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Toxoplasma gondii Hsp90: potential roles in essential cellular processes of the parasite

Published online by Cambridge University Press:  21 February 2014

SERGIO O. ANGEL ,
MARIA J. FIGUERAS ,
MARIA L. ALOMAR ,
PABLO C. ECHEVERRIA  and
BIN DENG
SERGIO O. ANGEL*
Affiliation:
Laboratorio de Parasitología Molecular, IIB-INTECH, CONICET-UNSAM, Av. Intendente Marino Km. 8·2, C.C 164, (B7130IIWA), Chascomús, Prov. Buenos Aires, Argentina
MARIA J. FIGUERAS
Affiliation:
Laboratorio de Parasitología Molecular, IIB-INTECH, CONICET-UNSAM, Av. Intendente Marino Km. 8·2, C.C 164, (B7130IIWA), Chascomús, Prov. Buenos Aires, Argentina
MARIA L. ALOMAR
Affiliation:
Laboratorio de Parasitología Molecular, IIB-INTECH, CONICET-UNSAM, Av. Intendente Marino Km. 8·2, C.C 164, (B7130IIWA), Chascomús, Prov. Buenos Aires, Argentina
PABLO C. ECHEVERRIA
Affiliation:
Département de Biologie Cellulaire Université de Genève Sciences III, Geneva, Switzerland
BIN DENG
Affiliation:
Biology Department, Vermont Genetics Network Proteomics Facility, The University of Vermont, 337 marsh Life Science Building, 109 Carrigan Drive, Burlington, VT 05405, USA
*
*Corresponding author. Laboratorio de Parasitología Molecular, IIB-INTECH, CONICET-UNSAM, Av. Intendente Marino Km. 8·2, C.C 164, (B7130IIWA), Chascomús, Prov. Buenos Aires, Argentina. E-mail: sangel@intech.gov.ar
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Summary

Hsp90 is a widely distributed and highly conserved molecular chaperone that is ubiquitously expressed throughout nature, being one of the most abundant proteins within non-stressed cells. This chaperone is up-regulated following stressful events and has been involved in many cellular processes. In Toxoplasma gondii, Hsp90 could be linked with many essential processes of the parasite such as host cell invasion, replication and tachyzoite-bradyzoite interconversion. A Protein-Protein Interaction (PPI) network approach of TgHsp90 has allowed inferring how these processes may be altered. In addition, data mining of T. gondii phosphoproteome and acetylome has allowed the generation of the phosphorylation and acetylation map of TgHsp90. This review focuses on the potential roles of TgHsp90 in parasite biology and the analysis of experimental data in comparison with its counterparts in yeast and humans.

Keywords

Toxoplasma gondiiHsp90cell cyclepost-translational modificationdevelopment
Type
Special Issue Article
Information
Parasitology , Volume 141 , Special Issue 9: Heat shock proteins as drug targets in infectious diseases , August 2014 , pp. 1138 - 1147
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Ahn, H. J., Kim, S. and Nam, W. (2003). Molecular cloning of the 82-kDa heat shock protein (HSP90) of Toxoplasma gondii associated with the entry into and growth in host cells. Biochemical and Biophysical Research Communication 311, 654–659.Google Scholar
Angel, S. O., Matrajt, M. and Echeverria, P. C. (2013). A review of recent patents on the protozoan parasite HSP90 as a drug target. Recent Patent on Biotechnology 7, 2–8.CrossRefGoogle ScholarPubMed
Bedin, M., Catelli, M. G., Cabanie, L., Gaben, A. M. and Mester, J. (2009). Indirect participation of Hsp90 in the regulation of the cyclin E turnover. Biochemical Pharmacology 77, 151–158.Google Scholar
Behnke, M. S., Wootton, J. C., Lehmann, M. M., Radke, J. B., Lucas, O., Nawas, J., Sibley, L. D. and White, M. W. (2010). Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii . PLoS One 5, e12354.Google Scholar
Bogumil, D. and Dagan, T. (2012). Cumulative impact of chaperone-mediated folding on genome evolution. Biochemistry 51, 9941–9953.Google Scholar
Bohne, W., Heesemann, J. and Gross, U. (1994). Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infection and Immunity 62, 1761–1767.Google Scholar
Burrows, F., Zhang, H. and Kamal, A. (2004). Hsp90 activation and cell cycle regulation. Cell Cycle 3, 1530–1536.Google Scholar
Carlier, Y., Truyens, C., Deloron, P. and Peyron, F. (2012). Congenital parasitic infections: a review. Acta Tropica 121, 55–70.Google Scholar
Carruthers, V. and Boothroyd, J. C. (2007). Pulling together: an integrated model of Toxoplasma cell invasion. Current Opinion in Microbiology 10, 83–89.CrossRefGoogle ScholarPubMed
Catlett, M. G. and Kaplan, K. B. (2006). Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. Journal of Biological Chemistry 281, 33739–33748.CrossRefGoogle ScholarPubMed
Croken, M. M., Nardelli, S. C. and Kim, K. (2012). Chromatin modifications, epigenetics, and how protozoan parasites regulate their lives. Trends in Parasitology 28, 202–213.Google Scholar
Dalmasso, M. C., Sullivan, W. J. Jr. and Angel, S. O. (2011). Canonical and variant histones of protozoan parasites. Frontiers in Bioscience (Landmark Ed) 16, 2086–2105.Google Scholar
Dubey, J. P., Miller, N. L. and Frenkel, J. K. (1970). Toxoplasma gondii life cycle in cats. Journal of the American Veterinary Medical Association 157, 1767–1770.Google Scholar
Dubey, J. P., Lindsay, D. S. and Speer, C. A. (1998). Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267–299.Google Scholar
Dzierszinski, F., Nishi, M., Ouko, L. and Roos, D. S. (2004). Dynamics of Toxoplasma gondii differentiation. Eukaryotic Cell 3, 992–1003.Google Scholar
Echeverria, P. C., Matrajt, M., Harb, O. S., Zappia, M. P., Costas, M. A., Roos, D. S., Dubremetz, J. F. and Angel, S. O. (2005). Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. Journal of Molecular Biology 350, 723–734.Google Scholar
Echeverria, P. C., Figueras, M. J., Vogler, M., Kriehuber, T., de Miguel, N., Deng, B., Dalmasso, M. C., Matthews, D. E., Matrajt, M., Haslbeck, M., Buchner, J. and Angel, S. O. (2010). The Hsp90 co-chaperone p23 of Toxoplasma gondii: identification, functional analysis and dynamic interactome determination. Molecular and Biochemical Parasitology 172, 129–140.Google Scholar
Echeverria, P. C., Bernthaler, A., Dupuis, P., Mayer, B. and Picard, D. (2011). An interaction network predicted from public data as a discovery tool: application to the Hsp90 molecular chaperone machine. PLoS One 6, e26044.Google Scholar
Figueras, M. J., Martin, O. A., Echeverria, P. C., de Miguel, N., Naguleswaran, A., Sullivan, W. J. Jr., Corvi, M. M. and Angel, S. O. (2012). Toxoplasma gondii Sis1-like J-domain protein is a cytosolic chaperone associated to HSP90/HSP70 complex. International Journal for Biological Macromolecules 50, 725–733.Google Scholar
Gubbels, M. J., White, M. and Szatanek, T. (2008). The cell cycle and Toxoplasma gondii cell division: tightly knit or loosely stitched? International Journal of Parasitology 38, 1343–1358.CrossRefGoogle ScholarPubMed
Haarberg, H. E., Paraiso, K. H., Wood, E., Rebecca, V. W., Sondak, V. K., Koomen, J. M. and Smalley, K. S. (2013). Inhibition of Wee1, AKT, and CDK4 underlies the efficacy of the HSP90 inhibitor XL888 in an in vivo model of NRAS-mutant melanoma. Molecular Cancer Therapeutics 12, 901–912.Google Scholar
Halonen, S. K. and Weiss, L. M. (2013). Toxoplasmosis. Handbook of Clinical Neurology 114, 125–145.Google Scholar
Jackson, S. E. (2013). Hsp90: structure and function. Topics in Current Chemistry 328, 155–240.Google Scholar
Jeffers, V. and Sullivan, W. J. Jr. (2012). Lysine acetylation is widespread on proteins of diverse function and localization in the protozoan parasite Toxoplasma gondii . Eukaryotic Cell 11, 735–742.Google Scholar
Konrad, C., Queener, S. F., Wek, R. C. and Sullivan, W. J. Jr. (2013). Inhibitors of eIF2alpha dephosphorylation slow replication and stabilize latency in Toxoplasma gondii . Antimicrobial Agents and Chemotherapy 57, 1815–1822.Google Scholar
Kovacs, J. J., Murphy, P. J., Gaillard, S., Zhao, X., Wu, J. T., Nicchitta, C. V., Yoshida, M., Toft, D. O., Pratt, W. B. and Yao, T. P. (2005). HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Molecular Cell 18, 601–607.Google Scholar
Li, J. and Buchner, J. (2013). Structure, function and regulation of the hsp90 machinery. Biomedical Journal 36, 106–117.Google Scholar
Li, J., Soroka, J. and Buchner, J. (2012). The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochimica et Biophysica Acta 1823, 624–635.Google Scholar
Liwak, U. and Ananvoranich, S. (2009). Toxoplasma gondii: over-expression of lactate dehydrogenase enhances differentiation under alkaline conditions. Experimental Parasitology 122, 155–161.Google Scholar
Lourido, S., Tang, K. and Sibley, L. D. (2012). Distinct signalling pathways control Toxoplasma egress and host-cell invasion. EMBO Journal 31, 4524–4534.Google Scholar
Makhnevych, T. and Houry, W. A. (2012). The role of Hsp90 in protein complex assembly. Biochimica et Biophysica Acta 1823, 674–682.Google Scholar
Martinez-Ruiz, A., Villanueva, L., Gonzalez de Orduna, C., Lopez-Ferrer, D., Higueras, M. A., Tarin, C., Rodriguez-Crespo, I., Vazquez, J. and Lamas, S. (2005). S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proceedings of the National Academy of Sciences USA 102, 8525–8530.Google Scholar
McClellan, A. J., Xia, Y., Deutschbauer, A. M., Davis, R. W., Gerstein, M. and Frydman, J. (2007). Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131, 121–135.Google Scholar
Meissner, M. and Soldati, D. (2005). The transcription machinery and the molecular toolbox to control gene expression in Toxoplasma gondii and other protozoan parasites. Microbes and Infection 7, 1376–1384.Google Scholar
Miman, O., Mutlu, E. A., Ozcan, O., Atambay, M., Karlidag, R. and Unal, S. (2010). Is there any role of Toxoplasma gondii in the etiology of obsessive-compulsive disorder? Psychiatry Research 177, 263–265.Google Scholar
Mimnaugh, E. G., Worland, P. J., Whitesell, L. and Neckers, L. M. (1995). Possible role for serine/threonine phosphorylation in the regulation of the heteroprotein complex between the hsp90 stress protein and the pp60v-src tyrosine kinase. Journal of Biological Chemistry 270, 28654–28659.Google Scholar
Mollapour, M. and Neckers, L. (2012). Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochimica et Biophysica Acta 1823, 648–655.Google Scholar
Mollapour, M., Tsutsumi, S., Donnelly, A. C., Beebe, K., Tokita, M. J., Lee, M. J., Lee, S., Morra, G., Bourboulia, D., Scroggins, B. T., Colombo, G., Blagg, B. S., Panaretou, B., Stetler-Stevenson, W. G., Trepel, J. B., Piper, P. W., Prodromou, C., Pearl, L. H. and Neckers, L. (2010 a). Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Molecular Cell 37, 333–343.CrossRefGoogle ScholarPubMed
Mollapour, M., Tsutsumi, S. and Neckers, L. (2010 b). Hsp90 phosphorylation, Wee1 and the cell cycle. Cell Cycle 9, 2310–2316.Google Scholar
Mollapour, M., Tsutsumi, S., Kim, Y. S., Trepel, J. and Neckers, L. (2011 a). Casein kinase 2 phosphorylation of Hsp90 threonine 22 modulates chaperone function and drug sensitivity. Oncotarget 2, 407–417.Google Scholar
Mollapour, M., Tsutsumi, S., Truman, A. W., Xu, W., Vaughan, C. K., Beebe, K., Konstantinova, A., Vourganti, S., Panaretou, B., Piper, P. W., Trepel, J. B., Prodromou, C., Pearl, L. H. and Neckers, L. (2011 b). Threonine 22 phosphorylation attenuates Hsp90 interaction with cochaperones and affects its chaperone activity. Molecular Cell 41, 672–681.Google Scholar
Murphy, P. J., Morishima, Y., Kovacs, J. J., Yao, T. P. and Pratt, W. B. (2005). Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. Journal of Biological Chemistry 280, 33792–33799.Google Scholar
Narasimhan, J., Joyce, B. R., Naguleswaran, A., Smith, A. T., Livingston, M. R., Dixon, S. E., Coppens, I., Wek, R. C. and Sullivan, W. J. Jr. (2008). Translation regulation by eukaryotic initiation factor-2 kinases in the development of latent cysts in Toxoplasma gondii . Journal of Biological Chemistry 283, 16591–16601.CrossRefGoogle ScholarPubMed
Nathan, D. F. and Lindquist, S. (1995). Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Molecular Cellular Biology 15, 3917–3925.Google Scholar
Ogiso, H., Kagi, N., Matsumoto, E., Nishimoto, M., Arai, R., Shirouzu, M., Mimura, J., Fujii-Kuriyama, Y. and Yokoyama, S. (2004). Phosphorylation analysis of 90 kDa heat shock protein within the cytosolic arylhydrocarbon receptor complex. Biochemistry 43, 15510–15519.Google Scholar
Park, J. H., Kim, S. H., Choi, M. C., Lee, J., Oh, D. Y., Im, S. A., Bang, Y. J. and Kim, T. Y. (2008). Class II histone deacetylases play pivotal roles in heat shock protein 90-mediated proteasomal degradation of vascular endothelial growth factor receptors. Biochemical and Biophysical Research Communication 368, 318–322.Google Scholar
Park, M. H., Kwon, Y. J., Jeong, H. Y., Lee, H. Y., Hwangbo, Y., Yoon, H. J. and Shim, S. H. (2012). Association between intracellular infectious agents and schizophrenia. Clinical Psychopharmacology and Neuroscience 10, 117–123.Google Scholar
Pavithra, S. R., Kumar, R. and Tatu, U. (2007). Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum . PLOS Computational Biology 3, 1701–1715.Google Scholar
Pearl, L. H., Prodromou, C. and Workman, P. (2008). The Hsp90 molecular chaperone: an open and shut case for treatment. Biochemical Journal 410, 439–453.Google Scholar
Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cellular and Molecular Life Sciences 59, 1640–1648.Google Scholar
Picard, D., Suslova, E. and Briand, P. A. (2006). 2-color photobleaching experiments reveal distinct intracellular dynamics of two components of the Hsp90 complex. Experimental Cell Research 312, 3949–3958.Google Scholar
Pratt, W. B. and Toft, D. O. (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Experimental Biology and Medicine 228, 111–133.Google Scholar
Prodromou, C. and Pearl, L. H. (2003). Structure and functional relationships of Hsp90. Current Cancer Drug Targets 3, 301–323.Google Scholar
Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W. and Pearl, L. H. (1997). Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65–75.Google Scholar
Radke, J. R., Striepen, B., Guerini, M. N., Jerome, M. E., Roos, D. S. and White, M. W. (2001). Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii . Molecular and Biochemical Parasitology 115, 165–175.Google Scholar
Radke, J. R., Guerini, M. N., Jerome, M. and White, M. W. (2003). A change in the premitotic period of the cell cycle is associated with bradyzoite differentiation in Toxoplasma gondii . Molecular and Biochemical Parasitology 131, 119–127.Google Scholar
Retzlaff, M., Hagn, F., Mitschke, L., Hessling, M., Gugel, F., Kessler, H., Richter, K. and Buchner, J. (2010). Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Molecular Cell 37, 344–354.Google Scholar
Rochani, A. K., Singh, M. and Tatu, U. (2013). Heat shock protein 90 inhibitors as broad spectrum anti-infectives. Current Pharmaceutical Design 19, 377–386.Google Scholar
Roy, N., Nageshan, R. K., Ranade, S. and Tatu, U. (2012). Heat shock protein 90 from neglected protozoan parasites. Biochimica et Biophysica Acta 1823, 707–711.Google Scholar
Sawarkar, R., Sievers, C. and Paro, R. (2012). Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149, 807–818.Google Scholar
Scroggins, B. T., Robzyk, K., Wang, D., Marcu, M. G., Tsutsumi, S., Beebe, K., Cotter, R. J., Felts, S., Toft, D., Karnitz, L., Rosen, N. and Neckers, L. (2007). An acetylation site in the middle domain of Hsp90 regulates chaperone function. Molecular Cell 25, 151–159.Google Scholar
Shao, J., Hartson, S. D. and Matts, R. L. (2002). Evidence that protein phosphatase 5 functions to negatively modulate the maturation of the Hsp90-dependent heme-regulated eIF2alpha kinase. Biochemistry 41, 6770–6779.Google Scholar
Sharma, P. and Chitnis, C. E. (2013). Key molecular events during host cell invasion by Apicomplexan pathogens. Current Opinion in Microbiology 16, 432–437.Google Scholar
Shonhai, A., Maier, A. G., Przyborski, J. M. and Blatch, G. L. (2011). Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis. Protein and Peptide Letters 18, 143–157.Google Scholar
Soroka, J., Wandinger, S. K., Mausbacher, N., Schreiber, T., Richter, K., Daub, H. and Buchner, J. (2012). Conformational switching of the molecular chaperone Hsp90 via regulated phosphorylation. Molecular Cell 45, 517–528.Google Scholar
Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U. and Pavletich, N. P. (1997). Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239–250.Google Scholar
Striepen, B., Jordan, C. N., Reiff, S. and van Dooren, G. G. (2007). Building the perfect parasite: cell division in apicomplexa. PLoS Pathogen 3, e78.Google Scholar
Suvorova, E. S., Radke, J. B., Ting, L. M., Vinayak, S., Alvarez, C. A., Kratzer, S., Kim, K., Striepen, B. and White, M. W. (2013). A nucleolar AAA-NTPase is required for parasite division. Molecular Microbiology 90, 338–355. doi: 10.1111/mmi.12367.Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.Google Scholar
Tomavo, S. and Boothroyd, J. C. (1995). Interconnection between organellar functions, development and drug resistance in the protozoan parasite, Toxoplasma gondii . International Journal for Parasitology 25, 1293–1299.Google Scholar
Treeck, M., Sanders, J. L., Elias, J. E. and Boothroyd, J. C. (2011). The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites’ boundaries. Cell Host and Microbe 10, 410–419.Google Scholar
Tsutsumi, S., Mollapour, M., Graf, C., Lee, C. T., Scroggins, B. T., Xu, W., Haslerova, L., Hessling, M., Konstantinova, A. A., Trepel, J. B., Panaretou, B., Buchner, J., Mayer, M. P., Prodromou, C. and Neckers, L. (2009). Hsp90 charged-linker truncation reverses the functional consequences of weakened hydrophobic contacts in the N domain. Nature Structural and Molecular Biology 16, 1141–1147.Google Scholar
Ueno, A., Dautu, G., Haga, K., Munyaka, B., Carmen, G., Kobayashi, Y. and Igarashi, M. (2011). Toxoplasma gondii: a bradyzoite-specific DnaK-tetratricopeptide repeat (DnaK-TPR) protein interacts with p23 co-chaperone protein. Experimental Parasitology 127, 795–803.Google Scholar
Vanagas, L., Jeffers, V., Bogado, S. S., Dalmasso, M. C., Sullivan, W. J. Jr. and Angel, S. O. (2012). Toxoplasma histone acetylation remodelers as novel drug targets. Expert Review of Anti-Infective Therapy 10, 1189–1201.Google Scholar
Wang, X., Song, X., Zhuo, W., Fu, Y., Shi, H., Liang, Y., Tong, M., Chang, G. and Luo, Y. (2009). The regulatory mechanism of Hsp90alpha secretion and its function in tumor malignancy. Proceedings of the National Academy of Sciences USA 106, 21288–21293.Google Scholar
Xu, W., Mollapour, M., Prodromou, C., Wang, S., Scroggins, B. T., Palchick, Z., Beebe, K., Siderius, M., Lee, M. J., Couvillon, A., Trepel, J. B., Miyata, Y., Matts, R. and Neckers, L. (2012). Dynamic tyrosine phosphorylation modulates cycling of the HSP90-P50(CDC37)-AHA1 chaperone machine. Molecular Cell 47, 434–443.Google Scholar
Xue, B., Jeffers, V., Sullivan, W. J. and Uversky, V. N. (2013). Protein intrinsic disorder in the acetylome of intracellular and extracellular Toxoplasma gondii . Molecular BioSystems 9, 645–657.Google Scholar
Yu, X., Guo, Z. S., Marcu, M. G., Neckers, L., Nguyen, D. M., Chen, G. A. and Schrump, D. S. (2002). Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. Journal of the National Cancer Institute 94, 504–513.Google Scholar
Zhou, Q., Agoston, A. T., Atadja, P., Nelson, W. G. and Davidson, N. E. (2008). Inhibition of histone deacetylases promotes ubiquitin-dependent proteasomal degradation of DNA methyltransferase 1 in human breast cancer cells. Molecular Cancer Research 6, 873–883.Google Scholar
Zhou, W., Quan, J. H., Lee, Y. H., Shin, D. W. and Cha, G. H. (2013). Proliferation require down-regulation of host Nox4 expression via activation of PI3 Kinase/Akt signaling pathway. PLoS ONE 8, e66306.Google Scholar
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