Functional Compartmentalization of HSP60-Survivin Interaction between Mitochondria and Cytosol in Cancer Cells
Abstract
:1. Introduction
2. HSP60 Functions in Normal and Cancer Cells
2.1. Pro-Survival Function of HSP60 in Mitochondria
2.2. Dual Functions of HSP60 in Cytosol
2.3. Mitochondrial HSP60 Shuttling to the Cytosol in Relationship to Its Functions
3. Survivin in Normal and Cancer Cells
3.1. Pro-Survival Function of Survivin in Mitochondria
3.2. Arguable Dual Function of Cytosolic Survivin
4. HSP60–Survivin Interaction
4.1. Interaction between HSP60 and Survivin in Mitochondria
4.2. Interaction between HSP60 and Survivin in Cytosol
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Castilla, C.; Congregado, B.; Conde, J.M.; Medina, R.; Torrubia, F.J.; Japon, M.A.; Saez, C. Immunohistochemical expression of Hsp60 correlates with tumor progression and hormone resistance in prostate cancer. Urology 2010, 76, 1017.e1–1017.e6. [Google Scholar] [CrossRef] [PubMed]
- Hamelin, C.; Cornut, E.; Poirier, F.; Pons, S.; Beaulieu, C.; Charrier, J.P.; Haidous, H.; Cotte, E.; Lambert, C.; Piard, F.; et al. Identification and verification of heat shock protein 60 as a potential serum marker for colorectal cancer. FEBS J. 2011, 278, 4845–4859. [Google Scholar] [CrossRef] [Green Version]
- Hwang, Y.J.; Lee, S.P.; Kim, S.Y.; Choi, Y.H.; Kim, M.J.; Lee, C.H.; Lee, J.Y.; Kim, D.Y. Expression of heat shock protein 60 kDa is upregulated in cervical cancer. Yonsei Med. J. 2009, 50, 399–406. [Google Scholar] [CrossRef] [Green Version]
- Hjerpe, E.; Egyhazi, S.; Carlson, J.; Stolt, M.F.; Schedvins, K.; Johansson, H.; Shoshan, M.; Avall-Lundqvist, E. HSP60 predicts survival in advanced serous ovarian cancer. Int. J. Gynecol. Cancer 2013, 23, 448–455. [Google Scholar] [CrossRef] [PubMed]
- Li, X.S.; Xu, Q.; Fu, X.Y.; Luo, W.S. Heat shock protein 60 overexpression is associated with the progression and prognosis in gastric cancer. PLoS ONE 2014, 9, e107507. [Google Scholar] [CrossRef] [PubMed]
- Desmetz, C.; Bibeau, F.; Boissiere, F.; Bellet, V.; Rouanet, P.; Maudelonde, T.; Mange, A.; Solassol, J. Proteomics-based identification of HSP60 as a tumor-associated antigen in early stage breast cancer and ductal carcinoma in situ. J. Proteome Res. 2008, 7, 3830–3837. [Google Scholar] [CrossRef] [PubMed]
- Tsai, Y.P.; Yang, M.H.; Huang, C.H.; Chang, S.Y.; Chen, P.M.; Liu, C.J.; Teng, S.C.; Wu, K.J. Interaction between HSP60 and beta-catenin promotes metastasis. Carcinogenesis 2009, 30, 1049–1057. [Google Scholar] [CrossRef]
- Zhou, C.; Sun, H.; Zheng, C.; Gao, J.; Fu, Q.; Hu, N.; Shao, X.; Zhou, Y.; Xiong, J.; Nie, K.; et al. Oncogenic HSP60 regulates mitochondrial oxidative phosphorylation to support Erk1/2 activation during pancreatic cancer cell growth. Cell Death Dis. 2018, 9, 161. [Google Scholar] [CrossRef] [Green Version]
- Ghosh, J.C.; Dohi, T.; Kang, B.H.; Altieri, D.C. Hsp60 regulation of tumor cell apoptosis. J. Biol. Chem. 2008, 283, 5188–5194. [Google Scholar] [CrossRef] [Green Version]
- Ikawa, S.; Weinberg, R.A. An interaction between p21ras and heat shock protein hsp60, a chaperonin. Proc. Natl. Acad. Sci. USA 1992, 89, 2012–2016. [Google Scholar] [CrossRef] [Green Version]
- Kirchhoff, S.R.; Gupta, S.; Knowlton, A.A. Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation 2002, 105, 2899–2904. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.H.; Lin, K.H.; Yu, J.S.; Wu, T.J.; Lee, W.C.; Chao, C.C.; Pan, T.L.; Yeh, C.T. Targeting HSP60 by subcutaneous injections of jetPEI/HSP60-shRNA destabilizes cytoplasmic survivin and inhibits hepatocellular carcinoma growth. Mol. Carcinog. 2018, 57, 1087–1101. [Google Scholar] [CrossRef] [PubMed]
- Tang, H.; Li, J.; Liu, X.; Wang, G.; Luo, M.; Deng, H. Down-regulation of HSP60 Suppresses the Proliferation of Glioblastoma Cells via the ROS/AMPK/mTOR Pathway. Sci. Rep. 2016, 6, 28388. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chun, J.N.; Choi, B.; Lee, K.W.; Lee, D.J.; Kang, D.H.; Lee, J.Y.; Song, I.S.; Kim, H.I.; Lee, S.H.; Kim, H.S.; et al. Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation. PLoS ONE 2010, 5, e9422. [Google Scholar] [CrossRef] [PubMed]
- Samali, A.; Cai, J.; Zhivotovsky, B.; Jones, D.P.; Orrenius, S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J. 1999, 18, 2040–2048. [Google Scholar] [CrossRef] [Green Version]
- Chan, J.Y.; Cheng, H.L.; Chou, J.L.; Li, F.C.; Dai, K.Y.; Chan, S.H.; Chang, A.Y. Heat shock protein 60 or 70 activates nitric-oxide synthase (NOS) I- and inhibits NOS II-associated signaling and depresses the mitochondrial apoptotic cascade during brain stem death. J. Biol. Chem. 2007, 282, 4585–4600. [Google Scholar] [CrossRef] [Green Version]
- Jakic, B.; Buszko, M.; Cappellano, G.; Wick, G. Elevated sodium leads to the increased expression of HSP60 and induces apoptosis in HUVECs. PLoS ONE 2017, 12, e0179383. [Google Scholar] [CrossRef] [Green Version]
- Mita, A.C.; Mita, M.M.; Nawrocki, S.T.; Giles, F.J. Survivin: Key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin. Cancer Res. 2008, 14, 5000–5005. [Google Scholar] [CrossRef] [Green Version]
- Mobahat, M.; Narendran, A.; Riabowol, K. Survivin as a preferential target for cancer therapy. Int. J. Mol. Sci. 2014, 15, 2494–2516. [Google Scholar] [CrossRef]
- Hunter, A.M.; LaCasse, E.C.; Korneluk, R.G. The inhibitors of apoptosis (IAPs) as cancer targets. Apoptosis 2007, 12, 1543–1568. [Google Scholar] [CrossRef]
- Chen, X.; Duan, N.; Zhang, C.; Zhang, W. Survivin and Tumorigenesis: Molecular Mechanisms and Therapeutic Strategies. J. Cancer 2016, 7, 314–323. [Google Scholar] [CrossRef] [PubMed]
- Garg, H.; Suri, P.; Gupta, J.C.; Talwar, G.P.; Dubey, S. Survivin: A unique target for tumor therapy. Cancer Cell Int. 2016, 16, 49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, D.; Hu, C.; Li, H. Survivin as a novel target protein for reducing the proliferation of cancer cells. Biomed. Rep. 2018, 8, 399–406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Y.; Liu, D.; Zhou, Y.; Xie, J.; Lee, R.J.; Cai, Y.; Teng, L. Silencing of Survivin Expression Leads to Reduced Proliferation and Cell Cycle Arrest in Cancer Cells. J. Cancer 2015, 6, 1187–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Z.; Wang, T.; Zhang, Z.; Tang, S.; Feng, S.; Yue, M.; Hu, M.; Xuan, L.; Chen, Y. Survivin downregulation using siRNA nanoliposomes inhibits cell proliferation and promotes the apoptosis of MHCC-97H hepatic cancer cells: An in vitro and in vivo study. Oncol. Lett. 2017, 13, 2723–2730. [Google Scholar] [CrossRef] [Green Version]
- Dohi, T.; Beltrami, E.; Wall, N.R.; Plescia, J.; Altieri, D.C. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J. Clin. Investig. 2004, 114, 1117–1127. [Google Scholar] [CrossRef]
- Angell, H. A study into the potential role of Survivin localization in resistance to drug-induced apoptosis. Biosci. Horiz. 2008, 1, 85–91. [Google Scholar] [CrossRef]
- Arora, V.; Cheung, H.H.; Plenchette, S.; Micali, O.C.; Liston, P.; Korneluk, R.G. Degradation of survivin by the X-linked inhibitor of apoptosis (XIAP)-XAF1 complex. J. Biol. Chem. 2007, 282, 26202–26209. [Google Scholar] [CrossRef] [Green Version]
- Kim, W.; Ryu, J.; Kim, J.E. CCAR2/DBC1 and Hsp60 Positively Regulate Expression of Survivin in Neuroblastoma Cells. Int. J. Mol. Sci. 2019, 20, 131. [Google Scholar] [CrossRef] [Green Version]
- Cappello, F.; Conway de Macario, E.; Marasa, L.; Zummo, G.; Macario, A.J. Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol. Ther. 2008, 7, 801–809. [Google Scholar] [CrossRef]
- Itoh, H.; Komatsuda, A.; Ohtani, H.; Wakui, H.; Imai, H.; Sawada, K.; Otaka, M.; Ogura, M.; Suzuki, A.; Hamada, F. Mammalian HSP60 is quickly sorted into the mitochondria under conditions of dehydration. Eur. J. Biochem. 2002, 269, 5931–5938. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.K.; Kim, K.; Ryu, J.W.; Ryu, T.Y.; Lim, J.H.; Oh, J.H.; Min, J.K.; Jung, C.R.; Hamamoto, R.; Son, M.Y.; et al. The novel prognostic marker, EHMT2, is involved in cell proliferation via HSPD1 regulation in breast cancer. Int. J. Oncol. 2019, 54, 65–76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, F.; Duan, Y.; Yang, F.; Trexler, C.; Wang, H.; Huang, L.; Li, Y.; Tang, H.; Wang, G.; Fang, X.; et al. Deletion of heat shock protein 60 in adult mouse cardiomyocytes perturbs mitochondrial protein homeostasis and causes heart failure. Cell Death Differ. 2019. [CrossRef] [PubMed] [Green Version]
- Cohen-Sfady, M.; Pevsner-Fischer, M.; Margalit, R.; Cohen, I.R. Heat shock protein 60, via MyD88 innate signaling, protects B cells from apoptosis, spontaneous and induced. J. Immunol. 2009, 183, 890–896. [Google Scholar] [CrossRef] [Green Version]
- Xanthoudakis, S.; Roy, S.; Rasper, D.; Hennessey, T.; Aubin, Y.; Cassady, R.; Tawa, P.; Ruel, R.; Rosen, A.; Nicholson, D.W. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J. 1999, 18, 2049–2056. [Google Scholar] [CrossRef] [Green Version]
- Chen, T.H.; Liu, S.W.; Chen, M.R.; Cho, K.H.; Chen, T.Y.; Chu, P.H.; Kao, Y.Y.; Hsu, C.H.; Lin, K.M. Neonatal Death and Heart Failure in Mouse with Transgenic HSP60 Expression. Biomed. Res. Int. 2015, 2015, 539805. [Google Scholar] [CrossRef] [Green Version]
- Shan, Y.X.; Liu, T.J.; Su, H.F.; Samsamshariat, A.; Mestril, R.; Wang, P.H. Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J. Mol. Cell. Cardiol. 2003, 35, 1135–1143. [Google Scholar] [CrossRef]
- Ghosh, J.C.; Siegelin, M.D.; Dohi, T.; Altieri, D.C. Heat shock protein 60 regulation of the mitochondrial permeability transition pore in tumor cells. Cancer Res. 2010, 70, 8988–8993. [Google Scholar] [CrossRef] [Green Version]
- Kalderon, B.; Kogan, G.; Bubis, E.; Pines, O. Cytosolic Hsp60 can modulate proteasome activity in yeast. J. Biol. Chem. 2015, 290, 3542–3551. [Google Scholar] [CrossRef] [Green Version]
- Chandra, D.; Choy, G.; Tang, D.G. Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: Evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J. Biol. Chem. 2007, 282, 31289–31301. [Google Scholar] [CrossRef] [Green Version]
- Dunajova, L.; Cash, E.; Markus, R.; Rochette, S.; Townley, A.R.; Wheatley, S.P. The N-terminus of survivin is a mitochondrial-targeting sequence and Src regulator. J. Cell Sci. 2016, 129, 2707–2712. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wheatley, S.P. The functional repertoire of survivin’s tails. Cell Cycle 2015, 14, 261–268. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoel, A.W.; Yu, P.; Nguyen, K.P.; Sui, X.; Plescia, J.; Altieri, D.C.; Conte, M.S. Mitochondrial heat shock protein-90 modulates vascular smooth muscle cell survival and the vascular injury response in vivo. Am. J. Pathol. 2012, 181, 1151–1157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adrain, C.; Creagh, E.M.; Martin, S.J. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 2001, 20, 6627–6636. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, Z.; Yao, X.; Wu, M. Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J. Biol. Chem. 2003, 278, 23130–23140. [Google Scholar] [CrossRef] [Green Version]
- Park, S.H.; Shin, I.; Kim, N.D. An Inhibitor of the Interaction of Survivin with Smac in Mitochondria Promotes Apoptosis. Chem. Asian J. 2019, 14, 4035–4041. [Google Scholar] [CrossRef]
- Dohi, T.; Xia, F.; Altieri, D.C. Compartmentalized phosphorylation of IAP by protein kinase A regulates cytoprotection. Mol. Cell 2007, 27, 17–28. [Google Scholar] [CrossRef] [Green Version]
- Fortugno, P.; Wall, N.R.; Giodini, A.; O’Connor, D.S.; Plescia, J.; Padgett, K.M.; Tognin, S.; Marchisio, P.C.; Altieri, D.C. Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function. J. Cell Sci. 2002, 115, 575–585. [Google Scholar]
- Beltrami, E.; Plescia, J.; Wilkinson, J.C.; Duckett, C.S.; Altieri, D.C. Acute ablation of survivin uncovers p53-dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J. Biol. Chem. 2004, 279, 2077–2084. [Google Scholar] [CrossRef] [Green Version]
- Tu, S.P.; Liston, P.; Cui, J.T.; Lin, M.C.; Jiang, X.H.; Yang, Y.; Gu, Q.; Jiang, S.H.; Lum, C.T.; Kung, H.F.; et al. Restoration of XAF1 expression induces apoptosis and inhibits tumor growth in gastric cancer. Int. J. Cancer 2009, 125, 688–697. [Google Scholar] [CrossRef]
- Zhu, L.M.; Shi, D.M.; Dai, Q.; Cheng, X.J.; Yao, W.Y.; Sun, P.H.; Ding, Y.; Qiao, M.M.; Wu, Y.L.; Jiang, S.H.; et al. Tumor suppressor XAF1 induces apoptosis, inhibits angiogenesis and inhibits tumor growth in hepatocellular carcinoma. Oncotarget 2014, 5, 5403–5415. [Google Scholar] [CrossRef] [PubMed]
- Best, S.A.; Nwaobasi, A.N.; Schmults, C.D.; Ramsey, M.R. CCAR2 Is Required for Proliferation and Tumor Maintenance in Human Squamous Cell Carcinoma. J. Investig. Dermatol. 2017, 137, 506–512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Restelli, M.; Magni, M.; Ruscica, V.; Pinciroli, P.; De Cecco, L.; Buscemi, G.; Delia, D.; Zannini, L. A novel crosstalk between CCAR2 and AKT pathway in the regulation of cancer cell proliferation. Cell Death Dis. 2016, 7, e2453. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, W.; Cheon, M.G.; Kim, J.E. Mitochondrial CCAR2/DBC1 is required for cell survival against rotenone-induced mitochondrial stress. Biochem. Biophys. Res. Commun. 2017, 485, 782–789. [Google Scholar] [CrossRef]
- Faried, A.; Sohda, M.; Nakajima, M.; Miyazaki, T.; Kato, H.; Kuwano, H. Expression of heat-shock protein Hsp60 correlated with the apoptotic index and patient prognosis in human oesophageal squamous cell carcinoma. Eur. J. Cancer 2004, 40, 2804–2811. [Google Scholar] [CrossRef]
- Zhu, H.; Wang, Q.; Hu, C.; Zhang, W.; Quan, L.; Liu, M.; Xu, N.; Xiao, Z. High expression of survivin predicts poor prognosis in esophageal squamous cell carcinoma following radiotherapy. Tumour Biol. 2011, 32, 1147–1153. [Google Scholar] [CrossRef]
- Zhao, J.; Tenev, T.; Martins, L.M.; Downward, J.; Lemoine, N.R. The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J. Cell Sci. 2000, 113, 4363–4371. [Google Scholar]
- Kelly, R.J.; Lopez-Chavez, A.; Citrin, D.; Janik, J.E.; Morris, J.C. Impacting tumor cell-fate by targeting the inhibitor of apoptosis protein survivin. Mol. Cancer 2011, 10, 35. [Google Scholar] [CrossRef] [Green Version]
- Shen, J.; Liu, J.; Long, Y.; Miao, Y.; Su, M.; Zhang, Q.; Han, H.; Hao, X. Knockdown of survivin expression by siRNAs enhances chemosensitivity of prostate cancer cells and attenuates its tumorigenicity. Acta Biochim. Biophys. Sin. 2009, 41, 223–230. [Google Scholar] [CrossRef] [Green Version]
- Tong, W.W.; Tong, G.H.; Kong, H.; Liu, Y. The tumor promoting roles of HSP60 and HIF2alpha in gastric cancer cells. Tumour Biol. 2016, 37, 9849–9854. [Google Scholar] [CrossRef]
- Zhang, K.; Li, Y.; Liu, W.; Gao, X. Silencing survivin expression inhibits the tumor growth of non-small-cell lung cancer cells in vitro and in vivo. Mol. Med. Rep. 2015, 11, 639–644. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez-Diez, M.; Santamaria, G.; Ortega, A.D.; Cuezva, J.M. Biogenesis and dynamics of mitochondria during the cell cycle: Significance of 3’UTRs. PLoS ONE 2006, 1, e107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Huang, Y.-H.; Yeh, C.-T. Functional Compartmentalization of HSP60-Survivin Interaction between Mitochondria and Cytosol in Cancer Cells. Cells 2020, 9, 23. https://doi.org/10.3390/cells9010023
Huang Y-H, Yeh C-T. Functional Compartmentalization of HSP60-Survivin Interaction between Mitochondria and Cytosol in Cancer Cells. Cells. 2020; 9(1):23. https://doi.org/10.3390/cells9010023
Chicago/Turabian StyleHuang, Ya-Hui, and Chau-Ting Yeh. 2020. "Functional Compartmentalization of HSP60-Survivin Interaction between Mitochondria and Cytosol in Cancer Cells" Cells 9, no. 1: 23. https://doi.org/10.3390/cells9010023