Amino Acids

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Expression of cationic amino acid transporters in pig skeletal muscles during postnatal development

  • Aiko Ishida
  • Akane Ashihara
  • Kazuki Nakashima
  • Masaya Katsumata
Original Article
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Abstract

The cationic amino acid transporter (CAT) protein family transports lysine and arginine in cellular amino acid pools. We hypothesized that CAT expression changes in pig skeletal muscles during rapid pig postnatal development. We aimed to investigate the tissue distribution and changes in the ontogenic expression of CATs in pig skeletal muscles during postnatal development. Six piglets at 1, 12, 26, 45, and 75 days old were selected from six litters, and their longissimus dorsi (LD), biceps femoris (BF), and rhomboideus (RH) muscles, and their stomach, duodenum, jejunum, ileum, colon, liver, kidney, heart, and cerebrum were collected. CAT-1 was expressed in all the 12 tissues investigated. CAT-2 (CAT-2A isoform) expression was highest in the skeletal muscle and liver and lowest in the jejunum, ileum, kidney, and heart. CAT-3 was expressed mainly in the colon and detected in the jejunum, ileum, and cerebrum. The CAT-1 expression was higher in the skeletal muscle of day 1 pigs than in that of older pigs (P < 0.05). The CAT-2 mRNA level was lowest at day 1, but increased with postnatal development (P < 0.05). There was no significant change in CAT-1 expression among the LD, BF, and RH during postnatal development (P > 0.05); however, there was a change in CAT-2 expression. The CAT-2 expression was highest in the LD of 12-, 26-, 45-, and 75-day-old pigs, followed by the BF and RH (P < 0.05). These results suggest that CAT-1 and CAT-2 play different roles in pig skeletal muscles during postnatal development.

Keywords

Cationic amino acid transporter Pig Postnatal development Skeletal muscle 

Supplementary material

726_2017_2478_MOESM1_ESM.pptx (2.9 mb)
Supplementary material 1 (PPTX 2985 kb)

References

  1. Capanni C, Squarzoni S, Petrini S et al (1998) Increase of neuronal nitric oxide synthase in rat skeletal muscle during ageing. Biochem Biophys Res Commun 245:216–219. doi:10.1006/bbrc.1998.8404 CrossRefPubMedGoogle Scholar
  2. Chang WJ, Iannaccone ST, Lau KS et al (1996) Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93:9142–9147CrossRefPubMedPubMedCentralGoogle Scholar
  3. Christensen HN (1990) Role of amino acid transport and countertransport in nutrition and metabolism. Physiol Rev 70:43–77PubMedGoogle Scholar
  4. Christova T, Grozdanovic Z, Gossrau R (1997) Nitric oxide synthase (NOS) I during postnatal development in rat and mouse skeletal muscle. Acta Histochem 99:311–324. doi:10.1016/S0065-1281(97)80025-6 CrossRefPubMedGoogle Scholar
  5. Closs EI, Lyons CR, Kelly C, Cunningham JM (1993) Characterization of the third member of the MCAT family of cationic amino acid transporters. Identification of a domain that determines the transport properties of the MCAT proteins. J Biol Chem 268:20796–20800PubMedGoogle Scholar
  6. Closs EI, Gräf P, Habermeier A, Cunningham JM, Förstermann U (1997) Human cationic amino acid transporters hCAT-1, hCAT-2A, and hCAT-2B: three related carriers with distinct transport properties. Biochemistry 36:6462–6468. doi:10.1021/bi962829p CrossRefPubMedGoogle Scholar
  7. Cui Z, Zharikov S, Xia SL, Anderson SI, Law AS, Archibald AL, Block ER (2005) Molecular cloning, characterization, and chromosomal assignment of porcine cationic amino acid transporter-1. Genomics 85:352–359. doi:10.1016/j.ygeno.2004.11.006 CrossRefPubMedGoogle Scholar
  8. Davies AS (1972) Postnatal changes in the histochemical fibre types of procine skeletal muscle. J Anat 113:213–240PubMedPubMedCentralGoogle Scholar
  9. Davis TA, Fiorotto ML, Nguyen HV, Reeds PJ (1989) Protein turnover in skeletal muscle of suckling rats. Am J Physiol 257:R1141–R1146PubMedGoogle Scholar
  10. Fowden AL, Apatu RS, Silver M (1995) The glucogenic capacity of the fetal pig: developmental regulation by cortisol. Exp Physiol 80:457–467. doi:10.1113/expphysiol.1995.sp003860 CrossRefPubMedGoogle Scholar
  11. Goldspink DF, Kelly FJ (1984) Protein turnover and growth in the whole body, liver and kidney of the rat from the foetus to senility. Biochem J 217:507–516. doi:10.1042/bj2170507 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Harrison AP, Latorre R, Dauncey MJ (1997) Postnatal development and differentiation of myofibres in functionally diverse porcine skeletal muscles. Reprod Fertil Dev 9:731–740. doi:10.1071/R97026 CrossRefPubMedGoogle Scholar
  13. Heo J, Kattesh HG, Roberts MP, Schneider JF (2003) Plasma levels of cortisol and corticosteroid-binding globulin (CBG) and hepatic CBG mRNA expression in pre- and postnatal pigs. Domest Anim Endocrinol 25:263–273. doi:10.1016/S0739-7240(03)00055-9 CrossRefPubMedGoogle Scholar
  14. Hosokawa H, Sawamura T, Kobayashi S, Ninomiya H, Miwa S, Masaki T (1997) Cloning and characterization of a brain-specific cationic amino acid transporter. J Biol Chem 272:8717–8722. doi:10.1074/jbc.272.13.8717 CrossRefPubMedGoogle Scholar
  15. Humphrey BD, Stephensen CB, Calvert CC, Klasing KC (2004) Glucose and cationic amino acid transporter expression in growing chickens (Gallus gallus domesticus). Comp Biochem Physiol Part A Mol Integr Physiol 138:515–525. doi:10.1016/j.cbpb.2004.06.016 CrossRefGoogle Scholar
  16. Ishida A, Kyoya T, Nakashima K, Katsumata M (2011) Muscle protein metabolism during compensatory growth with changing dietary lysine levels from deficient to sufficient in growing rats. J Nutr Sci Vitaminol 57:401–408CrossRefPubMedGoogle Scholar
  17. Ishida A, Ashihara A, Nakashima K, Katsumata M (2013) Expression of amino acid transporter in porcine skeletal muscles during postnatal development. EAAP publication No. 134, pp 395–396 (abs.) Google Scholar
  18. Ito K, Groudine M (1997) A new member of the cationic amino acid transporter family is preferentially expressed in adult mouse brain. J Biol Chem 272:26780–26786. doi:10.1074/jbc.272.42.26780 CrossRefPubMedGoogle Scholar
  19. Kakuda DK, Finley KD, Maruyama M, MacLeod CL (1998) Stress differentially induces cationic amino acid transporter gene expression. Biochim Biophys Acta 1414:75–84. doi:10.1016/S0005-2736(98)00155-2 CrossRefPubMedGoogle Scholar
  20. Karlsson A, Enfalt AC, Essen-Gustavsson B, Lundstrom K, Rydhmer L, Stern S (1993) Muscle histochemical and biochemical properties in relation to meat quality during selection for increased lean tissue growth rate in pigs. J Anim Sci 71:930–938. doi:10.2527/1993.714930x CrossRefPubMedGoogle Scholar
  21. Katsumata M, Yamaguchi T, Ishida A, Ashihara A (2017) Changes in muscle fiber type and expression of mRNA of myosin heavy chain protein isoforms in porcine muscle during pre and postnatal development. Anim Sci J 88:364–371. doi:10.1111/asj.12641 CrossRefPubMedGoogle Scholar
  22. Kattesh HG, Charles SF, Baumbach GA, Gillespie BE (1990) Plasma cortisol distribution in the pig from birth to six weeks of age. Biol Neonate 58:220–226CrossRefPubMedGoogle Scholar
  23. Kobzik L, Reid MB, Bredt DS, Stamler JS (1994) Nitric oxide in skeletal muscle. Nature 372:546–548. doi:10.1038/372546a0 CrossRefPubMedGoogle Scholar
  24. Lefaucheur L, Vigneron P (1986) Post-natal changes in some histochemical and enzymatic characteristics of three pig muscles. Meat Sci 16:199–216. doi:10.1016/0309-1740(86)90026-4 CrossRefPubMedGoogle Scholar
  25. Lefaucheur L, Ecolan P, Plantard L, Gueguen N (2002) New insights into muscle fiber types in the pig. J Histochem Cytochem 50:719–730. doi:10.1177/002215540205000513 CrossRefPubMedGoogle Scholar
  26. Lefaucheur L, Lebret B, Ecolan P et al (2011) Muscle characteristics and meat quality traits are affected by divergent selection on residual feed intake in pigs1. J Anim Sci 89:996–1010. doi:10.2527/jas.2010-3493 CrossRefPubMedGoogle Scholar
  27. Liu J, Hatzoglou M (1998) Control of expression of the gene for the arginine transporter Cat-1 in rat liver cells by glucocorticoids and insulin. Amino Acids 15:321–337. doi:10.1007/bf01320897 CrossRefPubMedGoogle Scholar
  28. Liu R, Li Y, Zhang W, Fu Q, Liu N, Zhou G (2015) Activity and expression of nitric oxide synthase in pork skeletal muscles. Meat Sci 99:25–31. doi:10.1016/j.meatsci.2014.08.010 CrossRefPubMedGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2−ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  30. MacLeod CL, Kakuda DK (1996) Regulation of CAT: cationic amino acid transporter gene expression. Amino Acids 11:171–191. doi:10.1007/bf00813859 PubMedGoogle Scholar
  31. McConell GK, Bradley SJ, Stephens TJ, Canny BJ, Kingwell BA, Lee-Young RS (2007) Skeletal muscle nNOSμ protein content is increased by exercise training in humans. Am J Physiol Regul Integr Comp Physiol 293:R821–R828. doi:10.1152/ajpregu.00796.2006 CrossRefPubMedGoogle Scholar
  32. Nygard A-B, Jørgensen CB, Cirera S, Fredholm M (2007) Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol 8:67. doi:10.1186/1471-2199-8-67 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 18:49–57. doi:10.1093/emboj/18.1.49 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Stathopulos PB, Lu X, Shen J et al (2001) Increased l-arginine uptake and inducible nitric oxide synthase activity in aortas of rats with heart failure. Am J Physiol Heart Circ Physiol 280:H859–H867PubMedGoogle Scholar
  35. Suzuki A, Cassens RG (1980) A histochemical study of myofiber types in muscle of the growing pig. J Anim Sci 51:1449–1461. doi:10.2134/jas1981.5161449x CrossRefPubMedGoogle Scholar
  36. Uddin MJ, Cinar MU, Tesfaye D, Looft C, Tholen E, Schellander K (2011) Age-related changes in relative expression stability of commonly used housekeeping genes in selected porcine tissues. BMC Res Notes 4:441. doi:10.1186/1756-0500-4-441 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034CrossRefPubMedPubMedCentralGoogle Scholar
  38. Verrey F, Closs EI, Wagner CA, Palacin M, Endou H, Kanai Y (2003) CATs and HATs: the SLC7 family of amino acid transporters. Pflügers Arch 447:532–542. doi:10.1007/s00424-003-1086-z CrossRefPubMedGoogle Scholar
  39. Zhi A, Feng D, Zhou X et al (2008) Molecular cloning, tissue distribution and segmental ontogenetic regulation of b[0, +] amino acid transporter in lantang pigs. Asian Aust J Anim Sci 21:9CrossRefGoogle Scholar
  40. Zou S, Zhi A, Zhou X et al (2009) Molecular cloning, segmental distribution and ontogenetic regulation of cationic amino acid transporter 2 in pigs. Asian Aust J Anim Sci 22:712–720CrossRefGoogle Scholar
  41. Zuo J, Xia W, Xu M et al (2013) Molecular cloning, tissue distribution and expression of the porcine cationic amino acid transporter CAT3. J Anim Vet Adv 12:1070–1077. doi:10.3923/javaa.2013.1070.1077 Google Scholar

Copyright information

© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  • Aiko Ishida
    • 1
  • Akane Ashihara
    • 1
  • Kazuki Nakashima
    • 1
  • Masaya Katsumata
    • 1
    • 2
  1. 1.Institute of Livestock and Grassland ScienceNAROTsukubaJapan
  2. 2.School of Veterinary ScienceAzabu UniversitySagamiharaJapan

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