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Cell Stress and Chaperones

, Volume 20, Issue 1, pp 159–168 | Cite as

Hsp70 and lipid peroxide levels following heat stress in Xeropicta derbentina (Krynicki 1836) (Gastropoda, Pulmonata) with regard to different colour morphs

  • A. Dieterich
  • S. Troschinski
  • S. Schwarz
  • M. A. Di Lellis
  • A. Henneberg
  • U. Fischbach
  • M. Ludwig
  • U. Gärtner
  • R. Triebskorn
  • H.-R. Köhler
Original Paper

Abstract

Terrestrial snails which live under dry and hot conditions need efficient mechanisms of adaptation to counteract the problems of desiccation and over-heating. A profoundly heat tolerant snail species is the Mediterranean Xeropicta derbentina, exhibiting different shell colour morphs ranging from pale white to darkly banded. Considering that dark-pigmented snails are believed to have a disadvantage due to faster heating, we investigated possible differences in the stress markers Hsp70 and lipid peroxideation between four pre-defined colour morphs which were exposed to different temperatures for eight hours. The highest Hsp70 levels were observed in response to 38-40 °C. Levels decreased when this temperature was exceeded. Snails of a pre-defined colour category 3 (with a large black band at the umbilicus side of the shell) showed the most prominent Hsp70 response. Lipid peroxideation levels also showed a maximum at 38 °C but displayed a second peak at rather high temperatures at which the Hsp70 level already had decreased (45-48 °C). Particularly pure white snails (category 1) and the most pigmented ones (category 4) were found to have different levels of lipid peroxidation at 38 °C and 45 °C compared to the other morphs. A hypothesis involving a combined two-phase defence mechanism, to which both, the Hsp70 protection system and the antioxidant defence system, may contribute, is discussed.

Keywords

FOX assay Heat stress Hsp70 level Lipid peroxidation Shell colouration 

Notes

Acknowledgements

The authors would like to thank Christophe Mazzia, University of Avignon, for the provision of our sampling site in Modène. The study was funded by the German Research Council (DFG, Ko 1978/5-3) and the Twinning Projects Grant of Tübingen University. The authors would like to thank two unknown reviewers for their useful comments on an earlier version of this manuscript.

References

  1. Abele D, Burlando B, Viarengo A, Pörtner H-O (1998) Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comparative Biochemistry and Physiology Part B: Biochem. Mol. Biol. 120:425–435. doi: 10.1016/S0305-0491(98)10028-7
  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126PubMedCrossRefGoogle Scholar
  3. Arad Z, Goldenberg S, Avivi T, Heller J (1993) Intraspecific variation in resistance to desiccation in the land snail Theba pisana. Int J Biometeorol 37:183–189. doi: 10.1007/BF01387520 CrossRefGoogle Scholar
  4. Aubry S, Labaune C, Magnin F, Roche P, Kiss L (2006) Active and passive dispersal of an invading land snail in Mediterranean France. J Anim Ecol 75:802–813. doi: 10.1111/j.1365-2656.2006.01100.x PubMedCrossRefGoogle Scholar
  5. Bahrndorff S, Holmstrup M, Petersen H, Loeschcke V (2006) Geographic variation for climatic stress resistance traits in the springtail Orchesella cincta. J Insect Physiol 52:951–959. doi: 10.1016/j.jinsphys.2006.06.005 PubMedCrossRefGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254. doi: 10.1006/abio.1976.9999 PubMedCrossRefGoogle Scholar
  7. Cain A (1977) The uniqueness of the polymorphism of Cepaea (Pulmonata: Helicidae) in western Europe. J Conchol 29:129Google Scholar
  8. Chang H-W (1991) Activity and weight loss in relation to solar radiation in the polymorphic land snail Cepaea nemoralis. J Zool 225:213–225. doi: 10.1111/j.1469-7998.1991.tb03812.x CrossRefGoogle Scholar
  9. Comuzzi C, Polese P, Melchior A, Portanova R, Tolazzi M (2003) OLVERSTAT: a new utility for multipurpose analysis. An application to the investigation of dioxygenated Co(II) complex formation in dimethylsulfoxide solution. Talanta 59:67–80. doi: 10.1016/S0039-9140(02)00457-5 PubMedCrossRefGoogle Scholar
  10. Cowie RH (1984) Ecogenetics of Theba pisana (Pulmonata: Helicidae) at the northern edge of its range. Malacologia 25:361–380Google Scholar
  11. Cowie RH (1985) Microhabitat choice and high temperature tolerance in the land snail Theba pisana (Mollusca: Gastropoda). J Zool 207:201–211CrossRefGoogle Scholar
  12. Cowie RH (1992) Shell pattern polymorphism in a 13-year study of the land snail Theba Pisana (Müller) (Pulmonata : Helicidae) vol 34. vol 1–2. Institute of Malacology, Ann Arbor, MI, ETATS-UNISGoogle Scholar
  13. Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710PubMedCrossRefGoogle Scholar
  14. Di Lellis M, Seifan M, Troschinski S, Mazzia C, Capowiez Y, Triebskorn R, Köhler H-R (2012) Solar radiation stress in climbing snails: behavioural and intrinsic features define the Hsp70 level in natural populations of Xeropicta derbentina (Pulmonata). Cell Stress Chaperones 17:717–727PubMedCentralPubMedCrossRefGoogle Scholar
  15. Di Lellis MA et al (2014) Phenotypic diversity, population structure, and stress protein-based capacitoring in populations of Xeropicta derbentina, a heat-tolerant land snail species. Cell Stress Chaperones. doi: 10.1007/s12192-014-0503-x Google Scholar
  16. Dieterich A et al. (2012) Daily and seasonal changes in heat exposure and the Hsp70 level of individuals from a field population of Xeropicta derbentina (Krynicki 1836) (Pulmonata, Hygromiidae) in Southern France Cell Stress and Chaperones:1–10 doi: 10.1007/s12192-012-0393-8
  17. Dittbrenner N, Lazzara R, Köhler H-R, Mazzia C, Capowiez Y, Triebskorn R (2009) Heat tolerance in Mediterranean land snails: histopathology after exposure to different temperature regimes. J Molluscan Stud 75:9–18. doi: 10.1093/mollus/eyn033 CrossRefGoogle Scholar
  18. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  19. Fink AL (1999) Chaperone-Mediated Protein Folding. Physiol Rev 79:425–449PubMedGoogle Scholar
  20. Goodhart CB (1987) Why are some snails visibly polymorphic, and others not? Biol J Linn Soc 31:35–58. doi: 10.1111/j.1095-8312.1987.tb01979.x CrossRefGoogle Scholar
  21. Gutteridge J (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828PubMedGoogle Scholar
  22. Gutteridge JMC, Halliwell B (1990) The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 15:129–135. doi: 10.1016/0968-0004(90)90206-Q PubMedCrossRefGoogle Scholar
  23. Halliwell B, Gutteridge JMC (1989) Free Radicals in Biology and Medicine, 2nd edn. Clarendon Press, Oxford, UKGoogle Scholar
  24. Hazel WN, Johnson MS (1990) Microhabitat choice and polymorphism in the land snail Theba pisana (Muller). Heredity 65:449–454CrossRefGoogle Scholar
  25. Heath DJ (1975) Colour, sunlight and internal temperatures in the land-snail Cepaea nemoralis (L.). Oecologia 19:29–38CrossRefGoogle Scholar
  26. Hendrick JP, Hartl F (1993) Molecular Chaperone Functions of Heat-Shock Proteins. Annu Rev Biochem 62:349–384. doi: 10.1146/annurev.bi.62.070193.002025 PubMedCrossRefGoogle Scholar
  27. Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation Free Radical. Biol Med 19:271–280. doi: 10.1016/0891-5849(95)00020-X Google Scholar
  28. Jäättelä M (1999) Heat shock proteins as cellular lifeguards. Ann Med 31:261–271. doi: 10.3109/07853899908995889 PubMedCrossRefGoogle Scholar
  29. Jena KB, Verlecar XN, Chainy GBN (2009) Application of oxidative stress indices in natural populations of Perna viridis as biomarker of environmental pollution. Mar Pollut Bull 58:107–113. doi: 10.1016/j.marpolbul.2008.08.018 PubMedCrossRefGoogle Scholar
  30. Johnson MS (2011) Thirty-four years of climatic selection in the land snail Theba pisana Heredity 106:741–748 doi:http://www.nature.com/hdy/journal/v106/n5/suppinfo/hdy2010114s1.html
  31. Kiss L, Labaune C, Magnin F, Aubry S (2005) Plasticity of the life cycle of Xeropicta derbentina (Krynicki, 1836), a recently introduced snail in mediterranean France. J Molluscan Stud 71:221–231. doi: 10.1093/mollus/eyi030 CrossRefGoogle Scholar
  32. Köhler H-R, Bartussek C, Eckwert H, Farian K, Gränzer S, Knigge T, Kunz N (2001) The hepatic stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution. J Aquat Ecosyst Stress Recover 8:261–279CrossRefGoogle Scholar
  33. Köhler H-R, Lazzara R, Dittbrenner N, Capowiez Y, Mazzia C, Triebskorn R (2009) Snail phenotypic variation and stress proteins: do different heat response strategies contribute to Waddington's widget in field populations? J Exp Zool B Mol Dev Evol 312B:136–147. doi: 10.1002/jez.b.21253 CrossRefGoogle Scholar
  34. Köhler H-R, Schultz C, Scheil AE, Triebskorn R, Seifan M, Di Lellis MA (2013) Historic data analysis reveals ambient temperature as a source of phenotypic variation in populations of the land snail Theba pisana. Biol J Linn Soc 109:241–256. doi: 10.1111/bij.12035 CrossRefGoogle Scholar
  35. Krebs RA, Feder ME (1997) Natural variation in the expression of the heat-shock protein Hsp70 in a population of Drosophila melanogaster and its correlation with tolerance of ecologically relevant thermal stress Evolution:173–179Google Scholar
  36. Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186. doi: 10.1152/japplphysiol.01267.2001 PubMedGoogle Scholar
  37. Mayer M, Bukau B (2005) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684PubMedCentralPubMedCrossRefGoogle Scholar
  38. McQuaid CD, Branch GM, Frost PGH (1979) Aestivation behaviour and thermal relations of the pulmonate Theba pisana in a semi-arid environment. J Therm Biol 4:47–55. doi: 10.1016/0306-4565(79)90045-7 CrossRefGoogle Scholar
  39. Meister A (1988) Glutathione metabolism and its selective modification. J Biol Chem 263:17205–17208PubMedGoogle Scholar
  40. Monserrat JM, Geracitano LA, Pinho GLL, Vinagre TM, Faleiros M, Alciati JC, Bianchini A (2003) Determination of Lipid Peroxides in Invertebrates Tissues Using the Fe(III) Xylenol Orange Complex Formation. Arch Environ Contam Toxicol 45:177–183PubMedCrossRefGoogle Scholar
  41. Moreno-Rueda G (2008) The colour white diminishes weight loss during aestivation in the arid-dwelling land snail Sphincterochila (Albea) candidissima. Iberus 26:47–51Google Scholar
  42. Ozgo M, Schilthuizen M (2012) Evolutionary change in Cepaea nemoralis shell colour over 43 years. Glob Chang Biol 18:74–81. doi: 10.1111/j.1365-2486.2011.02514.x CrossRefGoogle Scholar
  43. Pannunzio TM, Storey KB (1998) Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. J Exp Mar Biol Ecol 221:277–292. doi: 10.1016/S0022-0981(97)00132-9 CrossRefGoogle Scholar
  44. Pomeroy D (1968) Dormancy in the land snail, Helicella virgata (Pulminata : Helicidae) Australian. J Zool 16:857–869. doi: 10.1071/ZO9680857 Google Scholar
  45. Radwan MA, El-Gendy KS, Gad AF (2010) Biomarkers of oxidative stress in the land snail, Theba pisana for assessing ecotoxicological effects of urban metal pollution. Chemosphere 79:40–46. doi: 10.1016/j.chemosphere.2010.01.056 PubMedCrossRefGoogle Scholar
  46. Regteren Altena, C.O. van (1960) On the occurrence of a species of Xeropicta in France. Basteria 24:21–25Google Scholar
  47. Reuner A, Bruemmer F, Schill RO (2008) Heat shock proteins (Hsp70) and water content in the estivating Mediterranean Grunt Snail (Cantareus apertus). Comp Biochem Physiol B-Biochem Mol Biol 151:28–31PubMedCrossRefGoogle Scholar
  48. Richardson AMM (1974) Differential Climatic Selection in Natural Population of Land Snail Cepaea nemoralis. Nature 247:572–573CrossRefGoogle Scholar
  49. Richardson AMM (1979) Morph frequencies of empty intact shells from Cepaea nemoralis (L.) colonies on snad dunes in South West England. J Molluscan Stud 45:98–107Google Scholar
  50. Scheil AE, Köhler H-R, Triebskorn R (2011) Heat tolerance and recovery in Mediterranean land snails after pre-exposure in the field. J Molluscan Stud 77:165–174. doi: 10.1093/mollus/eyr003 CrossRefGoogle Scholar
  51. Scheil AE, Gärtner U, Köhler H-R (2012a) Colour polymorphism and thermal capacities in Theba pisana (O.F. Müller 1774). J Therm Biol 37:462–467. doi: 10.1016/j.jtherbio.2012.03.006 CrossRefGoogle Scholar
  52. Scheil AE, Scheil V, Triebskorn R, Capowiez Y, Mazzia C, Kohler HR (2012b) Shell colouration and antioxidant defence capacity in Theba pisana (OF Muller, 1774). Molluscan Res 32:132–136Google Scholar
  53. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295PubMedGoogle Scholar
  54. Silvertown J et al (2011) Citizen Science Reveals Unexpected Continental-Scale Evolutionary Change in a Model Organism. PLoS ONE 6:e18927. doi: 10.1371/journal.pone.0018927 PubMedCentralPubMedCrossRefGoogle Scholar
  55. Sørensen JG, Michalak P, Justesen J, Loeschcke V (1999) Expression of the Heat-Shock Protein HSP70 in Drosophila buzzatii Lines Selected for Thermal Resistance. Hereditas 131:155–164. doi: 10.1111/j.1601-5223.1999.00155.x PubMedCrossRefGoogle Scholar
  56. Sørensen JG, Dahlgaard J, Loeschcke V (2001) Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits. Funct Ecol 15:289–296. doi: 10.1046/j.1365-2435.2001.00525.x CrossRefGoogle Scholar
  57. Staikou AE (1999) Shell Temperature, Activity and Resistance to Desiccation in the Polymorphic Land Snail Cepaea vindobonensis. J Molluscan Stud 65:171–184. doi: 10.1093/mollus/65.2.171 CrossRefGoogle Scholar
  58. Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res = Revista brasileira de pesquisas medicas e biologicas / Sociedade Brasileira de Biofisica [et al] 29:1715–1733Google Scholar
  59. Troschinski S, Di Lellis MA, Sereda S, Hauffe T, Wilke T, Triebskorn R, Köhler H-R (2014) Intraspecific Variation in Cellular and Biochemical Heat Response Strategies of Mediterranean Xeropicta derbentina [Pulmonata, Hygromiidae]. PLoS ONE 9:e86613. doi: 10.1371/journal.pone.0086613 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Zhou J, Wang L, Xin Y, Wang W-N, He W-Y, Wang A-L, Liu Y (2010) Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J Therm Biol 35:284–289. doi: 10.1016/j.jtherbio.2010.06.004 CrossRefGoogle Scholar

Copyright information

© Cell Stress Society International 2014

Authors and Affiliations

  • A. Dieterich
    • 1
  • S. Troschinski
    • 1
  • S. Schwarz
    • 1
  • M. A. Di Lellis
    • 1
  • A. Henneberg
    • 1
  • U. Fischbach
    • 2
  • M. Ludwig
    • 2
  • U. Gärtner
    • 2
  • R. Triebskorn
    • 1
  • H.-R. Köhler
    • 1
  1. 1.Animal Physiological Ecology, University of TübingenTübingenGermany
  2. 2.Institute of Applied ResearchUniversity of Applied SciencesEsslingenGermany

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