Follistatin: A novel therapeutic for the improvement of muscle regenerations

Journal of Pharmacology and Experimental Therapeutics

Volumn 349, Issue 2, 2014, Pages 355-371

  Yaden, Benjamin C ^a,b   Croy, Johnny E ^b   Wang, Yan ^b   Wilson, Jonathan M ^a   Datta Mannan, Amita ^b   Shetler, Pamela ^b   Milner, Andrea ^b   Bryant, Henry U ^b   Andrews, Jessica ^b   Dai, Guoli ^a   Krishnan, Venkatesh ^b  

^a INDIANA UNIVERSITY   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLISTATIN; HEPARIN; IMMUNOGLOBULIN FC FRAGMENT; TRANSCRIPTION FACTOR PAX7;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DISEASE SEVERITY; DOSAGE SCHEDULE COMPARISON; DRUG POTENCY; FEMALE; IMMOBILIZATION; MACROPHAGE; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE INJURY; MUSCLE MASS; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; WEIGHT GAIN;

ANIMALS; FOLLISTATIN; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; MICE; MUSCLE, SKELETAL; PROTEIN ENGINEERING; RECOMBINANT FUSION PROTEINS; REGENERATION;

EID: 84898794781     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.211169     Document Type: Article

References (50)

1. Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, and Patel K (2004) Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol 270:19-30
2. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, and Chazaud B (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057-1069
3. Bilezikjian LM, Blount AL, Leal AM, Donaldson CJ, Fischer WH, and Vale WW (2004) Autocrine/paracrine regulation of pituitary function by activin, inhibin and follistatin. Mol Cell Endocrinol 225:29-36
4. Burkholder TJ, Fingado B, Baron S, and Lieber RL (1994) Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J Morphol 221:177-190
5. Cash JN, Rejon CA, McPherron AC, Bernard DJ, and Thompson TB (2009) The structure of myostatin:follistatin 288: insights into receptor utilization and heparin binding. EMBO J 28:2662-2676
6. Datta-Mannan A, Yaden B, Krishnan V, Jones BE, and Croy JE (2013) An engineered human follistatin variant: insights into the pharmacokinetic and pharmocodynamic relationships of a novel molecule with broad therapeutic potential. J Pharmacol Exp Ther 344:616-623
7. Dennis RA, Przybyla B, Gurley C, Kortebein PM, Simpson P, Sullivan DH, and Peterson CA (2008) Aging alters gene expression of growth and remodeling factors in human skeletal muscle both at rest and in response to acute resistance exercise. Physiol Genomics 32:393-400
8. De Pasquale L, D'Amico A, Verardo M, Petrini S, Bertini E, and De Benedetti F (2012) Increased muscle expression of interleukin-17 in Duchenne muscular dystrophy. Neurology 78:1309-1314
9. Fumagalli M, Musso T, Vermi W, Scutera S, Daniele R, Alotto D, Cambieri I, Ostorero A, Gentili F, and Caposio P, et al. (2007) Imbalance between activin A and follistatin drives postburn hypertrophic scar formation in human skin. Exp Dermatol 16:600-610
10. Funaba M, Ikeda T, Ogawa K, and Abe M (2003) Calcium-regulated expression of activin A in RBL-2H3 mast cells. Cell Signal 15:605-613
11. Garry DJ, Meeson A, Elterman J, Zhao Y, Yang P, Bassel-Duby R, and Williams RS (2000) Myogenic stem cell function is impaired in mice lacking the forkhead/winged helix protein MNF. Proc Natl Acad Sci USA 97:5416-5421
12. Gilson H, Schakman O, Kalista S, Lause P, Tsuchida K, and Thissen JP (2009) Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am J Physiol Endocrinol Metab 297: E157-E164
13. Gressner OA, Lahme B, Siluschek M, Rehbein K, Weiskirchen R, and Gressner AM (2008) Intracrine signalling of activin A in hepatocytes upregulates connective tissue growth factor (CTGF/CCN2) expression. Liver Int 28:1207-1216
14. Haidl ID and Jefferies WA (1996) The macrophage cell surface glycoprotein F4/80 is a highly glycosylated proteoglycan. Eur J Immunol 26:1139-1146
15. Hashimoto O, Kawasaki N, Tsuchida K, Shimasaki S, Hayakawa T, and Sugino H (2000) Difference between follistatin isoforms in the inhibition of activin signalling: activin neutralizing activity of follistatin isoforms is dependent on their affinity for activin. Cell Signal 12:565-571
16. Hill JJ, Davies MV, Pearson AA, Wang JH, Hewick RM, Wolfman NM, and Qiu Y (2002) The myostatin propeptide and the follistatin-related gene are inhibitory binding proteins of myostatin in normal serum. J Biol Chem 277:40735-40741
17. Jansson JO,Moverare-Skrtic S, Berndtsson A, Wernstedt I, Carlsten H, and Ohlsson C (2006) Leukemia inhibitory factor reduces body fat mass in ovariectomized mice. Eur J Endocrinol 154:349-354
18. Jones KL, Mansell A, Patella S, Scott BJ, Hedger MP, de Kretser DM, and Phillips DJ (2007) Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia. Proc Natl Acad Sci USA 104:16239-16244
19. Kawai M, Bessho K, Maruyama H, Miyazaki J, and Yamamoto T (2006) Simultaneous gene transfer of bone morphogenetic protein (BMP) -2 and BMP-7 by in vivo electroporation induces rapid bone formation and BMP-4 expression. BMC Musculoskelet Disord 7:62
20. Kocic J, Santibanez JF, Krstic A, Mojsilovic S, Ilic V, and Bugarski D (2013) Interleukin-17 modulates myoblast cell migration by inhibiting urokinase type plasminogen activator expression through p38 mitogen-Activated protein kinase. Int J Biochem Cell Biol 45:464-475
21. Kumar TR (2005) Too many follistatins: racing inside and getting out of the cell. Endocrinology 146:5048-5051
22. Lee SJ (2007) Quadrupling muscle mass in mice by targeting TGF-beta signaling pathways. PLoS ONE 2:e789
23. Lee SJ, Huynh TV, Lee YS, Sebald SM, Wilcox-Adelman SA, Iwamori N, Lepper C, Matzuk MM, and Fan CM (2012) Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway. Proc Natl Acad Sci USA 109:E2353-E2360
24. Loria P, Petraglia F, ConcariM, BertolottiM,Martella P, Luisi S, Grisolia C, Foresta C, Volpe A, and Genazzani AR, et al. (1998) Influence of age and sex on serum concentrations of total dimeric activin A. Eur J Endocrinol 139:487-492
25. Mann CJ, Perdiguero E, Kharraz Y, Aguilar S, Pessina P, Serrano AL, andMunoz-Canoves P (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1:21
26. Morales MG, Cabello-Verrugio C, Santander C, Cabrera D, Goldschmeding R, and Brandan E (2011) CTGF/CCN-2 over-expression can directly induce features of skeletal muscle dystrophy. J Pathol 225:490-501
27. Munitz A, Waddell A, Seidu L, Cole ET, Ahrens R, Hogan SP, and Rothenberg ME (2008) Resistin-like molecule alpha enhances myeloid cell activation and promotes colitis. J Allergy Clin Immunol 122:1200-1207
28. Reame NE, Lukacs JL, Olton P, Ansbacher R, and Padmanabhan V (2007) Differential effects of aging on activin A and its binding protein, follistatin, across the menopause transition. Fertil Steril 88:1003-1005
29. Rodin DA, Abbot SD, Saade G, and Clayton RN (1990) Comparison of the pretranslational regulation of FSH synthesis by gonadal steroids in rats and mice. J Mol Endocrinol 4:159-167
30. Roopenian DC and Akilesh S (2007) FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 7:715-725
31. Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D, and Shimizu H (2008) Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol 180:2581-2587
32. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, and Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777-786
33. Shen W, Prisk V, Li Y, Foster W, and Huard J (2006) Inhibited skeletal muscle healing in cyclooxygenase-2 gene-deficient mice: the role of PGE2 and PGF2alpha. J Appl Physiol (1985) 101:1215-1221
34. Sidis Y, Mukherjee A, Keutmann H, Delbaere A, Sadatsuki M, and Schneyer A (2006) Biological activity of follistatin isoforms and follistatin-like-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins. Endocrinology 147:3586-3597
35. Sidis Y, Schneyer AL, and Keutmann HT (2005) Heparin and activin-binding determinants in follistatin and FSTL3. Endocrinology 146:130-136
36. Sierra-Filardi E, Puig-Kröger A, Blanco FJ, Nieto C, Bragado R, Palomero MI, Bernabéu C, Vega MA, and Corbí AL (2011) Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 117:5092-5101
37. Sugama K, Suzuki K, Yoshitani K, Shiraishi K, and Kometani T (2012) IL-17, neutrophil activation and muscle damage following endurance exercise. Exerc Immunol Rev 18:116-127
38. Sugino K, Kurosawa N, Nakamura T, Takio K, Shimasaki S, Ling N, Titani K, and Sugino H (1993) Molecular heterogeneity of follistatin, an activin-binding protein. Higher affinity of the carboxyl-terminal truncated forms for heparan sulfate proteoglycans on the ovarian granulosa cell. J Biol Chem 268:15579-15587
39. Sun G, Haginoya K, Wu Y, Chiba Y, Nakanishi T, Onuma A, Sato Y, Takigawa M, Iinuma K, and Tsuchiya S (2008) Connective tissue growth factor is overexpressed in muscles of human muscular dystrophy. J Neurol Sci 267:48-56
40. Teo AK, Ali Y, Wong KY, Chipperfield H, Sadasivam A, Poobalan Y, Tan EK, Wang ST, Abraham S, and Tsuneyoshi N, et al. (2012) Activin and BMP4 synergistically promote formation of definitive endoderm in human embryonic stem cells. Stem Cells 30:631-642
41. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, and Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275:40235-40243
42. Torchinsky MB and Blander JM (2010) T helper 17 cells: discovery, function, and physiological trigger. Cell Mol Life Sci 67:1407-1421
43. Tsuchida K (2008) Myostatin inhibition by a follistatin-derived peptide ameliorates the pathophysiology of muscular dystrophy model mice. Acta Myol 27:14-18
44. Vieira Potter VJ, Strissel KJ, Xie C, Chang E, Bennett G, Defuria J, Obin MS, and Greenberg AS (2012) Adipose tissue inflammation and reduced insulin sensitivity in ovariectomized mice occurs in the absence of increased adiposity. Endocrinology 153:4266-4277
45. Wang Q, Keutmann HT, Schneyer AL, and Sluss PM (2000) Analysis of human follistatin structure: identification of two discontinuous N-terminal sequences coding for activin A binding and structural consequences of activin binding to native proteins. Endocrinology 141:3183-3193
46. Wozniak AC and Anderson JE (2007) Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236:240-250
47. Yin D and Tang JG (2001) Gene therapy for streptozotocin-induced diabetic mice by electroporational transfer of naked human insulin precursor DNA into skeletal muscle in vivo. FEBS Lett 495:16-20
48. Yuen CW and Ge W (2004) Follistatin suppresses FSHbeta but increases LHbeta expression in the goldfish -evidence for an activin-mediated autocrine/paracrine system in fish pituitary. Gen Comp Endocrinol 135:108-115
49. Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, Rosenfeld R, Chen Q, Boone T, and Simonet WS, et al. (2010) Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142:531-543
50. Zhu J, Li Y, Lu A, Gharaibeh B, Ma J, Kobayashi T, Quintero AJ, and Huard J (2011) Follistatin improves skeletal muscle healing after injury and disease through an interaction with muscle regeneration, angiogenesis, and fibrosis. Am J Pathol 179: 915-930.