Skip to main content
SpringerLink
Log in

Histological change and heat shock protein 70 expression in different tissues of Japanese flounder Paralichthys olivaceus in response to elevated temperature

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

High temperature influences the homeostasis of fish. We investigated the effects of elevated temperature on tissues of Japanese flounder (Paralichthys olivaceus) by analyzing the histology and heat shock protein 70 (hsp70) expression of fish reared in warm conditions. In this study, temperature was increased at 1±0.5°C/day starting at 24±0.5°C, and was kept at that temperature for 5 days before the next rise. After raising temperature at the rate up to 32±0.5°C, tissue samples from midgut, spleen, stomach, liver, muscle, gill, heart, trunk kidney and brain were collected for histological analysis and mRNA assay. Almost all the tissues showed changes in morphological structure and hsp70 level at 32±0.5°C. Histological assessment of the tissues indicated that the gill had the most serious damage, including highly severe epithelial lifting and edema, curved tips and hyperemia at the ending of the lamellars, desquamation and necrosis. The next most severe damage was found in liver and kidney. The hsp70 levels in all the tissues first increased and then decreased. The gut, stomach, muscle, heart, and brain had the highest expressions in 6 h, whereas the spleen, liver, gill and kidney had the highest expressions in 2 h. Therefore, tissues with the most significant lesions (especially gill and liver) responded much earlier (2 h) in hsp70 expression than other tissues, and these tissues demonstrated the most marked histological disruption and elevated mRNA levels, making them ideal candidates for further studies on the thermal physiology of this species.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad S M, Shah F A, Bhat F A, Bhat J I A, Balkhi M H. 2011. Thermal adaptability and disease association in common carp (Cyprinus carpio communis) acclimated to different (four) temperatures. J. Therm. Biol., 36(8): 492–497.

    Article  Google Scholar 

  • Axenov-Gribanov D V, Bedulina D S, Shatilina Z M, Lubyaga Y A, Vereshchagina K P, Timofeyev M A. 2014. A cellular and metabolic assessment of the thermal stress responses in the endemic gastropod Benedictia limnaeoides ongurensis from Lake Baikal. Comp. Biochem. Phys. B, 167: 16–22.

    Article  Google Scholar 

  • Benville Jr. P E, Smith C E, Shanks W E. 1968. Some toxic effects of dimethyl sulfoxide in salmon and trout. Toxicol. Appl. Pharm., 12(2): 156–178.

    Article  Google Scholar 

  • Bowyer J N, Qin J G, Adams L R, Thomson M J S, Stone D A J. 2012. The response of digestive enzyme activities and gut histology in yellowtail kingfish (Seriola lalandi) to dietary fish oil substitution at different temperatures. Aquaculture, 368: 19–28.

    Article  Google Scholar 

  • Caballero M, Obach A, Rosenlund G, Montero D, Gisvold M, Izquierdo M. 2002. Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture, 214(1): 253–271.

    Article  Google Scholar 

  • Chen Q, Luo Z, Zheng J, Li X, Liu C, Zhao Y, Gong Y. 2012. Protective effects of calcium on copper toxicity in Pelteobagrus fulvidraco: Copper accumulation, enzymatic activities, histology. Ecotox. Environ. Safe., 76: 126–134.

    Article  Google Scholar 

  • Cheng P, Liu X, Zhang G, He J. 2007. Cloning and expression analysis of a HSP70 gene from Pacific abalone (Haliotis discus hannai). Fish Shellfish Immun., 22(1): 77–87.

    Article  Google Scholar 

  • Cnaani A. 2006. Genetic perspective on stress response and disease resistance in aquaculture. Isr. J. Aquaculture — Bamidgeh, 58(4): 375–383.

    Google Scholar 

  • Dalela R C, Bhatnagar M C, Tyagi A K, Verma S R. 1979. Histological damage of gills in Channa gachua after acute and subacute exposure to endosulfan and rogor. Mikroskopie, 35(11–12): 301.

    Google Scholar 

  • Dash G, Yonzone P, Chanda M, Paul M. 2011. Histopathological changes in Labeo rohita (Hamilton) fingerlings to various acclimation temperatures. Chron. Young Sci., 2(1): 29–36.

    Article  Google Scholar 

  • De Vico G, Cataldi M, Carella F, Marino F, Passantino A. 2008. Histological, histochemical and morphometric changes of splenic melanomacrophage centers (Smmcs) in sparicotyle-infected cultured sea breams (Sparus aurata). Immunopharm Immunot., 30(1): 27–35.

    Article  Google Scholar 

  • Delaney M A, Klesius P H. 2004. Hypoxic conditions induce Hsp70 production in blood, brain and head kidney of juvenile Nile tilapia Oreochromis niloticus (L.). Aquaculture, 236(1): 633–644.

    Article  Google Scholar 

  • Dent L, Lutterschmidt W I. 2003. Comparative thermal physiology of two sympatric sunfishes (Centrarchidae: Perciformes) with a discussion of microhabitat utilization. J. Therm. Biol., 28(1): 67–74.

    Article  Google Scholar 

  • Dyer S D, Dickson K L, Zimmerman E G, Sanders B M. 1991. Tissue-specific patterns of synthesis of heat-shock proteins and thermal tolerance of the fathead minnow (Pimephales promelas). Can. J. Zool., 69(8): 2 021–2 027.

    Article  Google Scholar 

  • Feder M E, Hofmann G E. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol., 61(1): 243–282.

    Article  Google Scholar 

  • Feng L F, Miao W. 2008. Comparative analysis of the Hsp70 mRNA expression and heat tolerance in two regional Carchesium polypinum at different latitudes. Acta Zool. Sin., 54(3): 525–530.

    Google Scholar 

  • Flores-Lopes F, Thomaz A T. 2011. Histopathologic alterations observed in fish gills as a tool in environmental monitoring. Braz. J. Biol., 71(1): 179–188.

    Article  Google Scholar 

  • Fonds M, Tanaka M, Van der Veer H W. 1995. Feeding and growth of juvenile Japanese flounder Paralichthys olivaceus in relation to temperature and food supply. Neth. J. Sea Res., 34(1): 111–118.

    Article  Google Scholar 

  • Haensly W E, Neff J M, Sharp J R, Morris A C, Bedgood M F, Boem P D. 1982. Histopathology of Pleuronectes platessa L. from Aber Wrach and Aber Benoit, Brittany, France: long-term effects of the Amoco Cadiz crude oil spill. J. Fish Dis., 5(5): 365–391.

    Article  Google Scholar 

  • Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol., 8(2): R19.

    Article  Google Scholar 

  • Hochachka P W, Somero G N. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press on Demand, New York.

    Google Scholar 

  • Iwata N, Kikuchi K, Honda H, Kiyono M, Kurokura H. 1994. Effects of temperature on the growth of Japanese flounder. Fish. Sci., 60: 527–531.

    Article  Google Scholar 

  • Jacobs D, Esmond E F, Melisky E L, Hocutt C H. 1981. Morphological changes in gill epithelia of heat-stressed rainbow trout, Salmo gairdneri: evidence in support of a temperature-induced surface area change hypothesis. Can. J. Fish. Aquat. Sci., 38(1): 16–22.

    Article  Google Scholar 

  • Kondo H, Watabe S. 2004. Temperature-dependent enhancement of cell proliferation and mRNA expression for type I collagen and HSP70 in primary cultured goldfish cells. Comp. Biochem. Phys. A, 138(2): 221–228.

    Article  Google Scholar 

  • Lindquist S, Craig E A. 1988. The heat-shock proteins. Annu. Rev. Genet., 22(1): 631–677.

    Article  Google Scholar 

  • Liu X, Luo Z, Xiong B, Liu X, Zhao Y, Hu G, Lv G. 2010. Effect of waterborne copper exposure on growth, hepatic enzymatic activities and histology in Synechogobius hasta. Ecotox. Environ. Safe., 73(6): 1 286–1 291.

    Article  Google Scholar 

  • Liu Y, Ma D, Zhao C, Wang W, Zhang X, Liu X, Liu Y, Xiao Z, Xu S, Xiao Y. 2014. Histological and enzymatic responses of Japanese flounder (Paralichthys olivaceus) and its hybrids (P. olivaceus ♀ × P. dentatus ♂) to chronic heat stress. Fish Physiol. Biochem., 40(4): 1 031–1 041.

    Google Scholar 

  • Madeira D, Narciso L, Cabral H N, Diniz M S, Vinagre C. 2012. Thermal tolerance of the crab Pachygrapsus marmoratus: intraspecific differences at a physiological (CTMax) and molecular level (Hsp70). Cell Stress Chaperon, 17(6): 707–716.

    Article  Google Scholar 

  • Mallatt J. 1985. Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fish. Aquat. Sci., 42(4): 630–648.

    Article  Google Scholar 

  • McHugh K J, Smit N J, Van Vuren J H J, Van Dyk J C, Bervoets L, Covaci A, Wepener V. 2011. A histology-based fish health assessment of the tigerfish, Hydrocynus vittatus from a DDT-affected area. Phys. Chem. Earth, 36(14): 895–904.

    Article  Google Scholar 

  • Meseguer J, Lopez-Ruiz A, Esteban M A. 1994. Melanomacrophages of the seawater teleosts, sea bass (Dicentrarchus labrax) and gilthead seabream (Sparus aurata): morphology, formation and possible function. Cell Tissue Res., 277(1): 1–10.

    Google Scholar 

  • Mora C, Ospina A. 2001. Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific). Mar. Biol., 139(4): 765–769.

    Article  Google Scholar 

  • Nascimento A A, Araújo F G, Gomes I D, Mendes R M M, Sales A. 2012. Fish gills alterations as potential biomarkers of environmental quality in a eutrophized tropical river in south-eastern Brazil. Anat. Histol. Embryol., 41(3): 209–216.

    Article  Google Scholar 

  • Osovitz C J, Hofmann G E. 2005. Thermal history-dependent expression of the hsp70 gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. J. Exp. Mar. Biol. Ecol., 327(2): 134–143.

    Article  Google Scholar 

  • Passantino L, Cianciotta A, Jirillo F, Carrassi M, Jirillo E, Passantino G F. 2005. Lymphoreticular system in fish: erythrocyte-mediated immunomodulation of macrophages contributes to the formation of melanomacrophage centers. Immunopharm. Immunot., 27(1): 147–161.

    Article  Google Scholar 

  • Rojas L M, Mata C, Oliveros A, Salazar-Lugo R. 2013. Histology of gill, liver and kidney in juvenile fish Colossoma macropomum exposed to three temperatures. Rev. Biol. Trop., 61(2): 797–806.

    Google Scholar 

  • Rombough P J, Garside E T. 1977. Hypoxial death inferred from thermally induced injuries at upper lethal temperatures, in the banded killifish, Fundulus diaphanous (LeSueur). Can. J. Zool., 55(10): 1 705–1 719.

    Article  Google Scholar 

  • Salazar-Lugo R, Mata C, Oliveros A, Rojas L M, Lemus M, Rojas-Villarroel E. 2011. Histopathological changes in gill, liver and kidney of neotropical fish Colossoma macropomum exposed to paraquat at different temperatures. Environ. Toxicol. Phar., 31(3): 490–495.

    Article  Google Scholar 

  • Smith L S. 1989. Digestive functions in teleost fishes. In: Halver J E ed. Fish Nutrition. Academic Press, New York, USA. p.331–421.

    Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3(7): research0034.

    Google Scholar 

  • Wang Y, Xu J, Sheng L, Zheng Y. 2007. Field and laboratory investigations of the thermal influence on tissue-specific Hsp70 levels in common carp (Cyprinus carpio). Comp. Biochem. Phys. A, 148(4): 821–827.

    Article  Google Scholar 

  • Wood L A, Brown I R, Youson J H. 1999. Tissue and developmental variations in the heat shock response of sea lampreys (Petromyzon marinus): effects of an increase in acclimation temperature. Comp. Biochem. Physiol. A, 123(1): 35–42.

    Article  Google Scholar 

  • Yang R, Xie C, Fan Q, Gao C, Fang L. 2010. Ontogeny of the digestive tract in yellow catfish Pelteobagrus fulvidraco larvae. Aquaculture, 302(1): 112–123.

    Article  Google Scholar 

  • Yokoyama S, Koshio S, Takakura N, Oshida K, Ishikawa M, Gallardo-Cigarroa F J, Teshima S-I. 2005. Dietary bovine lactoferrin enhances tolerance to high temperature stress in Japanese flounder Paralichthys olivaceus. Aquaculture, 249(1): 367–373.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Yifan Liu  (柳意樊), Daoyuan Ma  (马道远), Zhizhong Xiao  (肖志忠), Shihong Xu  (徐世宏), Yanfeng Wang  (王彦丰), Yufu Wang  (王雨福), Yongshuang Xiao  (肖永双), Qinghua Liu  (刘清华) & Jun Li  (李军)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yifan Liu  (柳意樊) & Yufu Wang  (王雨福)

  3. Nantong Branch, Institute of Oceanology, Chinese Academy of Sciences, Nantong, 226019, China

    Yongshuang Xiao  (肖永双)

  4. Weihai Shenghang Aquatic Product Science and Technology Co. Ltd., Weihai, 264200, China

    Zongcheng Song  (宋宗诚)

  5. Rizhao Proliferation Station of Marine Aquatic Resources, Rizhao, 276805, China

    Zhaojun Teng  (滕照军)

Authors
  1. Yifan Liu  (柳意樊)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daoyuan Ma  (马道远)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhizhong Xiao  (肖志忠)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shihong Xu  (徐世宏)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanfeng Wang  (王彦丰)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yufu Wang  (王雨福)
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yongshuang Xiao  (肖永双)
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zongcheng Song  (宋宗诚)
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhaojun Teng  (滕照军)
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qinghua Liu  (刘清华)
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jun Li  (李军)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qinghua Liu  (刘清华) or Jun Li  (李军).

Additional information

Supported by the Modern Agro-Industry Technology Research System of China (No. nycytx-50), the Key Innovation Program of Chinese Academy of Sciences, the Experiment and Demonstration of Scientific and Technical Innovation on Modern Ecological Ocean Agriculture (No. KSC2-EW-B-3), the Transformation Fund for Agricultural Science and Technology Achievements (No. 2013GB2C600263), the Science-Technology R&D Project of Shandong Province (No. 2011GHy11530), the Shandong Province Agricultural Seed Project (No. 2014–2016), the Jiangsu Provincial Natural Science Foundation of China (No. BK2012222), and the Fundamental Research Project of Technology Program of Qingdao, China (Nos. 12-1-4-8(6)-jch, 12-1-4-8-(7)-jch, 12-4-1-51-hy)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Ma, D., Xiao, Z. et al. Histological change and heat shock protein 70 expression in different tissues of Japanese flounder Paralichthys olivaceus in response to elevated temperature. Chin. J. Ocean. Limnol. 33, 11–19 (2015). https://doi.org/10.1007/s00343-015-4028-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-015-4028-7

Keyword

Search

Navigation