Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp

Sjannie Lefevre, Jonathan A. W. Stecyk, May-Kristin Torp, Lisa Y. Løvold, Christina Sørensen, Ida B. Johansen, Kåre-Olav Stensløkken, Christine S. Couturier, Katherine A. Sloman, Göran E. Nilsson

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Abstract

Crucian carp (Carassius carassius) survive without oxygen for several months, but it is unknown whether they are able to protect themselves from cell death normally caused by the absence, and particularly return, of oxygen. Here, we quantified cell death in brain tissue from crucian carp exposed to anoxia and re-oxygenation using the terminal deoxy-nucleotidyl transferase dUTP nick-end labelling (TUNEL) assay, and cell proliferation by immunohistochemical staining for proliferating cell nuclear antigen (PCNA) as well as PCNA mRNA expression. We also measured mRNA and protein expression of the apoptosis executer protease caspase 3, in laboratory fish exposed to anoxia and re-oxygenation and fish exposed to seasonal anoxia and re-oxygenation in their natural habitat over the year. Finally, a behavioural experiment was used to assess the ability to learn and remember how to navigate in a maze to find food, before and after exposure to anoxia and re-oxygenation. The number of TUNEL-positive cells in the telencephalon increased after 1~day of re-oxygenation following 7 days of anoxia, indicating increased cell death. However, there were no consistent changes in whole-brain expression of caspase 3 in either laboratory-exposed or naturally exposed fish, indicating that cell death might occur via caspase-independent pathways or necrosis. Re-oxygenated crucian carp appeared to have lost the memory of how to navigate in a maze (learnt prior to anoxia exposure), while the ability to learn remained intact. PCNA mRNA was elevated after re-oxygenation, indicating increased neurogenesis. We conclude that anoxia tolerance involves not only protection from damage but also repair after re-oxygenation.
Original languageEnglish
Pages (from-to)3883-3895
Number of pages13
JournalJournal of Experimental Biology
Volume220
Issue number21
DOIs
Publication statusPublished - 1 Nov 2017

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Carassius
Brain Death
Carps
oxygenation
Memory Disorders
anoxia
brain
cell death
hypoxia
Cell Death
proliferating cell nuclear antigen
Proliferating Cell Nuclear Antigen
antigen
Fishes
Aptitude
caspase-3
Transferases
transferases
Caspase 3
Messenger RNA

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Lefevre, S., Stecyk, J. A. W., Torp, M-K., Løvold, L. Y., Sørensen, C., Johansen, I. B., ... Nilsson, G. E. (2017). Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp. Journal of Experimental Biology, 220(21), 3883-3895. https://doi.org/10.1242/jeb.165118
Lefevre, Sjannie ; Stecyk, Jonathan A. W. ; Torp, May-Kristin ; Løvold, Lisa Y. ; Sørensen, Christina ; Johansen, Ida B. ; Stensløkken, Kåre-Olav ; Couturier, Christine S. ; Sloman, Katherine A. ; Nilsson, Göran E. / Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp. In: Journal of Experimental Biology. 2017 ; Vol. 220, No. 21. pp. 3883-3895.
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Lefevre, S, Stecyk, JAW, Torp, M-K, Løvold, LY, Sørensen, C, Johansen, IB, Stensløkken, K-O, Couturier, CS, Sloman, KA & Nilsson, GE 2017, 'Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp', Journal of Experimental Biology, vol. 220, no. 21, pp. 3883-3895. https://doi.org/10.1242/jeb.165118

Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp. / Lefevre, Sjannie; Stecyk, Jonathan A. W.; Torp, May-Kristin; Løvold, Lisa Y.; Sørensen, Christina; Johansen, Ida B.; Stensløkken, Kåre-Olav ; Couturier, Christine S.; Sloman, Katherine A.; Nilsson, Göran E.

In: Journal of Experimental Biology, Vol. 220, No. 21, 01.11.2017, p. 3883-3895.

Research output: Contribution to journalArticle

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AU - Lefevre, Sjannie

AU - Stecyk, Jonathan A. W.

AU - Torp, May-Kristin

AU - Løvold, Lisa Y.

AU - Sørensen, Christina

AU - Johansen, Ida B.

AU - Stensløkken, Kåre-Olav

AU - Couturier, Christine S.

AU - Sloman, Katherine A.

AU - Nilsson, Göran E.

PY - 2017/11/1

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