期刊论文详细信息
BMC Genomics
Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus
Yuen Kwong Ip1  Toong Jin Lam1  Sinnakaruppan Mathavan3  Wing-Kin Sung3  Shaojiang Cai4  Zhengjun Li2  Eei Yin Lui2  Siew Hong Lam1 
[1] Department of Biological Science, National University of Singapore, S3-Level 5, 14 Science Drive 4, 117543 Singapore, Singapore;NUS Environmental Research Institute, National University of Singapore, 5A Engineering Drive, 117411 Singapore, Singapore;Genome Institute of Singapore, 60 Biopolis Street, 138672, Singapore, Singapore;School of Computing, National University of Singapore, 13 Computing Drive, 117417 Singapore, Singapore
关键词: Mozambique tilapia Oreochromis mossambicus;    Euryhaline fish gills;    Cellular remodeling;    Iono-osmoregulation;    Signaling pathways;    Gene expression;    RNA sequencing;    Transcriptomic analysis;   
Others  :  1128436
DOI  :  10.1186/1471-2164-15-921
 received in 2014-06-04, accepted in 2014-10-13,  发布年份 2014
PDF
【 摘 要 】

Background

The Mozambique tilapia Oreochromis mossambicus has the ability to adapt to a broad range of environmental salinities and has long been used for investigating iono-osmoregulation. However, to date most studies have focused mainly on several key molecules or parameters hence yielding a limited perspective of the versatile iono-osmoregulation in the euryhaline fish. This study aimed to capture transcriptome-wide differences between the freshwater- and seawater-acclimated gills of the Mozambique tilapia.

Results

We have identified over 5000 annotated gene transcripts with high homology (E-value <1.0E-50) to human genes that were differentially expressed in freshwater- and seawater-acclimated gills of the Mozambique tilapia. These putative human homologs were found to be significantly associated with over 50 canonical signaling pathways that are operating in at least 23 biological processes in relation to branchial iono-osmoregulation and cellular remodeling. The analysis revealed multiple signaling pathways in freshwater-acclimated gills acting in concert to maintain cellular homeostasis under hypo-osmotic environment while seawater-acclimated gills abounded with molecular signals to cope with the higher cellular turn-over rate, energetics and iono-regulatory demands under hyper-osmostic stress. Additionally, over 100 transcripts encoding putative inorganic ion transporters/channels were identified, of which several are well established in gill iono-regulation while the remainder are lesser known. We have also validated the expression profiles of 47 representative genes in freshwater- and seawater-acclimated gills, as well as in hypersaline-acclimated (two-fold salinity of seawater) gills. The findings confirmed that many of these responsive genes retained their expression profiles in hypersaline-acclimated gills as in seawater-acclimated gills, although several genes had changed significantly in their expression level/direction in hypersaline-acclimated gills.

Conclusions

This is the first study that has provided an unprecedented transcriptomic-wide perspective of gill iono-osmoregulation since such studies were initiated more than 80 years ago. It has expanded our molecular perspective from a relatively few well-studied molecules to a plethora of gene transcripts and a myriad of canonical signaling pathways driving various biological processes that are operating in gills under hypo-osmotic and hyper-osmotic stresses. These findings would provide insights and resources to fuel future studies on gill iono-osmoregulation and cellular remodeling in response to salinity challenge and acclimation.

【 授权许可】

   
2014 Lam et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150223112557356.pdf 2942KB PDF download
Figure 8. 89KB Image download
Figure 7. 72KB Image download
Figure 6. 62KB Image download
Figure 5. 151KB Image download
Figure 4. 145KB Image download
Figure 3. 92KB Image download
Figure 2. 96KB Image download
Figure 1. 124KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】
  • [1]Schultz ET, McCormick SD: Euryhalinity in an Evolutionary Context. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:477-533.
  • [2]Kültz D: Osmosensing. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:45-68.
  • [3]Marshall WS: Mechanosensitive signalling in fish gill and other ion transporting epithelia. Acta Physiol 2011, 202:487-499.
  • [4]Edwards SL, Marshall WS: Principles and Patterns of Osmoregulation and Euryhalinities in Fishes. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:1-44.
  • [5]Evans DH, Piermarini PM, Choe KP: The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid–base regulation, and excretion of nitrogenous waste. Physiol Rev 2005, 85:97-177.
  • [6]Hwang PP, Lee TH: New insights into fish ion regulation and mitochondrion- rich cells. Comp Biochem Physiol A 2007, 148:479-497.
  • [7]Hwang PP, Lee TH, Lin LY: Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 2011, 301:R28-R47.
  • [8]Hiroi J, McCormick SD: New insights into gill ionocyte and ion transporter function in euryhaline and diadromous fish. Respir Physiol Neurobiol 2012, 184:257-268.
  • [9]Brauner CJ, Gonzalez RJ, Wilson JM: Extreme Environments: Hypersaline, Alkaline and Ion-poor Waters. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:435-476.
  • [10]Gonzalez RJ: The physiology of hyper-salinity tolerance in teleost fish: a review. J Comp Physiol B 2012, 182:321-329.
  • [11]Marshall WS: Osmoregulation in Estuarine and Intertidal Fishes. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:395-434.
  • [12]Fiol DF, Chan SY, Kültz D: Identification and pathway analysis of immediate hyperosmotic stress responsive molecular mechanisms in tilapia (Oreochromis mossambicus) gill. Comp Biochem Physiol Part D Genomics Proteomics 2006, 1:344-356.
  • [13]Kalujnaia S, McWilliam IS, Zaguinaiko VA, Feilen AL, Nicholson J, Hazon N, Cutler CP, Cramb G: Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla. Physiol Genomics 2007, 31:385-401.
  • [14]Evans TG, Somero GN: A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fish Gillichthys mirabilis: osmosensors to effectors. J Exp Biol 2008, 211:3636-3649.
  • [15]Tse WK, Sun J, Zhang H, Law AY, Yeung BH, Chow SC, Qiu JW, Wong CK: Transcriptomic and iTRAQ proteomic approaches reveal novel short-term hyperosmotic stress responsive proteins in the gill of the Japanese eel (Anguilla japonica). J Proteomics 2013, 89:81-94.
  • [16]Ramsköld D, Wang ET, Burge CB, Sandberg R: An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 2009, 5:e1000598.
  • [17]Ridley A: Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006, 16:522-529.
  • [18]Shen L, Turner JR: Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 2005, 16:3919-3936.
  • [19]Karnaky KJ Jr: Teleost Osmoregulation: Changes in the Tight Junction in Response to the Salinity of the Environment. In Tight Junctions. Edited by Cereijido M. Boca Raton, FL: CRC; 1991:175-185.
  • [20]Tipsmark CK, Baltzegar DA, Ozden O, Grubb BJ, Borski RJ: Salinity regulates claudin mRNA and protein expression in the teleost gill. Am J Physiol Regul Integr Comp Physiol 2008, 294:R1003-R1014.
  • [21]Duffy NM, Bui P, Bagherie-Lachidan M, Kelly SP: Epithelial remodelling and claudin mRNA abundance in the gill and kidney of puffer fish (Tetraodon biocellatus) acclimated to altered environmental ion levels. J Comp Physiol B 2011, 181:219-238.
  • [22]Hoffman E, Lambert I, Pedersen S: Physiology of cell volume regulation in vertebrates. Physiol Rev 2009, 89:193-277.
  • [23]Kültz D, Burg M: Evolution of osmotic stress signaling via MAP kinase cascades. J Exp Biol 1998, 201:3015-3021.
  • [24]Kültz D, Avila K: Mitogen activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp Biochem Physiol B 2001, 129:821-829.
  • [25]Dubois JM, Rouzaire-Dubois B: The influence of cell volume changes on tumour cell proliferation. Eur Biophys J 2004, 33:227-232.
  • [26]Rouzaire-Dubois B, O’Regan S, Dubois JM: Cell size-dependent and independent proliferation of rodent neuroblastoma glioma cells. J Cell Physiol 2005, 203:243-250.
  • [27]Kültz D, Chakravarty D, Adilakshmi T: A novel 14-3-3 gene is osmoregulated in gill epithelium of the euryhaline teleost Fundulus heteroclitus. J Exp Biol 2001, 204:2975-2985.
  • [28]Kohn A, Chakravarty D, Kültz D: Teleost Fh14-3-3a protein protects Xenopus oocytes from hyperosmolality. J Exp Zool Part A Comp Exp Biol 2003, 299:103-109.
  • [29]Takei Y, McCormick SD: Hormonal Control of Fish Euryhalinity. In Euryhaline Fishes. Fish Physiology, Volume 32. Edited by Mccormick SD, Farrell AP, Brauner CJ. Amsterdam: Academic; 2012:69-123.
  • [30]Fiol DF, Sanmarti E, Sacchi R, Kültz D: A novel tilapia prolactin receptor is functionally distinct from its paralog. J Exp Biol 2009, 212:2007-2015.
  • [31]Breves JP, Watanabe S, Kaneko T, Hirano T, Grau EG: Prolactin restores branchial mitochondrion-rich cells expressing Na+/Cl- cotransporter in hypophysectomized Mozambique tilapia. Am J Physiol Regul Integr Comp Physiol 2010, 299:R702-R710.
  • [32]Fournier D, Luft FC, Bader M, Ganten D, Andrade-Navarro MA: Emergence and evolution of the renin-angiotensin-aldosterone system. J Mol Med 2012, 90:495-508.
  • [33]Janicke M, Carney TJ, Hammerschmidt M: Foxi3 transcription factors and Notch signaling control the formation of skin ionocytes from epidermal precursors of the zebrafish embryo. Dev Biol 2007, 307:258-271.
  • [34]Esaki M, Hoshijima K, Nakamura N, Munakata K, Tanaka M, Ookata K, Asakawa K, Kawakami K, Wang W, Weinberg ES, Hirose S: Mechanism of development of ionocytes rich in vacuolar-type H-ATPase in the skin of zebrafish larvae. Dev Biol 2009, 329:116-129.
  • [35]Chang WJ, Horng JL, Yan JJ, Hsiao CD, Hwang PP: The transcription factor, glial cell missing 2, is involved in differentiation and functional regulation of H-ATPase-rich cells in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 2009, 296:R1192-R1201.
  • [36]Thermes V, Lin CC, Hwang PP: Expression of Ol-foxi3 and Na/K-ATPase in ionocytes during the development of euryhaline medaka (Oryzias latipes) embryos. Gene Expr Patterns 2010, 10:185-192.
  • [37]Kültz D, Bastrop R, Jürss K, Siebers D: Mitochondria rich (MR) cells and the activities of the Na+/K + -ATPase and carbonic anhydrase in the gill and opercular epithelium of Oreochromis mossambicus adapted to various salinities. Comp Biochem Physiol B 1992, 102:293-301.
  • [38]Kammerer BD, Sardella BA, Kültz D: Salinity stress results in rapid cell cycle changes of tilapia (Oreochromis mossambicus) gill epithelial cells. J Exp Zool A Ecol Genet Physiol 2009, 311:80-90.
  • [39]Inokuchi M, Kaneko T: Recruitment and degeneration of mitochondrion-rich cells in the gills of Mozambique tilapia Oreochromis mossambicus during adaptation to a hyperosmotic environment. Comp Biochem Physiol A Mol Integr Physiol 2012, 162:245-251.
  • [40]Kültz D, Chakravarty D: Hyperosmolality in the form of elevated NaCl but not urea causes DNA damage in murine kidney cells. Proc Natl Acad Sci U S A 2001, 98:1999-2004.
  • [41]Zhang Z, Dmitrieva NI, Park JH, Levine RL, Burg MB: High urea and NaCl carbonylate proteins in renal cells in culture and in vivo, and high urea causes 8-oxoguanine lesions in their DNA. Proc Natl Acad Sci U S A 2004, 101:9491-9496.
  • [42]Kültz D: Hyperosmolality triggers oxidative damage in kidney cells. Proc Natl Acad Sci U S A 2004, 101:9177-9178.
  • [43]Chretien M, Pisam M: Cell renewal and differentiation in the gill epithelium of fresh-water-adapted or salt-water adapted euryhaline fish as revealed by [H-3] thymidine autoradiography. Biol Cell 1986, 56:137-150.
  • [44]Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T: Evidence for an apical Na–Cl cotransporter involved in ion uptake in teleost fish. J Exp Biol 2008, 211:2584-2599.
  • [45]Horng JL, Hwang PP, Shin TH, Wen ZH, Lin CS, Lin LY: Chloride transport in mitochondrion-rich cells of euryhaline tilapia (Oreochromis mossambicus) larvae. Am J Physiol Cell Physiol 2009, 297:C845-C854.
  • [46]Kumai Y, Perry SF: Ammonia excretion via Rhcg1 facilitates Na+ uptake in larval zebrafish, Danio rerio, in acidic water. Am J Physiol Regul Integr Comp Physiol 2011, 301:R1517-R1528.
  • [47]Wilson JM, Laurent P, Tufts BL, Benos DJ, Donowitz M, Vogl AW, Randall DJ: NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J Exp Biol 2000, 203:2279-2296.
  • [48]Katoh F, Hyodo S, Kaneko T: Vacuolar-type proton pump in the basolateral plasma membrane energizes ion uptake in branchial mitochondria-rich cells of killifish Fundulus heteroclitus, adapted to a low ion environment. J Exp Biol 2003, 206:793-803.
  • [49]Furukawa F, Watanabe S, Inokuchi M, Kaneko T: Responses of gill mitochondria-rich cells in Mozambique tilapia exposed to acidic environments (pH 4.0) in combination with different salinities. Comp Biochem Physiol A Mol Integr Physiol 2011, 158:468-476.
  • [50]Tang CH, Lee TH: Ion-deficient environment induces the expression of basolateral chloride channel, ClC-3-like protein, in gill mitochondrion-rich cells for chloride uptake of the tilapia Oreochromis mossambicus. Physiol Biochem Zool 2011, 84:54-67.
  • [51]Hwang PP: Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 2009, 212:1745-1752.
  • [52]Inokuchi M, Hiroi J, Watanabe S, Lee KM, Kaneko T: Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria rich cells of Mozambique tilapia (Oreochromis mossambicus) acclimated to a wide range of salinities. Comp Biochem Physiol A Mol Integr Physiol 2008, 151:151-158.
  • [53]Inokuchi M, Hiroi J, Watanabe S, Hwang PP, Kaneko T: Morphological and functional classification of ion-absorbing mitochondria-rich cells in the gills of Mozambique tilapia. J Exp Biol 2009, 212:1003-1010.
  • [54]Feeney GP, Zheng D, Kille P, Hogstrand C: The phylogeny of teleost ZIP and ZnT zinc transporters and their tissue specific expression and response to zinc in zebrafish. Biochim Biophys Acta 2005, 1732:88-95.
  • [55]De Maio A, Vega VL, Contreras JE: Gap junctions, homeostasis, and injury. J Cell Physiol 2002, 191:269-28.
  • [56]Peiris TH, Oviedo NJ: Gap junction proteins: master regulators of the planarian stem cell response to tissue maintenance and injury. Biochim Biophys Acta 1828, 2013:109-117.
  • [57]Ouattara N, Bodinier C, Negre-Sadargues G, D’Cotta H, Messad S, Charmanteir G, Panfili J, Baroiller JF: Changes in gill ionocyte morphology and function following transfer from fresh to hypersaline waters in the tilapia Sarotherodon melanotheron. Aquaculture 2009, 290:155-164.
  • [58]Watanabe S, Kaneko T, Aida K: Aquaporin-3 expressed in the basolateral membrane of gill chloride cells in Mozambique tilapia Oreochromis mossambicus adapted to freshwater and seawater. J Exp Biol 2005, 208:2673-2682.
  • [59]Hara-Chikuma M, Verkman AS: Roles of aquaporin-3 in the epidermis. J Invest Dermatol 2008, 128:2145-2151.
  • [60]Lyons TP, Riedesel ML: Glycerol-induced hyperhydration: its effects on fluid compartments in the rat. Life Sci 1993, 53:1779-1787.
  • [61]Sardella B, Matey V, Cooper J, Gonzalez R, Brauner CJ: Physiological, biochemical, and morphological indicators of osmoregulatory stress in ‘California’ Mozambique tilapia (Oreochromis mossambicus x O. urolepis hornorum) exposed to hypersaline water. J Exp Biol 2004, 207:1399-1413.
  • [62]Amasheh S, Milatz S, Krug SM, Bergs M, Amasheh M, Schulzke JD, Fromm M: Na + absorption defends from paracellular back-leakage by claudin-8 upregulation. Biochem Biophys Res Commun 2009, 378:45-50.
  • [63]Jablonski EM, Webb AN, McConnell NA, Riley MC, Hughes FM Jr: Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am J Physiol Cell Physiol 2004, 286:C975-C985.
  • [64]Seoh ML, Ng CH, Yong J, Lim L, Leung T: ArhGAP15, a novel human RacGAP protein with GTPase binding property. FEBS Lett 2003, 539:131-137.
  • [65]Comes N, Buie LK, Borrás T: Evidence for a role of angiopoietin-like 7 (ANGPTL7) in extracellular matrix formation of the human trabecular meshwork: implications for glaucoma. Genes Cells 2011, 16:243-259.
  • [66]Zhang CC, Kaba M, Ge G, Xie K, Tong W, Hug C, Lodish HF: Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med 2006, 12:240-245.
  • [67]Breves JP, Seale AP, Helms RE, Tipsmark CK, Hirano T, Grau EG: Dynamic gene expression of GH/PRL-family hormone receptors in gill and kidney during freshwater-acclimation of Mozambique tilapia. Comp Biochem Physiol A Mol Integr Physiol 2011, 158:194-200.
  • [68]Lee CE, Bell MA: Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol Evol 1999, 14:284-288.
  • [69]NCBI Nucleotide database [http://www.ncbi.nlm.nih.gov/nuccore/ webcite]
  • [70]Oreochromis niloticus (Nile Tilapia) protein database [ftp://ftp.ncbi.nih.gov/genomes/Oreochromis_niloticus/protein/ webcite]
  • [71]Danio rerio (Zebrafish) protein database [ftp://ftp.ncbi.nih.gov/genomes/D_rerio/protein/ webcite]
  • [72]NCBI Blast databases [ftp://ftp.ncbi.nih.gov/blast/db/ webcite]
  • [73]Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
  • [74]Ingenuity Pathway Analysis™ (IPA) software [http://www.ingenuity.com webcite]
  • [75]NCBI Gene database http://www.ncbi.nlm.nih.gov/gene webcite
  • [76]GeneCard database [http://www.genecards.org/ webcite]
  • [77]Primer3Plus software [http://www.bioinformatics.nl/cgi-bin/primer3plus/primer3plus.cgi webcite]
  • [78]NCBI Sequence Read Archive (SRA) [http://www.ncbi.nlm.nih.gov/sra webcite]
  文献评价指标  
  下载次数:0次 浏览次数:10次