Transcriptional responses to hypoxia are enhanced by recurrent hypoxia (hypoxic preconditioning) in the epaulette shark

Kalle T. Rytkönen, Gillian M C Renshaw, Petra P. Vainio, Kevin J. Ashton, Grant Williams-Pritchard, Erica H. Leder, Mikko Nikinmaa

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Abstract

All animals require molecular oxygen for aerobic energy production, and oxygen availability has played a particularly important role in the evolution of aquatic animals. This study investigates how previous exposure to hypoxia (preconditioning) primes protective transcriptional responses in a hypoxia-tolerant vertebrate species, the epaulette shark (Hemiscyllium ocellatum). The epaulette shark is a basal cartilaginous fish that in its natural environment experiences cyclic hypoxic periods. We evaluated whether the transcription of a set of crucial prosurvival genes is affected differently by a single short-term (2 h) exposure to sublethal hypoxia compared with eight such successive hypoxia exposures (hypoxia preconditioning). We discovered that hypoxia preconditioning amplifies transcriptional responses compared with animals that experienced a single hypoxic bout. In the heart we observed that hypoxic preconditioning, but not a single hypoxic exposure, resulted in higher transcript levels of genes that regulate oxygen and energy homeostasis, including those of hypoxia-inducible factor-1 alpha, adenosine signaling pathway components, and genes affecting circulation [prostaglandin synthetase 2 (cox-2) and natriuretic peptide C]. This suggests that in a single short-term hypoxic bout, the responses to low oxygen are regulated at the level of pre-existing proteins or translational and posttranslational machinery, whereas transcriptional responses are induced in experiments that parallel the natural environmental cycles of oxygen availability. These findings have general implications for understanding how vertebrates regulate protective gene expression upon physiological stress.

Original languageEnglish
Pages (from-to)1090-1097
Number of pages8
JournalPhysiological Genomics
Volume44
Issue number22
DOIs
Publication statusPublished - 15 Nov 2012

Fingerprint

Sharks
Oxygen
Vertebrates
Gene Components
Hypoxia-Inducible Factor 1
Natriuretic Peptides
Physiological Stress
Prostaglandin-Endoperoxide Synthases
Adenosine
Genes
Hypoxia
Fishes
Homeostasis
Gene Expression
Proteins

Cite this

Rytkönen, Kalle T. ; Renshaw, Gillian M C ; Vainio, Petra P. ; Ashton, Kevin J. ; Williams-Pritchard, Grant ; Leder, Erica H. ; Nikinmaa, Mikko. / Transcriptional responses to hypoxia are enhanced by recurrent hypoxia (hypoxic preconditioning) in the epaulette shark. In: Physiological Genomics. 2012 ; Vol. 44, No. 22. pp. 1090-1097.
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Transcriptional responses to hypoxia are enhanced by recurrent hypoxia (hypoxic preconditioning) in the epaulette shark. / Rytkönen, Kalle T.; Renshaw, Gillian M C; Vainio, Petra P.; Ashton, Kevin J.; Williams-Pritchard, Grant; Leder, Erica H.; Nikinmaa, Mikko.

In: Physiological Genomics, Vol. 44, No. 22, 15.11.2012, p. 1090-1097.

Research output: Contribution to journalArticleResearchpeer-review

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