Abstract
Trypanosoma cruzi is the causal agent of Chagas’ disease, a debilitating disorder affecting millions of people in several countries. A flagellated protozoan parasite, T. cruzi has a complex life cycle that involves infecting an insect and a mammalian host. During its life cycle, the parasite undergoes several kinds of stress, prominent among which is heat stress. To deal with this environmental challenge, molecular chaperones and proteases, also known as heat shock proteins (HSPs), are induced as part of the stress response. Several families of HSPs are synthesized by T. cruzi, including members of the major HSP classes such as HSP70, HSP90, HSP100, HSP40, chaperonins and small HSPs, and these proteins show conserved and unique features. In this review we describe these proteins and the corresponding gene expression patterns and discuss their relevance to the biology of the parasite.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- Clp:
-
Caseinolytic protease
- CHR:
-
Cellular homeostasis response
- CSR:
-
Cellular stress response
- HSP:
-
Heat shock protein
- LIT:
-
Liver infusion tryptose
- NBD:
-
Nucleotide-binding domains
- ROS:
-
Reactive oxidative species
- sHSP:
-
Small heat shock protein
- UTR:
-
Untranslated region
References
Alcina A, Urzainqui A, Carrasco L (1988) The heat-shock response in Trypanosoma cruzi. Eur J Biochem 172:121–127
Asea A (2003) Chaperokine-induced signal transduction pathways. Exerc Immunol Rev 9:25–33
Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, Tarleton RL (2005) The Trypanosoma cruzi proteome. Science 309:473–476
Batista TM, Marques JT (2011) RNAi pathways in parasitic protists and worms. J Proteomics 74:1504–1514
Campos RA, da Silva ML, da Costa GV, Bisch PM, Peralta JM, Silva R, Rondinelli E, Urményi TP (2012) Gene expression and molecular modeling of the HSP104 chaperone of Trypanosoma cruzi. Genet Mol Res 11:2122–2129
Carreira MA, Tibbetts RS, Olson CL, Schuster C, Renz M, Engman DM, Goldenberg S (1998) TcDJ1, a putative mitochondrial DnaJ protein in Trypanosoma cruzi. FEMS Microbiol Lett 166:141–146
Carvalho JF, de Carvalho EF, Rondinelli E, Silva R, de Castro FT (1987) Protein biosynthesis changes in Trypanosoma cruzi induced by supra-optimal temperature. Exp Cell Res 168:338–346
Contreras VT, Salles JM, Thomas N, Morel CM, Goldenberg S (1985) In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol Biochem Parasitol 16:315–327
Cuervo P, Domont GB, De Jesus JB (2010) Proteomics of trypanosomatids of human medical importance. J Proteomics 73:845–867
de Carvalho EF, de Castro FT, Rondinelli E, Soares CMA, Carvalho JF (1990) HSP 70 gene expression in Trypanosoma cruzi is regulated at different levels. J Cell Physiol 143:439–444
de Carvalho EF, de Castro FT, Rondinelli E, Carvalho JF (1994) Physiological aspects of Trypanosoma cruzi gene regulation during heat-shock. Biol Res 27:225–231
de Marval MG, Souto-Padrón T, Gottesdiener K, Silva R, van der Ploeg LH, Rondinelli E (1993) Heat shock proteins in Trypanosoma cruzi: identification and localization of HSP70 and HSP60 proteins and structure of HSP60 genes (brief report). Biol Res 26:313–314
Doyle SM, Wickner S (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34:40–48
Dragon EA, Sias SR, Kato EA, Gabe JD (1987) The genome of Trypanosoma cruzi contains a constitutively expressed, tandemly arranged multicopy gene homologous to a major heat shock protein. Mol Cell Biol 7:1271–1275
Edkins AL, Ludewig MH, Blatch GL (2004) A Trypanosoma cruzi heat shock protein 40 is able to stimulate the adenosine triphosphate hydrolysis activity of heat shock protein 70 and can substitute for a yeast heat shock protein 40. Int J Biochem Cell Biol 36:1585–1598
El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran A-N, Ghedin E, Worthey EA, Delcher AL, Blandin G et al (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409–415
Engman DM, Kirchhoff LV, Donelson JE (1989a) Molecular cloning of mtp70, a mitochondrial member of the hsp70 family. Mol Cell Biol 9:5163–5168
Engman DM, Sias SR, Gabe JD, Donelson JE, Dragon EA (1989b) Comparison of HSP70 genes from two strains of Trypanosoma cruzi. Mol Biochem Parasitol 37:285–287
Engman DM, Dragon EA, Donelson JE (1990) Human humoral immunity to hsp70 during Trypanosoma cruzi infection. J Immunol 144:3987–3991
Engman DM, Fehr SC, Donelson JE (1992) Specific functional domains of mitochondrial hsp70s suggested by sequence comparison of the trypanosome and yeast proteins. Mol Biochem Parasitol 51:153–155
Engman DM, Henkle-Dührsen K, Kirchhoff LV, Donelson JE (1995) Trypanosoma cruzi: accumulation of polycistronic hsp70 RNAs during severe heat shock. Exp Parasitol 80:575–577
Fernandes M, Silva R, Rössle SC, Bisch PM, Rondinelli E, Urményi TP (2005) Gene characterization and predicted protein structure of the mitochondrial chaperonin HSP10 of Trypanosoma cruzi. Gene 349:135–142
Flechas ID, Cuellar A, Cucunubá ZM, Rosas F, Velasco V, Steindel M, Thomas MDC, López MC, González JM, Puerta CJ (2009) Characterising the KMP-11 and HSP-70 recombinant antigens’ humoral immune response profile in chagasic patients. BMC Infect Dis 9:186
Folgueira C, Requena JM (2007) A post genomic view of the heat shock proteins in kinetoplastids. FEMS Microbiol Rev 31:359–377
Franzén O, Ochaya S, Sherwood E, Lewis MD, Llewellyn MS, Miles MA, Andersson B (2011) Shotgun sequencing analysis of Trypanosoma cruzi I sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Negl Trop Dis 5:e984
Garcia S, Rodrigues V, Garcia N, Mello M (2011) Prevalence and intensity of infection, metacyclogenesis and nuclear phenotypes in panstrongylus megistus (Burmeister, 1835) after ingestion of Trypanosoma cruzi (Chagas, 1909) II and subjection to heat shock. Braz J Biol 71:491–500
Giambiagi-de Marval M, Gottesdiener K, Rondinelli E, van der Ploeg LH (1993) Predicted amino acid sequence and genomic organization of Trypanosoma cruzi hsp 60 genes. Mol Biochem Parasitol 58:25–31
Giambiagi-deMarval M, Souto-Padrón T, Rondinelli E (1996) Characterization and cellular distribution of heat-shock proteins HSP70 and HSP60 in Trypanosoma cruzi. Exp Parasitol 83:335–345
Giambiagi-de-Marval M, Lees RA, Monteiro BAG, Carvalho JFO, Gottesdiener K, de Castro FT, Rondinelli E (1993) The heat-shock response in Trypanosoma cruzi and Crithidia fasciculata. Cien Cult (São Paulo) 45:216–222
Graefe SEB, Wiesgigl M, Gaworski I, Macdonald A, Clos J (2002) Inhibition of HSP90 in Trypanosoma cruzi induces a stress response but no stage differentiation. Euk Cell 1:936–943
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858
Klein KG, Olson CL, Donelson JE, Engman DM (1995) Molecular comparison of the mitochondrial and cytoplasmic hsp70 of Trypanosoma cruzi, Trypanosoma brucei and Leishmania major. J Eukaryot Microbiol 42:473–476
Kramer S (2012) Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol Biochem Parasitol 181:61–72
Krautz GM, Peterson JD, Godsel LM, Krettli AU, Engman DM (1998) Human antibody responses to Trypanosoma cruzi 70-kD heat-shock proteins. Am J Trop Med Hyg 58:137–143
Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24:3633–3642
Kültz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67:225–257
Labriola CA, Giraldo AMV, Parodi AJ, Caramelo JJ (2011) Functional cooperation between BiP and calreticulin in the folding maturation of a glycoprotein in Trypanosoma cruzi. Mol Biochem Parasitol 175:112–117
Leung AKL, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40:205–215
Levy Yeyati P, Bonnefoy S, Mirkin G, Debrabant A, Lafon S, Panebra A, Gonzalez-Cappa E, Dedet JP, Hontebeyrie-Joskowicz M, Levin MJ (1992) The 70-kDa heat-shock protein is a major antigenic determinant in human Trypanosoma cruzi/Leishmania braziliensis braziliensis mixed infection. Immunol Lett 31:27–33
Louw CA, Ludewig MH, Mayer J, Blatch GL (2010) The Hsp70 chaperones of the Tritryps are characterized by unusual features and novel members. Parasitol Int 59:497–505
Martin F, Requena JM, Martin J, Alonso C, Lopez MC (1993) Cytoplasmic-nuclear translocation of the Hsp70 protein during environmental stress in Trypanosoma cruzi. Biochem Biophys Res Commun 196:1155–1162
Martínez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martínez LE, Manning-Cela RG, Figueroa-Angulo EE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010:525241
Nadeau K, Sullivan MA, Bradley M, Engman DM, Walsh CT (1992) 83-kilodalton heat shock proteins of trypanosomes are potent peptide-stimulated ATPases. Protein Sci 1:970–979
Názer E, Verdún RE, Sanchez DO (2011) Nucleolar localization of RNA binding proteins induced by actinomycin D and heat shock in Trypanosoma cruzi. PLoS One 6:e19920
Názer E, Verdún RE, Sanchez DO (2012) Severe heat shock induces nucleolar accumulation of mRNAs in Trypanosoma cruzi. PLoS One 7:e43715
Olson CL, Nadeau KC, Sullivan MA, Winquist AG, Donelson JE, Walsh CT, Engman DM (1994) Molecular and biochemical comparison of the 70-kDa heat shock proteins of Trypanosoma cruzi. J Biol Chem 269:3868–3874
Paba J, Santana JM, Teixeira ARL, Fontes W, Sousa MV, Ricart CAO (2004) Proteomic analysis of the human pathogen Trypanosoma cruzi. Proteomics 4:1052–1059
Palmer G, Louvion JF, Tibbetts RS, Engman DM, Picard D (1995) Trypanosoma cruzi heat-shock protein 90 can functionally complement yeast. Mol Biochem Parasitol 70:199–202
Pérez-Morales D, Ostoa-Saloma P, Espinoza B (2009) Trypanosoma cruzi SHSP16: characterization of an alpha-crystallin small heat shock protein. Exp Parasitol 123:182–189
Pérez-Morales D, Lanz-Mendoza H, Hurtado G, Martínez-Espinosa R, Espinoza B (2012) Proteomic analysis of Trypanosoma cruzi epimastigotes subjected to heat shock. J Biomed Biotechnol 2012:902803
Planelles L, Thomas M, Pulgar M, Marañón C, Grabbe S, Lopez MC (2002) Trypanosoma cruzi heat-shock protein-70 kDa, alone or fused to the parasite KMP11 antigen, induces functional maturation of murine dendritic cells. Immunol Cell Biol 80:241–247
Requena JM, Lopez MC, Jimenez-Ruiz A, de la Torre JC, Alonso C (1988) A head-to-tail tandem organization of hsp70 genes in Trypanosoma cruzi. Nucleic Acids Res 16:1393–1406
Requena JM, Lopez MC, Jimenez-Ruiz A, Morales G, Alonso C (1989) Complete nucleotide sequence of the hsp70 gene of Trypanosoma cruzi. Nucleic Acids Res 17:797–797
Requena JM, Jimenez-Ruiz A, Soto M, Assiego R, Santarén JF, Lopez MC, Patarroyo ME, Alonso C (1992) Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Mol Biochem Parasitol 53:201–211
Respuela P, Ferella M, Rada-Iglesias A, Åslund L (2008) Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J Biol Chem 283:15884–15892
Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266
Rodrigues DC, Silva R, Rondinelli E, Urményi TP (2010) Trypanosoma cruzi: modulation of HSP70 mRNA stability by untranslated regions during heat shock. Exp Parasitol 126:245–253
Rondinelli E (1994) Conservation of heat-shock proteins in Trypanosoma cruzi. Parasitol Today (Regul Ed) 10:172–176
Rondinelli E, Silva R, Carvalho JF, de Almeida Soares CM, de Carvalho EF, de Castro FT (1988) Trypanosoma cruzi: an in vitro cycle of cell differentiation in axenic culture. Exp Parasitol 66:197–204
Salmon D, Montero-Lomeli M, Goldenberg S (2001) A DnaJ-like protein homologous to the yeast co-chaperone Sis1 (TcJ6p) is involved in initiation of translation in Trypanosoma cruzi. J Biol Chem 276:43970–43979
Schmidt JC, Soares MJ, Goldenberg S, Pavoni DP, Krieger MA (2011) Characterization of TcSTI-1, a homologue of stress-induced protein-1, in Trypanosoma cruzi. Mem Inst Oswaldo Cruz 106:70–77
Shonhai A, Maier AG, Przyborski JM, Blatch GL (2011) Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis. Protein Pept Lett 18:143–157
Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185–194
Sullivan MA, Olson CL, Winquist AG, Engman DM (1994) Expression and localization of Trypanosoma cruzi hsp60. Mol Biochem Parasitol 68:197–208
Tibbetts RS, Kim IY, Olson CL, Barthel LM, Sullivan MA, Winquist AG, Miller SD, Engman DM (1994) Molecular cloning and characterization of the 78-kilodalton glucose-regulated protein of Trypanosoma cruzi. Infect Immun 62:2499–2507
Tibbetts RS, Jensen JL, Olson CL, Wang FD, Engman DM (1998) The DnaJ family of protein chaperones in Trypanosoma cruzi. Mol Biochem Parasitol 91:319–326
Urményi TP, Rodrigues DC, Silva R, Rondinelli E (2012) The stress response of Trypanosoma cruzi. In: Requena JM (ed) Stress response in microbiology. Caister Academic Press, Norwich, pp 345–373
Vonlaufen N, Kanzok SM, Wek RC, Sullivan WJ (2008) Stress response pathways in protozoan parasites. Cell Microbiol 10:2387–2399
Weatherly DB, Boehlke C, Tarleton RL (2009) Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genom 10:255
Wiesgigl M, Clos J (2001) Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol Biol Cell 12:3307–3316
Wilkinson SR, Kelly JM (2009) Trypanocidal drugs: mechanisms, resistance and new targets. Expert Rev Mol Med 11:e31
Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781–791
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Ürményi, T.P., Silva, R., Rondinelli, E. (2014). The Heat Shock Proteins of Trypanosoma cruzi . In: Santos, A., Branquinha, M., d’Avila-Levy, C., Kneipp, L., Sodré, C. (eds) Proteins and Proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry, vol 74. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7305-9_5
Download citation
DOI: https://doi.org/10.1007/978-94-007-7305-9_5
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-7304-2
Online ISBN: 978-94-007-7305-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)