Follistatin-like 1 in development and human diseases

Andrea Mattiotti, Stuti Prakash, Phil Barnett, Maurice J B van den Hoff, Andrea Mattiotti, Stuti Prakash, Phil Barnett, Maurice J B van den Hoff

Abstract

Follistatin-like 1 (FSTL1) is a secreted glycoprotein displaying expression changes during development and disease, among which cardiovascular disease, cancer, and arthritis. The cardioprotective role of FSTL1 has been intensively studied over the last years, though its mechanism of action remains elusive. FSTL1 is involved in multiple signaling pathways and biological processes, including vascularization and regulation of the immune response, a feature that complicates its study. Binding to the DIP2A, TLR4 and BMP receptors have been shown, but other molecular partners probably exist. During cancer progression and rheumatoid arthritis, controversial data have been reported with respect to the proliferative, apoptotic, migratory, and inflammatory effects of FSTL1. This controversy might reside in the extensive post-transcriptional regulation of FSTL1. The FSTL1 primary transcript also encodes for a microRNA (miR-198) in primates and multiple microRNA-binding sites are present in the 3'UTR. The switch between expression of the FSTL1 protein and miR-198 is an important regulator of tumour metastasis and wound healing. The glycosylation state of FSTL1 is a determinant of biological activity, in cardiomyocytes the glycosylated form promoting proliferation and the non-glycosylated working anti-apoptotic. Moreover, the glycosylation state shows differences between species and tissues which might underlie the differences observed in in vitro studies. Finally, regulation at the level of protein secretion has been described.

Keywords: Cancer; Cardiovascular disease; Fibrosis; Glycosylation; Immune disease; Inflammation; Obesity; Pulmonary disease; Signal transduction; miRNA.

Figures

Fig. 1
Fig. 1
Follistatin-like 1 in cardiovascular disease. Schematic representation of the known signaling pathways interacting with FSTL1 in cardiovascular disease. Grey components indicate unknown receptors. The coloured arrows denote the secreted Fstl1 (width relates amount). Coloured area defines different conditions. Image adjusted from http://smart.servier.com
Fig. 2
Fig. 2
Follistatin-like 1 in cancer and tumour. Schematic representation of the known signaling pathways interacting with FSTL1 during cancer growth and metastasis. Grey components indicate unknown receptors. Helical structures represent gene expression. Dashed arrow indicates translation from mRNA to protein. The dashed line separates different processes: tumour growth and metastasis. Image adjusted from http://smart.servier.com
Fig. 3
Fig. 3
Follistatin-like 1 in immune diseases. Schematic representation of the known signaling pathways interacting with FSTL1 during inflammatory processes. Grey components indicate unknown receptors. Helical structures represent gene expression. Dashed arrow indicates translation from mRNA to protein. The dashed line separates the two opposite effects of FSTL1: pro- and anti-inflammatory. Image adjusted from http://smart.servier.com

References

    1. Sylva M, Moorman AF, van den Hoff MJ. Follistatin-like 1 in vertebrate development. Birth Defects Res Embryo Today. 2013;99(1):61–69. doi: 10.1002/bdrc.21030.
    1. Shibanuma M, Mashimo J, Mita A, Kuroki T, Nose K. 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(1):13–19. doi: 10.1111/j.1432-1033.1993.tb18212.x.
    1. Zwijsen A, Blockx H, Van Arnhem W, Willems J, Fransen L, Devos K, Raymackers J, Van De Voorde A, Slegers H. Characterization of a rat C6 glioma-secreted follistatin-related protein (FRP). Cloning and sequence of the human homologue. Eur J Biochem. 1994;225(3):937–946. doi: 10.1111/j.1432-1033.1994.0937b.x.
    1. Hambrock HO, Kaufmann B, Muller S, Hanisch FG, Nose K, Paulsson M, Maurer P, Hartmann U. Structural characterization of TSC-36/Flik: analysis of two charge isoforms. J Biol Chem. 2004;279(12):11727–11735. doi: 10.1074/jbc.M309318200.
    1. Liu T, Qian WJ, Gritsenko MA, Camp DG, 2nd, Monroe ME, Moore RJ, Smith RD. Human plasma N-glycoproteome analysis by immunoaffinity subtraction, hydrazide chemistry, and mass spectrometry. J Proteome Res. 2005;4(6):2070–2080. doi: 10.1021/pr0502065.
    1. Adams D, Larman B, Oxburgh L. Developmental expression of mouse Follistatin-like 1 (Fstl1): dynamic regulation during organogenesis of the kidney and lung. Gene Expr Patterns. 2007;7(4):491–500. doi: 10.1016/j.modgep.2006.10.009.
    1. Wu Y, Zhou S, Smas CM. Downregulated expression of the secreted glycoprotein follistatin-like 1 (Fstl1) is a robust hallmark of preadipocyte to adipocyte conversion. Mech Dev. 2010;127(3–4):183–202. doi: 10.1016/j.mod.2009.12.003.
    1. Oshima Y, Ouchi N, Sato K, Izumiya Y, Pimentel DR, Walsh K. Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation. 2008;117(24):3099–3108. doi: 10.1161/CIRCULATIONAHA.108.767673.
    1. Lara-Pezzi E, Felkin LE, Birks EJ, Sarathchandra P, Panse KD, George R, Hall JL, Yacoub MH, Rosenthal N, Barton PJ. Expression of follistatin-related genes is altered in heart failure. Endocrinology. 2008;149(11):5822–5827. doi: 10.1210/en.2008-0151.
    1. van Wijk B, Gunst QD, Moorman AF, van den Hoff MJ. Cardiac regeneration from activated epicardium. PLoS One. 2012;7(9):e44692. doi: 10.1371/journal.pone.0044692.
    1. Ogura Y, Ouchi N, Ohashi K, Shibata R, Kataoka Y, Kambara T, Kito T, Maruyama S, Yuasa D, Matsuo K, Enomoto T, Uemura Y, Miyabe M, Ishii M, Yamamoto T, Shimizu Y, Walsh K, Murohara T. Therapeutic impact of follistatin-like 1 on myocardial ischemic injury in preclinical models. Circulation. 2012;126(14):1728–1738. doi: 10.1161/CIRCULATIONAHA.112.115089.
    1. Shimano M, Ouchi N, Nakamura K, van Wijk B, Ohashi K, Asaumi Y, Higuchi A, Pimentel DR, Sam F, Murohara T, van den Hoff MJ, Walsh K. Cardiac myocyte follistatin-like 1 functions to attenuate hypertrophy following pressure overload. Proc Natl Acad Sci USA. 2011;108(43):E899–E906. doi: 10.1073/pnas.1108559108.
    1. Wei K, Serpooshan V, Hurtado C, Diez-Cunado M, Zhao M, Maruyama S, Zhu W, Fajardo G, Noseda M, Nakamura K, Tian X, Liu Q, Wang A, Matsuura Y, Bushway P, Cai W, Savchenko A, Mahmoudi M, Schneider MD, van den Hoff MJ, Butte MJ, Yang PC, Walsh K, Zhou B, Bernstein D, Mercola M, Ruiz-Lozano P. Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature. 2015;525(7570):479–485. doi: 10.1038/nature15372.
    1. Maruyama S, Nakamura K, Papanicolaou KN, Sano S, Shimizu I, Asaumi Y, van den Hoff MJ, Ouchi N, Recchia FA, Walsh K. Follistatin-like 1 promotes cardiac fibroblast activation and protects the heart from rupture. EMBO Mol Med. 2016;8:949–966. doi: 10.15252/emmm.201506151.
    1. Tanaka K, Valero-Munoz M, Wilson RM, Essick EE, Fowler CT, Nakamura K, van den Hoff M, Ouchi N, Sam F. Follistatin like 1 regulates hypertrophy in heart failure with preserved ejection fraction. JACC Basic Transl Sci. 2016;1(4):207–221. doi: 10.1016/j.jacbts.2016.04.002.
    1. Meehan KL, Holland JW, Dawkins HJ. Proteomic analysis of normal and malignant prostate tissue to identify novel proteins lost in cancer. Prostate. 2002;50(1):54–63. doi: 10.1002/pros.10032.
    1. Trojan L, Schaaf A, Steidler A, Haak M, Thalmann G, Knoll T, Gretz N, Alken P, Michel MS. Identification of metastasis-associated genes in prostate cancer by genetic profiling of human prostate cancer cell lines. Anticancer Res. 2005;25(1A):183–191.
    1. Reddy SP, Britto R, Vinnakota K, Aparna H, Sreepathi HK, Thota B, Kumari A, Shilpa BM, Vrinda M, Umesh S, Samuel C, Shetty M, Tandon A, Pandey P, Hegde S, Hegde AS, Balasubramaniam A, Chandramouli BA, Santosh V, Kondaiah P, Somasundaram K, Rao MR. Novel glioblastoma markers with diagnostic and prognostic value identified through transcriptome analysis. Clin Cancer Res. 2008;14(10):2978–2987. doi: 10.1158/1078-0432.CCR-07-4821.
    1. Chan QK, Ngan HY, Ip PP, Liu VW, Xue WC, Cheung AN. Tumor suppressor effect of follistatin-like 1 in ovarian and endometrial carcinogenesis: a differential expression and functional analysis. Carcinogenesis. 2009;30(1):114–121. doi: 10.1093/carcin/bgn215.
    1. Tan X, Zhai Y, Chang W, Hou J, He S, Lin L, Yu Y, Xu D, Xiao J, Ma L, Wang G, Cao T, Cao G. Global analysis of metastasis-associated gene expression in primary cultures from clinical specimens of clear-cell renal-cell carcinoma. IntJ Cancer. 2008;123(5):1080–1088. doi: 10.1002/ijc.23637.
    1. Liu Y, Han X, Yu Y, Ding Y, Ni C, Liu W, Hou X, Li Z, Hou J, Shen D, Yin J, Zhang H, Thompson TC, Tan X, Cao G. A genetic polymorphism affects the risk and prognosis of renal cell carcinoma: association with follistatin-like protein 1 expression. Sci Rep. 2016;6:26689. doi: 10.1038/srep26689.
    1. Zhou X, Xiao X, Huang T, Du C, Wang S, Mo Y, Ma N, Murata M, Li B, Wen W, Huang G, Zeng X, Zhang Z. Epigenetic inactivation of follistatin-like 1 mediates tumor immune evasion in nasopharyngeal carcinoma. Oncotarget. 2016;7(13):16433–16444.
    1. Li D, Wang Y, Xu N, Wei Q, Wu M, Li X, Zheng P, Sun S, Jin Y, Zhang G, Liao R, Zhang P. Follistatin-like protein 1 is elevated in systemic autoimmune diseases and correlated with disease activity in patients with rheumatoid arthritis. Arthritis Res Ther. 2011;13(1):17. doi: 10.1186/ar3241.
    1. Shi DL, Shi GR, Xie J, Du XZ, Yang H. MicroRNA-27a inhibits cell migration and invasion of fibroblast-like synoviocytes by targeting follistatin-like protein 1 in rheumatoid arthritis. Mol Cells. 2016;39(8):611–618. doi: 10.14348/molcells.2016.0103.
    1. Wilson DC, Marinov AD, Blair HC, Bushnell DS, Thompson SD, Chaly Y, Hirsch R. 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(8):2510–2516. doi: 10.1002/art.27485.
    1. Wang Y, Li D, Xu N, Tao W, Zhu R, Sun R, Fan W, Zhang P, Dong T, Yu L. Follistatin-like protein 1: a serum biochemical marker reflecting the severity of joint damage in patients with osteoarthritis. Arthritis Res Ther. 2011;13(6):R193. doi: 10.1186/ar3522.
    1. Sylva M, Li VS, Buffing AA, van Es JH, van den Born M, van der Velden S, Gunst Q, Koolstra JH, Moorman AF, Clevers H, van den Hoff MJ. The BMP antagonist follistatin-like 1 is required for skeletal and lung organogenesis. PLoS One. 2011;6(8):e22616. doi: 10.1371/journal.pone.0022616.
    1. Geng Y, Dong Y, Yu M, Zhang L, Yan X, Sun J, Qiao L, Geng H, Nakajima M, Furuichi T, Ikegawa S, Gao X, Chen YG, Jiang D, Ning W. 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(17):7058–7063. doi: 10.1073/pnas.1007293108.
    1. Zhou J, Liao M, Hatta T, Tanaka M, Xuan X, Fujisaki K. Identification of a follistatin-related protein from the tick Haemaphysalis longicornis and its effect on tick oviposition. Gene. 2006;372:191–198. doi: 10.1016/j.gene.2005.12.020.
    1. Tanaka M, Murakami K, Ozaki S, Imura Y, Tong XP, Watanabe T, Sawaki T, Kawanami T, Kawabata D, Fujii T, Usui T, Masaki Y, Fukushima T, Jin ZX, Umehara H, Mimori T. 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(20):4278–4289. doi: 10.1111/j.1742-4658.2010.07816.x.
    1. Mouillet JF, Mishima T, Paffaro AM, Parks TW, Ziegler JA, Chu T, Sadovsky Y. The expression and post-transcriptional regulation of FSTL1 transcripts in placental trophoblasts. Placenta. 2015;36(11):1231–1238. doi: 10.1016/j.placenta.2015.09.005.
    1. Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol. 2006;175(1):77–85. doi: 10.1083/jcb.200603039.
    1. Zhang ZM, Zhang AR, Xu M, Lou J, Qiu WQ. TLR-4/miRNA-32-5p/FSTL1 signaling regulates mycobacterial survival and inflammatory responses in Mycobacterium tuberculosis-infected macrophages. Exp Cell Res. 2017;352(2):313–321. doi: 10.1016/j.yexcr.2017.02.025.
    1. Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, Isasi CR, Jimenez MC, Jordan LC, Judd SE, Lackland D, Lichtman JH, Lisabeth L, Liu S, Longenecker CT, Mackey RH, Matsushita K, Mozaffarian D, Mussolino ME, Nasir K, Neumar RW, Palaniappan L, Pandey DK, Thiagarajan RR, Reeves MJ, Ritchey M, Rodriguez CJ, Roth GA, Rosamond WD, Sasson C, Towfighi A, Tsao CW, Turner MB, Virani SS, Voeks JH, Willey JZ, Wilkins JT, Wu JH, Alger HM, Wong SS, Muntner P, American Heart Association Statistics Consortium, Stroke Statistics Study Heart Disease and Stroke Statistics—2017 update: a report from the American Heart Association. Circulation. 2017;135(10):e146–e603. doi: 10.1161/CIR.0000000000000485.
    1. El-Armouche A, Ouchi N, Tanaka K, Doros G, Wittkopper K, Schulze T, Eschenhagen T, Walsh K, Sam F. Follistatin-like 1 in chronic systolic heart failure: a marker of left ventricular remodeling. Circ Heart Fail. 2011;4(5):621–627. doi: 10.1161/CIRCHEARTFAILURE.110.960625.
    1. Widera C, Horn-Wichmann R, Kempf T, Bethmann K, Fiedler B, Sharma S, Lichtinghagen R, Leitolf H, Ivandic B, Katus HA, Giannitsis E, Wollert KC. Circulating concentrations of follistatin-like 1 in healthy individuals and patients with acute coronary syndrome as assessed by an immunoluminometric sandwich assay. Clin Chem. 2009;55(10):1794–1800. doi: 10.1373/clinchem.2009.129411.
    1. Zhang W, Wang W, Liu J, Li J, Wang J, Zhang Y, Zhang Z, Liu Y, Jin Y, Li J, Cao J, Wang C, Ning W, Wang J. Follistatin-like 1 protects against hypoxia-induced pulmonary hypertension in mice. Sci Rep. 2017;7:45820. doi: 10.1038/srep45820.
    1. Li BL, An JD, Feng S, Ge W. Change in serum follistatin-like protein 1 and its clinical significance in children with chronic heart failure. Zhongguo Dang Dai Er Ke Za Zhi. 2016;18(2):136–140.
    1. Widera C, Giannitsis E, Kempf T, Korf-Klingebiel M, Fiedler B, Sharma S, Katus HA, Asaumi Y, Shimano M, Walsh K, Wollert KC. Identification of follistatin-like 1 by expression cloning as an activator of the growth differentiation factor 15 gene and a prognostic biomarker in acute coronary syndrome. Clin Chem. 2012;58(8):1233–1241. doi: 10.1373/clinchem.2012.182816.
    1. van den Berg G, Somi S, Buffing AA, Moorman AF, van den Hoff MJ. Patterns of expression of the Follistatin and Follistatin-like1 genes during chicken heart development: a potential role in valvulogenesis and late heart muscle cell formation. Anat Rec (Hoboken) 2007;290(7):783–787. doi: 10.1002/ar.20559.
    1. Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD. Third universal definition of myocardial infarction. Glob Heart. 2012;7(4):275–295. doi: 10.1016/j.gheart.2012.08.001.
    1. Bhatt AS, Ambrosy AP, Velazquez EJ. Adverse remodeling and reverse remodeling after myocardial infarction. Curr Cardiol Rep. 2017;19(8):71. doi: 10.1007/s11886-017-0876-4.
    1. Di Meglio F, Castaldo C, Nurzynska D, Romano V, Miraglia R, Bancone C, Langella G, Vosa C, Montagnani S. Epithelial–mesenchymal transition of epicardial mesothelium is a source of cardiac CD117-positive stem cells in adult human heart. J Mol Cell Cardiol. 2010;49(5):719–727. doi: 10.1016/j.yjmcc.2010.05.013.
    1. Ouchi N, Asaumi Y, Ohashi K, Higuchi A, Sono-Romanelli S, Oshima Y, Walsh K. DIP2A functions as a FSTL1 receptor. J Biol Chem. 2010;285(10):7127–7134. doi: 10.1074/jbc.M109.069468.
    1. Lorell BH, Carabello BA. Left ventricular hypertrophy: pathogenesis, detection, and prognosis. Circulation. 2000;102(4):470–479. doi: 10.1161/01.CIR.102.4.470.
    1. Taegtmeyer H, Young ME, Lopaschuk GD, Abel ED, Brunengraber H, Darley-Usmar V, Des Rosiers C, Gerszten R, Glatz JF, Griffin JL, Gropler RJ, Holzhuetter HG, Kizer JR, Lewandowski ED, Malloy CR, Neubauer S, Peterson LR, Portman MA, Recchia FA, Van Eyk JE, Wang TJ, American Heart Association Council on Basic Cardiovascular Study Assessing cardiac metabolism: a scientific statement from the American Heart Association. Circ Res. 2016;118(10):1659–1701. doi: 10.1161/RES.0000000000000097.
    1. Seki M, Powers JC, Maruyama S, Zuriaga MA, Wu CL, Kurishima C, Kim L, Johnson J, Poidomani A, Wang T, Munoz E, Rajan S, Park JY, Walsh K, Recchia FA. Acute and chronic increases of circulating FSTL1 normalize energy substrate metabolism in pacing-induced heart failure. Circ Heart Fail. 2018;11(1):e004486. doi: 10.1161/CIRCHEARTFAILURE.117.004486.
    1. Ouchi N, Oshima Y, Ohashi K, Higuchi A, Ikegami C, Izumiya Y, Walsh K. 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(47):32802–32811. doi: 10.1074/jbc.M803440200.
    1. Liu S, Wang L, Wang W, Lin J, Han J, Sun H, Guo H, Sun R, Wu Q. TSC-36/FRP inhibits vascular smooth muscle cell proliferation and migration. Exp Mol Pathol. 2006;80(2):132–140. doi: 10.1016/j.yexmp.2005.07.005.
    1. Miyabe M, Ohashi K, Shibata R, Uemura Y, Ogura Y, Yuasa D, Kambara T, Kataoka Y, Yamamoto T, Matsuo K, Joki Y, Enomoto T, Hayakawa S, Hiramatsu-Ito M, Ito M, van den Hoff MJ, Walsh K, Murohara T, Ouchi N. Muscle-derived follistatin-like 1 functions to reduce neointimal formation after vascular injury. Cardiovasc Res. 2014
    1. Yang Y, Mu T, Li T, Xie S, Zhou J, Liu M, Li D. Effects of FSTL1 on the proliferation and motility of breast cancer cells and vascular endothelial cells. Thorac Cancer. 2017;8(6):606–612. doi: 10.1111/1759-7714.12491.
    1. Levine RA, Hagege AA, Judge DP, Padala M, Dal-Bianco JP, Aikawa E, Beaudoin J, Bischoff J, Bouatia-Naji N, Bruneval P, Butcher JT, Carpentier A, Chaput M, Chester AH, Clusel C, Delling FN, Dietz HC, Dina C, Durst R, Fernandez-Friera L, Handschumacher MD, Jensen MO, Jeunemaitre XP, Le Marec H, Le Tourneau T, Markwald RR, Merot J, Messas E, Milan DP, Neri T, Norris RA, Peal D, Perrocheau M, Probst V, Puceat M, Rosenthal N, Solis J, Schott JJ, Schwammenthal E, Slaugenhaupt SA, Song JK, Yacoub MH, Leducq Mitral Transatlantic Network Mitral valve disease—morphology and mechanisms. Nat Rev Cardiol. 2015;12(12):689–710. doi: 10.1038/nrcardio.2015.161.
    1. Prakash S, Borreguero LJJ, Sylva M, Flores Ruiz L, Rezai F, Gunst QD, de la Pompa JL, Ruijter JM, van den Hoff MJB. Deletion of Fstl1 (Follistatin-Like 1) from the endocardial/endothelial lineage causes mitral valve disease. Arterioscler Thromb Vasc Biol. 2017;254:116–130. doi: 10.1161/ATVBAHA.117.309089.
    1. Dina C, Bouatia-Naji N, Tucker N, Delling FN, Toomer K, Durst R, Perrocheau M, Fernandez-Friera L, Solis J, Le Tourneau T, Chen MH, Probst V, Bosse Y, Pibarot P, Zelenika D, Lathrop M, Hercberg S, Roussel R, Benjamin EJ, Bonnet F, Lo SH, Dolmatova E, Simonet F, Lecointe S, Kyndt F, Redon R, Le Marec H, Froguel P, Ellinor PT, Vasan RS, Bruneval P, Markwald RR, Norris RA, Milan DJ, Slaugenhaupt SA, Levine RA, Schott JJ, Hagege AA, France MVP, Jeunemaitre X, Leducq Mitral Transatlantic Network Genetic association analyses highlight biological pathways underlying mitral valve prolapse. Nat Genet. 2015;47(10):1206–1211. doi: 10.1038/ng.3383.
    1. Liotta LA, Stetler-Stevenson WG. Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res. 1991;51(18 Suppl):5054s–5059s.
    1. Woodhouse EC, Chuaqui RF, Liotta LA. General mechanisms of metastasis. Cancer. 1997;80(8 Suppl):1529–1537. doi: 10.1002/(SICI)1097-0142(19971015)80:8+<1529::AID-CNCR2>;2-F.
    1. Liu Y, Tan X, Liu W, Chen X, Hou X, Shen D, Ding Y, Yin J, Wang L, Zhang H, Yu Y, Hou J, Thompson TC, Cao G. Follistatin-like protein 1 plays a tumor suppressor role in clear-cell renal cell carcinoma. Chin J Cancer. 2018;37(1):2. doi: 10.1186/s40880-018-0267-2.
    1. Chiou J, Su CY, Jan YH, Yang CJ, Huang MS, Yu YL, Hsiao M. Decrease of FSTL1-BMP4-Smad signaling predicts poor prognosis in lung adenocarcinoma but not in squamous cell carcinoma. Sci Rep. 2017;7(1):9830. doi: 10.1038/s41598-017-10366-2.
    1. Torres S, Bartolome RA, Mendes M, Barderas R, Fernandez-Acenero MJ, Pelaez-Garcia A, Pena C, Lopez-Lucendo M, Villar-Vazquez R, de Herreros AG, Bonilla F, Casal JI. Proteome profiling of cancer-associated fibroblasts identifies novel proinflammatory signatures and prognostic markers for colorectal cancer. Clin Cancer Res. 2013;19(21):6006–6019. doi: 10.1158/1078-0432.CCR-13-1130.
    1. Su S, Parris AB, Grossman G, Mohler JL, Wang Z, Wilson EM. Up-regulation of follistatin-like 1 by the androgen receptor and melanoma antigen-A11 in prostate cancer. Prostate. 2017;77(5):505–516. doi: 10.1002/pros.23288.
    1. Yang W, Wu Y, Wang C, Liu Z, Xu M, Zheng X. FSTL1 contributes to tumor progression via attenuating apoptosis in a AKT/GSK-3beta-dependent manner in hepatocellular carcinoma. Cancer Biomark. 2017;20(1):75–85. doi: 10.3233/CBM-170132.
    1. Sundaram GM, Ismail HM, Bashir M, Muhuri M, Vaz C, Nama S, Ow GS, Vladimirovna IA, Ramalingam R, Burke B, Tanavde V, Kuznetsov V, Lane EB, Sampath P. EGF hijacks miR-198/FSTL1 wound-healing switch and steers a two-pronged pathway toward metastasis. J Exp Med. 2017
    1. Lau MC, Ng KY, Wong TL, Tong M, Lee TK, Ming XY, Law S, Lee NP, Cheung AL, Qin YR, Chan KW, Ning W, Guan XY, Ma S. FSTL1 promotes metastasis and chemoresistance in esophageal squamous cell carcinoma through NFkappaB-bmp signaling cross-talk. Cancer Res. 2017;77(21):5886–5899. doi: 10.1158/0008-5472.CAN-17-1411.
    1. An J, Wang L, Zhao Y, Hao Q, Zhang Y, Zhang J, Yang C, Liu L, Wang W, Fang D, Lu T, Gao Y. Effects of FSTL1 on cell proliferation in breast cancer cell line MDAMB231 and its brain metastatic variant MDAMB231BR. Oncol Rep. 2017;38(5):3001–3010. doi: 10.3892/or.2017.6004.
    1. Mashimo J, Maniwa R, Sugino H, Nose K. Decrease in the expression of a novel TGF beta1-inducible and ras-recision gene, TSC-36, in human cancer cells. Cancer Lett. 1997;113(1–2):213–219. doi: 10.1016/S0304-3835(97)04700-9.
    1. Johnston IM, Spence HJ, Winnie JN, McGarry L, Vass JK, Meagher L, Stapleton G, Ozanne BW. Regulation of a multigenic invasion programme by the transcription factor, AP-1: re-expression of a down-regulated gene, TSC-36, inhibits invasion. Oncogene. 2000;19(47):5348–5358. doi: 10.1038/sj.onc.1203927.
    1. Sumitomo K, Kurisaki A, Yamakawa N, Tsuchida K, Shimizu E, Sone S, Sugino H. Expression of a TGF-beta1 inducible gene, TSC-36, causes growth inhibition in human lung cancer cell lines. Cancer Lett. 2000;155(1):37–46. doi: 10.1016/S0304-3835(00)00407-9.
    1. Ni X, Cao X, Wu Y, Wu J. FSTL1 suppresses tumor cell proliferation, invasion and survival in non-small cell lung cancer. Oncol Rep. 2018;39(1):13–20.
    1. Bae K, Park KE, Han J, Kim J, Kim K, Yoon KA. Mitotic cell death caused by follistatin-like 1 inhibition is associated with up-regulated Bim by inactivated Erk1/2 in human lung cancer cells. Oncotarget. 2016;7(14):18076–18084. doi: 10.18632/oncotarget.6729.
    1. Kudo-Saito C, Fuwa T, Murakami K, Kawakami Y. Targeting FSTL1 prevents tumor bone metastasis and consequent immune dysfunction. Cancer Res. 2013;73(20):6185–6193. doi: 10.1158/0008-5472.CAN-13-1364.
    1. Zhao W, Han HB, Zhang ZQ. Suppression of lung cancer cell invasion and metastasis by connexin43 involves the secretion of follistatin-like 1 mediated via histone acetylation. IntJ Biochem Cell Biol. 2011;43(10):1459–1468. doi: 10.1016/j.biocel.2011.06.009.
    1. Sakurai D, Yamaguchi A, Tsuchiya N, Yamamoto K, Tokunaga K. Expression of ID family genes in the synovia from patients with rheumatoid arthritis. Biochem Biophys Res Commun. 2001;284(2):436–442. doi: 10.1006/bbrc.2001.4974.
    1. Tanaka M, Ozaki S, Osakada F, Mori K, Okubo M, Nakao K. Cloning of follistatin-related protein as a novel autoantigen in systemic rheumatic diseases. Int Immunol. 1998;10(9):1305–1314. doi: 10.1093/intimm/10.9.1305.
    1. Ehara Y, Sakurai D, Tsuchiya N, Nakano K, Tanaka Y, Yamaguchi A, Tokunaga K. Follistatin-related protein gene (FRP) is expressed in the synovial tissues of rheumatoid arthritis, but its polymorphisms are not associated with genetic susceptibility. Clin Exp Rheumatol. 2004;22(6):707–712.
    1. Gorelik M, Wilson DC, Cloonan YK, Shulman ST, Hirsch R. Plasma follistatin-like protein 1 is elevated in Kawasaki disease and may predict coronary artery aneurysm formation. J Pediatr. 2012;161(1):116–119. doi: 10.1016/j.jpeds.2012.01.011.
    1. Newburger JW, Takahashi M, Burns JC. Kawasaki disease. J Am Coll Cardiol. 2016;67(14):1738–1749. doi: 10.1016/j.jacc.2015.12.073.
    1. Liu Y, Wei J, Zhao Y, Zhang Y, Han Y, Chen B, Cheng K, Jia J, Nie L, Cheng L. Follistatin-like protein 1 promotes inflammatory reactions in nucleus pulposus cells by interacting with the MAPK and NFkappaB signaling pathways. Oncotarget. 2017;8(26):43023–43034.
    1. Brand DD, Latham KA, Rosloniec EF. Collagen-induced arthritis. Nat Protoc. 2007;2(5):1269–1275. doi: 10.1038/nprot.2007.173.
    1. Khachigian LM. Collagen antibody-induced arthritis. Nat Protoc. 2006;1(5):2512–2516. doi: 10.1038/nprot.2006.393.
    1. Thornton S, Sowders D, Aronow B, Witte DP, Brunner HI, Giannini EH, Hirsch R. DNA microarray analysis reveals novel gene expression profiles in collagen-induced arthritis. Clin Immunol. 2002;105(2):155–168. doi: 10.1006/clim.2002.5227.
    1. Miyamae T, Marinov AD, Sowders D, Wilson DC, Devlin J, Boudreau R, Robbins P, Hirsch R. Follistatin-like protein-1 is a novel proinflammatory molecule. J Immunol. 2006;177(7):4758–4762. doi: 10.4049/jimmunol.177.7.4758.
    1. Clutter SD, Wilson DC, Marinov AD, Hirsch R. Follistatin-like protein 1 promotes arthritis by up-regulating IFN-gamma. J Immunol. 2009;182(1):234–239. doi: 10.4049/jimmunol.182.1.234.
    1. Murakami K, Tanaka M, Usui T, Kawabata D, Shiomi A, Iguchi-Hashimoto M, Shimizu M, Yukawa N, Yoshifuji H, Nojima T, Ohmura K, Fujii T, Umehara H, Mimori T. Follistatin-related protein/follistatin-like 1 evokes an innate immune response via CD14 and toll-like receptor 4. FEBS Lett. 2012;586(4):319–324. doi: 10.1016/j.febslet.2012.01.010.
    1. Tanaka M, Ozaki S, Kawabata D, Kishimura M, Osakada F, Okubo M, Murakami M, Nakao K, Mimori T. Potential preventive effects of follistatin-related protein/TSC-36 on joint destruction and antagonistic modulation of its autoantibodies in rheumatoid arthritis. Int Immunol. 2003;15(1):71–77. doi: 10.1093/intimm/dxg005.
    1. Kawabata D, Tanaka M, Fujii T, Umehara H, Fujita Y, Yoshifuji H, Mimori T, Ozaki S. Ameliorative effects of follistatin-related protein/TSC-36/FSTL1 on joint inflammation in a mouse model of arthritis. Arthritis Rheum. 2004;50(2):660–668. doi: 10.1002/art.20023.
    1. Dooley S, Herlitzka I, Hanselmann R, Ermis A, Henn W, Remberger K, Hopf T, Welter C. Constitutive expression of c-fos and c-jun, overexpression of ets-2, and reduced expression of metastasis suppressor gene nm23-H1 in rheumatoid arthritis. Ann Rheum Dis. 1996;55(5):298–304. doi: 10.1136/ard.55.5.298.
    1. Kim HJ, Kang WY, Seong SJ, Kim SY, Lim MS, Yoon YR. Follistatin-like 1 promotes osteoclast formation via RANKL-mediated NF-kappaB activation and M-CSF-induced precursor proliferation. Cell Signal. 2016;28(9):1137–1144. doi: 10.1016/j.cellsig.2016.05.018.
    1. Kagari T, Doi H, Shimozato T. The importance of IL-1 beta and TNF-alpha, and the noninvolvement of IL-6, in the development of monoclonal antibody-induced arthritis. J Immunol. 2002;169(3):1459–1466. doi: 10.4049/jimmunol.169.3.1459.
    1. Chaly Y, Fu Y, Marinov A, Hostager B, Yan W, Campfield B, Kellum JA, Bushnell D, Wang Y, Vockley J, Hirsch R. Follistatin-like protein 1 enhances NLRP3 inflammasome-mediated IL-1beta secretion from monocytes and macrophages. Eur J Immunol. 2014;44(5):1467–1479. doi: 10.1002/eji.201344063.
    1. Fan N, Sun H, Wang Y, Wang Y, Zhang L, Xia Z, Peng L, Hou Y, Shen W, Liu R, Yin J, Peng Y. Follistatin-like 1: a potential mediator of inflammation in obesity. Mediat Inflamm. 2013;2013:752519. doi: 10.1155/2013/752519.
    1. Adams DC, Karolak MJ, Larman BW, Liaw L, Nolin JD, Oxburgh L. Follistatin-like 1 regulates renal IL-1beta expression in cisplatin nephrotoxicity. Am J Physiol Renal Physiol. 2010;299(6):F1320–F1327. doi: 10.1152/ajprenal.00325.2010.
    1. Hayakawa S, Ohashi K, Shibata R, Kataoka Y, Miyabe M, Enomoto T, Joki Y, Shimizu Y, Kambara T, Uemura Y, Yuasa D, Ogawa H, Matsuo K, Hiramatsu-Ito M, van den Hoff MJ, Walsh K, Murohara T, Ouchi N. Cardiac myocyte-derived follistatin-like 1 prevents renal injury in a subtotal nephrectomy model. J Am Soc Nephrol. 2015;26(3):636–646. doi: 10.1681/ASN.2014020210.
    1. Le Luduec JB, Condamine T, Louvet C, Thebault P, Heslan JM, Heslan M, Chiffoleau E, Cuturi MC. An immunomodulatory role for follistatin-like 1 in heart allograft transplantation. Am J Transpl. 2008;8(11):2297–2306. doi: 10.1111/j.1600-6143.2008.02398.x.
    1. Pardo A, Gibson K, Cisneros J, Richards TJ, Yang Y, Becerril C, Yousem S, Herrera I, Ruiz V, Selman M, Kaminski N. Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med. 2005;2(9):e251. doi: 10.1371/journal.pmed.0020251.
    1. Dong Y, Geng Y, Li L, Li X, Yan X, Fang Y, Li X, Dong S, Liu X, Li X, Yang X, Zheng X, Xie T, Liang J, Dai H, Liu X, Yin Z, Noble PW, Jiang D, Ning W. Blocking follistatin-like 1 attenuates bleomycin-induced pulmonary fibrosis in mice. J Exp Med. 2015;212(2):235–252. doi: 10.1084/jem.20121878.
    1. Murphy N, Gaynor KU, Rowan SC, Walsh SM, Fabre A, Boylan J, Keane MP, McLoughlin P. Altered expression of bone morphogenetic protein accessory proteins in murine and human pulmonary fibrosis. Am J Pathol. 2016;186(3):600–615. doi: 10.1016/j.ajpath.2015.10.032.
    1. Vollmann EH, Cao L, Amatucci A, Reynolds T, Hamann S, Dalkilic-Liddle I, Cameron TO, Hossbach M, Kauffman KJ, Mir FF, Anderson DG, Novobrantseva T, Koteliansky V, Kisseleva T, Brenner D, Duffield J, Burkly LC. Identification of novel fibrosis modifiers by in vivo siRNA silencing. Mol Ther Nucleic Acids. 2017;7:314–323. doi: 10.1016/j.omtn.2017.04.014.
    1. Umezu T, Yamanouchi H, Iida Y, Miura M, Tomooka Y. Follistatin-like-1, a diffusible mesenchymal factor determines the fate of epithelium. Proc Natl Acad Sci USA. 2010;107(10):4601–4606. doi: 10.1073/pnas.0909501107.
    1. Miller M, Esnault S, Kurten RC, Kelly EA, Beppu A, Das S, Rosenthal P, Ramsdell J, Croft M, Zuraw B, Jarjour N, Hamid Q, Broide DH. Segmental allergen challenge increases levels of airway follistatin-like 1 in patients with asthma. J Allergy Clin Immunol. 2016;138(2):596–599 e594. doi: 10.1016/j.jaci.2016.01.019.
    1. Miller M, Beppu A, Rosenthal P, Pham A, Das S, Karta M, Song DJ, Vuong C, Doherty T, Croft M, Zuraw B, Zhang X, Gao X, Aceves S, Chouiali F, Hamid Q, Broide DH. Fstl1 promotes asthmatic airway remodeling by inducing oncostatin M. J Immunol. 2015;195(8):3546–3556. doi: 10.4049/jimmunol.1501105.
    1. Liu Y, Liu T, Wu J, Li T, Jiao X, Zhang H, Zhao J, Wang J, Liu L, Cao L, Li S, Xu J, Xu J, Ma X, Yang L, Dong L. The correlation between FSTL1 expression and airway remodeling in asthmatics. Mediat Inflamm. 2017;2017:7918472.
    1. Liu T, Liu Y, Miller M, Cao L, Zhao J, Wu J, Wang J, Liu L, Li S, Zou M, Xu J, Broide DH, Dong L. Autophagy plays a role in FSTL1-induced epithelial mesenchymal transition and airway remodeling in asthma. Am J Physiol Lung Cell Mol Physiol. 2017;313(1):L27–L40. doi: 10.1152/ajplung.00510.2016.
    1. Gugnoni M, Sancisi V, Manzotti G, Gandolfi G, Ciarrocchi A. Autophagy and epithelial-mesenchymal transition: an intricate interplay in cancer. Cell Death Dis. 2016;7(12):e2520. doi: 10.1038/cddis.2016.415.
    1. Prieto-Echague V, Lodh S, Colman L, Bobba N, Santos L, Katsanis N, Escande C, Zaghloul NA, Badano JL. BBS4 regulates the expression and secretion of FSTL1, a protein that participates in ciliogenesis and the differentiation of 3T3-L1. Sci Rep. 2017;7(1):9765. doi: 10.1038/s41598-017-10330-0.
    1. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol. 2011;11(2):85–97. doi: 10.1038/nri2921.
    1. Iacomino G, Siani A. Role of microRNAs in obesity and obesity-related diseases. Genes Nutr. 2017;12:23. doi: 10.1186/s12263-017-0577-z.
    1. Yang Y, Liu J, Mao H, Hu YA, Yan Y, Zhao C. The expression pattern of Follistatin-like 1 in mouse central nervous system development. Gene Expr Patterns. 2009;9(7):532–540. doi: 10.1016/j.gep.2009.07.001.
    1. Liu R, Yang Y, Shen J, Chen H, Zhang Q, Ba R, Wei Y, Li KC, Zhang X, Zhao C. Fstl1 is involved in the regulation of radial glial scaffold development. Mol Brain. 2015;8:53. doi: 10.1186/s13041-015-0144-8.
    1. Li KC, Zhang FX, Li CL, Wang F, Yu MY, Zhong YQ, Zhang KH, Lu YJ, Wang Q, Ma XL, Yao JR, Wang JY, Lin LB, Han M, Zhang YQ, Kuner R, Xiao HS, Bao L, Gao X, Zhang X. Follistatin-like 1 suppresses sensory afferent transmission by activating Na+, K+-ATPase. Neuron. 2011;69(5):974–987. doi: 10.1016/j.neuron.2011.01.022.
    1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–297. doi: 10.1016/S0092-8674(04)00045-5.
    1. Laurence J. Translating MicroRNAs to the clinic. Amsterdam: Mica Haley, Elsevier; 2017.
    1. Hinske LC, Galante PA, Kuo WP, Ohno-Machado L. A potential role for intragenic miRNAs on their hosts’ interactome. BMC Genom. 2010;11:533. doi: 10.1186/1471-2164-11-533.
    1. Sundaram GM, Common JE, Gopal FE, Srikanta S, Lakshman K, Lunny DP, Lim TC, Tanavde V, Lane EB, Sampath P. ‘See-saw’ expression of microRNA-198 and FSTL1 from a single transcript in wound healing. Nature. 2013;495(7439):103–106. doi: 10.1038/nature11890.
    1. Wang M, Wang J, Kong X, Chen H, Wang Y, Qin M, Lin Y, Chen H, Xu J, Hong J, Chen YX, Zou W, Fang JY. MiR-198 represses tumor growth and metastasis in colorectal cancer by targeting fucosyl transferase 8. Sci Rep. 2014;4:6145. doi: 10.1038/srep06145.
    1. Wu S, Zhang G, Li P, Chen S, Zhang F, Li J, Jiang C, Chen X, Wang Y, Du Y, Sun Q, Zhao G. miR-198 targets SHMT1 to inhibit cell proliferation and enhance cell apoptosis in lung adenocarcinoma. Tumour Biol. 2016;37(4):5193–5202. doi: 10.1007/s13277-015-4369-z.
    1. McCarthy JJ. MicroRNA-206: the skeletal muscle-specific myomiR. Biochim Biophys Acta. 2008;1779(11):682–691. doi: 10.1016/j.bbagrm.2008.03.001.
    1. Amthor H, Connolly D, Patel K, Brand-Saberi B, Wilkinson DG, Cooke J, Christ B. The expression and regulation of follistatin and a follistatin-like gene during avian somite compartmentalization and myogenesis. Dev Biol. 1996;178(2):343–362. doi: 10.1006/dbio.1996.0223.
    1. Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell. 2002;9(3):587–600. doi: 10.1016/S1097-2765(02)00481-1.
    1. Lai L, Song Y, Liu Y, Chen Q, Han Q, Chen W, Pan T, Zhang Y, Cao X, Wang Q. MicroRNA-92a negatively regulates Toll-like receptor (TLR)-triggered inflammatory response in macrophages by targeting MKK4 kinase. J Biol Chem. 2013;288(11):7956–7967. doi: 10.1074/jbc.M112.445429.
    1. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42(Database issue):D68–D73. doi: 10.1093/nar/gkt1181.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj