Effects of the activin A-myostatin-follistatin system on aging bone and muscle progenitor cells

Experimental Gerontology

Volumn 48, Issue 2, 2013, Pages 290-297

  Bowser, Matthew ^a   Herberg, Samuel ^a   Arounleut, Phonepasong ^a   Shi, Xingming ^a   Fulzele, Sadanand ^a   Hill, William D ^a   Isales, Carlos M ^a   Hamrick, Mark W ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Bone marrow stromal cells; Differentiation; Myoblasts; Proliferation; Sarcopenia

Indexed keywords

ACTIVIN A; FOLLISTATIN; MYOSTATIN;

AGE; AGING; ANIMAL CELL; ARTICLE; BONE MARROW CELL; BONE MARROW STROMAL CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTENSOR DIGITORUM LONGUS MUSCLE; IN VITRO STUDY; MINERALIZATION; MOUSE; MUSCLE TWITCH; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLEUS MUSCLE;

ACTIVINS; AGING; ANIMALS; BONE REGENERATION; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FOLLISTATIN; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MYOBLASTS, SKELETAL; MYOSTATIN; SARCOPENIA; SIGNAL TRANSDUCTION; TIME FACTORS;

MUS;

EID: 84872827217     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.11.004     Document Type: Article

References (38)

1. Baccarelli A., Morpurgo P., Corsi A., Vaghi I., Fanelli M., Cremonesi G., Vaninetti S., Beck-Peccoz P., Spada A. Activin A serum levels and aging of the pituitary-gonadal axis: a cross-sectional study in middle-aged and elderly healthy subjects. Exp. Gerontol. 2001, 36:1403-1412.
2. Conboy I., Conboy M.J., Smythe G., Rando T.M. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302:1575-1577.
3. Dalbo V.J., Roberts M.D., Sunderland K.L., Poole C.N., Stout J.R., Beck T.W., Bemben M., Kerksick C.M. Acute loading and aging effects on myostatin pathway biomarkers in human skeletal muscle after three sequential bouts of resistance exercise. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:855-865.
4. Eijken M., Swagemakers S., Koedam M., Steenbergen C., Derkx P., Uitterlinden A.G., van der Spek P.J., Visser J.A., de Jong F.H., Pols H.A., van Leeuwen J.P. The activin A-follistatin system: potent regulator of human extracellular matrix mineralization. FASEB J. 2007, 21:2949-2960.
5. Elkasrawy M.N., Hamrick M.W. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J. Musculoskelet. Neuronal Interact. 2010, 10:56-63.
6. Elkasrawy M.N., Fulzele S., Bowser M., Wenger K., Hamrick M.W. Myostatin (GDF-8) inhibits chondrogenesis and chondrocyte proliferation in vitro by suppressing Sox-9 expression. Growth Factors 2011, 29:253-262.
7. Gilson H., Schakman O., Kalista S., Lause P., Tsuchida K., Thissen J.P. Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E157-E164.
8. Gregory C.A., Gunn W.G., Peister A., Prockop D.J. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal. Biochem. 2004, 329:77.
9. Hamrick M.W. A role for myokines in muscle-bone interactions. Exerc. Sport Sci. Rev. 2011, 39:43-47.
10. Hamrick M.W. The skeletal muscle secretome: an emerging player in muscle-bone crosstalk. Nature Bonekey 2012, 60:1-5.
11. Hamrick M.W., Ding K.H., Pennington C., Chao Y.J., Wu Y.D., Howard B., Immel D., Borlongan C., McNeil P.L., Bollag W.B., Curl W.W., Yu J., Isales C.M. Age-related loss of muscle mass and bone strength in mice is associated with a decline in physical activity and serum leptin. Bone 2006, 39:845-853.
12. Hamrick M.W., Shi X., Zhang W., Pennington C., Thakore H., Haque M., Kang B., Isales C.M., Fulzele S., Wenger K.H. Loss of myostatin (GDF-8) function increases osteogenic differentiation of bone marrow-derived stem cells but the osteogenic effect is ablated with unloading. Bone 2007, 40:1544-1553.
13. He L., Vichev K., Macharia R., Huang R., Christ B., Patel K., Amthor H. Activin A inhibits formation of skeletal muscle during chick development. Anat. Embryol. 2005, 209:401-407.
14. Hennebry A., Berry C., Siriett V., O'Callaghan P., Chau L., Watson T., Sharma M., Kambadur R. Myostatin regulates fiber-type composition of skeletal muscle by regulation MEF2 and MyoD gene expression. Am. J. Physiol. Cell Physiol. 2009, 296:C525-C534.
15. Holloszy J.O., Chen M., Cartee G., Young J.C. Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech. Aging Dev. 1991, 60:199-213.
16. Hurwitz J.M., Santoro N. Inhibins, activins and follistatin in the aging female and male. Semin. Reprod. Med. 2004, 22:209-217.
17. Jackson M., Luong D., Vang D.D., Garikipati D., Stanton J., Nelson O.L., Rodgers B. The aging myostatin null phenotype: reduced adiposity, cardiac hypertrophy, enhanced cardiac stress response, and sexual dimorphism. J. Endocrinol. 2012, 213:263-275.
18. Kellum E., Starr H., Arounleut P., Immel D., Fulzele S., Wenger K., Hamrick M.W. Myostatin (GDF-8) deficiency increases fracture callus size, Sox-5 expression, and callus bone volume. Bone 2009, 44:17-23.
19. Konopka A., Douglass M., Kaminsky L., Jemiolo B., Trappe T., Trappe S., Harper M. Molecular adaptations to aerobic exercise training in skeletal muscle of older women. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 65:1201-1207.
20. Kretlow J., Jin Y., Liu W., Zhang W., Hong T.H., Zhou G., Baggett L., Mikos A., Cao Y. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 2008, 9:60.
21. Lee S.J., Reed L.A., Davies M.V., Girgenrath S., Goad M.E., Tomkinson K.N., Wright J.F., Barker C., Ehrmantraut G., Holmstrom J., Trowell B., Gertz B., Jiang M.S., Sebald S.M., Matzuk M., Li E., Liang L.F., Quattlebaum E., Stotish R.L., Wolfman N.L. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18117-18122.
22. Lee S.J., Lee Y.S., Zimmers T.A., Soleimani A., Matzuk M., Tsuchida K., Cohn R.D., Barton E.R. Regulation of muscle mass by follistatins and activins. Mol. Endocrinol. 2010, 24:1998-2008.
23. Leger B., Derave W., De Bock K., Hespel P., Russell A.P. Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res. 2008, 11:163-175B.
24. Machida S., Booth F.W. Increased nuclear proteins in muscle satellite cells in aged animals as compared to young growing animals. Exp. Gerontol. 2004, 39:1521-1525.
25. Marcell T.J., Harman S.M., Urban R.J., Metz D.D., Rodgers B.D., Blackman M.R. Comparison of GH, IGF-1, and testosterone with mRNA of receptors and myostatin in older men. Am. J. Physiol. Endocrinol. Metab. 2001, 281:E1159-E1164.
26. McFarlane C., Hui G., Amanda W., Lau H., Lokireddy S., Xiaojia G., Mouly B., Butler-Browne G., Gluckman P., Sharma M., Kambadur R. Human myostatin negatively regulates human myoblast growth and differentiation. Am. J. Physiol. Cell Physiol. 2011, 301:C195-C203.
27. McKay B., Ogborn D.I., Bellamy L.M., Tarnopolsky M.A., Parise G. Myostatin is associated with age-related human muscle stem cell dysfunction. FASEB J. 2012, 26:2509-2521.
28. McPherron A.C., Lawler A., Lee S.J. Regulation of skeletal muscle mass in mice by a new TGF-β family member. Nature 1997, 387:83-90.
29. Morissette M.R., Stricker C., Rosenberg M.A., Buranasombati C., Levitan E.B., Mittleman M.A., Rosenzweig A. Effects of myostatin deletion in aging mice. Aging Cell 2009, 8:573-583.
30. Murphy K., Koopman R., Naim T., Leger B., Trieu J., Ibebunjo C., Lynch G.S. Antibody-directed myostatin inhibition in 21-mo-old mice reveals novel roles for myostatin signaling in skeletal muscle structure and function. FASEB J. 2010, 24:4433-4442.
31. Nomura T., Ueyama T., Ashihara E., Tateishi K., Asada S., Nakajima N., Isodono K., Takahashi T., Matsubara H., Oh H. Skeletal muscle-derived progenitors capable of differentiating into cardiomyocytes proliferate through myostatin-independent TGF-beta family signaling. Biochem. Biophys. Res. Commun. 2008, 365:863-869.
32. Pearsall R.S., Canalis E., Cornwall-Brady M., Underwood K.W., Haigis B., Ucran J., Kumar R., Pobre E., Grinberg A., Werner E.D., Glatt V., Stadmeyer L., Smith D., Seehra J., Bouxsein M.L. A soluble activin type IIA receptor induces bone formation and improves skeletal integrity. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7082-7087.
33. Siriett V., Salerno M.S., Berry C., Nicholas G., Bower R., Kambadur R., Sharma M. Antagonism of myostatin enhances muscle regeneration during sarcopenia. Mol Ther. 2007, 15(8):1463-1470.
34. Szulc P., Schoppet M., Goettsch C., Rauner M., Dschietzig T., Chapurlat R., Hofbauer L.C. Endocrine and clinical correlates of myostatin serum concentration in men-the STRAMBO study. J. Clin. Endocrinol. Metab. 2012, (Epub ahead of print).
35. Williams N.G., Interlichia J.P., Jackson M.F., Hwang D., Cohen O., Rodgers B. Endocrine actions of myostatin: systemic regulation of the IGF and IGF binding protein axis. Endocrinology 2011, 152:172-180.
36. Yarasheski K.E., Ghasin S., Sinha-Hikim I., Pak-Loduca J., Gonzalez-Cadavid N.F. Serum myostatin-immunoreactive protein is increased in 60-92year old women and men with muscle wasting. J. Nutr. Health Aging 2002, 6:343-348.
37. Zhang W., Ou G., Hamrick M., Hill W., Borke J., Wenger K., Chutkan N., Yu J., Mi Q.S., Isales C.M., et al. Age-related changes in the osteogenic differentiation potential of mouse bone marrow stromal cells. J. Bone Miner. Res. 2008, 23:1118-1128.
38. Zhu J., Li Y., Shen W., Qiao C., Ambrosio F., Lavasani M., Nozaki M., Branca M., Huard J. Relationships between transforming growth factor-β1, myostatin, and decorin. J. Biol. Chem. 2007, 282:25852-25863.