20-Hydroxyecdysone activates the protective arm of the RAAS via the MAS receptor

in Journal of Molecular Endocrinology
Authors:
René Lafont Biophytis, Sorbonne Université – BC9, Paris, France
Sorbonne Université, CNRS -Institut de Biologie Paris Seine (BIOSIPE), Paris, France

Search for other papers by René Lafont in
Current site
Google Scholar
PubMed Close
,
Maria Serova Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Maria Serova in
Current site
Google Scholar
PubMed Close
,
Blaise Didry-Barca Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Blaise Didry-Barca in
Current site
Google Scholar
PubMed Close
,
Sophie Raynal Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Sophie Raynal in
Current site
Google Scholar
PubMed Close
,
Louis Guibout Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Louis Guibout in
Current site
Google Scholar
PubMed Close
,
Laurence Dinan Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Laurence Dinan in
Current site
Google Scholar
PubMed Close
,
Stanislas Veillet Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Stanislas Veillet in
Current site
Google Scholar
PubMed Close
,
Mathilde Latil Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Mathilde Latil in
Current site
Google Scholar
PubMed Close
,
Waly Dioh Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Waly Dioh in
Current site
Google Scholar
PubMed Close
, and
Pierre J Dilda Biophytis, Sorbonne Université – BC9, Paris, France

Search for other papers by Pierre J Dilda in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0001-9916-8513

Correspondence should be addressed to P J Dilda: pierre.dilda@biophytis.com
DOI:
https://doi.org/10.1530/JME-21-0033
Volume/Issue:
Volume 68: Issue 2
Article Type:
Research Article
Page Range:
77–87
Online Publication Date:
23 Dec 2021
Copyright:
© Society for Endocrinology 2021
Collections:
Top-cited articles of 2023
Restricted access
Rent on DeepDyve

Sign up for journal news

20-Hydroxyecdysone (20E) is a steroid hormone that plays a key role in insect development through nuclear ecdysteroid receptors (EcR/RXR complex) and at least one membrane GPCR receptor (DopEcR). It also displays numerous pharmacological effects in mammals, where its mechanism of action is still debated, involving either an unidentified GPCR or the estrogen ERβ receptor. The goal of this study was to better understand 20E mechanism of action in mammals. A mouse myoblast cell line (C2C12) and the gene expression of myostatin (a negative regulator of muscle growth) were used as a reporter system of anabolic activity. Experiments using protein-bound 20E established the involvement of a membrane receptor. 20E-like effects were also observed with angiotensin(1–7), the endogenous ligand of MAS. Additionally, the effect on myostatin gene expression was abolished by Mas receptor knock-down using siRNA or pharmacological inhibitors. 17β-Estradiol (E2) also inhibited myostatin gene expression, but protein-bound E2 was inactive, and E2 activity was not abolished by angiotensin(1–7) antagonists. A mechanism involving cooperation between the MAS receptor and a membrane-bound palmitoylated estrogen receptor is proposed. The possibility to activate the MAS receptor with a safe steroid molecule is consistent with the pleiotropic pharmacological effects of ecdysteroids in mammals and, indeed, the proposed mechanism may explain the close similarity between the effects of angiotensin(1–7) and 20E. Our findings open up many possible therapeutic developments involving stimulation of the protective arm of the renin–angiotensin–aldosterone system (RAAS) with 20E.

Supplementary Materials

Journal of Molecular Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 1626 45 4
PDF Downloads 910 40 7

 

  • Collapse
  • Expand
Online ISSN:
1479-6813
Print ISSN:
0952-5041
Copyright:
© Society for Endocrinology 2021
Page(s):
11
Article Type:
Research Article
Received Date:
01 Oct 2021
Accepted Date:
26 Nov 2021
Print Publication Date:
01 Feb 2022
Online Publication Date:
23 Dec 2021
Keywords:
20-hydroxyecdysone (20E); MAS receptor; renin–angiotensin–aldosterone system (RAAS); ecdysteroid; G protein-coupled receptor (GPCR); estrogen; muscle; myoblast

  • Báthori M, Tóth N, Hunyadi A, Marki A & Zador E 2008 Phytoecdysteroids and anabolic-androgenic steroids-structure and effects on humans. Current Medicinal Chemistry 15 75–91. (https://doi.org/10.2174/092986708783330674)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bertrand C, Pignalosa A, Wanecq E, Rancoule C, Batut A, Deleruyelle S, Lionetti L, Valet P & Castan-Laurell I 2013 Effects of dietary eicosapentaenoic acid (EPA) supplementation in high-fat fed mice on lipid metabolism and apelin/APJ system in skeletal muscle. PLoS ONE 8 e78874. (https://doi.org/10.1371/journal.pone.0078874)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Breton C, Haenggeli C, Barberis C, Heitz F, Bader CR, Bernheim L & Tribollet E 2002 Presence of functional oxytocin receptors in cultured human myoblasts. Journal of Clinical Endocrinology and Metabolism 87 1415–1418. (https://doi.org/10.1210/jcem.87.3.8537)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chiang JY 2013 Bile acid metabolism and signaling. Comprehensive Physiology 3 1191–1212. (https://doi.org/10.1002/cphy.c120023)

  • Dinan L 2009 The Karlson lecture. Phytoecdysteroids: what use are they? Archives of Insect Biochemistry and Physiology 72 126–141. (https://doi.org/10.1002/arch.20334)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dinan L & Lafont R 2006 Effects and applications of arthropod steroid hormones (ecdysteroids) in mammals. Journal of Endocrinology 191 1–8. (https://doi.org/10.1677/joe.1.06900)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dinan L, Bourne P, Whiting P, Tsitsekli A, Saatov Z, Dhadialla TS, Hormann RE, Lafont R & Coll J 2003 Synthesis and biological activities of turkesterone 11alpha-acyl derivatives. Journal of Insect Science 3 6. (https://doi.org/10.1093/jis/3.1.6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dykens JA, Moos WH & Howell N 2005 Development of 17alpha-estradiol as a neuroprotective therapeutic agent: rationale and results from a phase I clinical study. Annals of the New York Academy of Sciences 1052 116–135. (https://doi.org/10.1196/annals.1347.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ehrhardt C, Wessels JT, Wuttke W & Seidlova-Wuttke D 2011 The effects of 20-hydroxyecdysone and 17beta-estradiol on the skin of ovariectomized rats. Menopause 18 323–327. (https://doi.org/10.1097/gme.0b013e3181f322e3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Evans PD, Bayliss A & Reale V 2014 GPCR-mediated rapid, non-genomic actions of steroids: comparisons between DmDopEcR and GPER1 (GPR30). General and Comparative Endocrinology 195 157–163. (https://doi.org/10.1016/j.ygcen.2013.10.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Feldman RD, Ding Q, Hussain Y, Limbird LE, Pickering JG & Gros R 2016 Aldosterone mediates metastatic spread of renal cancer via the G protein-coupled estrogen receptor (GPER). FASEB Journal 30 2086–2096. (https://doi.org/10.1096/fj.15-275552)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Filardo EJ, Quinn JA, Blang KI & Frackelton AR 2000 Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Molecular Endocrinology 14 1649–1660. (https://doi.org/10.1210/mend.14.10.0532)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Foucault AS, Mathe V, Lafont R, Even P, Dioh W, Veillet S, Tome D, Huneau JF, Hermier D & Quignard-Boulange A 2012 Quinoa extract enriched in 20-hydroxyecdysone protects mice from diet-induced obesity and modulates adipokines expression. Obesity 20 270–277. (https://doi.org/10.1038/oby.2011.257)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gao L, Cai G & Shi X 2008 β-Ecdysterone induces osteogenic differentiation in mouse mesenchymal stem cells and relieves osteoporosis. Biological and Pharmaceutical Bulletin 31 2245–2249. (https://doi.org/10.1248/bpb.31.2245)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Garratt M, Leander D, Pifer K, Bower B, Herrera JJ, Day SM, Fiehn O, Brooks SV & Miller RA 2019 17-Alpha estradiol ameliorates age-associated sarcopenia and improves late-life physical function in male mice but not in females or castrated males. Aging Cell 18 e12920. (https://doi.org/10.1111/acel.12920)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gorelick-Feldman J, Cohick W & Raskin I 2010 Ecdysteroids elicit a rapid Ca2+ flux leading to Akt activation and increased protein synthesis in skeletal muscle cells. Steroids 75 632–637. (https://doi.org/10.1016/j.steroids.2010.03.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heitsch H, Brovkovych S, Malinski T & Wiemer G 2001 Angiotensin-(1–7)-stimulated nitric oxide and superoxide release from endothelial cells. Hypertension 37 72–76. (https://doi.org/10.1161/01.hyp.37.1.72)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Isenmann E, Ambrosio G, Joseph JF, Mazzarino M, de la Torre X, Zimmer P, Kazlauskas R, Goebel C, Botre F & Diel P et al.2019 Ecdysteroids as non-conventional anabolic agent: performance enhancement by ecdysterone supplementation in humans. Archives of Toxicology 93 1807–1816. (https://doi.org/10.1007/s00204-019-02490-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jean-Baptiste G, Yang Z, Khoury C & Greenwood MT 2005 Lysophosphatidic acid mediates pleiotropic responses in skeletal muscle cells. Biochemical and Biophysical Research Communications 335 1155–1162. (https://doi.org/10.1016/j.bbrc.2005.08.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Karlson P 1983 Eighth Adolf Butenandt lecture. Why are so many hormones steroids? Hoppe-Seyler’s Zeitschrift für Physiologische Chemie 364 1067–1087. (https://doi.org/10.1515/bchm2.1983.364.2.1067)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Khanal RN & Nemere I 2007 Membrane receptors for vitamin D metabolites. Critical Reviews in Eukaryotic Gene Expression 17 31–47. (https://doi.org/10.1615/critreveukargeneexpr.v17.i1.30)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kizelsztein P, Govorko D, Komarnytsky S, Evans A, Wang Z, Cefalu WT & Raskin I 2009 20-Hydroxyecdysone decreases weight and hyperglycemia in a diet-induced obesity mice model. American Journal of Physiology: Endocrinology and Metabolism 296 E433–E439. (https://doi.org/10.1152/ajpendo.90772.2008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kotsyuruba AV, Bukchanevich OM, Tuganova AV & Tarakanov SS 1995 Mechanisms of the early effect of biologically active oxysterones calcitriol and ecdysterone, modulation of intracellular pools of arachidonic acid and products of its oxidative metabolism. Ukrainskii Biokhimicheskii Zhurnal 67 45–52.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kotsyuruba AV, Bukchanevich OM, Berdyshev AG, Meged OF, Hula NM, Mykhailik OM & Bakaï EA 1998 In vitro study of the early membrane effects of C27-steroid hormone ecdysterone, immobilized on the nanodispersed magnetite surface. Ukrainskii Biokhimicheskii Zhurnal 70 22–32.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kotsyuruba A, Bukchanevich O, Meged O, Tarakanov S, Berdyshev A & Tuganova A 1999 The C(27)-steroid hormones ecdysterone and calcitriol activate the phosphoinositide messenger cascade in its membrane phase of action. Ukrainskii Biokhimicheskii Zhurnal 71 27–32.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lagrange AH, Rønnekleiv OK & Kelly MJ 1997 Modulation of G protein-coupled receptors by an estrogen receptor that activates protein kinase A. Molecular Pharmacology 51 605–612. (https://doi.org/10.1124/mol.51.4.605)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lapenna S, Gemen R, Wollgast J, Worth A, Maragkoudakis P & Caldeira S 2015 Assessing herbal products with health claims. Critical Reviews in Food Science and Nutrition 55 1918–1928. (https://doi.org/10.1080/10408398.2012.726661)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lautner RQ, Villela DC, Fraga-Silva RA, Silva N, Verano-Braga T, Costa-Fraga F, Jankowski J, Jankowski V, Sousa F & Alzamora A et al.2013 Discovery and characterization of alamandine: a novel component of the renin-angiotensin system. Circulation Research 112 1104–1111. (https://doi.org/10.1161/CIRCRESAHA.113.301077)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Luo Y, Tanabe E, Kitayoshi M, Nishiguchi Y, Fujiwara R, Matsushima S, Sasaki T, Sasahira T, Chihara Y & Nakae D et al.2015 Expression of MAS1 in breast cancer. Cancer Science 106 1240–1248. (https://doi.org/10.1111/cas.12719)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maneix L, Antonson P, Humire P, Rochel-Maia S, Castaneda J, Omoto Y, Kim HJ, Warner M & Gustafsson JÅ 2015 Estrogen receptor beta exon 3-deleted mouse: the importance of non-ERE pathways in ERbeta signaling. PNAS 112 5135–5140. (https://doi.org/10.1073/pnas.1504944112)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Marino M & Ascenzi P 2006 Steroid hormone rapid signaling: the pivotal role of S-palmitoylation. IUBMB Life 58 716–719. (https://doi.org/10.1080/15216540601019485)

  • Meitzen J, Luoma JI, Boulware MI, Hedges VL, Peterson BM, Tuomela K, Britson KA & Mermelstein PG 2013 Palmitoylation of estrogen receptors is essential for neuronal membrane signaling. Endocrinology 154 4293–4304. (https://doi.org/10.1210/en.2013-1172)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Micevych P & Christensen A 2012 Membrane-initiated estradiol actions mediate structural plasticity and reproduction. Frontiers in Neuroendocrinology 33 331–341. (https://doi.org/10.1016/j.yfrne.2012.07.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Muñoz MC, Giani JF & Dominici FP 2010 Angiotensin-(1–7) stimulates the phosphorylation of Akt in rat extracardiac tissues in vivo via receptor Mas. Regulatory Peptides 161 1–7. (https://doi.org/10.1016/j.regpep.2010.02.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mykhaylyk OM, Kotzuruba AV, Buchanevich OM, Korduban AM, Meged EF & Gulaya NM 2001 Signal transduction of erythrocytes after specific binding of ecdysterone and cholesterol immobilized on nanodispersed magnetite. Journal of Magnetism and Magnetic Materials 225 226–234. (https://doi.org/10.1016/S0304-8853(0001262-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nervi C, Benedetti L, Minasi A, Molinaro M & Adamo S 1995 Arginine-vasopressin induces differentiation of skeletal myogenic cells and upregulation of myogenin and Myf-5. Cell Growth and Differentiation 6 81–89. (https://doi.org/10.3934/molsci.2018.2.131)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Omanakuttan A, Bose C, Pandurangan N, Kumar GB, Banerli A & Nair BG 2016 Nitric oxide and ERK mediates regulation of cellular processes by ecdysterone. Experimental Cell Research 346 167–175. (https://doi.org/10.1016/j.yexcr.2016.07.019)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parr M & Müller-Schöll A 2018 Pharmacology of doping agents – mechanisms promoting muscle hypertrophy. AIMS Molecular Science 5 131–159.

  • Parr MK, Zhao P, Haupt O, Ngueu ST, Hengevoss J, Fritzemeier KH, Piechotta M, Schlorer N, Muhn P & Zheng WY et al.2014 Estrogen receptor beta is involved in skeletal muscle hypertrophy induced by the phytoecdysteroid ecdysterone. Molecular Nutrition and Food Research 58 1861–1872. (https://doi.org/10.1002/mnfr.201300806)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parr MK, Botre F, Nass A, Hengevoss J, Diel P & Wolber G 2015 Ecdysteroids: a novel class of anabolic agents? Biology of Sport 32 169–173. (https://doi.org/10.5604/20831862.1144420)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pastore MB, Landeros RV, Chen DB & Magness RR 2019 Structural analysis of estrogen receptors: interaction between estrogen receptors and cav-1 within the caveolaedagger. Biology of Reproduction 100 495–504. (https://doi.org/10.1093/biolre/ioy188)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Prabhu VK & Nayar KK 1974 Crustecdysone is without estrogenic or antiestrogenic activity in the rat. Experientia 30 821. (https://doi.org/10.1007/BF01924207)

  • Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA & Hathaway HJ 2008 Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annual Review of Physiology 70 165–190. (https://doi.org/10.1146/annurev.physiol.70.113006.100518)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ruhs S, Nolze A, Hubschmann R & Grossmann C 2017 30 years of the mineralocorticoid receptor: nongenomic effects via the mineralocorticoid receptor. Journal of Endocrinology 234 T107–T124. (https://doi.org/10.1530/JOE-16-0659)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL & Touyz RM 2007 Angiotensin-(1–7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49 185–192. (https://doi.org/10.1161/01.HYP.0000251865.35728.2f)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sanchez M, Picard N, Sauve K & Tremblay A 2010 Challenging estrogen receptor beta with phosphorylation. Trends in Endocrinology and Metabolism 21 104–110. (https://doi.org/10.1016/j.tem.2009.09.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT & Bader M et al.2003 Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas. PNAS 100 8258–8263. (https://doi.org/10.1073/pnas.1432869100)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schreihofer DA, Duong P & Cunningham RL 2018 N-terminal truncations in sex steroid receptors and rapid steroid actions. Steroids 133 15–20. (https://doi.org/10.1016/j.steroids.2017.10.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Seidlova-Wuttke D, Christel D, Kapur P, Nguyen BT, Jarry H & Wuttke W 2010 β-Ecdysone has bone protective but no estrogenic effects in ovariectomized rats. Phytomedicine 17 884–889. (https://doi.org/10.1016/j.phymed.2010.03.021)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Semsarian C, Sutrave P, Richmond DR & Graham RM 1999 Insulin-like growth factor (IGF-I) induces myotube hypertrophy associated with an increase in anaerobic glycolysis in a clonal skeletal-muscle cell model. Biochemical Journal 339 443–451. (https://doi.org/10.1042/bj3390443)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Simakin S, Panyushkin V, Portugalov S, Kostina L & Martisorov E 1988 Combined application of preparation ecdysten and product bodrost during training in cyclic sports. Scientific Sports Bulletin 2 29–31.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sláma K & Lafont R 1995 Insect hormones – ecdysteroids: their presence and actions in vertebrates. European Journal of Entomology 92 355–377.

  • Sobrino A, Vallejo S, Novella S, Lazaro-Franco M, Mompeon A, Bueno-Beti C, Walther T, Sanchez-Ferrer C, Peiro C & Hermenegildo C 2017 Mas receptor is involved in the estrogen-receptor induced nitric oxide-dependent vasorelaxation. Biochemical Pharmacology 129 67–72. (https://doi.org/10.1016/j.bcp.2017.01.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, Macchiarulo A, Yamamoto H, Mataki C & Pruzanski M et al.2009 TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metabolism 10 167–177. (https://doi.org/10.1016/j.cmet.2009.08.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tipbunjong C, Kitiyanant Y, Chaturapanich G, Sornkaew N, Suksamrarn A, Kitiyanant N, Esser KA & Pholpramool C 2017 Natural diarylheptanoid compounds from Curcuma comosa Roxb. promote differentiation of mouse myoblasts C2C12 cells selectively via ER alpha receptors. Medicinal Chemistry Research 26 274–286. (https://doi.org/10.1007/s00044-016-1748-y)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tipbunjong C, Khuituan P, Kitiyanant Y, Suksamrarn A & Pholpramool C 2019 Diarylheptanoid 1-(4-hydroxyphenyl)-7-phenyl-(6E)-6-hepten-3-one enhances C2C12 myoblast differentiation by targeting membrane estrogen receptors and activates Akt-mTOR and p38 MAPK-NF-kappaB signaling axes. Journal of Natural Medicines 73 735–744. (https://doi.org/10.1007/s11418-019-01322-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tirupula KC, Zhang D, Osbourne A, Chatterjee A, Desnoyer R, Willard B & Karnik SS 2017 Mas C-terminal tail interacting proteins identified by mass spectrometry-based proteomic approach. PLoS ONE 10 e0140872. (https://doi.org/10.1371/journal.pone.0140872)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Toran-Allerand CD 2005 Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Annals of the New York Academy of Sciences 1052 136–144. (https://doi.org/10.1196/annals.1347.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Velders M, Schleipen B, Fritzemeier KH, Zierau O & Diel P 2012 Selective estrogen receptor-beta activation stimulates skeletal muscle growth and regeneration. FASEB Journal 26 1909–1920. (https://doi.org/10.1096/fj.11-194779)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wuttke W & Seidlova-Wuttke D 2015 Eine neue alternative für die prävention und therapie postmenopausaler erkrankungen, insbesondere des metabolischen syndroms. Journal für Gynäkologische Endokrinologie 25 6–12.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yaffe D & Saxel O 1977 Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270 725–727. (https://doi.org/10.1038/270725a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zubeldia JM, Hernández-Santana A, Jiménez-del-Rio M, Pérez-López V, Pérez-Machín R & García-Castellano JM 2012 In vitro characterization of the efficacy and safety profile of a proprietary Ajuga turkestanica extract. Chinese Medicine 3 215–222. (https://doi.org/10.4236/cm.2012.34031)

    • PubMed
    • Search Google Scholar
    • Export Citation