propensity to inhibit the effect induced by the cobalt chloride treatment. These data suggest that the Hsp27 predominantly exerts its protective effect by interfering with the components of the extrinsic pathway of apoptosis.
Keywords
apoptosis; cobalt chloride; extrinsic apoptosis; Fas-mediated apoptosis; heat shock protein 27; intrinsic apoptosis; mitochondria-dependent apoptosis; protein transduction domain; staurosporine; Tat peptide;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 7  (Related Records In Web of Science)
연도 인용수 순위
1 Ashkenazi, A. (2002). Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2, 420-430   DOI   PUBMED   ScienceOn
2 Bruey, J.M., Ducasse, C., Bonniaud, P., Ravagnan, L., Susin, S.A., Diaz-Latoud, C., Gurbuxani, S., Arrigo, A.P., Kroemer, G., Solary, E.I=et al. (2000). Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2, 645-652   DOI   ScienceOn
3 Ferns, G., Shams, S., and Shafi, S. (2006). Heat shock protein 27: its potential role in vascular disease. Int. J. Exp. Pathol.87, 253-274   DOI   ScienceOn
4 Fittipaldi, A., Ferrari, A., Zoppe, M., Arcangeli, C., Pellegrini, V., Beltram, F., and Giacca, M. (2003). Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem. 278, 34141-34149
5 Garrido, C., Bruey, J.M., Fromentin, A., Hammann, A., Arrigo, A.P., and Solary, E. (1999). HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 13, 2061-2070   DOI
6 Gustafsson, A.B., Sayen, M.R., Williams, S.D., Crow, M.T., and Gottlieb, R.A. (2002). TAT protein transduction into isolated perfused hearts: TAT-apoptosis repressor with caspase recruitment domain is cardioprotective. Circulation 106, 735-739   DOI   PUBMED
7 Jung, J.Y., and Kim, W.J. (2004). Involvement of mitochondrial- and Fas-mediated dual mechanism in $CoCl_2$-induced apoptosis of rat PC12 cells. Neurosci. Lett 371, 85-90   DOI   PUBMED   ScienceOn
8 Kumar, P., Krishna, V.D., Sulochana, P., Nirmala, G., Haridattatreya, M., and Satchidanandam, V. (2004). Cell-mediated immune responses in healthy children with a history of subclinical infection with Japanese encephalitis virus: analysis of CD4+ and CD8+ T cell target specificities by intracellular delivery of viral proteins using the human immunodeficiency virus Tat protein transduction domain. J. Gen. Virol. 85, 471-482   DOI   PUBMED   ScienceOn
9 Kwon, J.H., Kim, J.B., Lee, K.H., Kang, S.M., Chung, N., Jang, Y., and Chung, J.H. (2007). Protective effect of heat shock protein 27 using protein transduction domain-mediated delivery on ischemia/reperfusion heart injury. Biochem. Biophys. Res. Commun. 363, 399-404   DOI   ScienceOn
10 Li, H., Zhu, H., Xu, C.J., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501   DOI   ScienceOn
11 Li, Z.X., Ouyang, K.Q., Jiang, X., Wang, D., and Hu, Y. (2009). Curcumin induces apoptosis and inhibits growth of human Burkitt's lymphoma in xenograft mouse model. Mol. Cells 27, 283-289   DOI   ScienceOn
12 Schwarze, S.R., Ho, A., Vocero-Akbani, A., and Dowdy, S.F. (1999). In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285, 1569-1572   DOI   PUBMED   ScienceOn
13 Mai, J.C., Shen, H., Watkins, S.C., Cheng, T., and Robbins, P.D. (2002). Efficiency of protein transduction is cell type-dependent and is enhanced by dextran sulfate. J. Biol. Chem. 277, 30208-30218   DOI   ScienceOn
14 Mayorga, M., Bahi, N., Ballester, M., Comella, J.X., and Sanchis, D. (2004). Bcl-2 is a key factor for cardiac fibroblast resistance to programmed cell death. J. Biol. Chem. 279, 34882-34889   DOI   ScienceOn
15 Radford, N.B., Fina, M., Benjamin, I.J., Moreadith, R.W., Graves, K.H., Zhao, P., Gavva, S., Wiethoff, A., Sherry, A.D., Malloy, C.R.I= et al. (1996). Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc. Natl. Acad. Sci. USA 93, 2339-2342   DOI   ScienceOn
16 Zou, W., Yan, M., Xu, W., Huo, H., Sun, L., Zheng, Z., and Liu, X. (2001). Cobalt chloride induces PC12 cells apoptosis through reactive oxygen species and accompanied by AP-1 activation. J. Neurosci. Res. 64, 646-653   DOI   ScienceOn
17 Paul, C., Manero, F., Gonin, S., Kretz-Remy, C., Virot, S., and Arrigo, A.P. (2002). Hsp27 as a negative regulator of cytochrome C release. Mol. Cell Biol. 22, 816-834   DOI   ScienceOn
18 Ehrnsperger, M., Graber, S., Gaestel, M., and Buchner, J. (1997). Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16, 221-229   DOI   ScienceOn
19 Yu, W.R., Liu, T., Fehlings, T.K., and Fehlings, M.G. (2009). Involvement of mitochondrial signaling pathways in the mechanism of Fas-mediated apoptosis after spinal cord injury. Eur. J. Neurosci. 29, 114-1131   DOI   ScienceOn
20 Clark, J.I., and Muchowski, P.J. (2000). Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 10, 52-59   DOI   ScienceOn
21 Wadia, J.S., and Dowdy, S.F. (2003). Modulation of cellular function by TAT mediated transduction of full length proteins. Curr. Protein Pept. Sci. 4, 97-104   DOI   ScienceOn
22 Arya, R., Mallik, M., and Lakhotia, S.C. (2007). Heat shock genesintegrating cell survival and death. J. Biosci.32, 595-610   DOI   ScienceOn
23 Yue, T.L., Wang, C., Romanic, A.M., Kikly, K., Keller, P., DeWolf, W.E., Jr., Hart, T.K., Thomas, H.C., Storer, B., Gu, J.L., et al. (1998). Staurosporine-induced apoptosis in cardiomyocytes: A potential role of caspase-3. J. Mol. Cell. Cardiol. 30, 495-507   DOI   ScienceOn
24 Richard, J.P., Melikov, K., Brooks, H., Prevot, P., Lebleu, B., and Chernomordik, L.V. (2005). Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem. 280, 15300-15306   DOI   ScienceOn
25 Chauhan, A., Tikoo, A., Kapur, A.K., and Singh, M. (2007). The taming of the cell penetrating domain of the HIV Tat: myths and realities. J. Control Release 117, 148-162   DOI   ScienceOn
26 Concannon, C.G., Gorman, A.M., and Samali, A. (2003). On the role of Hsp27 in regulating apoptosis. Apoptosis 8, 61-70   DOI   ScienceOn
27 Pandey, P., Farber, R., Nakazawa, A., Kumar, S., Bharti, A., Nalin, C., Weichselbaum, R., Kufe, D., and Kharbanda, S. (2000). Hsp27 functions as a negative regulator of cytochrome c-dependent activation of procaspase-3. Oncogene 19, 1975-1981   DOI   ScienceOn
28 Delogu, G., Signore, M., Mechelli, A., and Famularo, G. (2002). Heat shock proteins and their role in heart injury. Curr. Opin. Crit. Care 8, 411-416   DOI   ScienceOn
29 Columbaro, M., Mattioli, E., Lattanzi, G., Rutigliano, C., Ognibene, A., Maraldi, N.M., and Squarzoni, S. (2001). Staurosporine treatment and serum starvation promote the cleavage of emerin in cultured mouse myoblasts: involvement of a caspase-dependent mechanism. FEBS Lett. 509, 423-429   DOI   ScienceOn
30 Futaki, S., Goto, S., and Sugiura, Y. (2003). Membrane permeability commonly shared among arginine-rich peptides. J. Mol. Recognit 16, 260-264   DOI   ScienceOn
31 Derossi, D., Joliot, A.H., Chassaing, G., and Prochiantz, A. (1994). The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269, 10444-10450
32 Gewies, A. (2003). Introduction to apoptosis. ApoReview, 1-26
33 Kim, D.T., Mitchell, D.J., Brockstedt, D.G., Fong, L., Nolan, G.P., Fathman, C.G., Engleman, E.G., and Rothbard, J.B. (1997). Introduction of soluble proteins into the MHC class I pathway by conjugation to an HIV tat peptide. J. Immunol. 159, 1666-1668
34 Lecoq, A., Moine, G., Bellanger, L., Drevet, P., Thai, R., Lajeunesse, E., Menez, A., and Leonetti, M. (2008). Increasing the humoral immunogenic properties of the HIV-1 Tat protein using a ligandstabilizing strategy. Vaccine 26, 2615-2626   DOI   ScienceOn
35 Martin, J.L., Mestril, R., Hilal-Dandan, R., Brunton, L.L., and Dillmann, W.H. (1997). Small heat shock proteins and protection against ischemic injury in cardiac myocytes. Circulation 96, 4343-4348   DOI   PUBMED   ScienceOn
36 Concannon, C.G., Orrenius, S., and Samali, A. (2001). Hsp27 inhibits cytochrome c-mediated caspase activation by sequestering both pro-caspase-3 and cytochrome c. Gene Exp.9, 195-201   DOI   PUBMED
37 Jung, J.Y., Mo, H.C., Yang, K.H., Jeong, Y.J., Yoo, H.G., Choi, N.K., Oh, W.M., Oh, H.K., Kim, S.H., Lee, J.H.I=et al. (2007). Inhibition by epigallocatechin gallate of CoCl2-induced apoptosis in rat PC12 cells. Life Sci. 80, 1355-1363   DOI   ScienceOn
38 Hotchkiss, R.S., McConnell, K.W., Bullok, K., Davis, C.G., Chang, K.C., Schwulst, S.J., Dunne, J.C., Dietz, G.P., Bahr, M., McDunn, J.E.I= et al. (2006). TAT-BH4 and TAT-Bcl-xL peptides protect against sepsis-induced lymphocyte apoptosis in vivo. J. Immunol 176, 5471-5477   DOI
39 Kumar, P., Wu, H., McBride, J.L., Jung, K.E., Kim, M.H., Davidson, B.L., Lee, S.K., Shankar, P., and Manjunath, N. (2007). Transvascular delivery of small interfering RNA to the central nervous system. Nature 448, 39-43   DOI   ScienceOn
40 Arakawa, M., Yasutake, M., Miyamoto, M., Takano, T., Asoh, S., and Ohta, S. (2007). Transduction of anti-cell death protein FNK protects isolated rat hearts from myocardial infarction induced by ischemia/reperfusion. Life Sci.80, 2076-2084   DOI   ScienceOn
41 Kim, T.G., Befus, N., and Langridge, W.H. (2004). Co-immunization with an HIV-1 Tat transduction peptide-rotavirus enterotoxin fusion protein stimulates a Th1 mucosal immune response in mice. Vaccine 22, 431-438   DOI   ScienceOn
42 Chandel, N.S., Maltepe, E., Goldwasser, E., Mathieu, C.E., Simon, M.C., and Schumacker, P.T. (1998). Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95, 11715-11720   DOI   ScienceOn
43 Kim, S.G., Park, M.Y., Kim, C.H., Sohn, H.J., Kim, H.S., Park, J.S., Kim, H.J., Oh, S.T., and Kim, T.G. (2008). Modification of CEA with both CRT and TAT PTD induces potent anti-tumor immune responses in RNA-pulsed DC vaccination. Vaccine 26, 6433-6440   DOI   ScienceOn
44 Slee, E.A., Harte, M.T., Kluck, R.M., Wolf, B.B., Casiano, C.A., Newmeyer, D.D., Wang, H.G., Reed, J.C., Nicholson, D.W., Alnemri, E.S., et al. (1999). Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144, 281-292   DOI   ScienceOn
45 Trost, S.U., Omens, J.H., Karlon, W.J., Meyer, M., Mestril, R., Covell, J.W., and Dillmann, W.H. (1998). Protection against myocardial dysfunction after a brief ischemic period in transgenic mice expressing inducible heat shock protein 70. J. Clin. Invest. 101, 855-862   DOI   ScienceOn
46 Whitlock, N.A., Lindsey, K., Agarwal, N., Crosson, C.E., and Ma, J.X. (2005). Heat shock protein 27 delays Ca2+-induced cell death in a caspase-dependent and -independent manner in rat retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46, 1085-1091   DOI   ScienceOn
47 Shaw, P.A., Catchpole, I.R., Goddard, C.A., and Colledge, W.H. (2008). Comparison of protein transduction domains in mediating cell delivery of a secreted CRE protein. Biochemistry 47, 1157-1166   DOI   ScienceOn
48 Latchman, D.S. (2005). HSP27 and cell survival in neurones. Int. J. Hyperthermia 21, 393-402   DOI   ScienceOn
49 Prochiantz, A. (2000). Messenger proteins: homeoproteins, TAT and others. Curr. Opin. Cell Biol. 12, 400-406   DOI   PUBMED   ScienceOn
50 Charette, S.J., Lavoie, J.N., Lambert, H., and Landry, J. (2000). Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol. Cell. Biol. 20, 7602-7612   DOI   ScienceOn
51 Sartorius, U., Schmitz, I., and Krammer, P.H. (2001). Molecular mechanisms of death-receptor-mediated apoptosis. Chembiochem 2, 20-29   DOI   ScienceOn
52 Zhao, M., and Weissleder, R. (2004). Intracellular cargo delivery using tat peptide and derivatives. Med. Res. Rev. 24, 1-12   DOI   ScienceOn
53 Garrido, C. (2002). Size matters: of the small HSP27 and its large oligomers. Cell Death Differ. 9, 483-485   DOI   PUBMED   ScienceOn
54 Wadia, J.S., and Dowdy, S.F. (2005). Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Adv. Drug Deliv. Rev. 57, 579-596   DOI   ScienceOn