Skip to main content
SpringerLink
Log in

Cloning and expression analysis of hypoxia-related gene HO in cobia

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

The heme oxygenase gene plays a role in many biological processes and is an important protective factor in hypoxic stress. Research on the HO gene of fishes has attracted increasing attention, but there is yet little information about the cobia (Rachycentron canadum) heme oxygenase gene. In this study, the full-length cDNA of the cobia heme oxygenase gene (heme oxygenase, HO) was cloned using rapid amplification of cDNA ends technology. The full-length cDNA was 1639 bp and the open reading frame (ORF) was 840 bp encoding 279 amino acids, with 5′-UTR 518 bp and 3′-UTR 281 bp. The results of real-time quantitative PCR showed that cobia HO was expressed in all the tissues tested, with the highest expression in gills. The mRNA expression of gill HO increased after hypoxia stress. There was no significant change in the expression of HO mRNA in the liver after hypoxia stress. The amino acid sequences of HO in diverse fish and mammals have varying levels of homology. Our results indicate that the biological functions of HO may be similar in fish and mammals, suggesting an important protective factor in response to hypoxic stress.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdalla M, Mathahs M, Ahmad I (2012) Protective role of heme oxygenase-1 in liver. Biologia 67(4). https://doi.org/10.2478/s11756-012-0058-1

  • Amenyogbe E, Chen G, Wang Z (2019) Identification, characterization, and expressions profile analysis of growth hormone receptors (GHR1 and GHR2) in hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus polyphekadion ♂). Genomics. 112:1–9. https://doi.org/10.1016/j.ygeno.2019.05.012

    Article  CAS  PubMed  Google Scholar 

  • Basu M, Paichha M, Lenka SS, Chakrabarty R, Samanta M (2016) Hypoxic stress: impact on the modulation of TLR2, TLR4, NOD1 and NOD2 receptor and their downstream signalling genes expression in catla (Catla catla). Mol Biol Rep 43:1–9

    Article  CAS  Google Scholar 

  • Bowden T J (2008) Modulation of the immune system of fish by their environment. Fish & Shellfish Immunology, 25(4): 0–383, 373

  • Chen S (2016) Study on physiological tissue and related gene expression changes in the liver and organs of the ovoid liver and organs under acute and chronic hypoxia stress. Shanghai Ocean University 02:70–79

    Google Scholar 

  • Chen S, Wang P, District and Jun, et al (2016) The effects of acute and chronic hypoxia stress on the damage and antioxidant effects of Trachinotus ovatus liver tissue in young fish. J Zool 51(6):1049–1058

    Google Scholar 

  • Chen Y, Fan Z, Yang Y, Gu C (2019) Iron metabolism and its contribution to cancer (review). Int J Oncol. https://doi.org/10.3892/ijo.2019.4720

  • Chixiao J, Xu X (2009) Advances in the study of hemoglobin oxygenase-1. China Medical Guide 27:11–12

    Google Scholar 

  • Elgrabli D, Dachraoui W, Hde M, Ménard-Moyon C, Bégin D, Bégin-Colin S et al (2017) Intracellular degradation of functionalized carbon nanotube/iron oxide hybrids is modulated by iron via Nrf2 pathway. Sci Rep 7(1). https://doi.org/10.1038/srep40997

  • Faek-San, Shu X (2000) heat shock protein and apoptosis. J Hubei Inst Sci Technol (medical edition), (01): 72–73

  • Foulds CE, Treviño LS, York B, Walker CL (2017) Endocrine-disrupting chemicals and fatty liver disease. Nat. Rev Endocrinol 13(8):445–457

    Article  CAS  Google Scholar 

  • Fraser ST, Midwinter RG, Berger BS, Stocker R (2011) Heme oxygenase-1: a critical link between Iron metabolism, erythropoiesis, and development. Advances in Hematology 2011:1–6. https://doi.org/10.1155/2011/473709

    Article  CAS  Google Scholar 

  • Giorgi C, Marchi S, Simoes ICM, Ren Z, Morciano G, Perrone M et al (2018) Mitochondria and reactive oxygen species in aging and age-related diseases. Mitochondria and Longevity 340:209–344. https://doi.org/10.1016/bs.ircmb.2018.05.006

    Article  CAS  Google Scholar 

  • Guo H (2009) Artificial transcription factor construction of special upward HO-1 gene expression. Third Military Medical University, (06): 43–66

  • Heath AG (1988) Anaerobic and aerobic energy metabolism in brain and liver tissue from rainbow trout (Salmo gairdneri) and bullhead catfish (Ictalurus nebulosus). J Exp Zool 248(2):140–146

    Article  CAS  Google Scholar 

  • Koppang EO, Fischer U, Moore L et al (2010) Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. J Anat 217(6):728–739

    Article  CAS  Google Scholar 

  • Kurz T, Eaton JW, Brunk UT (2011) The role of lysosomes in iron metabolism and recycling. Int J Biochem Cell Biol 43(12):1686–1697. https://doi.org/10.1016/j.biocel.2011.08.016

    Article  CAS  PubMed  Google Scholar 

  • Lai KP, Tam N, Wang SY, Lin X, Chan TF, Au DWT, Wu RSS, Kong RYC (2020) Hypoxia causes sex-specific hepatic toxicity at the transcriptome level in marine medaka (Oryzias melastigma). Aquat Toxicol 105520:105520. https://doi.org/10.1016/j.aquatox.2020.105520

    Article  CAS  Google Scholar 

  • Leffler CW, Parfenova H, Jaggar JH (2011) Carbon monoxide as an endogenous vascular modulator. Am J Phys Heart Circ Phys 301(1):H1–H11. https://doi.org/10.1152/ajpheart.00230.2011

    Article  CAS  Google Scholar 

  • Li Y (2015) Low oxygen protection effect of zebrafish hemoglobin and oxygenase 1 and genetically modified fish research. Central China Normal University, (01): 50–57

  • Li Y, Xu G, Xiao J et al (2017) Study on the protective effect of hemoglobin oxygenase 1 in low oxygen stress in zebrafish. Aquat Biol 1:43–49

    Google Scholar 

  • Li L, Zhao Q, He J et al (2018) TIGAR gene over-expresses its effect on low oxygen compound oxygen damage to hippocampus neurons in rats. Ziru J Med 33(03):230–233

    Google Scholar 

  • Lin C-H, Lo W-C, Hsiao M, Tseng C-J (2003) Interaction of carbon monoxide and adenosine in the nucleus tractus solitarii of rats. Hypertension 42(3):380–385. https://doi.org/10.1161/01.hyp.0000088561.17252.42

    Article  CAS  PubMed  Google Scholar 

  • Liu F (2014) Cloning, expression and function analysis of two hemoglobin oxygenates genes in Trachidermus fasciatus. Shandong University 10:80–88

    Google Scholar 

  • Mali F (2009) Study on the change and effect of hemoglobin oxygenase-1/carbon monoxide system (HO-1/CO) in oxygen-deprived ischemic brain in newborn mice. Tianjin Medical University 27:65–71

    Google Scholar 

  • Medina MV, Sapochnik D, Garcia Sola ME, Coso OA (2019) Regulation of the expression of heme oxygenase-1. Signal Transduction, Gene Promoter Activation and Beyond. Antioxid Redox Signal. https://doi.org/10.1089/ars.2019.7991

  • Mo J, Yu X (1998) Advances in the study of hemoglobin oxygenase. Biotechnol Bull 02:19–24

    Google Scholar 

  • Muñoz-Sánchez J, Chánez-Cárdenas ME (2014) A review on hemeoxygenase-2: focus on cellular protection and oxygen response. Oxidative Med Cell Longev 2014:1–16. https://doi.org/10.1155/2014/604981

    Article  CAS  Google Scholar 

  • Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090 (Review)

    Article  CAS  Google Scholar 

  • Padmavathy P, Ramanathan N, Francis T (2003) Glucose, lactate and pyruvate metabolism in Labeo rohita with reference to ambient oxygen. Asian Fish. Sci. 16:51–58

    Google Scholar 

  • Panchenko MV, Farber HW, Korn JH (2000) Induction of heme oxygenase-1 by hypoxia and free radicals in human dermal fibroblasts. Am J Physiol Cell Physiol 278:C92–C101

    Article  CAS  Google Scholar 

  • Rashid I, Baisvar VS, Singh M, Kumar R, Srivastava P, Kushwaha B, Pathak AK (2020) Isolation and characterization of hypoxia inducible heme oxygenase 1 (HMOX1) gene in Labeo rohita. Genomics 112:2327–2333. https://doi.org/10.1016/j.ygeno.2020.01.004

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Sharma J, Ahmad T, Chakrabarti R (2016) Oxygen stress: impact on innate immune system, antioxidant defence system and expression of HIF-1α and ATPase 6 genes in Catla catla, fish Physiol. Biochem. 42:673–688

    CAS  Google Scholar 

  • Su-in (2012) Cloning and expression of the gene of hemoglobin-oxygenase-1 (HO-1). Huazhong Agricultural University, (02): 60–65

  • Sun W, Zhao X, Wang G et al (2003) Changes in biological function of small intestine epithelial cell brush-like dipeptide transport vector after hypoxic reoxygenation damage and regulation of growth hormone. PLA Med J 28(11):1025–1027

    CAS  Google Scholar 

  • Tao W, Wang L, Hou S et al (2014) Study on the expression characteristics and functions of zebrafish HO1 gene. Aquat Biol 38(02):209–215

    CAS  Google Scholar 

  • Tvrdá E, Massanyi P, Lukáč N (2017) Physiological and pathological roles of free radicals in male reproduction, Spermatozoa - Facts and Perspectives, Rosaria Meccariello and Rosanna Chianese, IntechOpen, DOI: https://doi.org/10.5772/intechopen.70793. Available from: https://www.intechopen.com/books/spermatozoa-facts-and-perspectives/physiological-and-pathological-roles-of-free-radicals-in-male-reproduction

  • Tzaneva V, Perry SF (2014) Heme oxygenase-1 (HO-1) mediated respiratory responses to hypoxia in the goldfish, Carassius auratus. Respir Physiol Neurobiol 199:1–8

    Article  CAS  Google Scholar 

  • Varghese T, Pal AK, Mishal P, Sahu NP, Dasgupta S (2017) Physiological and molecular responses of a bottom dwelling carp, Cirrhinus mrigala to short-term environmental hypoxia. Turk J Fish Aquac Sci 18:483–490

    Google Scholar 

  • Wang D (2010) Screening of the low oxygen reaction gene of mackerel and the characteristic analysis of hemoglobin oxygenase-1 gene. Institute of Aquatic Biology. Institute of Aquatic Biology. Chinese Academy of Sciences, Beijing, pp 50–59

    Google Scholar 

  • Wang X (2013) Expression analysis of microtubation protein-related genes and heat shock protein 70 under low oxygen stress. Huazhong Agricultural University, (02): 69–75

  • Wang Q, Yan T, Zhou F (2012) Advances in the study of the causes of low oxygen and their effects in near shore and estuary. Mar Environ Sci 5:153–156

    Google Scholar 

  • Wang Z, Liang H, Du X et al (2013) Cloning and expression analysis of the HSP60 gene of Ma’s beaded mother behestafever shock protein HSP60 gene. J Guangdong Ocean Univ 33(06):14–23

    CAS  Google Scholar 

  • Wenjun C, Zhenxuan X, Xuehong Z et al (2004) Advances in human hemoglobin oxygenase-1 research. Life Sci 14(4):204–207

    Google Scholar 

  • Xiao W (2015) The hypoxia signaling pathway and hypoxic adaptation in fishes. Sci China Life Sci 58(2):148–155

    Article  CAS  Google Scholar 

  • Xiong X, Huang G, Peng Y et al (2016) Effects of low oxygen stress on the growth, energy metabolism and oxidative stress of young fish. Aquatic J 40(1):73–82

    CAS  Google Scholar 

  • Xu Z (2018) Study on the differential proteomics and heat shock-induced four-fold sports species of grass fish under low oxygen stress. Shanghai Ocean University, (05): 55–60

  • Yan N, Kong X, Jiang H (2012) Advances in the function and expression regulation of hemoglobin and oxygenase-1 in fish. Biol Teach 36(12):2–3

    Google Scholar 

  • Yang X, Huang W, Wei Z et al (2006) Signaling pathways inducing HO-1 gene expression. J Clin Pathol 26(3):238–242

    CAS  Google Scholar 

  • Yang M, Fan J, Du J, Peng X (2020) Small-molecule fluorescent probes for imaging gaseous signaling molecules: current progress and future implication. Chem Sci 11:5127–5141. https://doi.org/10.1039/d0sc01482f

    Article  CAS  Google Scholar 

  • Zhang Z, Zhou W, Chen G et al (2013) Effect of soybean meal content in feed on carbon and nitrogen stable isotope fractionation of military Cao fish larvae. Guangdong Ocean Univ J 33(06):30–36

    Google Scholar 

  • Zhao Y (2018) Study on the regulation of low oxygen stress transcriptome and its main difference gene expression. Qinghai University 09:63–84

    Google Scholar 

  • Zhu CD, Wang ZH, Yan B (2013) Strategies for hypoxia adaptation in fish species: a review. J Comp Physiol B 183(8):1005–1013

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Our sincere acknowledgement goes to the funders of this study.

Data availability statement

Upon reasonable demand, the data supporting the results of this study are obtainable from the corresponding author.

Funding

This work was supported by grants from the China Agriculture Research System (CARS-47), Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang) (ZJW-2019-06)], and Guangdong Ocean University Undergraduate Innovation and Entrepreneurship Training Program (CXXL2018131).

Author information

Author notes

  1. Rui-tao Xie and Eric Amenyogbe contributed equally to this work.

Authors and Affiliations

  1. Fishery College, Guangdong Ocean University, Zhanjiang, 524025, China

    Rui-tao Xie, Eric Amenyogbe, Wei-zheng Wang, Zhi-xiong Guo, Gang Chen & Jian-sheng Huang

  2. Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Zhanjiang, 524025, China

    Gang Chen & Jian-sheng Huang

  3. Guangdong Provincial Key Laboratory of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang, 524088, China

    Gang Chen & Jian-sheng Huang

Authors
  1. Rui-tao Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric Amenyogbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei-zheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhi-xiong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jian-sheng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed equally to this work.

Corresponding author

Correspondence to Jian-sheng Huang.

Ethics declarations

Conflict of interest

The authors confirm that there are no conflicts of interest.

Ethics statement

This study was conducted in compliance with the Guangdong Ocean University Research Council’s Guide for the Care and Use of Laboratory Animals. Fish were anesthetized with ethyl-3-aminobenzoate methanesulfonate (MS-222; Sigma, USA) for tissue collection.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, Rt., Amenyogbe, E., Wang, Wz. et al. Cloning and expression analysis of hypoxia-related gene HO in cobia. Aquacult Int 29, 75–89 (2021). https://doi.org/10.1007/s10499-020-00611-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-020-00611-3

Keywords

Search

Navigation