The role of GDF11 in aging and skeletal muscle, cardiac and bone homeostasis

References

• Ahn S-T, Suh S-I, Moon H, Hyun C. 2016. Evaluation of growth differentiation factor 11 (GDF11) levels in dogs with chronic mitral valve insufficiency. Can J Vet Res. 80:90–92.
   PubMed Web of Science ®Google Scholar
• Añón-Hidalgo J, Catalán V, Rodríguez A, Ramírez B, Silva C, Galofré JC, Salvador J, Frühbeck G, Gómez-Ambrosi J. 2019. Circulating GDF11 levels are decreased with age but are unchanged with obesity and type 2 diabetes. Aging. 11:1733–1744.
   PubMedGoogle Scholar
• Barrios‐Silva LV, Parnell M, Shinwari ZB, Chaudhary GA, Xenofontos T, van Bekhoven A, McArthur S, Elliott B. 2018. Activin subfamily peptides predict chronological age in humans. Physiol Rep. 6:e13823.
   PubMed Web of Science ®Google Scholar
• Beggs ML, Nagarajan R, Taylor-Jones JM, Nolen G, MacNicol M, Peterson CA. 2004. Alterations in the TGFbeta signaling pathway in myogenic progenitors with age. Aging Cell. 3:353–361.
   PubMed Web of Science ®Google Scholar
• Brack AS, Rando T. 2007. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev. 3:226–237.
   PubMed Web of Science ®Google Scholar
• Bueno J, Ynigo M, de Miguel C, Gonzalo‐Daganzo R, Richart A, Vilches C, Regidor C, García‐Marco J, Flores-Ballester E, et al. 2016. Growth differentiation factor 11 (GDF 11): a promising anti‐ageing factor–is highly concentrated in platelets. Vox Sang. 111:434–436.
   PubMed Web of Science ®Google Scholar
• Butcher JT, Ali MI, Ma MW, McCarthy CG, Islam BN, Fox LG, Mintz JD, Larion S, Fulton DJ, Stepp D. 2017. Effect of myostatin deletion on cardiac and microvascular function. Physiol Rep. 5:e13525.
   Web of Science ®Google Scholar
• Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, Mikels AJ, Agrawal S, Schaffer DV, Conboy I. 2009. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell. 8:676–689.
   PubMed Web of Science ®Google Scholar
• Chakkalakal JV, Jones KM, Basson MA, Brack A. 2012. The aged niche disrupts muscle stem cell quiescence. Nature. 490:355.
   PubMed Web of Science ®Google Scholar
• Chen Y, Guo Q, Zhang M, Song S, Quan T, Zhao T, Li H, Guo L, Jiang T, Wang G. 2016. Relationship of serum GDF11 levels with bone mineral density and bone turnover markers in postmenopausal Chinese women. Bone Res. 4:16012.
   PubMed Web of Science ®Google Scholar
• Constam DB. 2014. Regulation of TGFβ and related signals by precursor proceedings. Semin Cell Dev Biol (Elsevier). 85–97.
   Google Scholar
• Cosgrove BD, Gilbert PM, Porpiglia E, Mourkioti F, Lee SP, Corbel SY, Llewellyn ME, Delp SL, Blau H. 2014. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med. 20:255.
   PubMed Web of Science ®Google Scholar
• Derynck R, Budi E. 2019. Specificity, versatility, and control of TGF-β family signaling. Sci Signal. 12:eaav5183.
   PubMed Web of Science ®Google Scholar
• Di Loreto R, Murphy CT. 2015. The cell biology of aging. Mol Biol Cell 26:4524–4531.
   PubMedGoogle Scholar
• Du G-Q, Shao Z-B, Wu J, Yin W-J, Li S-H, Wu J, Weisel RD, Tian J-W, Li R-K. 2017. Targeted myocardial delivery of GDF11 gene rejuvenates the aged mouse heart and enhances myocardial regeneration after ischemia–reperfusion injury. Basic Res Cardiol. 112:7.
   PubMed Web of Science ®Google Scholar
• Duran J, Troncoso MF, Lagos D, Ramos S, Marin G, Estrada M. 2018. GDF11 modulates Ca(2+)-dependent Smad2/3 signaling to prevent cardiomyocyte hypertrophy. IJMS Sci. 19:1508.
   Google Scholar
• Egerman MA, Glass DJ. 2014. Signaling pathways controlling skeletal muscle mass. Crit Rev Biochem Mol Biol. 49:59–68.
   PubMed Web of Science ®Google Scholar
• Egerman MA, Cadena SM, Gilbert JA, Meyer A, Nelson HN, Swalley SE, Mallozzi C, Jacobi C, Jennings LL, Clay I, et al. 2015. GDF11 Increases with age and inhibits skeletal muscle regeneration. Cell Metab. 22:164–174.
   PubMed Web of Science ®Google Scholar
• Elkasrawy MN, Hamrick MW. 2010. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J Musculoskelet Neuronal Interact. 10:56–63.
   PubMed Web of Science ®Google Scholar
• Elliott BT, Herbert P, Sculthorpe N, Grace FM, Stratton D, Hayes L. 2017. Lifelong exercise, but not short‐term high‐intensity interval training, increases GDF 11, a marker of successful aging: a preliminary investigation. Physiol Rep. 5:e13343.
   PubMed Web of Science ®Google Scholar
• Gamer LW, Cox KA, Small C, Rosen V. 2001. Gdf11 is a negative regulator of chondrogenesis and myogenesis in the developing chick limb. Dev Biol. 229:407–420.
   PubMed Web of Science ®Google Scholar
• Gamer LW, Wolfman NM, Celeste AJ, Hattersley G, Hewick R, Rosen V. 1999. A novel BMP expressed in developing mouse limb, spinal cord, and tail bud is a potent mesoderm inducer in Xenopus embryos. Dev Biol. 208:222–232.
   PubMed Web of Science ®Google Scholar
• García-Prat L, Martínez-Vicente M, Perdiguero E, Ortet L, Rodríguez-Ubreva J, Rebollo E, Ruiz-Bonilla V, Gutarra S, Ballestar E, Serrano AL, et al. 2016. Autophagy maintains stemness by preventing senescence. Nature. 529:37.
   PubMed Web of Science ®Google Scholar
• Hammers DW, Merscham‐Banda M, Hsiao JY, Engst S, Hartman JJ, Sweeney H. 2017. Supraphysiological levels of GDF11 induce striated muscle atrophy. EMBO Mol Med. 9:531–544.
   PubMed Web of Science ®Google Scholar
• Hamrick MW, Shi X, Zhang W, Pennington C, Thakore H, Haque M, Kang B, Isales CM, Fulzele S, Wenger KH. 2007. Loss of myostatin (GDF8) function increases osteogenic differentiation of bone marrow-derived mesenchymal stem cells but the osteogenic effect is ablated with unloading. Bone. 40:1544–1553.
   PubMed Web of Science ®Google Scholar
• Harper SC, Johnson J, Borghetti G, Zhao H, Wang T, Wallner M, Kubo H, Feldsott EA, Yang Y, Joo Y. 2018. GDF11 decreases pressure overload-induced hypertrophy, but can cause severe cachexia and premature death. Circ Res. 123:1220–1231.
   PubMed Web of Science ®Google Scholar
• Hinken AC, Powers JM, Luo G, Holt JA, Billin AN, Russell AJ. 2016. Lack of evidence for GDF11 as a rejuvenator of aged skeletal muscle satellite cells. Aging Cell. 15:582–584.
   PubMed Web of Science ®Google Scholar
• Huang Z, Chen D, Zhang K, Yu B, Chen X, Meng J. 2007. Regulation of myostatin signaling by c-Jun N-terminal kinase in C2C12 cells. Cell Signal. 19:2286–2295.
   PubMed Web of Science ®Google Scholar
• Ibebunjo C, Chick JM, Kendall T, Eash JK, Li C, Zhang Y, Vickers C, Wu Z, Clarke BA, Shi J, et al. 2013. Genomic and proteomic profiling reveals reduced mitochondrial function and disruption of the neuromuscular junction driving rat sarcopenia. Mol Cell Biol. 33:194–212.
   PubMed Web of Science ®Google Scholar
• Jones JE, Cadena SM, Gong C, Wang X, Chen Z, Wang SX, Vickers C, Chen H, Lach-Trifilieff E, Hadcock JR, Glass DJ. 2018. Supraphysiologic administration of GDF11 induces cachexia in part by upregulating GDF15. Cell Rep. 22:1522–1530.
   PubMed Web of Science ®Google Scholar
• Kalampouka I, van Bekhoven A, Elliott B. 2018. Differing effects of younger and older human plasma on C2C12 myocytes in vitro. Front Physiol. 9:152.
   PubMed Web of Science ®Google Scholar
• Kenyon CJ. 2010. The genetics of ageing. Nature. 464:504–512.
   PubMed Web of Science ®Google Scholar
• Lakshman KM, Bhasin S, Corcoran C, Collins-Racie LA, Tchistiakova L, Forlow SB, Ledger KS, Burczynski ME, Dorner AJ, LaVallie ER. 2009. Measurement of myostatin concentrations in human serum: circulating concentrations in young and older men and effects of testosterone administration. Mol Cell Endocrinol. 302:26–32.
   PubMed Web of Science ®Google Scholar
• Latres E, Mastaitis J, Fury W, Miloscio L, Trejos J, Pangilinan J, Okamoto H, Cavino K, Na E, Papatheodorou A, et al. 2017. Activin A more prominently regulates muscle mass in primates than does GDF8. Nat Commun. 8:15153–15153.
   PubMed Web of Science ®Google Scholar
• Lee SJ, McPherron AC. 2001. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA. 98:9306–9311.
   PubMed Web of Science ®Google Scholar
• Lee S-J. 2010. Extracellular regulation of myostatin: a molecular rheostat for muscle mass. Immunol Endocr Metab Agents Med Chem. 10:183–194.
   PubMedGoogle Scholar
• Li Z, Kawasumi M, Zhao B, Moisyadi S, Yang J. 2010. Transgenic over-expression of growth differentiation factor 11 propeptide in skeleton results in transformation of the seventh cervical vertebra into a thoracic vertebra. Mol Reprod Dev. 77:990–997.
   PubMed Web of Science ®Google Scholar
• Liu A, Dong W, Peng J, Dirsch O, Dahmen U, Fang H, Zhang C, Sun J. 2018. Growth differentiation factor 11 worsens hepatocellular injury and liver regeneration after liver ischemia reperfusion injury. Faseb J 32:5186–5198.
   PubMed Web of Science ®Google Scholar
• Liu W, Zhou L, Zhou C, Zhang S, Jing J, Xie L, Sun N, Duan X, Jing W, Liang X, et al. 2016. GDF11 decreases bone mass by stimulating osteoclastogenesis and inhibiting osteoblast differentiation. Nat Commun. 7:12794.
   PubMed Web of Science ®Google Scholar
• Loffredo FS, Steinhauser ML, Jay SM, Gannon J, Pancoast JR, Yalamanchi P, Sinha M, Dall’Osso C, Khong D, Shadrach JL, et al. 2013. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell. 153:828–839.
   PubMed Web of Science ®Google Scholar
• López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. 2013. The hallmarks of aging. Cell. 153:1194–1217.
   PubMed Web of Science ®Google Scholar
• Lu Q, Tu M-L, Li C-J, Zhang L, Jiang T-J, Liu T, Luo X-H. 2016. GDF11 inhibits bone formation by activating Smad2/3 in bone marrow mesenchymal stem cells. Calcif Tissue Int. 99:500–509.
   PubMed Web of Science ®Google Scholar
• Massague J. 2008. TGFbeta in cancer. Cell. 134:215–230.
   PubMed Web of Science ®Google Scholar
• McPherron A, Huynh T, Lee S-J. 2009. Redundancy of myostatin and growth/differentiation factor 11 function. BMC Dev Biol. 9:24.
   PubMed Web of Science ®Google Scholar
• McPherron AC, Lawler AM, Lee SJ. 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 387:83–90.
   PubMed Web of Science ®Google Scholar
• McPherron AC, Lawler AM, Lee S-J. 1999. Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat Genet. 22:260–264.
   PubMed Web of Science ®Google Scholar
• McPherron AC, Lee SJ. 1997. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA. 94:12457–12461.
   PubMed Web of Science ®Google Scholar
• McPherron AC. 2010. Metabolic functions of myostatin and GDF11. Immunol Endocr Metab Agents Med Chem. 10:217–231.
   PubMedGoogle Scholar
• Morikawa M, Derynck R, Miyazono K. 2016. TGF-β and the TGF-β family: context-dependent roles in cell and tissue physiology. Cold Spring Harb Perspect Biol. 8:a021873.
   PubMed Web of Science ®Google Scholar
• Nakashima M, Toyono T, Akamine A, Joyner A. 1999. Expression of growth/differentiation factor 11, a new member of the BMP/TGFbeta superfamily during mouse embryogenesis. Mech Dev. 80:185–189.
   PubMed Web of Science ®Google Scholar
• Niccoli T, Partridge L. 2012. Ageing as a risk factor for disease. Curr Biol. 22:R741–R752.
   PubMed Web of Science ®Google Scholar
• Olson KA, Beatty AL, Heidecker B, Regan MC, Brody EN, Foreman T, Kato S, Mehler RE, Singer BS, Hveem K, et al. 2015. Association of growth differentiation factor 11/8, putative anti-ageing factor, with cardiovascular outcomes and overall mortality in humans: analysis of the Heart and Soul and HUNT3 cohorts. Eur Heart J. 36:3426–3434.
   PubMed Web of Science ®Google Scholar
• Poggioli T, Vujic A, Yang P, Macias-Trevino C, Uygur A, Loffredo FS, Pancoast JR, Cho M, Goldstein J, Tandias RM, et al. 2016. Circulating growth differentiation factor 11/8 levels decline with age. Circ Res. 118:29–37.
   PubMed Web of Science ®Google Scholar
• Rizzoli R, Reginster J-Y, Arnal J-F, Bautmans I, Beaudart C, Bischoff-Ferrari H, Biver E, Boonen S, Brandi M-L, Chines A. 2013. Quality of life in sarcopenia and frailty. Calcif Tissue Int. 93:101–120.
   PubMed Web of Science ®Google Scholar
• Rodgers BD, Eldridge JA. 2015. Reduced circulating GDF11 is unlikely responsible for age-dependent changes in mouse heart, muscle, and brain. Endocrinology. 156:3885–3888.
   PubMed Web of Science ®Google Scholar
• Roh JD, Hobson R, Chaudhari V, Quintero P, Yeri A, Benson M, Xiao C, Zlotoff D, Bezzerides V, Houstis N, et al. 2019. Activin type II receptor signaling in cardiac aging and heart failure. Sci Transl Med. 11:eaau8680.
   PubMed Web of Science ®Google Scholar
• Schafer MJ, Atkinson EJ, Vanderboom PM, Kotajarvi B, White TA, Moore MM, Bruce CJ, Greason KL, Suri RM, Khosla S. 2016. Quantification of GDF11 and myostatin in human aging and cardiovascular disease. Cell Metab. 23:1207–1215.
   PubMed Web of Science ®Google Scholar
• Semba RD, Zhang P, Zhu M, Fabbri E, Gonzalez-Freire M, Carlson OD, Moaddel R, Tanaka T, Egan JM, Ferrucci L. 2018. Relationship of circulating growth and differentiation factors 8 and 11 and their antagonists as measured using liquid chromatography–tandem mass spectrometry with age and skeletal muscle strength in healthy adults. J Gerontol A Biol Sci Med Sci. 74:129–136.
   Web of Science ®Google Scholar
• Sharma M, Kambadur R, Matthews KG, Somers WG, Devlin GP, Conaglen JV, Fowke PJ, Bass JJ. 1999. Myostatin, a transforming growth factor-beta superfamily member, is expressed in heart muscle and is upregulated in cardiomyocytes after infarct. J Cell Physiol. 180:1–9.
   PubMed Web of Science ®Google Scholar
• Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, Miller C, Regalado SG, Loffredo FS, Pancoast JR, et al. 2014. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science. 344:649–652.
   PubMed Web of Science ®Google Scholar
• Smith SC, Zhang X, Zhang X, Gross P, Starosta T, Mohsin S, Franti M, Gupta P, Hayes D, Myzithras M, et al. 2015. GDF11 does not rescue aging-related pathological hypertrophy. Circ Res. 117:926–932.
   PubMed Web of Science ®Google Scholar
• Thies RS, Chen T, Davies MV, Tomkinson KN, Pearson AA, Shakey QA, Wolfman NM. 2001. GDF-8 propeptide binds to GDF-8 and antagonizes biological activity by inhibiting GDF-8 receptor binding. Growth Factors.18:251–259.
   PubMed Web of Science ®Google Scholar
• Tian J, Lei XX, Xuan L, Tang JB, Cheng B. 2018. The effects of aging, diabetes mellitus, and antiplatelet drugs on growth factors and anti-aging proteins in platelet-rich plasma. Platelets. 25:1–7.
   Google Scholar
• Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ. 2009. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol. 296:C1258–C1C70.
   PubMed Web of Science ®Google Scholar
• Walker RG, Czepnik M, Goebel EJ, McCoy JC, Vujic A, Cho M, Oh J, Aykul S, Walton KL, Schang G, et al. 2017. Structural basis for potency differences between GDF8 and GDF11. BMC Biol. 15:19.
   PubMed Web of Science ®Google Scholar
• Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee S-J. 2003. Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA. 100:15842–15846.
   PubMed Web of Science ®Google Scholar
• Wu H-H, Ivkovic S, Murray RC, Jaramillo S, Lyons KM, Johnson JE, Calof A. 2003. Autoregulation of neurogenesis by GDF11. Neuron. 37:197–207.
   PubMed Web of Science ®Google Scholar
• Yang R, Fu S, Zhao L, Zhen B, Ye L, Niu X, Li X, Zhang P, Bai J. 2017. Quantitation of circulating GDF-11 and β2-MG in aged patients with age-related impairment in cognitive function. Clin Sci. 131:1895–1904.
   PubMed Web of Science ®Google Scholar
• Yarasheski K, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid NF. 2002. Serum myostatin-immunoreactive protein is increased in 60–92 year old women and men with muscle wasting. J Nutr Health Aging. 6:343–348.
   PubMedGoogle Scholar
• Zhang X, Tan H, Shi Z, Li N, Jia Y, Hao Z. 2019. Growth differentiation factor 11 is involved in isoproterenol–induced heart failure. Mol Med Rep. 19:4109–4118.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Shao J, Wang Z, Yang T, Liu S, Liu Y, Fan X, Ye W. 2015. Growth differentiation factor 11 is a protective factor for osteoblastogenesis by targeting PPARgamma. Gene. 557:209–214.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Sharma N, Dukes D, Myzithras MB, Gupta P, Khalil A, Kahn J, Ahlberg JS, Hayes DB, Franti M. 2017. GDF11 treatment attenuates the recovery of skeletal muscle function after injury in older rats. AAPS J. 19:431–437.
   PubMed Web of Science ®Google Scholar
• Zimmers TA, Jiang Y, Wang M, Liang TW, Rupert JE, Au ED, Marino FE, Couch ME, Koniaris L. 2017. Exogenous GDF11 induces cardiac and skeletal muscle dysfunction and wasting. Basic Res Cardiol. 112:48.
   PubMed Web of Science ®Google Scholar