Thermal stress induces heat shock protein 70 and apoptosis during embryo development in a Neotropical freshwater fish
Camila F. Sales A * , Flavia S. Lemos A * , Roberto D. V. S. Morais A , Ralph G. Thomé B , Helio B. Santos B , Ana P. B. Pinheiro A , Nilo Bazzoli C and Elizete Rizzo
A D
+ Author Affiliations
- Author Affiliations
A Universidade Federal de Minas Gerais, Departamento de Morfologia, Instituto de Ciências Biológicas, C. P. 486, 31270-901 Belo Horizonte, Minas Gerais, Brazil.
B Universidade Federal de São João Del Rei, Laboratório de Processamento de Tecidos, 35501-296 Divinópolis, Minas Gerais, Brazil.
C Pontifícia Universidade Católica de Minas Gerais, Programa de Pós-graduação em Zoologia de Vertebrados, 30535-610 Belo Horizonte, Minas Gerais, Brazil.
D Corresponding author. Emails: ictio@icb.ufmg.br; elizeterizzo@gmail.com
Reproduction, Fertility and Development 31(3) 547-556 https://doi.org/10.1071/RD18217
Submitted: 9 June 2018 Accepted: 13 September 2018 Published: 30 October 2018
Abstract
Fish embryos are particularly vulnerable to temperature changes, with the effects varying with developmental stage. The major aim of the present study was to analyse the relationship between apoptosis and heat shock protein (HSP) 70 during embryo development under thermal stress conditions. To this end, Prochilodus lineatus embryos at the blastopore closure stage were subjected to one of three thermal treatments for 1 h (Group 1, 25°C (control); Group 2, 20°C; Group 3, 30°C) and then examined at 0, 4 and 8 h posttreatment (h.p.t.). The viability of embryos was highest in Group 1 (81.33 ± 16.65%), followed by Group 3 and Group 2 (75.33 ± 12.10% and 68.67 ± 16.86% respectively), with significant difference between Groups 1 and 2 (P < 0.05). At 0 h.p.t., embryos subjected to thermal stress (Group 3) had a significantly higher number of terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL)- and caspase-3-labelled cells, and a lower number of HSP70-positive cells than those in the control group. At 4 h.p.t., there was a decrease in the TUNEL reaction and an increase in HSP70 in embryos in Group 3. At 8 h.p.t., the size of Group 3 embryos was significantly smaller than that of Group 1 embryos. The results indicate a cytoprotective role for HSP70, regulating caspase-3-mediated apoptosis during embryo development of P. lineatus; however, this mechanism is not effective in controlling embryo viability and larval malformations.
Additional keywords: caspase-3, Prochilodus lineatus, terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL).
References
Agnello, M., Bosco, L., Chiarelli, R., Martino, C., and Roccheri, M. C. (2015). The role of autophagy and apoptosis during embryo development. In ‘Cell Death – Autophagy, apoptosis and necrosis’. (Ed. T. Ntuli.) pp. 83–112. (IntechOpen: London.)Boglione, C., Gisbert, E., Gavaia, P., Witten, P. E., Moren, M., Fontagné, S., and Koumoundouros, G. (2013). Skeletal anomalies in reared European fish larvae and juveniles. Part 2: main typologies, occurrences and causative factors. Rev. Aquacult. 5, S121–S167.
| Skeletal anomalies in reared European fish larvae and juveniles. Part 2: main typologies, occurrences and causative factors.Crossref | GoogleScholarGoogle Scholar |
Botta, P., Sciara, A., Arranz, S., Murgas, L. D. S., Pereira, G. J. M., and Oberlenderb, G. (2010). Study of the embrionary development in sábalo (Prochilodus lineatus). Arch. Med. Vet. 42, 109–114.
| Study of the embrionary development in sábalo (Prochilodus lineatus).Crossref | GoogleScholarGoogle Scholar |
Brett, J. R. (1971). Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd). Integr. Comp. Biol. 11, 99–113.
| Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd).Crossref | GoogleScholarGoogle Scholar |
Candal, E., Anadón, R., Caruncho, H., and Rodríguez-Moldes, I. (2001). Proliferation, cell death and reelin expression during development of the retina in a teleost, the common trout (Salmo trutta fario). Int. J. Dev. Biol. 45, S69–S70.
Carpenter, C. M., and Hofmann, G. E. (2000). Expression of 70 kDa heat shock proteins in antarctic and New Zealand notothenioid fish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 125, 229–238.
| Expression of 70 kDa heat shock proteins in antarctic and New Zealand notothenioid fish.Crossref | GoogleScholarGoogle Scholar |
Chatterjee, S., and Burns, T. F. (2017). Targeting heat shock proteins in cancer: a promising therapeutic approach. Int. J. Mol. Sci. 18, 1–39.
Cole, L. K., and Ross, L. S. (2001). Apoptosis in the developing zebrafish embryo. Dev. Biol. 240, 123–142.
| Apoptosis in the developing zebrafish embryo.Crossref | GoogleScholarGoogle Scholar |
Creagh, E. M., Sheehan, D., and Cotter, T. G. (2000). Heat shock proteins – modulators of apoptosis in tumour cells. Leukemia 14, 1161–1173.
Das, T., Pal, A. K., Chakraborty, S. K., Manush, S. M., Dalvi, R. S., Sarma, K., and Mukherjee, S. C. (2006). Thermal dependence of embryonic development and hatching rate in Labeo rohita (Hamilton, 1822). Aquaculture 255, 536–541.
| Thermal dependence of embryonic development and hatching rate in Labeo rohita (Hamilton, 1822).Crossref | GoogleScholarGoogle Scholar |
de Amorim, M. P., Gomes, B. V. C., Martins, Y. S., Sato, Y., Rizzo, E., and Bazzoli, N. (2009). Early development of the silver catfish Rhamdia quelen (Quoy & Gaimard, 1824) (Pisces: Heptapteridae) from the São Francisco River Basin, Brazil. Aquacult. Res. 40, 172–180.
| Early development of the silver catfish Rhamdia quelen (Quoy & Gaimard, 1824) (Pisces: Heptapteridae) from the São Francisco River Basin, Brazil.Crossref | GoogleScholarGoogle Scholar |
Domingos, F. F. T., Thomé, R. G., Martinelli, P. M., Sato, Y., Bazzoli, N., and Rizzo, E. (2013). Role of HSP70 in the regulation of the testicular apopstosis in a seasonal breeding teleos Prochilodus argenteus from the São Francisco River, Brazil. Microsc. Res. Tech. 76, 350–356.
| Role of HSP70 in the regulation of the testicular apopstosis in a seasonal breeding teleos Prochilodus argenteus from the São Francisco River, Brazil.Crossref | GoogleScholarGoogle Scholar |
Dudgeon, D., Arthington, A. H., Gessner, M. O., Kawabata, Z. I., Knowler, D. J., Lévêque, C., Naiman, R. J., Prieur-Richard, A. H., Soto, D., Stiassny, M. L. J., and Sullivan, C. A. (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Rev. Camb. Philos. Soc. 81, 163–182.
| Freshwater biodiversity: importance, threats, status and conservation challenges.Crossref | GoogleScholarGoogle Scholar |
Evans, T. G., Yamamoto, Y., Jeffery, W. R., and Krone, P. H. (2005). Zebrafish Hsp70 is required for embryonic lens formation. Cell Stress Chaperones 10, 66–78.
| Zebrafish Hsp70 is required for embryonic lens formation.Crossref | GoogleScholarGoogle Scholar |
Firkus, T., Rahel, F. J., Bergman, H. L., and Cherrington, B. D. (2018). Warmed winter water temperatures alter reproduction in two fish species. Environ. Manage. 61, 291–303.
| Warmed winter water temperatures alter reproduction in two fish species.Crossref | GoogleScholarGoogle Scholar |
Gashegu, J., Philippson, C., Vanmuylder, N., Choa-Duterre, M., Rooze, M., and Louryan, S. (2006). Correlation of Hsp110 expression with caspase-3 and -9 during apoptosis induced by in vivo embryonic exposition to retinoic acid or irradiation in early mouse craniofacial development. Orthod. Craniofac. Res. 9, 84–92.
| Correlation of Hsp110 expression with caspase-3 and -9 during apoptosis induced by in vivo embryonic exposition to retinoic acid or irradiation in early mouse craniofacial development.Crossref | GoogleScholarGoogle Scholar |
Gomes, B. V. C., Scarpelli, R. S., Arantes, F. P., Sato, Y., Bazzoli, N., and Rizzo, E. (2007). Comparative oocyte morphology and early development in three species of trahiras from the São Francisco River basin, Brazil. J. Fish Biol. 70, 1412–1429.
| Comparative oocyte morphology and early development in three species of trahiras from the São Francisco River basin, Brazil.Crossref | GoogleScholarGoogle Scholar |
Hansen, T. K., and Falk-Petersen, I. B. (2001). The influence of rearing temperature on early development and growth of spotted wolffish Anarhichas minor (Olafsen). Aquacult. Res. 32, 369–378.
| The influence of rearing temperature on early development and growth of spotted wolffish Anarhichas minor (Olafsen).Crossref | GoogleScholarGoogle Scholar |
Hashimoto, H., Toyohara, Y., Women, M. K., and Nishinomiya, I. (1998). Induction of apoptosis in fish cells by hypertonic stress. Fish. Sci. 64, 820–825.
| Induction of apoptosis in fish cells by hypertonic stress.Crossref | GoogleScholarGoogle Scholar |
Hooven, T. A., Yamamoto, Y., and Jeffery, W. R. (2004). Blind cavefish and heat shock protein chaperones: a novel role for hsp90α in lens apoptosis. Int. J. Dev. Biol. 48, 731–738.
| Blind cavefish and heat shock protein chaperones: a novel role for hsp90α in lens apoptosis.Crossref | GoogleScholarGoogle Scholar |
Jeppesen, E., Meerhoff, M., Holmgren, K., González-Bergonzoni, I., Teixeira-de Mello, F., Declerck, S. A. J., De Meester, L., Søndergaard, M., Lauridsen, T. L., Bjerring, R., Conde-Porcuna, J. M., Mazzeo, N., Iglesias, C., Reizenstein, M., Malmquist, H. J., Liu, Z., Balayla, D., and Lazzaro, X. (2010). Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646, 73–90.
| Impacts of climate warming on lake fish community structure and potential effects on ecosystem function.Crossref | GoogleScholarGoogle Scholar |
Jian, C. Y., Cheng, S. Y., and Chen, J. C. (2003). Temperature and salinity tolerances of yellowfin sea bream, Acanthopagrus latus, at different salinity and temperature levels. Aquacult. Res. 34, 175–185.
| Temperature and salinity tolerances of yellowfin sea bream, Acanthopagrus latus, at different salinity and temperature levels.Crossref | GoogleScholarGoogle Scholar |
Johnson, S. L. (2004). Factors influencing stream temperatures in small streams: substrate effects and a shading experiment. Can. J. Fish. Aquat. Sci. 61, 913–923.
| Factors influencing stream temperatures in small streams: substrate effects and a shading experiment.Crossref | GoogleScholarGoogle Scholar |
Kane, D. A., and Kimmel, C. B. (1993). The zebrafish midblastula transition. Development 119, 447–456.
Kerr, J. F. R., Wyllie, A. H., and Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239–257.
| Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics.Crossref | GoogleScholarGoogle Scholar |
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253–310.
| Stages of embryonic development of the zebrafish.Crossref | GoogleScholarGoogle Scholar |
Krone, P. H., Sass, J. B., and Lele, Z. (1997). Heat shock protein gene expression during embryonic development of the zebrafish. Cell. Mol. Life Sci. 53, 122–129.
| Heat shock protein gene expression during embryonic development of the zebrafish.Crossref | GoogleScholarGoogle Scholar |
Krumschnabel, G., and Podrabsky, J. E. (2009). Fish as model systems for the study of vertebrate apoptosis. Apoptosis 14, 1–21.
| Fish as model systems for the study of vertebrate apoptosis.Crossref | GoogleScholarGoogle Scholar |
Kvitt, H., Rosenfeld, H., and Tchernov, D. (2016). The regulation of thermal stress induced apoptosis in corals reveals high similarities in gene expression and function to higher animals. Sci. Rep. 6, 30359.
| The regulation of thermal stress induced apoptosis in corals reveals high similarities in gene expression and function to higher animals.Crossref | GoogleScholarGoogle Scholar |
Langford, T. E. L. (2001). Thermal discharges and pollution. In ‘Encyclopedia of Ocean Sciences’. (Eds J. H. Steele, S. A. Thorpe and K. K. Turekian.) pp. 2933–2940. (Academic Press: Amsterdam.)
Li, A. J., Leung, P. T. Y., Bao, V. W. W., Lui, G. C. S., and Leung, K. M. Y. (2015). Temperature-dependent physiological and biochemical responses of the marine medaka Oryzias melastigma with consideration of both low and high thermal extremes. J. Therm. Biol. 54, 98–105.
| Temperature-dependent physiological and biochemical responses of the marine medaka Oryzias melastigma with consideration of both low and high thermal extremes.Crossref | GoogleScholarGoogle Scholar |
Lindquist, S., and Craig, E. (1988). The heat-shock proteins. Annu. Rev. Genet. 22, 631–677.
| The heat-shock proteins.Crossref | GoogleScholarGoogle Scholar |
Meimaridou, E., Gooljar, S. B., and Chapple, J. P. (2009). From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery. J. Mol. Endocrinol. 42, 1–9.
| From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery.Crossref | GoogleScholarGoogle Scholar |
Ninhaus-Silveira, A., Foresti, F., and De Azevedo, A. (2006). Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiformes; Prochilodontidae). Zygote 14, 217–229.
| Structural and ultrastructural analysis of embryonic development of Prochilodus lineatus (Valenciennes, 1836) (Characiformes; Prochilodontidae).Crossref | GoogleScholarGoogle Scholar |
Ojanguren, A. F., and Braña, F. (2003). Effects of size and morphology on swimming performance in juvenile brown trout (Salmo trutta L.). Ecol. Freshwat. Fish 12, 241–246.
| Effects of size and morphology on swimming performance in juvenile brown trout (Salmo trutta L.).Crossref | GoogleScholarGoogle Scholar |
Ørnsrud, R., Gil, L., and Waagbø, R. (2004a). Teratogenicity of elevated egg incubation temperature and egg vitamin A status in Atlantic salmon, Salmo salar L. J. Fish Dis. 27, 213–223.
| Teratogenicity of elevated egg incubation temperature and egg vitamin A status in Atlantic salmon, Salmo salar L.Crossref | GoogleScholarGoogle Scholar |
Ørnsrud, R., Wargelius, A., Sæle, Ø., Pittman, K., and Waagbø, R. (2004b). Influence of egg vitamin a status and egg incubation temperature on subsequent development of the early vertebral column in Atlantic salmon fry. J. Fish Biol. 64, 399–417.
| Influence of egg vitamin a status and egg incubation temperature on subsequent development of the early vertebral column in Atlantic salmon fry.Crossref | GoogleScholarGoogle Scholar |
Parcellier, A., Gurbuxani, S., Schmitt, E., Solary, E., and Garrido, C. (2003). Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways. Biochem. Biophys. Res. Commun. 304, 505–512.
| Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways.Crossref | GoogleScholarGoogle Scholar |
Pelegri, F. (2003). Maternal factors in zebrafish development. Dev. Dyn. 228, 535–554.
| Maternal factors in zebrafish development.Crossref | GoogleScholarGoogle Scholar |
Perini, Vda R., Paschoalini, A. L., Cruz, C. K., Rocha Rde, C., Senhorini, J. A., Ribeiro, D. M., Formagio, P. S., Bazzoli, N., and Rizzo, E. (2013). Profiles of sex steroids, fecundity and spawning of a migratory characiform fish from the Paraguay–Paraná basin: a comparative study in a three-river system. Fish Physiol. Biochem. 39, 1473–1484.
| Profiles of sex steroids, fecundity and spawning of a migratory characiform fish from the Paraguay–Paraná basin: a comparative study in a three-river system.Crossref | GoogleScholarGoogle Scholar |
Politis, S. N., Mazurais, D., Servili, A., Zambonino-Infante, J.-L., Miest, J. J., Sørensen, S. R., Tomkiewicz, J., and Butts, I. A. E. (2017). Temperature effects on gene expression and morphological development of European eel, Anguilla anguilla larvae. PLoS One 12, e0182726.
| Temperature effects on gene expression and morphological development of European eel, Anguilla anguilla larvae.Crossref | GoogleScholarGoogle Scholar |
Rizzo, E., Godinho, H. P., and Sato, Y. (2003). Short-term storage of oocytes from the neotropical teleost fish Prochilodus marggravii. Theriogenology 60, 1059–1070.
| Short-term storage of oocytes from the neotropical teleost fish Prochilodus marggravii.Crossref | GoogleScholarGoogle Scholar |
Saleh, A., Srinivasula, S. M., Balkir, L., Robbins, P. D., and Alnemri, E. S. (2000). Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2, 476–483.
| Negative regulation of the Apaf-1 apoptosome by Hsp70.Crossref | GoogleScholarGoogle Scholar |
Santacruz, H., Vriz, S., and Angelier, N. (1997). Molecular characterization of a heat shock cognate cDNA of zebrafish, hsc70, and developmental expression of the corresponding transcripts. Dev. Genet. 21, 223–233.
| Molecular characterization of a heat shock cognate cDNA of zebrafish, hsc70, and developmental expression of the corresponding transcripts.Crossref | GoogleScholarGoogle Scholar |
Santos, H. B., Sato, Y., Moro, L., Bazzoli, N., and Rizzo, E. (2008). Relationship among follicular apoptosis, integrin β1 and collagen type IV during early ovarian regression in the teleost Prochilodus argenteus after induced spawning. Cell Tissue Res. 332, 159–170.
| Relationship among follicular apoptosis, integrin β1 and collagen type IV during early ovarian regression in the teleost Prochilodus argenteus after induced spawning.Crossref | GoogleScholarGoogle Scholar |
Somero, G. N. (2010). The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J. Exp. Biol. 213, 912–920.
| The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’.Crossref | GoogleScholarGoogle Scholar |
Stefanovic, D. I., Manzon, L. A., McDougall, C. S., Boreham, D. R., Somers, C. M., Wilson, J. Y., and Manzon, R. G. (2016). Thermal stress and the heat shock response in embryonic and young of the year juvenile lake whitefish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 193, 1–10.
| Thermal stress and the heat shock response in embryonic and young of the year juvenile lake whitefish.Crossref | GoogleScholarGoogle Scholar |
Takle, H., McLeod, A., and Andersen, O. (2006). Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 144, 188–198.
| Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos.Crossref | GoogleScholarGoogle Scholar |
Uchida, D., Yamashita, M., Kitano, T., and Iguchi, T. (2002). Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol. 205, 711–718.
Viveiros, A. T. M., and Godinho, H. P. (2009). Sperm quality and cryopreservation of Brazilian freshwater fish species: a review. Fish Physiol. Biochem. 35, 137–150.
| Sperm quality and cryopreservation of Brazilian freshwater fish species: a review.Crossref | GoogleScholarGoogle Scholar |
Wargelius, A., Fjelldal, P. G., and Hansen, T. (2005). Heat shock during early somitogenesis induces caudal vertebral column defects in Atlantic salmon (Salmo salar). Dev. Genes Evol. 215, 350–357.
| Heat shock during early somitogenesis induces caudal vertebral column defects in Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar |
Whitehouse, L. M., McDougall, C. S., Stefanovic, D. I., Boreham, D. R., Somers, C. M., Wilson, J. Y., and Manzon, R. G. (2017). Development of the embryonic heat shock response and the impact of repeated thermal stress in early stage lake whitefish (Coregonus clupeaformis) embryos. J. Therm. Biol. 69, 294–301.
| Development of the embryonic heat shock response and the impact of repeated thermal stress in early stage lake whitefish (Coregonus clupeaformis) embryos.Crossref | GoogleScholarGoogle Scholar |
Wiegand, M. D., Hataley, J. M., Kitchen, C. L., and Buchanan, L. G. (1989). Induction of developmental abnormalities in larval goldfish, Carassius auratus L., under cool incubation conditions. J. Fish Biol. 35, 85–95.
| Induction of developmental abnormalities in larval goldfish, Carassius auratus L., under cool incubation conditions.Crossref | GoogleScholarGoogle Scholar |
Yabu, T., Todoriki, S., and Yamashita, M. (2001). Stress-induced apoptosis by heat shock, UV and γ-ray irradiation in zebrafish embryos detected by increased caspase activity and whole-mount TUNEL staining. Fish. Sci. 67, 333–340.
| Stress-induced apoptosis by heat shock, UV and γ-ray irradiation in zebrafish embryos detected by increased caspase activity and whole-mount TUNEL staining.Crossref | GoogleScholarGoogle Scholar |
