Effects of low-protein diet and feed restriction on mRNA expression of cationic amino acid transporters in porcine skeletal muscles.

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    • Source:
      Publisher: Wiley Country of Publication: Australia NLM ID: 100956805 Publication Model: Print Cited Medium: Internet ISSN: 1740-0929 (Electronic) Linking ISSN: 13443941 NLM ISO Abbreviation: Anim Sci J Subsets: MEDLINE
    • Publication Information:
      Publication: Richmond, Vic. : Wiley
      Original Publication: Tokyo, Japan : Japanese Society of Zootechnical Science [1999-
    • Subject Terms:
    • Abstract:
      We investigated the effects of a low-protein diet and feed restriction on the mRNA expression of cationic amino acid transporters (CATs) in the longissimus dorsi (LD), rhomboideus (RH), and biceps femoris (BF) muscles of pigs. Eighteen piglets were divided into three groups: a control (CP21%), low-protein diet (LP, CP16%), and feed-restricted diet (FR, CP21%, 76% feed intake of control pigs) groups. The expression levels of CAT-1 in the LD and BF muscles of LP pigs were higher than that of control pigs, whereas that of FR pigs showed no difference. The CAT-2A expression levels in the RH muscle of FR pigs were higher than that of control pigs. The free lysine concentrations in all muscles of LP and FR pigs were lower than that of control pigs. To examine the factors that affect CATs mRNA expression, we evaluated the effects of lysine, arginine, insulin-like growth factor-I, and dexamethasone on the expression of CATs in C2C12 myotubes. CAT-1 expression levels increased in lysine and/or arginine deprivation. We show that CAT-1 and CAT-2A expression levels in skeletal muscles differ in response to dietary treatments and CAT-1 expression in skeletal muscles appears to increase in response to low free lysine concentrations.
      (© 2023 Japanese Society of Animal Science.)
    • References:
      Adams, C. M. (2007). Role of the transcription factor ATF4 in the anabolic actions of insulin and the anti-anabolic actions of glucocorticoids. Journal of Biological Chemistry, 282, 16744-16753. https://doi.org/10.1074/jbc.M610510200.
      Baldijão, C., Atinmo, T., Pond, W. G., & Barnes, R. H. (1976). Plasma Adrenocorticosteroid levels in protein and energy restricted pigs. The Journal of Nutrition, 106, 952-957. https://doi.org/10.1093/jn/106.7.952.
      Bergström, J., Fürst, P., Norée, L. O., & Vinnars, E. (1974). Intracellular free amino acid concentration in human muscle tissue. Journal of Applied Physiology, 36, 693-697. https://doi.org/10.1152/jappl.1974.36.6.693.
      Bergström, J., Fürst, P., & Vinnars, E. (1990). Effect of a test meal, without and with protein, on muscle and plasma free amino acids. Clinical Science, 79, 331-337. https://doi.org/10.1042/cs0790331.
      Black, J. L., & Griffiths, D. A. (1975). Effects of live weight and energy intake on nitrogen balance and total N requirements of lambs. British Journal of Nutrition, 33, 399-413. https://doi.org/10.1079/BJN19750044.
      Campbell, R. G. (1988). Nutritional constraints to lean tissue accretion in farm animals. Nutrition Research Reviews, 1, 233-253. https://doi.org/10.1079/NRR19880016.
      Caputo, M., Pigni, S., Agosti, E., Daffara, T., Ferrero, A., Filigheddu, N., & Prodam, F. (2021). Regulation of GH and GH signaling by nutrients. Cell, 10, 1376. https://doi.org/10.3390/cells10061376.
      Cerqueira, F. M., Laurindo, F. R. M., & Kowaltowski, A. J. (2011). Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, Akt and mitochondrial biogenesis. PLoS ONE, 6, e18433. https://doi.org/10.1371/journal.pone.0018433.
      Christensen, H. N. (1990). Role of amino acid transport and countertransport in nutrition and metabolism. Physiological Reviews, 70, 43-77. https://doi.org/10.1152/physrev.1990.70.1.43.
      Closs, E. I. (2002). Expression, regulation and function of carrier proteins for cationic amino acids. Current Opinion in Nephrology and Hypertension, 11, 99-107. https://doi.org/10.1097/00041552-200201000-00015.
      Fernandez, J., Lopez, A. B., Wang, C., Mishra, R., Zhou, L., Yaman, I., Snider, M. D., & Hatzolgou, M. (2003). Transcriptional control of the arginine/lysine transporter, cat-1, by physiological stress. Journal of Biological Chemistry, 278, 50000-50009. https://doi.org/10.1074/jbc.M305903200.
      Harrison, A. P., Latorre, R., & Dauncey, M. J. (1997). Postnatal development and differentiation of myofibres in functionally diverse porcine skeletal muscles. Reproduction, Fertility and Development, 9, 731-740. https://doi.org/10.1071/R97026.
      Hartman, W. J., & Prior, R. L. (1997). Feeding and arginine deficient diets differentially alter free amino acid concentrations of hindlimb muscle in young rats. Amino Acids, 13, 219-236. https://doi.org/10.1007/BF01372589.
      Herbert, J. D., Coulson, R. A., & Hernandez, T. (1966). Free amino acids in the caiman and rat. Comparative Biochemistry and Physiology, 17, 583-598. https://doi.org/10.1016/0010-406X(66)90589-5.
      Hyatt, S. L., Aulak, K. S., Malandro, M., Kilberg, M. S., & Hatzoglou, M. (1997). Adaptive regulation of the cationic amino acid transporter-1 (Cat-1) in Fao cells. Journal of Biological Chemistry, 272, 19951-19957. https://doi.org/10.1074/jbc.272.32.19951.
      Ishida, A., Ashihara, A., Nakashima, K., & Katsumata, M. (2017). Expression of cationic amino acid transporters in pig skeletal muscles during postnatal development. Amino Acids, 49, 1805-1814. https://doi.org/10.1007/s00726-017-2478-2.
      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. Journal of Nutritional Science and Vitaminology, 57, 401-408. https://doi.org/10.3177/jnsv.57.401.
      Ishida, A., Kyoya, T., Nakashima, K., & Katsumata, M. (2012). Nitrogen balance during compensatory growth when changing the levels of dietary lysine from deficiency to sufficiency in growing pigs. Animal Science Journal, 83, 743-749. https://doi.org/10.1111/j.1740-0929.2012.01018.x.
      Isley, W. L., Underwood, L. E., & Clemmons, D. R. (1983). Dietary components that regulate serum somatomedin-C concentrations in humans. The Journal of Clinical Investigation, 71, 175-182. https://doi.org/10.1172/JCI110757.
      Kakuda, D. K., Finley, K. D., Maruyama, M., & MacLeod, C. L. (1998). Stress differentially induces cationic amino acid transporter gene expression. Biochimica et Biophysica Acta - Biomembranes, 1414, 75-84. https://doi.org/10.1016/S0005-2736(98)00155-2.
      Kilberg, M. S., Shan, J., & Su, N. (2009). ATF4-dependent transcription mediates signaling of amino acid limitation. Trends in Endocrinology and Metabolism, 20, 436-443. https://doi.org/10.1016/j.tem.2009.05.008.
      Latres, E., Amini, A. R., Amini, A. A., Griffiths, J., Martin, F. J., Wei, Y., Lin, H. C., Yancopoulos, G. D., & Glass, D. J. (2005). Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. Journal of Biological Chemistry, 280, 2737-2744. https://doi.org/10.1074/jbc.M407517200.
      Li, Y., Li, F., Duan, Y., Guo, Q., Wang, W., Wen, C., Huang, X., & Yin, Y. (2017). The protein and energy metabolic response of skeletal muscle to the low-protein diets in growing pigs. Journal of Agricultural and Food Chemistry, 65, 8544-8551. https://doi.org/10.1021/acs.jafc.7b02461.
      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. https://doi.org/10.1007/BF01320897.
      Lunn, P. G., & Austin, S. (1983). Differences in nitrogen metabolism between protein-deficient and energy-deficient rats with similarly restricted growth rates. Annals of Nutrition and Metabolism, 27, 242-251. https://doi.org/10.1159/000176666.
      Mandal, A., Das, S., Kumar, A., Roy, S., Verma, S., Ghosh, A. K., Singh, R., Abhishek, K., Saini, S., Sardar, A. H., Purkait, B., Kumar, A., Mandal, C., & Das, P. (2017). l-arginine uptake by cationic amino acid transporter promotes intra-macrophage survival of Leishmania donovani by enhancing arginase-mediated polyamine synthesis. Frontiers in Immunology, 8, 839. https://doi.org/10.3389/fimmu.2017.00839.
      Mashima, D., Oka, Y., Gotoh, T., Tomonaga, S., Sawano, S., Nakamura, M., Tatsumi, R., & Mizunoya, W. (2019). Correlation between skeletal muscle fiber type and free amino acid levels in Japanese Black steers. Animal Science Journal, 90, 604-609. https://doi.org/10.1111/asj.13185.
      NARO. (2005). Japanese feeding standard for swine. Japan Livestock Industry Association.
      Ruusunen, M., Partanen, K., Pösö, R., & Puolanne, E. (2007). The effect of dietary protein supply on carcass composition, size of organs, muscle properties and meat quality of pigs. Livestock Science, 107, 170-181. https://doi.org/10.1016/j.livsci.2006.09.021.
      Schäfer, S. C., Wallerath, T., Closs, E. I., Schmidt, C., Schwarz, P. M., Förstermann, U., & Lehr, H.-A. (2005). Dexamethasone suppresses eNOS and CAT-1 and induces oxidative stress in mouse resistance arterioles. American Journal of Physiology. Heart and Circulatory Physiology, 288, H436-H444. https://doi.org/10.1152/ajpheart.00587.2004.
      Simmons, W. W., Closs, E. I., Cunningham, J. M., Smith, T. W., & Kelly, R. A. (1996). Cytokines and insulin induce cationic amino acid transporter (CAT) expression in cardiac myocytes: Regulation of L-arginine transport and no production by by CAT-1, CAT-2A, and CAT-2B. Journal of Biological Chemistry, 271, 11694-11702. https://doi.org/10.1074/jbc.271.20.11694.
      Simmons, W. W., Ungureanu-Longrois, D., Smith, G. K., Smith, T. W., & Kelly, R. A. (1996). Glucocorticoids regulate inducible nitric oxide synthase by inhibiting tetrahydrobiopterin synthesis and L-arginine transport. Journal of Biological Chemistry, 271, 23928-23937. https://doi.org/10.1074/jbc.271.39.23928.
      Skiba, G., Raj, S., Poławska, E., Pastuszewska, B., Elminowska-Wenda, G., Bogucka, J., & Knecht, D. (2012). Profile of fatty acids, muscle structure and shear force of musculus longissimus dorsi (MLD) in growing pigs as affected by energy and protein or protein restriction followed by realimentation. Meat Science, 91, 339-346. https://doi.org/10.1016/j.meatsci.2012.02.013.
      Soliman, A. T., Hassan, A. E. H. I., Aref, M. K., Hintz, R. L., Rosenfeld, R. G., & Rogol, A. D. (1986). Serum insulin-like growth factors I and II concentrations and growth hormone and insulin responses to arginine infusion in children with protein-energy malnutrition before and after nutritional rehabilitation. Pediatric Research, 20, 1122-1130. https://doi.org/10.1203/00006450-198611000-00012.
      Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., Gonzalez, M., Yancopoulos, G. D., & Glass, D. J. (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Molecular Cell, 14, 395-403. https://doi.org/10.1016/S1097-2765(04)00211-4.
      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 Biology, 3, 1-12. https://doi.org/10.1186/gb-2002-3-7-research0034.
      Verrey, F., Closs, E. I., Wagner, C. A., Palacin, M., Endou, H., & Kanai, Y. (2003). CATs and HATs: The SLC7 family of amino acid transporters. Pflügers Archiv, 447, 532-542. https://doi.org/10.1007/s00424-003-1086-z.
      Wang, D., Wan, X., Peng, J., Xiong, Q., Niu, H., Li, H., Chai, J., & Jiang, S. (2017). The effects of reduced dietary protein level on amino acid transporters and mTOR signaling pathway in pigs. Biochemical and Biophysical Research Communications, 485, 319-327. https://doi.org/10.1016/j.bbrc.2017.02.084.
      Wu, G., Flynn, N. E., Flynn, S. P., Jolly, C. A., & Davis, P. K. (1999). Dietary protein or arginine deficiency impairs constitutive and inducible nitric oxide synthesis by young rats. The Journal of Nutrition, 129, 1347-1354. https://doi.org/10.1093/jn/129.7.1347.
      Yeramian, A., Martin, L., Serrat, N., Arpa, L., Soler, C., Bertran, J., McLeod, C., Palacín, M., Modolell, M., Lloberas, J., & Celada, A. (2006). Arginine transport via cationic amino acid transporter 2 plays a critical regulatory role in classical or alternative activation of macrophages. The Journal of Immunology, 176, 5918-5924. https://doi.org/10.4049/jimmunol.176.10.5918.
      Yin, J., Li, Y., Zhu, X., Han, H., Ren, W., Chen, S., Bin, P., Liu, G., Huang, X., Fang, R., Wang, B., Wang, K., Sun, L., Li, T., & Yin, Y. (2017). Effects of long-term protein restriction on meat quality, muscle amino acids, and amino acid transporters in pigs. Journal of Agricultural and Food Chemistry, 65, 9297-9304. https://doi.org/10.1021/acs.jafc.7b02746.
    • Grant Information:
      17K15362 Ministry of Education, Science, and Culture, Japan; 26850170 Ministry of Education, Science, and Culture, Japan
    • Contributed Indexing:
      Keywords: cationic amino acid transporter; feed restriction; low-protein; pig; skeletal muscle
    • Accession Number:
      0 (Amino Acid Transport Systems, Basic)
      K3Z4F929H6 (Lysine)
      94ZLA3W45F (Arginine)
      0 (RNA, Messenger)
    • Publication Date:
      Date Created: 20230808 Date Completed: 20231102 Latest Revision: 20231102
    • Publication Date:
      20240829
    • Accession Number:
      10.1111/asj.13861
    • Accession Number:
      37551564