Skip to main content
SpringerLink
Log in

Effects of osmotic stress on the expression profiling of aquaporin genes in the roughskin sculpin (Trachidermus fasciatus)

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Aquaporins (AQPs) are a family of integral membrane proteins that have been shown to be important for osmoregulation in many vertebrates. To identify potential stress resistance-related aqp genes in salinity adaptation of the roughskin sculpin Trachidermus fasciatus, we investigated the time-course expression dynamics of seven aquaporin genes (aqpl, 4, 7, 8, 10, 11 and 12) in three osmoregulatory tissues (kidney, gill and intestine) and one metabolic tissue (liver). The fish were subjected to two different acute osmotic treatments (seawater-to-freshwater transfer respectively achieved in 1 h and 24 h, namely, E-acute and acute group). The expression profiling of the seven aqp genes were performed using quantitative real-time PCR (qRT-PCR). At the time of all sampling time points (0 h, 12 h, 24 h and 48 h), no expression of aqp4 was found in the gill, liver and intestine; no expression of aqp7 was found in the gill and liver. Significant differences of aqp expression were determined in the four target tissues, and the mRNA levels were largely variable among gene members and tissues. Similar patterns of the time-course expression were detected in most of the aqp genes in T. fasciatus between the two acute groups, except that only one gene (aqpl2) in the kidney and three genes (aqp7, aqp8 and aqp10) in the intestine revealed different expression patterns. These results suggest that the expression response of aqp genes was similar under osmotic changes with different rates.

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

Similar content being viewed by others

References

  • Agre P, King L S, Yasui M, et al. 2002. Aquaporin water channels-from atomic structure to clinical medicine. Journal of Physiology, 542(1): 3–16, doi: https://doi.org/10.1113/jphysiol.2002.020818

    Google Scholar 

  • An K W, Kim N N, Choi C Y. 2008. Cloning and expression of aquaporin 1 and arginine vasotocin receptor mRNA from the black porgy, Acanthopagrus schlegeli: effect of freshwater acclimation. Fish Physiology and Biochemistry, 34(2): 185–194, doi: https://doi.org/10.1007/s10695-007-9175-0

    Google Scholar 

  • Aoki M, Kaneko T, Katoh F, et al. 2003. Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. Journal of Experimental Biology, 206(19): 3495–3505, doi: https://doi.org/10.1242/jeb.00579

    Google Scholar 

  • Cao Jun, Shi Feng. 2019. Comparative analysis of the aquaporin gene family in 12 fish species. Animals, 9(5): 233, doi: https://doi.org/10.3390/ani9050233

    Google Scholar 

  • Cerdà J, Finn R N. 2010. Piscine aquaporins: an overview of recent advances. Journal of Experimental Zoology Part A, 313A(10): 623–650, doi: https://doi.org/10.1002/jez.634

    Google Scholar 

  • Choi Y J, Shin H S, Kim N N, et al. 2013. Expression of aquaporin-3 and −8 mRNAs in the parr and smolt stages of sockeye salmon, Oncorhynchus nerka: effects of cortisol treatment and seawater acclimation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 165(2): 228–236

    Google Scholar 

  • Cutler C P, Cramb G. 2000. Water transport and aquaporin expression in fish. In: Hohmann S, Nielsen S, eds. Molecular Biology and Physiology of Water and Solute Transport. Boston: Springer, 433–441

    Google Scholar 

  • Cutler C P, Cramb G. 2002. Branchial expression of an aquaporin 3(AQP-3) homologue is downregulated in the European eel Anguilla anguilla following seawater acclimation. Journal of Experimental Biology, 205(17): 2643–2651

    Google Scholar 

  • Cutler C P, Martinez A S, Cramb G. 2007. The role of aquaporin 3 in teleost fish. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 148(1): 82–91

    Google Scholar 

  • Cutler C P, Philips C, Hazon N, et al. 2009. Aquaporin 8 (AQP8) intestinal mRNA expression increases in response to salinity acclimation in yellow and silver European eels (Anguilla anguilla). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 153(2): S78

    Google Scholar 

  • Engelund M B, Madsen S S. 2011. The role of aquaporins in the kidney of euryhaline teleosts. Frontiers in Physiology, 2: 51

    Google Scholar 

  • Engelund M B, Madsen S S. 2015. Tubular localization and expressional dynamics of aquaporins in the kidney of seawater-chal-lenged Atlantic salmon. Journal of Comparative Physiology B, 185(2): 207–223, doi: https://doi.org/10.1007/s00360-014-0878-0

    Google Scholar 

  • Finn R N, Cerdà J. 2011. Aquaporin evolution in fishes. Frontiers in Physiology, 2: 44

    Google Scholar 

  • Giffard-Mena I, Boulo V, Abed C, et al. 2011. Expression and localization of aquaporin 1a in the sea-bass (Dicentrarchus labrax) during Ontogeny. Frontiers in Physiology, 2: 34

    Google Scholar 

  • Giffard-Mena I, Boulo V, Aujoulat F, et al. 2007. Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): the effect of salinity on AQP1 and AQP3 expression. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 148(2): 430–444

    Google Scholar 

  • Giffard-Mena I, Lorin-Nebel C, Charmantier G, et al. 2008. Adaptation of the sea-bass (Dicentrarchus labrax) to fresh water: role of aquaporins and Na+/K+-ATPases. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 150(3): 332–338

    Google Scholar 

  • Gonzalez R J. 2012. The physiology of hyper-salinity tolerance in teleost fish: a review. Journal of Comparative Physiology B, 182(3): 321–329, doi: https://doi.org/10.1007/s00360-011-0624-9

    Google Scholar 

  • Gorelick D A, Praetorius J, Tsunenari T, et al. 2006. Aquaporin-11: a channel protein lacking apparent transport function expressed in brain. BMC Biochemistry, 7: 14, doi: https://doi.org/10.1186/1471-2091-7-14

    Google Scholar 

  • Goto A. 1990. Alternative life-history styles of Japanese freshwater sculpins revisited. Environmental Biology of Fishes, 28(1–4): 101–112, doi: https://doi.org/10.1007/BF00751030

    Google Scholar 

  • Hamdi M, Sanchez M A, Beene L C, et al. 2009. Arsenic transport by zebrafish aquaglyceroporins. BMC Molecular Biology, 10: 104, doi: https://doi.org/10.1186/1471-2199-10-104

    Google Scholar 

  • Hara-Chikuma M, Verkman A S. 2006. Physiological roles of glycerol-transporting aquaporins: the aquaglyceroporins. Cellular and Molecular Life Sciences CMLS, 63(12): 1386–1392, doi: https://doi.org/10.1007/s00018-006-6028-4

    Google Scholar 

  • Harper C, Wolf J C. 2009. Morphologic effects of the stress response in fish. Ilar Journal, 50(4): 387–396, doi: https://doi.org/10.1093/ilar.50.4.387

    Google Scholar 

  • Ip Y K, Soh M M L, Chen X L, et al. 2013. Molecular characterization of branchial aquaporin 1aa and effects of seawater acclimation, emersion or ammonia exposure on its mRNA expression in the gills, gut, kidney and skin of the freshwater climbing perch, Anabas testudineus. PLoS One, 8(4): e61163, doi: https://doi.org/10.1371/journal.pone.0061163

    Google Scholar 

  • Itoh T, Rai T, Kuwahara M, et al. 2005. Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochemical and Biophysical Research Communications, 330(3): 832–838, doi: https://doi.org/10.1016/j.bbrc.2005.03.046

    Google Scholar 

  • Jeong S Y, Kim J H, Lee W O, et al. 2014. Salinity changes in the anadromous river pufferfish, Takifugu obscurus, mediate gene regulation. Fish Physiology and Biochemistry, 40(1): 205–219, doi: https://doi.org/10.1007/s10695-013-9837-z

    Google Scholar 

  • Kim Y K, Lee S Y, Kim B S, et al. 2014. Isolation and mRNA expression analysis of aquaporin isoforms in marine medaka Oryzias dancena, a euryhaline teleost. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 171: 1–8

    Google Scholar 

  • Kim Y K, Watanabe S, Kaneko T, et al. 2010. Expression of aquaporins 3, 8 and 10 in the intestines of freshwater- and seawater-acclimated Japanese eels Anguilla japonica. Fisheries Science, 76(4): 695–702, doi: https://doi.org/10.1007/s12562-010-0259-x

    Google Scholar 

  • King L S, Kozono D, Agre P. 2004. From structure to disease: the evolving tale of aquaporin biology. Nature Reviews Molecular Cell Biology, 5(9): 687–698, doi: https://doi.org/10.1038/nrm1469

    Google Scholar 

  • Lema S C, Carvalho P G, Egelston J N, et al. 2018. Dynamics of gene expression responses for ion transport proteins and aquaporins in the gill of a euryhaline pupfish during freshwater and high-salinity acclimation. Physiological and Biochemical Zoology, 91(6): 1148–1171, doi: https://doi.org/10.1086/700432

    Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the \({2^{ - {\rm{\Delta \Delta }}{C_{\rm{T}}}}}\) method. Methods, 25(4): 402–408, doi: https://doi.org/10.1006/meth.2001.1262

    Google Scholar 

  • Ma Qian, Liu Xinfu, Feng Wenrong, et al. 2018. Analyses of the molecular mechanisms associated with salinity adaption of Trachidermus fasciatus through combined iTRAQ-based proteomics and RNA sequencing-based transcriptomics. Progress in Biophysics and Molecular Biology, 136: 40–53, doi: https://doi.org/10.1016/j.pbio-molbio.2018.02.003

    Google Scholar 

  • Madsen S S, Engelund M B, Cutler C P. 2015. Water transport and functional dynamics of aquaporins in osmoregulatory organs of fishes. The Biological Bulletin, 229(1): 70–92, doi: https://doi.org/10.1086/BBLv229n1p70

    Google Scholar 

  • Marshall W S, Grosell M. 2006. Ion transport, osmoregulation, and acid-base balance. The Physiology of Fishes, 3: 177–230

    Google Scholar 

  • Martinez A S, Cutler C P, Wilson G D, et al. 2005. Regulation of expression of two aquaporin homologs in the intestine of the European eel: effects of seawater acclimation and cortisol treatment. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288(6): R1733–R1743, doi: https://doi.org/10.1152/ajpregu.00747.2004

    Google Scholar 

  • Mobasheri A, Marples D. 2004. Expression of the AQP-1 water channel in normal human tissues: a semiquantitative study using tissue microarray technology. American Journal of Physiology-Cell Physiology, 286(3): C529–C537, doi: https://doi.org/10.1152/ajpcell.00408.2003

    Google Scholar 

  • Nielsen S, Frokiaer J, Marples D, et al. 2002. Aquaporins in the kidney: from molecules to medicine. Physiological Reviews, 82(1): 205–244, doi: https://doi.org/10.1152/physrev.00024.2001

    Google Scholar 

  • Raldúa D, Otero D, Fabra M, et al. 2008. Differential localization and regulation of two aquaporin-1 homologs in the intestinal epithelia of the marine teleost Sparus aurata. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 294(3): R993–R1003, doi: https://doi.org/10.1152/ajpregu.00695.2007

    Google Scholar 

  • Santos C R A, Estêvāo M D, Fuentes J, et al. 2004. Isolation of a novel aquaglyceroporin from a marine teleost (Sparus auratus): function and tissue distribution. Journal of Experimental Biology, 207(7): 1217–1227, doi: https://doi.org/10.1242/jeb.00867

    Google Scholar 

  • Takata K, Matsuzaki T, Tajika Y. 2004. Aquaporins: water channel proteins of the cell membrane. Progress in Histochemistry and Cytochemistry, 39(1): 1–83, doi: https://doi.org/10.1016/j.proghi.2004.03.001

    Google Scholar 

  • Tingaud-Sequeira A, Calusinska M, Finn R N, et al. 2010. The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evolutionary Biology, 10: 38, doi: https://doi.org/10.1186/1471-2148-10-38

    Google Scholar 

  • Tingaud-Sequeira A, Chauvigné F, Fabra M, et al. 2008. Structural and functional divergence of two fish aquaporin-1 water channels following teleost-specific gene duplication. BMC Evolutionary Biology, 8: 259, doi: https://doi.org/10.1186/1471-2148-8-259

    Google Scholar 

  • Tipsmark C K, Sønsen K J, Madsen S S. 2010. Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. Journal of Experimental Biology, 213(3): 368–379, doi: https://doi.org/10.1242/jeb.034785

    Google Scholar 

  • Verkman A S, Binder D K, Bloch O, et al. 2006. Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochimica et Biophysica Acta (BBA)—Biomembranes, 1758(8): 1085–1093, doi: https://doi.org/10.1016/j.bbamem.2006.02.018

    Google Scholar 

  • Watanabe S, Kaneko T, Aida K. 2005. Aquaporin-3 expressed in the basolateral membrane of gill chloride cells in Mozambique tilapia Oreochromis mossambicus adapted to freshwater and seawater. Journal of Experimental Biology, 208(14): 2673–2682, doi: https://doi.org/10.1242/jeb.01684

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China

    Qian Ma

  2. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Qian Ma, Xinfu Liu, Ang Li, Shufang Liu & Zhimeng Zhuang

Authors
  1. Qian Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xinfu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shufang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhimeng Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qian Ma.

Additional information

Foundation item: The Qingdao Applied Basic Research Project under contract No. 14-2-4-15-jch; the National Natural Science Foundation of China under contract No. 31772828.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, Q., Liu, X., Li, A. et al. Effects of osmotic stress on the expression profiling of aquaporin genes in the roughskin sculpin (Trachidermus fasciatus). Acta Oceanol. Sin. 39, 19–25 (2020). https://doi.org/10.1007/s13131-020-1594-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-020-1594-0

Key words

Search

Navigation