Skip to main content
SpringerLink
Log in

Methionine restriction on lipid metabolism and its possible mechanisms

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Methionine restriction (MR) exerts many beneficial effects, such as increasing longevity, decreasing oxidative damage and alleviating inflammatory responses. Much attention has been recently focused on the effects of MR on metabolic health, especially lipid metabolism, since the increasing incidence of obesity, insulin resistance and type 2 diabetes causes a worldwide health problem. In general, MR is considered to increase de novo lipogenesis, lipolysis and fatty acid oxidation, with a result of reduced fat accumulation. However, different responses in lipid metabolism between adipose tissue and liver are declared. Therefore, in this review, we will focus on the changes of lipid metabolism responses to dietary MR. Moreover, the comparison of alterations of fat metabolism responses to dietary MR between adipose tissue and liver, and the comparison of changes between rodents and pigs is made to illustrate the tissue- and species-specific responses. In addition, the possible mechanisms that might be engaged in the regulation of MR diet on lipid metabolism are also discussed.

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

  • Ables GP, Perrone CE, Orentreich D, Orentreich N (2012) Methionine-restricted C57BL/6J mice are resistant to diet-induced obesity and insulin resistance but have low bone density. PLoS One 7(12):e51357. doi:10.1371/journal.pone.0051357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agha G, Houseman EA, Kelsey KT, Eaton CB, Buka SL, Loucks EB (2015) Adiposity is associated with DNA methylation profile in adipose tissue. Int J Epidemiol 44(4):1277–1287. doi:10.1093/ije/dyu236

    Article  PubMed  Google Scholar 

  • Anthony TG, Morrison CD, Gettys TW (2013) Remodeling of lipid metabolism by dietary restriction of essential amino acids. Diabetes 62(8):2635–2644. doi:10.2337/db12-1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boss O, Bachman E, Vidal-Puig A, Zhang CY, Peroni O, Lowell BB (1999) Role of the beta(3)-adrenergic receptor and/or a putative beta(4)-adrenergic receptor on the expression of uncoupling proteins and peroxisome proliferator-activated receptor-gamma coactivator-1. Biochem Biophys Res Commun 261(3):870–876. doi:10.1006/bbrc.1999.1145

    Article  CAS  PubMed  Google Scholar 

  • Cai D, Jia Y, Song H, Sui S, Lu J, Jiang Z, Zhao R (2014) Betaine supplementation in maternal diet modulates the epigenetic regulation of hepatic gluconeogenic genes in neonatal piglets. PLoS One 9(8):e105504. doi:10.1371/journal.pone.0105504

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai D, Wang J, Jia Y, Liu H, Yuan M, Dong H, Zhao R (2016) Gestational dietary betaine supplementation suppresses hepatic expression of lipogenic genes in neonatal piglets through epigenetic and glucocorticoid receptor-dependent mechanisms. Biochim Biophys Acta 1861(1):41–50. doi:10.1016/j.bbalip.2015.10.002

    Article  CAS  PubMed  Google Scholar 

  • Castellano R, Perruchot MH, Conde-Aguilera JA, van Milgen J, Collin A, Tesseraud S, Mercier Y, Gondret F (2015) A methionine deficient diet enhances adipose tissue lipid metabolism and alters anti-oxidant pathways in young growing pigs. PLoS One 10(7):e0130514. doi:10.1371/journal.pone.0130514

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Zhou X, Wu W, Wang X, Wang Y (2015) FTO-dependent function of N6-methyladenosine is involved in the hepatoprotective effects of betaine on adolescent mice. J Physiol Biochem 71(3):405–413. doi:10.1007/s13105-015-0420-1

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Meng Q, Wang C, Li H, Huang Z, Chen S, Xiao F, Guo F (2010) Leucine deprivation decreases fat mass by stimulation of lipolysis in white adipose tissue and upregulation of uncoupling protein 1 (UCP1) in brown adipose tissue. Diabetes 59(1):17–25. doi:10.2337/db09-0929

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Zhang Q, Meng Q, Xia T, Huang Z, Wang C, Liu B, Chen S, Xiao F, Du Y, Guo F (2011) Leucine deprivation stimulates fat loss via increasing CRH expression in the hypothalamus and activating the sympathetic nervous system. Mol Endocrinol 25(9):1624–1635. doi:10.1210/me.2011-0028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde-Aguilera JA, Barea R, Le Floc’h N, Lefaucheur L, van Milgen J (2010) A sulfur amino acid deficiency changes the amino acid composition of body protein in piglets. Animal 4(8):1349–1358. doi:10.1017/S1751731110000340

    Article  CAS  PubMed  Google Scholar 

  • Contreras GA, Lee YH, Mottillo EP, Granneman JG (2014) Inducible brown adipocytes in subcutaneous inguinal white fat: the role of continuous sympathetic stimulation. Am J Physiol Endocrinol Metab 307(9):E793–E799. doi:10.1152/ajpendo.00033.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corominas J, Ramayo-Caldas Y, Puig-Oliveras A, Estelle J, Castello A, Alves E, Pena RN, Ballester M, Folch JM (2013) Analysis of porcine adipose tissue transcriptome reveals differences in de novo fatty acid synthesis in pigs with divergent muscle fatty acid composition. BMC Genom 14:843. doi:10.1186/1471-2164-14-843

    Article  Google Scholar 

  • Deval C, Chaveroux C, Maurin AC, Cherasse Y, Parry L, Carraro V, Milenkovic D, Ferrara M, Bruhat A, Jousse C, Fafournoux P (2009) Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways. FEBS J 276(3):707–718. doi:10.1111/j.1742-4658.2008.06818.x

    Article  CAS  PubMed  Google Scholar 

  • Devenport L, Knehans A, Sundstrom A, Thomas T (1989) Corticosterone’s dual metabolic actions. Life Sci 45(15):1389–1396

    Article  CAS  PubMed  Google Scholar 

  • Dubin DT, Taylor RH (1975) The methylation state of poly A-containing messenger RNA from cultured hamster cells. Nucleic Acids Res 2(10):1653–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dudek SM, Semenkovich CF (1995) Essential amino acids regulate fatty acid synthase expression through an uncharged transfer RNA-dependent mechanism. J Biol Chem 270(49):29323–29329

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Wanders D, Stone KP, Van NT, Cortez CC, Gettys TW (2014) A systems biology analysis of the unique and overlapping transcriptional responses to caloric restriction and dietary methionine restriction in rats. FASEB J 28(6):2577–2590. doi:10.1096/fj.14-249458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goetz R (2013) Metabolism: adiponectin—a mediator of specific metabolic actions of FGF21. Nat Rev Endocrinol 9(9):506–508. doi:10.1038/nrendo.2013.146

    Article  CAS  PubMed  Google Scholar 

  • Granneman JG, Li P, Zhu Z, Lu Y (2005) Metabolic and cellular plasticity in white adipose tissue I: effects of beta3-adrenergic receptor activation. Am J Physiol Endocrinol Metab 289(4):E608–E616. doi:10.1152/ajpendo.00009.2005

    Article  CAS  PubMed  Google Scholar 

  • Hasek BE, Stewart LK, Henagan TM, Boudreau A, Lenard NR, Black C, Shin J, Huypens P, Malloy VL, Plaisance EP, Krajcik RA, Orentreich N, Gettys TW (2010) Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Regul Integr Comp Physiol 299(3):R728–R739. doi:10.1152/ajpregu.00837.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasek BE, Boudreau A, Shin J, Feng D, Hulver M, Van NT, Laque A, Stewart LK, Stone KP, Wanders D, Ghosh S, Pessin JE, Gettys TW (2013) Remodeling the integration of lipid metabolism between liver and adipose tissue by dietary methionine restriction in rats. Diabetes 62(10):3362–3372. doi:10.2337/db13-0501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haugland RA, Cline MG (1980) Post-transcriptional modifications of oat coleoptile ribonucleic acids. 5′-Terminal capping and methylation of internal nucleosides in poly(A)-rich RNA. Eur J Biochem 104(1):271–277

    Article  CAS  PubMed  Google Scholar 

  • Jackson JB, Pallas DC (2012) Circumventing cellular control of PP2A by methylation promotes transformation in an Akt-dependent manner. Neoplasia 14(7):585–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawasaki M, Miura Y, Yagasaki K (2010) Effects of sulfur amino acids, l: -methionine, l: -cystine and l: -cysteine on lipoprotein lipase and hormone-sensitive lipase in differentiated mouse 3T3-L1 adipocytes. Cytotechnology 62(3):225–233. doi:10.1007/s10616-010-9282-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacasa D, Agli B, Giudicelli Y (1988) Permissive action of glucocorticoids on catecholamine-induced lipolysis: direct “in vitro” effects on the fat cell beta-adrenoreceptor-coupled-adenylate cyclase system. Biochem Biophys Res Commun 153(2):489–497

    Article  CAS  PubMed  Google Scholar 

  • Lees EK, Krol E, Shearer K, Mody N, Gettys TW, Delibegovic M (2014a) Effects of hepatic protein tyrosine phosphatase 1B and methionine restriction on hepatic and whole-body glucose and lipid metabolism in mice. Metabolism 64(2):305–314. doi:10.1016/j.metabol.2014.10.038

    Article  PubMed  PubMed Central  Google Scholar 

  • Lees EK, Krol E, Grant L, Shearer K, Wyse C, Moncur E, Bykowska AS, Mody N, Gettys TW, Delibegovic M (2014b) Methionine restriction restores a younger metabolic phenotype in adult mice with alterations in fibroblast growth factor 21. Aging Cell 13(5):817–827. doi:10.1111/acel.12238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Jiang C, Xu G, Wang N, Zhu Y, Tang C, Wang X (2008) Homocysteine upregulates resistin production from adipocytes in vivo and in vitro. Diabetes 57:817–827. doi:10.2337/db07-0617

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Tian H, Lam KS, Lin S, Hoo RC, Konishi M, Itoh N, Wang Y, Bornstein SR, Xu A, Li X (2013) Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metab 17(5):779–789. doi:10.1016/j.cmet.2013.04.005

    Article  CAS  PubMed  Google Scholar 

  • Malloy VL, Krajcik RA, Bailey SJ, Hristopoulos G, Plummer JD, Orentreich N (2006) Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction. Aging Cell 5(4):305–314. doi:10.1111/j.1474-9726.2006.00220.x

    Article  CAS  PubMed  Google Scholar 

  • Malloy VL, Perrone CE, Mattocks DAL, Ables GP, Caliendo NS, Orentreich DS, Orentreich N (2013) Methionine restriction prevents the progression of hepatic steatosis in leptin-deficient obese mice. Metabolism 62(11):1651–1661. doi:10.1016/j.metabol.2013.06.012

    Article  CAS  PubMed  Google Scholar 

  • Mentch SJ, Mehrnohamadi M, Huang L, Liu XJ, Gupta D, Mattocks D, Padilla PG, Ables G, Bamman MM, Thalacker-Mercer AE, Nichenametla SN, Locasale JW (2015) Histone methylation dynamics and gene regulation occur through the sensing of one-carbon metabolism. Cell Metab 22(5):861–873. doi:10.1016/j.cmet.2015.08.024

    Article  CAS  PubMed  Google Scholar 

  • Miller RA, Buehner G, Chang Y, Harper JM, Sigler R, Smith-Wheelock M (2005) Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4(3):119–125. doi:10.1111/j.1474-9726.2005.00152.x

    Article  CAS  PubMed  Google Scholar 

  • Moore JS, Monson JP, Kaltsas G, Putignano P, Wood PJ, Sheppard MC, Besser GM, Taylor NF, Stewart PM (1999) Modulation of 11beta-hydroxysteroid dehydrogenase isozymes by growth hormone and insulin-like growth factor: in vivo and in vitro studies. J Clin Endocrinol Metab 84(11):4172–4177. doi:10.1210/jcem.84.11.6108

    CAS  PubMed  Google Scholar 

  • Narayan P, Rottman FM (1992) Methylation of mRNA. Adv Enzymol Relat Areas Mol Biol 65:255–285

    CAS  PubMed  Google Scholar 

  • O’Hea EK, Leveille GA (1969) Significance of adipose tissue and liver as sites of fatty acid synthesis in the pig and the efficiency of utilization of various substrates for lipogenesis. J Nutr 99(3):338–344

    PubMed  Google Scholar 

  • Orentreich N, Matias JR, DeFelice A, Zimmerman JA (1993) Low methionine ingestion by rats extends life span. J Nutr 123(2):269–274

    CAS  PubMed  Google Scholar 

  • Orgeron ML, Stone KP, Wanders D, Cortez CC, Van NT, Gettys TW (2014) The impact of dietary methionine restriction on biomarkers of metabolic health. Glucose Homeost Pathog Diabetes Mellit 121:351–376. doi:10.1016/B978-0-12-800101-1.00011-9

    Article  CAS  Google Scholar 

  • Owen BM, Ding X, Morgan DA, Coate KC, Bookout AL, Rahmouni K, Kliewer SA, Mangelsdorf DJ (2014) FGF21 acts centrally to induce sympathetic nerve activity, energy expenditure, and weight loss. Cell Metab 20(4):670–677. doi:10.1016/j.cmet.2014.07.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patil YN, Dille KN, Burk DH, Cortez CC, Gettys TW (2015) Cellular and molecular remodeling of inguinal adipose tissue mitochondria by dietary methionine restriction. J Nutr Biochem 26(11):1235–1247. doi:10.1016/j.jnutbio.2015.05.016

    Article  CAS  PubMed  Google Scholar 

  • Perrone CE, Mattocks DA, Hristopoulos G, Plummer JD, Krajcik RA, Orentreich N (2008) Methionine restriction effects on 11 -HSD1 activity and lipogenic/lipolytic balance in F344 rat adipose tissue. J Lipid Res 49(1):12–23. doi:10.1194/jlr.M700194-JLR200

    Article  CAS  PubMed  Google Scholar 

  • Perrone CE, Mattocks DA, Jarvis-Morar M, Plummer JD, Orentreich N (2010) Methionine restriction effects on mitochondrial biogenesis and aerobic capacity in white adipose tissue, liver, and skeletal muscle of F344 rats. Metabolism 59(7):1000–1011. doi:10.1016/j.metabol.2009.10.023

    Article  CAS  PubMed  Google Scholar 

  • Perrone CE, Mattocks DA, Plummer JD, Chittur SV, Mohney R, Vignola K, Orentreich DS, Orentreich N (2012) Genomic and metabolic responses to methionine-restricted and methionine-restricted, cysteine-supplemented diets in Fischer 344 rat inguinal adipose tissue, liver and quadriceps muscle. J Nutrigenet Nutrigenomics 5(3):132–157. doi:10.1159/000339347

    Article  CAS  PubMed  Google Scholar 

  • Plaisance EP, Henagan TM, Echlin H, Boudreau A, Hill KL, Lenard NR, Hasek BE, Orentreich N, Gettys TW (2010) Role of beta-adrenergic receptors in the hyperphagic and hypermetabolic responses to dietary methionine restriction. Am J Physiol Regul Integr Comp Physiol 299(3):R740–R750. doi:10.1152/ajpregu.00838.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaisance EP, Van N, Orgeron M, McDaniel AN, Behrens PH, Gettys TW, Anthony TG (2012) Role of general control nonderepressible 2 (GCN2) kinase in mediating responses to dietary methionine restriction. FASEB J 26(1_MeetingAbstracts):255-1

    Google Scholar 

  • Richie JP Jr, Leutzinger Y, Parthasarathy S, Malloy V, Orentreich N, Zimmerman JA (1994) Methionine restriction increases blood glutathione and longevity in F344 rats. FASEB J 8(15):1302–1307

    CAS  PubMed  Google Scholar 

  • Sanchez-Roman I, Gomez A, Gomez J, Suarez H, Sanchez C, Naudi A, Ayala V, Portero-Otin M, Lopez-Torres M, Pamplona R, Barja G (2011) Forty percent methionine restriction lowers DNA methylation, complex I ROS generation, and oxidative damage to mtDNA and mitochondrial proteins in rat heart. J Bioenerg Biomembr 43(6):699–708. doi:10.1007/s10863-011-9389-9

    Article  CAS  PubMed  Google Scholar 

  • Stone KP, Wanders D, Orgeron M, Cortez CC, Gettys TW (2014) Mechanisms of increased in vivo insulin sensitivity by dietary methionine restriction in mice. Diabetes 63(11):3721–3733. doi:10.2337/db14-0464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stone KP, Wanders D, Calderon LF, Spurgin SB, Scherer PE, Gettys TW (2015) Compromised responses to dietary methionine restriction in adipose tissue but not liver of ob/ob mice. Obesity 23(9):1836–1844. doi:10.1002/oby.21177

    Article  CAS  PubMed  Google Scholar 

  • Tomas E, Tsao TS, Saha AK, Murrey HE, Zhang Cc C, Itani SI, Lodish HF, Ruderman NB (2002) Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc Natl Acad Sci USA 99(25):16309–16313. doi:10.1073/pnas.222657499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villena JA, Roy S, Sarkadi-Nagy E, Kim KH, Sul HS (2004) Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J Biol Chem 279(45):47066–47075. doi:10.1074/jbc.M403855200

    Article  CAS  PubMed  Google Scholar 

  • Volpe JJ, Marasa JC (1975) Hormonal regulation of fatty acid synthetase, acetyl-CoA carboxylase and fatty acid synthesis in mammalian adipose tissue and liver. Biochim Biophys Acta 380(3):454–472

    Article  CAS  PubMed  Google Scholar 

  • Wanders D, Burk DH, Cortez CC, Van NT, Stone KP, Baker M, Mendoza T, Mynatt RL, Gettys TW (2015) UCP1 is an essential mediator of the effects of methionine restriction on energy balance but not insulin sensitivity. FASEB J 29(6):2603–2615. doi:10.1096/fj.14-270348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanders D, Stone KP, Forney LA, Cortez CC, Dille KN, Simon J, Xu M, Hotard EC, Nikonorova IA, Pettit AP, Anthoy TG, Gettys TW (2016) Role of GCN2-independent signaling through a non-canonical PERK/NRF2 pathway in the physiological responses to dietary methionine restriction. Diabetes. doi:10.2337/db15-1324

    PubMed  Google Scholar 

  • Wang LJ, Zhang HW, Zhou JY, Liu Y, Yang Y, Chen XL, Zhu CH, Zheng RD, Ling WH, Zhu HL (2014) Betaine attenuates hepatic steatosis by reducing methylation of the MTTP promoter and elevating genomic methylation in mice fed a high-fat diet. J Nutr Biochem 25(3):329–336. doi:10.1016/j.jnutbio.2013.11.007

    Article  PubMed  Google Scholar 

  • Wang X, Zhu L, Chen J, Wang Y (2015) mRNA m(6)A methylation downregulates adipogenesis in porcine adipocytes. Biochem Biophys Res Commun 459(2):201–207. doi:10.1016/j.bbrc.2015.02.048

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Dou X, Zhou Z, Song Z (2016) Adipose tissue-liver axis in alcoholic liver disease. World J Gastrointest Pathophysiol 7(1):17–26. doi:10.4291/wjgp.v7.i1.17

    Article  PubMed  PubMed Central  Google Scholar 

  • Wood SL, Emmison N, Borthwick AC, Yeaman SJ (1993) The protein phosphatases responsible for dephosphorylation of hormone-sensitive lipase in isolated rat adipocytes. Biochem J 295(Pt2):531–535. doi:10.1042/bj2950531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8(11):1288–1295. doi:10.1038/nm788

    Article  CAS  PubMed  Google Scholar 

  • Ying Y, Yun J, Guoyao W, Kaiji S, Zhaolai D, Zhenlong W (2015) Dietary l-methionine restriction decreases oxidative stress in porcine liver mitochondria. Exp Gerontol 65:35–41. doi:10.1016/j.exger.2015.03.004

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Yang Y, Sun BF, Shi Y, Yang X, Xiao W, Hao YJ, Ping XL, Chen YS, Wang WJ, Jin KX, Wang X, Huang CM, Fu Y, Ge XM, Song SH, Jeong HS, Yanagisawa H, Niu Y, Jia GF, Wu W, Tong WM, Okamoto A, He C, Rendtlew Danielsen JM, Wang XJ, Yang YG (2014) FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell Res 24(12):1403–1419. doi:10.1038/cr.2014.151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Chen J, Chen J, Wu W, Wang X, Wang Y (2015) The beneficial effects of betaine on dysfunctional adipose tissue and N6-methyladenosine mRNA methylation requires the AMP-activated protein kinase alpha1 subunit. J Nutr Biochem 26(12):1678–1684. doi:10.1016/j.jnutbio.2015.08.014

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by National Basic Research Program of China (2013CB127301, 2013CB127306), National Natural Science Foundation of China (31402089) and National Science and Technology Support Project (2013BAD21B04).

Author information

Author notes

    Authors and Affiliations

    1. Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock and Poultry, Changsha, 410125, Hunan, China

      Xihong Zhou, Liuqin He, Dan Wan, Huansheng Yang, Kang Yao, Xin Wu & Yulong Yin

    2. University of the Chinese Academy of Sciences, Beijing, 10008, China

      Liuqin He

    3. Texas A&M University, College Station, TX, USA

      Guoyao Wu

    Authors
    1. Xihong Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Liuqin He
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Dan Wan
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Huansheng Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Kang Yao
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Guoyao Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Xin Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Yulong Yin
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Xin Wu or Yulong Yin.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Handling Editor: H. Jakubowski.

    X. Zhou and L. He made equal contributions to this study, so they are joint first authors.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhou, X., He, L., Wan, D. et al. Methionine restriction on lipid metabolism and its possible mechanisms. Amino Acids 48, 1533–1540 (2016). https://doi.org/10.1007/s00726-016-2247-7

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00726-016-2247-7

    Keywords

    Search

    Navigation