Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Relationship between heat shock protein levels and infectivity in Trichinella spiralis larvae exposed to different stressors

  • 86 Accesses

  • 9 Citations


The aim of the present study was to investigate the relationship between infectivity and the levels of two major heat shock proteins (Hsp70 and Hsp60) in Trichinella spiralis larvae. Parasites were exposed to either sublethal thermal stress (43 and 45°C) or to warm or cold temperature oxidative stress. The stressed larvae were then inoculated into female CD1 mice to determine their infectivity. Hsps were detected and quantified by Western blotting using monoclonal antibodies. Infectivity was expressed as larvae per gram of muscle. Warm temperature oxidative stress (20 mM H2O2 at 37°C) caused a significant increase in Hsp levels and total loss of infectivity. Cold oxidative stress (20 mM H2O2 at 4°C) caused no alterations in either Hsp levels or infectivity. However, high oxidative stress and cold (200 mM H2O2 at 4°C) caused a slight increase in Hsp60 levels and a drastic reduction in infectivity. Exposure of the larvae to 43 or 45°C did not significantly alter Hsp levels or infectivity. These results show that (i) cold reduces the deleterious effects of oxidative stress; (ii) heat induces neither increased Hsp60/Hsp70 levels nor reduces infectivity; (iii) increased Hsp levels induced by oxidative stress may cause lower infectivity.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. Beissinger M, Buchner J (1998) How chaperones fold proteins. Biol Chem 379:245–259

  2. Brand T, Weistein P, Mehlan B, Weinbach E (1952) Observation on the metabolism of bacteria free larvae of Trichinella spiralis. Exp Parasitol 1:245–255

  3. Buchmeier NA, Heffron F (1990) Salmonella proteins induced following phagocytosis by macrophages are controlled by multiple regulons. Science 248:730–732

  4. Buttke TM, Sandstrom PA (1994). Oxidative stress as a mediator of apoptosis. Immunol Today 15:7–10

  5. Callahan HL, Crouch RK, James ER (1988) Helminth anti-oxidant enzymes: a protective mechanism against host oxidant?. Parasitol Today 4:218–225

  6. Callahan HL, Crouch RK, James ER (1990) Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 100:407–415

  7. Carvalho MGC, Fournier MV (1991) Effect of heat shock on gene expression of Aedes albopictus cells infected with Mayaro virus. Res Virol 142:25–31

  8. Das M, Mukherjee SB, Shaha C (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 114:2461–2469

  9. Davis SR, Lushbaugh WB (1992) Characterization of the heat-shock response of Trichomonas vaginalis. Am Soc Trop Med Hyg 47:70–77

  10. Forreiter C, Nover L (1998) Heat induced stress proteins and the concept of molecular chaperones. J Biosci 23:287–302

  11. Gounaris K, Smith VP, Selkirk ME (1996) Structural organisation and lipid composition of the epicuticular accessory layer of infective larvae of Trichinella spiralis. Biochim Biophys Acta 1281:91–100

  12. Hadas E, Rodríguez-Caabeiro F, Jiménez-González A (1994) Oxidant defence enzymes in different isolates of Trichinella. Acta Parasitol 39:32–36

  13. Henkle-Dührsen K, Kampkötter A (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114:129–142

  14. Hunter KW, Cook CL, Hayunga EG (1984) Leishmania differentiation in vitro: induction of heat shock proteins. Biochem Biophys Res Comm 125:755–760

  15. Jenkins DC, Carrington TS (1981) An in vitro screening test for compounds active against the parenteral stages of Trichinella spiralis. Trop Med Parasitol 32:31–34

  16. Kazura JW, Meshnick SR (1984) Scavenger enzymes and resistance to oxygen mediated damage in Trichinella spiralis. Mol Biochem Parasitol 10:1–10

  17. Khassaf M, McArdle A, Esanu C, Vasilaki A, McArdle F, Griffiths RD, Brodie DA, Jackson MJ (2003) Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J Physiol 549:645–652

  18. Kim CW (1983) Epidemiology II: Geographic distribution and prevalence. In: Campbell WC (ed) Trichinella and Trichinellosis. Plenum Press, New York

  19. Ko RC, Fan L (1996) Heat shock response of Trichinella spiralis and T. pseudospiralis. Parasitology 112:89–95

  20. La Rosa G, Pozio E, Rossi P, Murell KD (1992) Allozyme analysis of Trichinella isolates from various host species and geographical regions. J Parasitol 78:641–646

  21. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

  22. Leppä S, Sistonen L (1997) Heat shock response—pathophysiological implications. Ann Med 29:73–78

  23. Lindquist S (1986) The heat shock response. Annu Rev Biochem 55:1151–1191

  24. Maresca B, Carratú L (1992) The biology of heat shock response in parasites. Parasitol Today 8:260–266

  25. Maresca B, Kobayashi GS (1994) Hsp70 in parasite: as an inducible protective protein and as an antigen. Experientia 11/12:1067–1074

  26. Martínez J, Pérez-Serrano J, Bernadina WE, Rodríguez-Caabeiro F (1999) In vitro stress response to elevated temperature, hydrogen peroxide and mebendazole in Trichinella spiralis muscle larvae. Int J Parasitol 29:1457–1464

  27. Martínez J, Pérez-Serrano J, Bernadina WE, Rodríguez-Caabeiro F (2002) Oxidative, heat and anthelminthic stress response in four species of Trichinella: comparative study. J Exp Zool 293:664–674

  28. Mestril R, Chi SH, Sayen MR, O’Reilly K, Dillmann WH (1994) Expression of inducible stress protein 70 in rat heart myogenic cells confers protection against simulated ischaemia-induced injury. J Clin Invest 93:759–767

  29. Newport GR, Culpepper J. Agabian N (1988) Parasite heat-shock proteins. Parasitol Today 4:306–312

  30. Ou X, Thomas GR, Chacón MR, Tang L, Selkirk ME (1995) Brugia malayi: differential susceptibility to and metabolism of hydrogen peroxide in adults and Microfilariae. Exp Parasitol 80:530–540

  31. Polla SB (1991) Heat shock proteins in host-parasite interactions. Immunol Today 3:38–41

  32. Rzepczyk C, Bishop CJ (1984) Immunological and ultrastructural aspects of the cell-mediated killing of Dirofilaria immitis microfilariae. Parasite Immunol 6:443–457

  33. Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

  34. Selkirk ME, Smith VP, Thomas GR, Gounaris K (1998) Resistance of filarial nematode parasites to oxidative stress. Int J Parasitol 28:1315–1332

  35. Selvan S, Grewal PS, Leustek T, Gaugler R (1996) Heat shock enhances thermotolerance of infective juvenile insect-parasitic nematodes Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae). Experientia 52:727–730

  36. Smejkal RM, Wolff R, Olenick JG (1988) Leishmania braziliensis panamensis: increased infectivity resulting from heat shock. Exp Parasitol 65:1–9

  37. Sokolova JB (1978) The effect of temperature on the viability of different species of Trichinella. Vopr Prirod Ochagov Bolez 10:185–187

  38. Terlecky SR (1994) Hsp70s and lysosomal proteolysis. Experientia 50:1021–1025

  39. Test ST, Weiss SJ (1984) Quantitative and temporal characterisation of the extracellular H2O2 generated by human neutrophils. J Biol Chem 259:399–405

  40. Ueom J, Kwon S, Kim S, Chae Y, Lee K (2003) Acquisition of heat shock tolerance by regulation of intracellular redox states. Biochim Biophys Acta 1642:9–16

  41. Van Leeuwen MAW (1995) Heat-shock and stress response of the parasitic nematode Haemonchus contortus. Parasitol Res 81:706–709

  42. Van der Ploeg LHT, Giannini SH, Cantor CR (1985) Heat shock genes: regulatory role for differentiation in parasitic protozoa. Science 228:1443–1446

  43. Weiss SJ, Test ST, Eckmann CM, Roos D, Regiani S (1986) Brominating oxidants generated by human eosinophils. Science 234:200–203

  44. Welch WJ (1992) Mammalian stress response: cell physiology, structure/function of stress proteins and implications for medicine and diseases. Physiol Rev 4:1063–1081

  45. Woods IB, Amaral NK, Bairden K, Duncan JL, Kassai T, Malone JB, Pankavich JA, Reinecke RK, Slocombe O, Taylor SM, Vercruysse J (1995) World Association for the Advancement of Veterinary Parasitology (WAAVP) second edition of guidelines for evaluating the efficacy of anthelminthics in ruminants (bovine, ovine, caprine). Vet Parasitol 58:181–213

Download references


This study was funded by the Spanish Ministry of Science and Technology (reference AGL2000-1792). The experiments comply with the current laws of Spain.

Author information

Correspondence to J. Martínez.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martínez, J., Rodríguez-Caabeiro, F. Relationship between heat shock protein levels and infectivity in Trichinella spiralis larvae exposed to different stressors. Parasitol Res 97, 213–218 (2005). https://doi.org/10.1007/s00436-005-1420-9

Download citation


  • Stress Protein
  • Coiled Shape
  • Heat Shock Protein Level
  • Trichinella Spiralis
  • Major Heat Shock Protein