Skip to main content
SpringerLink
Log in

Up-regulation of the arginine vasotocin precursor gene from Paralichthys olivaceus: isolation and expression upon acute pathogen invasion

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Arginine vasotocin (AVT) is a neurohypophysial hormone of non-mammal vertebrates functions in various physiological processes and homologous to mammal vasopressin. In this study, a full-length cDNA coding for a putative AVT precursor was isolated from flounder, Paralichthys olivaceus by rapid amplification of cDNA ends. It was 641 bp long, coding 153 amino acids, and consisted in 69 bp long 5′-untranslated region (UTR), 462 bp open reading frame and 110 bp 3′-UTR. The putative amino acid sequence of flounder AVT was determined, and compared with other AVTs from different species. Also, 1,447 bp of flounder AVT gene, corresponding to the isolated cDNA region with 2 introns within it, was isolated. Reverse transcription polymerase chain reaction result showed that flounder AVT was strongly expressed in the brain but not in the any other tissues examined, confirming it is brain-specific gene. Expression profile of the AVT, together with arylalkylamine N-acetyltransferase, heat shock protein 70, interferon-stimulated gene 15 and natural resistance-associated macrophage protein genes were surveyed from Streptococcus iniae infected flounders by real-time quantitative PCR. It revealed that flounder AVT is up-regulated under acute stress compared to the non-challenged control.

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

Similar content being viewed by others

References

  • Abu-Basha EA, Yibchok-Anun S, Hsu WH (2002) Glucose dependency of arginine vasopressin-induced insulin and glucagon release from the perfused rat pancreas. Metabolism 51:1184–1190

    Article  CAS  PubMed  Google Scholar 

  • Acher R (1996) Molecular evolution of fish neurohypophysial hormones: neutral and selective evolutionary mechanisms. Gen Comp Endocrinol 102:157–172

    Article  CAS  PubMed  Google Scholar 

  • Agniswamy J, Lei B, Musser JM, Sun PD (2004) Insight of host immune evasion mediated by two variants of group a Streptococcus Mac protein. J Biol Chem 279:52789–52796

    Article  CAS  PubMed  Google Scholar 

  • Araya MT, Markham F, Mateo DR, McKenna P, Johnson GR, Berthe FC, Siah A (2010) Identification and expression of immune-related genes in hemocytes of soft-shell clams, Mya arenaria, challenged with Vibrio splendidus. Fish Shellfish Immunol 29:557–564

    Article  CAS  PubMed  Google Scholar 

  • Arushanian EB, Beier EV (2002) Immunotropic properties of pineal melatonin. Eksp Klin Farmakol 65:73–80

    CAS  PubMed  Google Scholar 

  • Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16

    Article  CAS  PubMed  Google Scholar 

  • Bond H, Winter MJ, Warne JM, McCrohan CR, Balment RJ (2002) Plasma concentrations of arginine vasotocin and urotensin II are reduced following transfer of the euryhaline flounder (Platichthys flesus) from seawater to fresh water. Gen Comp Endocrinol 125:113–120

    Article  CAS  PubMed  Google Scholar 

  • Bond H, Warne JM, Balment RJ (2007) Effect of acute restraint on hypothalamic pro-vasotocin mRNA expression in flounder, Platichthys flesus. Gen Comp Endocrinol 153:221–227

    Article  CAS  PubMed  Google Scholar 

  • Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ (2005) A review of the multiple actions of melatonin on the immune system. Endocrine 27:189–200

    Article  CAS  PubMed  Google Scholar 

  • Carrillo-Vico A, Reiter RJ, Lardone PJ, Herrera JL, Fernandez-Montesinos R, Guerrero JM, Pozo D (2006) The modulatory role of melatonin on immune responsiveness. Curr Opin Investig Drugs 7:423–431

    CAS  PubMed  Google Scholar 

  • Falcon J, Galarneau KM, Weller JL, Ron B, Chen G, Coon SL, Klein DC (2001) Regulation of arylalkylamine N-acetyltransferase-2 (AANAT2, EC 2.3.1.87) in the fish pineal organ: evidence for a role of proteasomal proteolysis. Endocrinology 142:1804–1813

    Article  CAS  PubMed  Google Scholar 

  • Gastel JA, Roseboom PH, Rinaldi PA, Weller JL, Klein DC (1998) Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation. Science 279:1358–1360

    Article  CAS  PubMed  Google Scholar 

  • Gilchriest BJ, Tipping DR, Levy A, Baker BI (1998) Diurnal changes in the expression of genes encoding for arginine vasotocin and pituitary pro-opiomelanocortin in the rainbow trout (Oncorhynchus mykiss): correlation with changes in plasma hormones. J Neuroendocrinol 10:937–943

    Article  CAS  PubMed  Google Scholar 

  • Gilchriest BJ, Tipping DR, Hake L, Levy A, Baker BI (2000) The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J Neuroendocrinol 12:795–801

    Article  CAS  PubMed  Google Scholar 

  • Godwin J, Sawby R, Warner RR, Crews D, Grober MS (2000) Hypothalamic arginine vasotocin mRNA abundance variation across sexes and with sex change in a coral reef fish. Brain Behav Evol 55:77–84

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Evans AK, Bass AH (2003) Putative isotocin distributions in sonic fish: relation to vasotocin and vocal-acoustic circuitry. J Comp Neurol 462:1–14

    Article  PubMed Central  PubMed  Google Scholar 

  • Gozdowska M, Kleszczynska A, Sokolowska E, Kulczykowska E (2006) Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp Biochem Physiol B 143:330–334

    Article  CAS  PubMed  Google Scholar 

  • Gray DA, Fleming PA, Nicolson SW (2004) Dietary intake effects on arginine vasotocin and aldosterone in cloacal fluid of whitebellied sunbirds (Nectarinia talatala). Comp Biochem Physiol A 138:441–449

    Article  CAS  Google Scholar 

  • Guibbolini ME, Pierson PM, Lahlou B (2000) Neurohypophysial hormone receptors and second messengers in trout hepatocytes. J Endocrinol 167:137–144

    Article  CAS  PubMed  Google Scholar 

  • Henry J, Cornet V, Bernay B, Zatylny-Gaudin C (2013) Identification and expression of two oxytocin/vasopressin-related peptides in the cuttlefish Sepia officinalis. Peptides 46:159–166

    Article  CAS  PubMed  Google Scholar 

  • Hiraoka S, Ando H, Ban M, Ueda H, Urano A (1997) Changes in expression of neurohypophysial hormone genes during spawning migration in chum salmon, Oncorhynchus keta. J Mol Endocrinol 18:49–55

    Article  CAS  PubMed  Google Scholar 

  • Hur SP, Takeuchi Y, Esaka Y, Nina W, Park YJ, Kang HC, Jeong HB, Lee YD, Kim SJ, Takemura A (2011) Diurnal expression patterns of neurohypophysial hormone genes in the brain of the threespot wrasse Halichoeres trimaculatus. Comp Biochem Physiol A 158:490–497

    Article  Google Scholar 

  • Hyodo S, Ishii S, Joss JM (1997) Australian lungfish neurohypophysial hormone genes encode vasotocin and [Phe2]mesotocin precursors homologous to tetrapod-type precursors. Proc Natl Acad Sci USA 94:13339–13344

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klein DC, Coon SL, Roseboom PH, Weller JL, Bernard M, Gastel JA, Zatz M, Iuvone PM, Rodriguez IR, Begay V (1997) The melatonin rhythm-generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland. Recent Prog Horm Res 52:307–358

    CAS  PubMed  Google Scholar 

  • Kleszczynska A, Sokolowska E, Kulczykowska E (2012) Variation in brain arginine vasotocin (AVT) and isotocin (IT) levels with reproductive stage and social status in males of three-spined stickleback (Gasterosteus aculeatus). Gen Comp Endocrinol 175:290–296

    Article  CAS  PubMed  Google Scholar 

  • Kulczykowska E, Warne JM, Balment RJ (2001) Day-night variations in plasma melatonin and arginine vasotocin concentrations in chronically cannulated flounder (Platichthys flesus). Comp Biochem Physiol A 130:827–834

    Article  CAS  Google Scholar 

  • Kwon MG, Kim JW, Park MA, Hwang JY, Choi HS, Kim MC, Park DW, Jung JM, Park CI (2013) Microarray analysis of gene expression in peripheral blood leucocytes from rock bream (Oplegnathus fasciatus) after stimulation by LPS, ConA/PMA, and poly I:C. Genes Genomics 35:343–353

    Article  CAS  Google Scholar 

  • Liu CS, Sun Y, Zhang M, Sun L (2010) Identification and analysis of a Sciaenops ocellatus ISG15 homologue that is involved in host immune defense against bacterial infection. Fish Shellfish Immunol 29:167–174

    Article  CAS  PubMed  Google Scholar 

  • Maestroni GJ (2001) The immunotherapeutic potential of melatonin. Expert Opin Investig Drugs 10:467–476

    Article  CAS  PubMed  Google Scholar 

  • Motohashi E, Hamabata T, Ando H (2008) Structure of neurohypophysial hormone genes and changes in the levels of expression during spawning season in grass puffer (Takifugu niphobles). Gen Comp Endocrinol 155:456–463

    Article  CAS  PubMed  Google Scholar 

  • Olson KR (2002) Gill circulation: regulation of perfusion distribution and metabolism of regulatory molecules. J Exp Zool 293:320–335

    Article  CAS  PubMed  Google Scholar 

  • Piesiewicz A, Kedzierska U, Adamska I, Usarek M, Zeman M, Skwarlo-Sonta K, Majewski PM (2012) Pineal arylalkylamine N-acetyltransferase (Aanat) gene expression as a target of inflammatory mediators in the chicken. Gen Comp Endocrinol 179:143–151

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Illamola A, Lopez Patino MA, Soengas JL, Ceinos RM, Miguez JM (2011) Diurnal rhythms in hypothalamic/pituitary AVT synthesis and secretion in rainbow trout: evidence for a circadian regulation. Gen Comp Endocrinol 170:541–549

    Article  CAS  PubMed  Google Scholar 

  • Ronald de Kloet ER (2010) From vasotocin to stress and cognition. Eur J Pharmacol 626:18–26

    Article  PubMed  Google Scholar 

  • Salek SJ, Sullivan CV, Godwin J (2002) Arginine vasotocin effects on courtship behavior in male white perch (Morone americana). Behav Brain Res 133:177–183

    Article  CAS  PubMed  Google Scholar 

  • Searcy BT, Walthers EA, Heppner BL, Thompson RR, Moore FL (2009) Identification of mesotocin and vasotocin nucleotide sequences in two species of urodele amphibian. Gen Comp Endocrinol 160:111–116

    Article  CAS  PubMed  Google Scholar 

  • Semsar K, Godwin J (2003) Social influences on the arginine vasotocin system are independent of gonads in a sex-changing fish. J Neurosci 23:4386–4393

    CAS  PubMed  Google Scholar 

  • Smith RF, French NP, Saphier PW, Lowry PJ, Veldhuis JD, Dobson H (2003) Identification of stimulatory and inhibitory inputs to the hypothalamic–pituitary–adrenal axis during hypoglycaemia or transport in ewes. J Neuroendocrinol 15:572–585

    Article  CAS  PubMed  Google Scholar 

  • Sumby P, Barbian KD, Gardner DJ, Whitney AR, Welty DM, Long RD, Bailey JR, Parnell MJ, Hoe NP, Adams GG (2005) Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci USA 102:1679–1684

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suzuki M, Hyodo S, Urano A (1992) Cloning and sequence analyses of vasotocin and isotocin precursor cDNAs in the masu salmon, Oncorhynchus masou: evolution of neurohypophysial hormone precursors. Zoolog Sci 9:157–167

    CAS  PubMed  Google Scholar 

  • Thulin P, Johansson L, Low DE, Gan BS, Kotb M, McGeer A, Norrby-Teglund A (2006) Viable group A Streptococci in macrophages during acute soft tissue infection. PLoS Med 3:371–379

    Article  CAS  Google Scholar 

  • Warne JM, Hazon N, Rankin JC, Balment RJ (1994) A radioimmunoassay for the determination of arginine vasotocin (AVT): plasma and pituitary concentrations in fresh- and seawater fish. Gen Comp Endocrinol 96:438–444

    Article  CAS  PubMed  Google Scholar 

  • Warne JM, Hyodo S, Harding K, Balment RJ (2000) Cloning of pro-vasotocin and pro-isotocin cDNAs from the flounder Platichthys flesus; levels of hypothalamic mRNA following acute osmotic challenge. Gen Comp Endocrinol 119:77–84

    Article  CAS  PubMed  Google Scholar 

  • Warne JM, Harding KE, Balment RJ (2002) Neurohypophysial hormones and renal function in fish and mammals. Comp Biochem Physiol B 132:231–237

    Article  CAS  PubMed  Google Scholar 

  • Warne JM, Bond H, Weybourne E, Sahajpal V, Lu W, Balment RJ (2005) Altered plasma and pituitary arginine vasotocin and hypothalamic provasotocin expression in flounder (Platichthys flesus) following hypertonic challenge and distribution of vasotocin receptors within the kidney. Gen Comp Endocrinol 144:240–247

    Article  CAS  PubMed  Google Scholar 

  • Zipfel PF, Hallstrom T, Riesbeck K (2013) Human complement control and complement evasion by pathogenic microbes–tipping the balance. Mol Immunol 56:152–160

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by Fishery Commercialization Technology Development Program (311070-3), Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea. This work was funded by a research Grant (RP-2013-AQ-183) from the National Fisheries Research and Development Institute (NFRDI), Republic of Korea.

Conflict of interest

Authors declared no conflict of interest on this manuscript.

Author information

Authors and Affiliations

  1. Department of Marine Life Sciences, School of Marine Biomedical Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, 690-756, Republic of Korea

    Seongdo Lee, Jehee Lee, Yu-Cheol Kim, Hyowon Kim, Thanthrige Thiunuwan Priyathilaka & W. D. Niroshana Wickramaarachchi

  2. Marine Science Institute, Jeju National University, 3288 Hamdoek-ri, Jocheon-eup, Jeju-si, Jeju Special Self-Governing Province, 695-965, Republic of Korea

    Bongsoo Lim & Hyung-Bok Jeong

  3. Department of Biology, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 690-756, Republic of Korea

    Se-Jae Kim

  4. New Strategy Research Center, NFRDI, 216 Gijanghaean-ro, Gijang-eup, Gijang-gun, Pusan, 619-705, Republic of Korea

    Shin-Kwon Kim

Authors
  1. Seongdo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bongsoo Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jehee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Cheol Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hyowon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thanthrige Thiunuwan Priyathilaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. W. D. Niroshana Wickramaarachchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Se-Jae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shin-Kwon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hyung-Bok Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hyung-Bok Jeong.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, S., Lim, B., Lee, J. et al. Up-regulation of the arginine vasotocin precursor gene from Paralichthys olivaceus: isolation and expression upon acute pathogen invasion. Genes Genom 36, 443–453 (2014). https://doi.org/10.1007/s13258-014-0178-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-014-0178-9

Keywords

Search

Navigation