Skip to main content
SpringerLink
Log in

Cloning and molecular characterization of cationic amino acid transporter y+LAT1 in grass carp (Ctenopharyngodon idellus)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The solute carrier family 7A, member 7 gene encodes the light chain- y+L amino acid transporter-1 (y+LAT1) of the heterodimeric carrier responsible for cationic amino acid (CAA) transport across the basolateral membranes of epithelial cells in intestine and kidney. Rising attention has been given to y+LAT1 involved in CAA metabolic pathways and growth control. The molecular characterization and function analysis of y+LAT1 in grass carp (Ctenopharyngodon idellus) is currently unknown. In the present study, full-length cDNA (2,688 bp), which encodes y+LAT1 and contains a 5′-untranslated region (319 bp), an open reading frame (1,506 bp) and a 3′-untranslated region (863 bp), has been cloned from grass carp. Amino acid sequence of grass carp y+LAT1 contains 11 transmembrane domains and shows 95 %, 80 % and 75 % sequence similarity to zebra fish, amphibian and mammalian y+LAT1, respectively. The tissue distribution and expression regulation by fasting of y+LAT1 mRNA were analyzed using real-time PCR. Our results showed that y+LAT1 mRNA was highly expressed in midgut, foregut and spleen while weakly expressed in hindgut, kidney, gill, brain, heart, liver and muscle. Nutritional status significantly influenced y+LAT1 mRNA expression in fish tissues, such as down-regulation of y+LAT1 mRNA expression after fasting (14 days).

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

  • Aranda A, Sánchez-Vázquez F, Madrid J (2001) Effect of short-term fasting on macronutrient self-selection in sea bass. Physiol Behav 73(1):105–109

    Article  CAS  PubMed  Google Scholar 

  • Barilli A, Rotoli BM, Visigalli R, Bussolati O, Gazzola GC, Kadija Z, Rodi G, Mariani F, Ruzza ML, Luisetti M, Dall’Asta V (2010) In Lysinuric Protein Intolerance system y+L activity is defective in monocytes and in GM-CSF-differentiated macrophages. Orphanet J Rare Dis 5:32

    Article  PubMed Central  PubMed  Google Scholar 

  • Barilli A, Rotoli BM, Visigalli R, Bussolati O, Gazzola GC, Dall’Asta V (2011) Arginine transport in human monocytic leukemia THP-1 cells during macrophage differentiation. J Leukocyte Biol 90(2):293–303

    Article  CAS  PubMed  Google Scholar 

  • Bröer A, Wagner C, Lang F, Bröer S (2000) The heterodimeric amino acid transporter 4F2hc/y+LAT2 mediates arginine efflux in exchange with glutamine. Biochem J 349(Pt 3):787

    PubMed  Google Scholar 

  • Cheeseman CI, Gupta AK, Yao SYM, Young JD (2001) Distribution of the y+LAT1 cationic amino acid transporter in the epithelial cells of rat small intestine. FASEB J 15(5):A838

    Google Scholar 

  • Chillaron J, Roca R, Valencia A, Zorzano A, Palacín M (2001) Heteromeric amino acid transporters: biochemistry, genetics, and physiology. Am J Physiol-Renal Physiol 281(6):F995–F1018

    CAS  PubMed  Google Scholar 

  • Cooper C, Shayeghi M, Techau M, Capdevila D, MacKenzie S, Durrant C, Bury N (2007) Analysis of the rainbow trout solute carrier 11 family reveals iron import⩽ pH 7.4 and a functional isoform lacking transmembrane domains 11 and 12. FEBS Lett 581(14):2599–2604

    Article  CAS  PubMed  Google Scholar 

  • Dall’Asta V, Bussolati O, Sala R, Rotoli BM, Sebastio G, Sperandeo MP, Andria G, Gazzola GC (2000) Arginine transport through system y+L in cultured human fibroblasts: normal phenotype of cells from LPI subjects. Am J Physiol-Cell Ph 279(6):C1829–C1837

    Google Scholar 

  • Dave MH, Schulz N, Zecevic M, Wagner CA, Verrey F (2004) Expression of heteromeric amino acid transporters along the murine intestine. J Physiol 558(2):597–610

    Article  CAS  PubMed  Google Scholar 

  • Deves R, Boyd C (1998) Transporters for cationic amino acids in animal cells: discovery, structure, and function. Physiol Rev 78(2):487–545

    CAS  PubMed  Google Scholar 

  • Deves R, Chavez P, Boyd C (1992) Identification of a new transport system (y+L) in human erythrocytes that recognizes lysine and leucine with high affinity. J Physiol 454(1):491–501

    CAS  PubMed  Google Scholar 

  • Feng DY, Zhou XY, Zuo JJ, Zhang CM, Yin YL, Wang XQ, Wang T (2008) Segmental distribution and expression of two heterodimeric amino acid transporter mRNAs in the intestine of pigs during different ages. J Sci Food Agric 88(6):1012–1018

    Article  CAS  Google Scholar 

  • Gilbert ER, Li H, Ernmersonj DA, Webb KE, Wong EA (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86(8):1739–1753

    CAS  PubMed  Google Scholar 

  • Gu W, Fang J, Wang W, Fan M, Geng M, Li T, Chu W (2010) Molecular cloning, segmental distribution and ontogenetic expression of the amino acid transporter y+LAT1 in intestine of the Tibetan suckling piglets. J Food Agric Environ 8(2):1067–1072

    CAS  Google Scholar 

  • Habold C, Reichardt F, Foltzer-Jourdainne C, Lignot JH (2007) Morphological changes of the rat intestinal lining in relation to body stores depletion during fasting and after refeeding. Pflügers Arch 455(2):323–332

    Article  CAS  PubMed  Google Scholar 

  • Hakim Y, Harpaz S, Uni Z (2009) Expression of brush border enzymes and transporters in the intestine of European sea bass (Dicentrarchus labrax) following food deprivation. Aquaculture 290(1):110–115

    Article  CAS  Google Scholar 

  • Ihara T, Tsujikawa T, Fujiyama Y, Bamba T (2000) Regulation of PepT1 peptide transporter expression in the rat small intestine under malnourished conditions. Digestion 61(1):59–67

    Article  CAS  PubMed  Google Scholar 

  • Kanai Y, Fukasawa Y, Cha SH, Segawa H, Chairoungdua A, Matsuo H, Kim JY, Miyamoto K, Takeda E, Endou H (2000) Transport properties of a system y+L neutral and basic amino acid transporter. J Biol Chem 275(27):20787–20793

    Article  CAS  PubMed  Google Scholar 

  • Li CJ, Liu L, Chen XH, Zhang T, Gan F, Cheng BL (2010) Identification of a vasa homologue gene in grass carp and its expression pattern in tissues and during embryogenesis. Comp Biochem Physiol B: Biochem Mol Biol 157(2):159–166

    Article  Google Scholar 

  • Liao SF, Vanzant ES, Harmon DL, McLeod KR, Boling JA, Matthews JC (2009) Ruminal and abomasal starch hydrolysate infusions selectively decrease the expression of cationic amino acid transporter mRNA by small intestinal epithelia of forage-fed beef steers. J Dairy Sci 92(3):1124–1135

    Article  CAS  PubMed  Google Scholar 

  • Manjarin R, Steibel JP, Zamora V, Am-in N, Kirkwood RN, Ernst CW, Weber PS, Taylor NP, Trottier NL (2011) Transcript abundance of amino acid transporters, beta-casein, and alpha-lactalbumin in mammary tissue of periparturient, lactating, and postweaned sows. J Dairy Sci 94(7):3467–3476

    Article  CAS  PubMed  Google Scholar 

  • Mastroberardino L, Spindler B, Pfeiffer R, Skelly PJ, Loffing J, Shoemaker CB, Verrey F (1998) Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature 395(6699):288–291

    Article  CAS  PubMed  Google Scholar 

  • Mendes Ribeiro A, Brunini T, Yaqoob M, Aronson J, Mann G, Ellory J (1999) Identification of system y+L as the high-affinity transporter for l-arginine in human platelets: up-regulation of l-arginine influx in uraemia. Pflügers Arch 438(4):573–575

    Article  CAS  PubMed  Google Scholar 

  • Naruhashi K, Sai Y, Tamai I, Suzuki N, Tsuji A (2002) PepT1 mRNA expression is induced by starvation and its level correlates with absorptive transport of cefadroxil longitudinally in the rat intestine. Pharm Res 19(10):1417–1423

    Article  CAS  PubMed  Google Scholar 

  • Novak D, Matthews J, Beveridge M, Yao S, Young J, Kilberg M (1997) Demonstration of system y+L activity on the basal plasma membrane surface of rat placenta and developmentally regulated expression of 4F2HC mRNA. Placenta 18(8):643–648

    Article  CAS  PubMed  Google Scholar 

  • Ogihara H, Suzuki T, Nagamachi Y, Inui K, Takata K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochem J 31(3):169–174

    Article  CAS  PubMed  Google Scholar 

  • Oyanagi K, Nagao M (1998) Lysinuric protein intolerance and other cationic aminoacidurias. Ryōikibetsu shōkōgun shirīzu 19:562–564

    Google Scholar 

  • Palacín M, Estévez R, Bertran J, Zorzano A (1998) Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 78(4):969–1054

    PubMed  Google Scholar 

  • Palacín M, Borsani G, Sebastio G (2001) The molecular bases of cystinuria and lysinuric protein intolerance. Curr Opin Genet Dev 11(3):328–335

    Article  PubMed  Google Scholar 

  • Pfeiffer R, Rossier G, Spindler B, Meier C, Kühn L, Verrey F (1999) Amino acid transport of y+L-type by heterodimers of 4F2hc/CD98 and members of the glycoprotein-associated amino acid transporter family. EMBO J 18(1):49–57

    Article  CAS  PubMed  Google Scholar 

  • Pineda M, Fernández E, Torrents D, Estévez R, López C, Camps M, Lloberas J, Zorzano A, Palacín M (1999) Identification of a membrane protein, LAT-2, that co-expresses with 4F2 heavy chain, an L-type amino acid transport activity with broad specificity for small and large zwitterionic amino acids. J Biol Chem 274(28):19738–19744

    Article  CAS  PubMed  Google Scholar 

  • Rotoli BM, Dall’Asta V, Barilli A, D’Ippolito R, Tipa A, Olivieri D, Gazzola GC, Bussolati O (2007) Alveolar macrophages from normal subjects lack the NOS-related system y+ for arginine transport. Am J Respir Cell Mol Biol 37(1):105–112

    Article  CAS  PubMed  Google Scholar 

  • Sato H, Tamba M, Ishii T, Bannai S (1999) Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274(17):11455–11458

    Article  CAS  PubMed  Google Scholar 

  • Schwertfeger M, Pissowotzki K, Fleck C, Taylor PM (2003) Regulation of l-leucine transport in rat kidney by dexamethasone and triiodothyronine. Amino Acids 25(1):75–83

    CAS  PubMed  Google Scholar 

  • Sperandeo MP, Annunziata P, Bozzato A, Piccolo P, Maiuri L, D’Armiento M, Ballabio A, Corso G, Andria G, Borsani G (2007) SLC7A7 disruption causes fetal growth retardation by downregulating Igf1 in the mouse model of lysinuric protein intolerance. Am J Physiol-Cell Physiol 293(1):C191–C198

    Article  CAS  PubMed  Google Scholar 

  • Torrents D, Estévez R, Pineda M, Fernández E, Lloberas J, Shi YB, Zorzano A, Palacín M (1998) Identification and characterization of a membrane protein (y+L amino acid transporter-1) that associates with 4F2hc to encode the amino acid transport activity y+L. A candidate gene for lysinuric protein intolerance. J Biol Chem 273(49):32437–32445

    Article  CAS  PubMed  Google Scholar 

  • Torrents D, Mykkänen J, Pineda M, Feliubadaló L, Estévez R, de Cid R, Sanjurjo P, Zorzano A, Nunes V, Huoponen K (1999) Identification of SLC7A7, encoding y+LAT-1, as the lysinuric protein intolerance gene. Nat Genet 21(3):293–296

    Article  CAS  PubMed  Google Scholar 

  • Verrey F, Meier C, Rossier G, Kühn LC (2000) Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflügers Arch 440(4):503–512

    CAS  PubMed  Google Scholar 

  • Verrey F, Closs EI, Wagner CA, Palacin M, Endou H, Kanai Y (2004) CATs and HATs: the SLC7 family of amino acid transporters. Pflügers Arch 447(5):532–542

    Article  CAS  PubMed  Google Scholar 

  • Wagner CA, Lang F, Bröer S (2001) Function and structure of heterodimeric amino acid transporters. Am J Physiol-Cell Ph 281(4):C1077–C1093

    CAS  Google Scholar 

  • Wang L, Yang B, Wang R, Du X (2008) Extraction of pepsin-soluble collagen from grass carp (Ctenopharyngodon idella) skin using an artificial neural network. Food Chem 111(3):683–686

    Article  CAS  Google Scholar 

  • Zhi A, Zhou X, Zuo J, Zou S, Huang Z, Wang X, Tao L, Feng D (2010) Molecular cloning, tissue distribution and expression of porcine y+L amino acid transporter-1. Asian Aust J Anim 23:272–278

    CAS  Google Scholar 

Download references

Acknowledgments

We were grateful to Dr. Shan He (Huazhong Agricultural University, China) for her helpful review of the manuscript. This research was supported by Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (Project No. 2009QC022).

Author information

Authors and Affiliations

  1. Fisheries College, Huazhong Agricultural University, Wuhan, 430070, China

    Jixuan Yang, Qingsong Tan, Wenhuan Zhu, Chen Chen & Xufang Liang

  2. Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, Wuhan, 430070, China

    Qingsong Tan & Xufang Liang

  3. Key Laboratory of Ecological Impacts of Hydraulic-Projects and Restoration of Aquatic Ecosystem, Institute of Hydroecology, Ministry of Water Resources and Chinese Academy of Sciences, Wuhan, 430079, China

    Lei Pan

Authors
  1. Jixuan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qingsong Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenhuan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xufang Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lei Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qingsong Tan or Lei Pan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, J., Tan, Q., Zhu, W. et al. Cloning and molecular characterization of cationic amino acid transporter y+LAT1 in grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 40, 93–104 (2014). https://doi.org/10.1007/s10695-013-9827-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-013-9827-1

Keywords

Search

Navigation