Transcriptome analysis demonstrates that long noncoding RNA is involved in the hypoxic response in Larimichthys crocea
The large yellow croaker (Larimichthys crocea) has low hypoxia tolerance compared with other fish species, and the mRNA levels of hypoxia-inducible factor (HIF)-1α in its brain do not change markedly under hypoxic conditions. In this study, we investigated noncoding transcription in the hypoxic response mechanism of L. crocea. We generated a catalog of long noncoding RNAs (lncRNAs) from the brain of L. crocea individuals under hypoxic stress, investigated lncRNA expression patterns, and analyzed the HIF signaling pathway by RNA sequencing. Prolyl hydroxylase domain 2 (PHD2) expression significantly increased after 6 and 12 h of hypoxia, and a lncRNA (Linc_06633.1) was found in the upstream, antisense region of PHD2. Linc_06633.1 may be an important regulator that promotes PDH2 expression under hypoxia in L. crocea, and we constructed a regulatory profile of L. crocea under hypoxic conditions. To the best of our knowledge, it is the first study that has been conducted on hypoxia signaling pathway regulation by lncRNAs in L. crocea and elucidates the role played by lncRNAs in the regulation of the hypoxia stress response in teleost fish.
KeywordsLong noncoding RNA PHD2 HIF Larimichthys crocea Hypoxia
This study was supported by the Public Science and Technology Research Funds Projects of Ocean (no. 201505025) and the International Science and Technology Cooperation Program of China (no. 2015DFR30450).
- Gao JL, Chen YG (2014) Natural compounds regulate glycolysis in hypoxic tumor microenvironment. Biomed Res Int 2015:8Google Scholar
- Genciana T, Simona R, Samuela C, Giovanni B, Rosalba G, Marco S (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279(1):150–159Google Scholar
- Goff LA, Groff AF, Sauvageau M, Trayesgibson Z, Sanchezgomez DB, Morse M, Martin RD, Elcavage LE, Liapis SC, Gonzalezceleiro M (2015) Spatiotemporal expression and transcriptional perturbations by long noncoding RNAs in the mouse brain. Proc Natl Acad Sci 112(22):6855–6862CrossRefPubMedPubMedCentralGoogle Scholar
- Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Xian A, Fan L, Koziol MJ, Gnirke A, Nusbaum C (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28(5):503–510CrossRefPubMedPubMedCentralGoogle Scholar
- Jingqun A, Yinnan M, Li-Xin X, Dingding F, Mingji F, Shicui Z, Qiong S, Lv-Yun Z, Ting L, Yang D (2015) Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation. Science Foundation in China 11(3):8–8Google Scholar
- Kaelin WG (2007) Von Hippel-Lindau disease. Annu Rev Pathol 2(2):527–532Google Scholar
- Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea MD, Thomas K, Presser A, Bernstein BE, Van OA (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106(28):11667–11672CrossRefPubMedPubMedCentralGoogle Scholar
- Lutz PL, Nilsson GE (1997) The brain without oxygen. Landes BioscienceGoogle Scholar
- Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515CrossRefPubMedPubMedCentralGoogle Scholar
- Xu K, Liu Z (2007) The current stock of large yellow croaker Pseudosciaena crocea in the East China Sea with respects of its stock decline. Journal of Dalian Fisheries University 22(5):392–396Google Scholar
- Yang QL, Yao CL, Wang ZY (2012) Acute temperature and cadmium stress response characterization of small heat shock protein 27 in large yellow croaker, Larimichthys crocea. COMP BIOCHEM PHYS C 155(2):190–197Google Scholar
- Zhao F, Li YW, Pan HJ, Shi CB, Luo XC, Li AX, Wu SQ (2014) TAK1-binding proteins (TAB1 and TAB2) in grass carp (Ctenopharyngodon idella): identification, characterization, and expression analysis after infection with Ichthyophthirius multifiliis. Fish Shellfish Immun 38(2):389–399CrossRefGoogle Scholar