Follistatin-like protein 1 regulates chondrocyte proliferation and chondrogenic differentiation of mesenchymal stem cells

Annals of the Rheumatic Diseases

Volumn 74, Issue 7, 2015, Pages 1467-1473

  Chaly, Yury ^a   Blair, Harry C ^b,c   Smith, Sonja M ^a   Bushnell, Daniel S ^d   Marinov, Anthony D ^d   Campfield, Brian T ^d   Hirsch, Raphael ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COLLAGEN TYPE 2; FOLLISTATIN LIKE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; PROTEOGLYCAN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; FOLLISTATIN RELATED PROTEIN; FSTL1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GENE EXPRESSION; GROWTH REGULATION; HOMOZYGOTE; HUMAN; KNOCKOUT MOUSE; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEOGLYCAN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKELETON MALFORMATION; SKULL; WESTERN BLOTTING; ANIMAL; ANIMAL MODEL; CELL CULTURE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; EXTRACELLULAR MATRIX; FOLLISTATIN-RELATED PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; PROTEOGLYCANS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84934919856     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2013-204822     Document Type: Article

References (50)

1. Sekiya I, Vuoristo JT, Larson BL, et al. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci USA 2002;99:4397-402.
2. Onyekwelu I, Goldring MB, Hidaka C. Chondrogenesis, joint formation, and articular cartilage regeneration. J Cell Biochem 2009;107:383-92.
3. Rodrigues M, Griffith LG, Wells A. Growth factor regulation of proliferation and survival of multipotential stromal cells. Stem Cell Res Ther 2010;1:32.
4. Church VL, Francis-West P. Wnt signalling during limb development. Int J Dev Biol 2002;46:927-36.
5. de Crombrugghe B, Lefebvre V, Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 2001;13:721-7.
6. Shibanuma M, Mashimo J, Mita A, et al. Cloning from a mouse osteoblastic cell line of a set of transforming-growth-factor-beta 1-regulated genes, one of which seems to encode a follistatin-related polypeptide. Eur J Biochem 1993;217:13-19.
7. Wilson DC, Marinov AD, Blair HC, et al. Follistatin-like protein 1 is a mesenchyme-derived inflammatory protein and may represent a biomarker for systemic-onset juvenile rheumatoid arthritis. Arthritis Rheum 2010;62:2510-16.
8. Gorelik M, Wilson DC, Cloonan YK, et al. Plasma follistatin-like protein 1 is elevated in Kawasaki disease and may predict coronary artery Aneurysm formation. J Pediatr 2012;161:116-19.
9. Gorelik M, Fall N, Altaye M, et al. Follistatin-like protein 1 and the ferritin/erythrocyte sedimentation rate ratio are potential biomarkers for Dysregulated gene expression and macrophage activation syndrome in systemic juvenile idiopathic arthritis. J Rheumatol 2013;40:1191-9.
10. Miyamae T, Marinov AD, Sowders D, et al. Follistatin-like protein-1 is a novel proinflammatory molecule. J Immunol 2006;177:4758-62.
11. Clutter SD, Wilson DC, Marinov AD, et al. Follistatin-like protein 1 promotes arthritis by up-regulating IFN-gamma. J Immunol 2009;182:234-9.
12. Chaly Y, Marinov AD, Oxburgh L, et al. FSTL1 promotes arthritis in mice by enhancing inflammatory cytokine/chemokine expression. Arthritis Rheum 2012;64:1082-8.
13. Li KC, Zhang FX, Li CL, et al. Follistatin-like 1 suppresses sensory afferent transmission by activating Na+,K+-ATPase. Neuron 2011;69:974-87.
14. Oshima Y, Ouchi N, Sato K, et al. Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation 2008;117:3099-108.
15. Ouchi N, Oshima Y, Ohashi K, et al. Follistatin-like 1, a secreted muscle protein, promotes endothelial cell function and revascularization in ischemic tissue through a nitric-oxide synthase-dependent mechanism. J Biol Chem 2008;283:32802-11.
16. Liu S, Shen H, Xu M, et al. FRP inhibits ox-LDL-induced endothelial cell apoptosis through an Akt-NF-{kappa}B-Bcl-2 pathway and inhibits endothelial cell apoptosis in an apoE-knockout mouse model. Am J Physiol Endocrinol Metab 2010;299:E351-63.
17. Geng Y, Dong Y, Yu M, et al. Follistatin-like 1 (Fstl1) is a bone morphogenetic protein (BMP) 4 signaling antagonist in controlling mouse lung development. Proc Natl Acad Sci USA 2011;108:7058-63.
18. Sylva M, Li VS, Buffing AA, et al. The BMP antagonist follistatin-like 1 is required for skeletal and lung organogenesis. PLoS ONE 2011;6:e22616.
19. Towers P, Patel K, Withington S, et al. Flik, a chick follistatin-related gene, functions in gastrular dorsalisation/neural induction and in subsequent maintenance of midline Sonic hedgehog signalling. Dev Biol 1999;214:298-317.
20. Dal-Pra S, Furthauer M, Van-Celst J, et al. Noggin1 and Follistatin-like2 function redundantly to Chordin to antagonize BMP activity. Dev Biol 2006;298:514-26.
21. Tanaka M, Murakami K, Ozaki S, et al. DIP2 disco-interacting protein 2 homolog A (Drosophila) is a candidate receptor for follistatin-related protein/follistatin-like 1 - analysis of their binding with TGF-beta superfamily proteins. FEBS J 2010;277:4278-89.
22. Hardy S, Kitamura M, Harris-Stansil T, et al. Construction of adenovirus vectors through Cre-lox recombination. J Virol 1997;71:1842-9.
23. Burch WM, Van Wyk JJ. Triiodothyronine stimulates cartilage growth and maturation by different mechanisms. Am J Physiol 1987;252:E176-82.
24. Stockl S, Bauer RJ, Bosserhoff AK, et al. Sox9 modulates cell survival and adipogenic differentiation of multipotent adult rat mesenchymal stem cells. J Cell Sci 2013;126:2890-902.
25. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
26. Akiyama H, Chaboissier MC, Martin JF, et al. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 2002;16:2813-28.
27. Lefebvre V, Huang W, Harley VR, et al. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 1997;17:2336-46.
28. Ikeda T, Kamekura S, Mabuchi A, et al. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum 2004;50:3561-73.
29. Moser M, Binder O, Wu Y, et al. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol 2003;23:5664-79.
30. Gazzerro E, Pereira RC, Jorgetti V, et al. Skeletal overexpression of gremlin impairs bone formation and causes osteopenia. Endocrinology 2005;146:655-65.
31. Iwanaga H, Matsumoto T, Enomoto H, et al. Enhanced expression of insulin-like growth factor-binding proteins in human osteoarthritic cartilage detected by immunohistochemistry and in situ hybridization. Osteoarthritis Cartilage 2005;13:439-48.
32. Snelling SJB, Davidson RK, Culley K, et al. Evidence for a role of Dickoppf-3 (Dkk3) in osteoarthritis. Int J Exp Pathol 2011;92:A25-6.
33. Inkson CA, Ono M, Kuznetsov SA, et al. TGF-beta1 and WISP-1/CCN-4 can regulate each other's activity to cooperatively control osteoblast function. J Cell Biochem 2008;104:1865-78.
34. Zhang Y, Li J, Zhu J, et al. Enhanced cartilage formation by inhibiting cathepsin K expression in chondrocytes expanded in vitro. Biomaterials 2012;33:7394-404.
35. Wang YH, Sul HS. Pref-1 regulates mesenchymal cell commitment and differentiation through Sox9. Cell Metab 2009;9:287-302.
36. Van den Plas D, Merregaert J. In vitro studies on Itm2a reveal its involvement in early stages of the chondrogenic differentiation pathway. Biol Cell 2004;96:463-70.
37. Segawa Y, Muneta T, Makino H, et al. Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. J Orthop Res 2009;27:435-41.
38. Yoon BS, Ovchinnikov DA, Yoshii I, et al. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA 2005;102:5062-7.
39. Hill TP, Spater D, Taketo MM, et al. Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 2005;8:727-38.
40. Finnson KW, Chi Y, Bou-Gharios G, et al. TGF-b signaling in cartilage homeostasis and osteoarthritis. Front Biosci (Schol Ed) 2012;4:251-68.
41. Yang X, Chen L, Xu X, et al. TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 2001;153:35-46.
42. Pais H, Nicolas FE, Soond SM, et al. Analyzing mRNA expression identifies Smad3 as a microRNA-140 target regulated only at protein level. RNA 2010;16:489-94.
43. Kawakami Y, Rodriguez-Leon J, Izpisua Belmonte JC. The role of TGFbetas and Sox9 during limb chondrogenesis. Curr Opin Cell Biol 2006;18:723-9.
44. Tew SR, Hardingham TE. Regulation of SOX9 mRNA in human articular chondrocytes involving p38 MAPK activation and mRNA stabilization. J Biol Chem 2006;281:39471-9.
45. Prasadam I, Mao X, Wang Y, et al. Inhibition of p38 pathway leads to OA-like changes in a rat animal model. Rheumatology 2012;51:813-23.
46. Cravero JD, Carlson CS, Im HJ, et al. Increased expression of the Akt/PKB inhibitor TRB3 in osteoarthritic chondrocytes inhibits insulin-like growth factor 1-mediated cell survival and proteoglycan synthesis. Arthritis Rheum 2009;60:492-500.
47. Wang Y, Li D, Xu N, et al. Follistatin-like protein 1: a serum biochemical marker reflecting the severity of joint damage in patients with osteoarthritis. Arthritis Res Ther 2011;13:R193.
48. Stenberg J, Ruetschi U, Skioldebrand E, et al. Quantitative proteomics reveals regulatory differences in the chondrocyte secretome from human medial and lateral femoral condyles in osteoarthritic patients. Proteome Sci 2013;11:43.
49. Blaney Davidson EN, Scharstuhl A, Vitters EL, et al. Reduced transforming growth factor-beta signaling in cartilage of old mice: role in impaired repair capacity. Arthritis Res Ther 2005;7:R1338-47.
50. Blaney Davidson EN, van der Kraan PM, van den Berg WB. TGF-beta and osteoarthritis. Osteoarthritis Cartilage 2007;15:597-604.