Role of secreted modular calcium-binding protein 1 (SMOC1) in transforming growth factor β signalling and angiogenesis

Cardiovascular Research

Volumn 106, Issue 2, 2015, Pages 284-294

  Awwad, Khader ^a   Hu, Jiong ^a   Shi, Lei ^a   Mangels, Nicole ^a   Abdel Malik, Randa ^a   Zippel, Nina ^a   Fisslthaler, Beate ^a   Eble, Johannes A ^b   Pfeilschifter, Josef ^c   Popp, Rüdiger ^a   Fleming, Ingrid ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Angiogenesis; Endoglin; Extracellular matrix; Matricellular protein; Transforming growth factor beta

Indexed keywords

ALPHA2 INTEGRIN; CALBINDIN; ENDOGLIN; MICRORNA 223; SMAD2 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; ACTIVIN RECEPTOR 1; ACVRL1 PROTEIN, MOUSE; OSTEONECTIN; SMOC-1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTERY ENDOTHELIUM; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PIG; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RETINA; SPROUTING; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; CELL PROLIFERATION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEONECTIN; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SWINE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84929073404     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv098     Document Type: Article

References (56)

1. Rivera LB, Bradshaw AD, Brekken RA. The regulatory function of SPARC in vascular biology. Cell Mol Life Sci 2011;68:3165-3173.
2. Chiodoni C, Colombo MP, Sangaletti S. Matricellular proteins: from homeostasis to inflammation, cancer, and metastasis. Cancer Metastasis Rev 2010;29:295-307.
3. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 2002;14:608-616.
4. Raines E, Lane T, Iruela-Arispe M, Ross R, Sage E. The extracellular glycoprotein SPARC interacts with platelet-derived growth factor(PDGF)-AB and-BB and inhibits the binding of PDGF to its receptors. Proc Natl Acad Sci USA 1992;89:1281-1285.
5. Kupprion C, Motamed K, Sage EH. SPARC (BM-40, osteonectin) inhibits the mitogenic effectofvascular endothelial growth factoronmicrovascular endothelial cells.JBiol Chem 1998;273:29635-29640.
6. Motamed K, Blake D, Angello J, Allen B, Rapraeger A, Hauschka S, Sage E. Fibroblast growth factor receptor-1 mediates the inhibition of endothelial cell proliferation and the promotion of skeletal myoblast differentiation by SPARC: a role for protein kinase A. J Cell Biochem 2003;90:408-423.
7. Francki A, Motamed K, McClure T, Kaya M, Murri C, Blake D, Carbon J, Sage E. SPARC regulates cell cycle progression in mesangial cells via its inhibition of IGF-dependent signaling. J Cell Biochem 2003;88:802-811.
8. Francki A, McClure T, Brekken R, Motamed K, Murri C, Wang T, Sage E.SPARC regulates TGF-beta1-dependent signaling in primary glomerular mesangial cells. J Cell Biochem 2004;91:915-925.
9. Gersdorff N, Muller M, Schall A, Miosge N. Secreted modular calcium-binding protein-1 localization during mouse embryogenesis. Histochem Cell Biol 2006;126:705-712.
10. Okada I, Hamanoue H, Terada K, Tohma T, Megarbane A, Chouery E, Abou-Ghoch J, Jalkh N, Cogulu O, Ozkinay F, Horie K, Takeda J, Furuichi T, Ikegawa S, Nishiyama K, Miyatake S, Nishimura A, Mizuguchi T, Niikawa N, Hirahara F, Kaname T, Yoshiura K, Tsurusaki Y, Doi H, Miyake N, Furukawa T, Matsumoto N, Saitsu H. SMOC1 is essential for ocular and limb development in humans and mice. Am J Hum Genet 2011;88:30-41.
11. Vannahme C, Smyth N, Miosge N, Gosling S, Frie C, Paulsson M, Maurer P, Hartmann U. Characterization of SMOC-1, a novel modular calcium-binding protein in basement membranes. J Biol Chem 2002;277:37977-37986.
12. Bradshaw AD. Diverse biological functions of the SPARC family of proteins. Int J Biochem Cell Biol 2012;44:480-488.
13. Choi YA, Lim J, Kim KM, Acharya B, Cho JY, Bae YC, Shin HI, Kim SY, Park EK. Secretome analysis of human BMSCs and identification of SMOC1 as an important ECM protein in osteoblast differentiation. J Proteome Res 2010;9:2946-2956.
14. Novinec M, Kovacic L, Skrlj N, Turk V, Lenarcic B. Recombinant human SMOCs produced by in vitro refolding: calcium-binding properties and interactions with serum proteins. Protein Expr Purif 2008;62:75-82.
15. Di Niro R, Sulic AM, Mignone F, D'Angelo S, Bordoni R, Iacono M, Marzari R, Gaiotto T, Lavric M, Bradbury ARM, Biancone L, Zevin-Sonkin D, De Bellis G, Santoro C, Sblattero D. Rapid interactome profiling by massive sequencing. Nucl Acids Res 2010; 38:e110.
16. Brellier F, Ruggiero S, Zwolanek D, Martina E, Hess D, Brown-Luedi M, Hartmann U, Koch M, Merlo A, Lino M, Chiquet-Ehrismann R. SMOC1 is a tenascin-C interacting protein over-expressed in brain tumors. Matrix Biol 2011;30:225-233.
17. Boon K, Edwards J, Eberhart C, Riggins G. Identification of astrocytoma associated genes including cell surface markers. BMC Cancer 2004;4:39.
18. Abouzeid H, Boisset G, Favez T, Youssef M, Marzouk I, Shakankiry N, Bayoumi N, Descombes P, Agosti C, Munier FL, Schorderet DF. Mutations in the SPARC-related modular calcium-binding protein 1 gene, SMOC1, cause Waardenburg anophthalmia syndrome. Am J Hum Genet 2011;88:92-98.
19. Sherva R, Miller MB, Lynch AI, Devereux RB, Rao DC, Oberman A, Hopkins PN, Kitzman DW, Atwood LD, Arnett DK. A whole genome scan for pulse pressure/stroke volume ratio in African Americans: the hyperGEN study. Am J Hypertens 2007; 20:398-402.
20. Rocnik EF, Liu P, Sato K, Walsh K, Vaziri C. The novel SPARC family member SMOC-2 potentiates angiogenic growth factor activity. J Biol Chem 2006;281:22855-22864.
21. Albig AR, Roy TG, Becenti DJ, Schiemann WP. Transcriptome analysisofendothelial cell gene expression induced by growth on matrigel matrices: identification and characterization of MAGP-2 and lumican as novel regulators of angiogenesis. Angiogenesis 2007; 10:197-216.
22. Thomas JT, Canelos P, Luyten FP, MoosM Jr. Xenopus SMOC-1 Inhibits bone morpho-genetic protein signaling downstreamof receptor binding andis essential for postgastru-lation development in Xenopus. J Biol Chem 2009;284:18994-19005.
23. Vuilleumier R, Springhorn A, Patterson L, Koidl S, Hammerschmidt M, Affolter M, Pyrowolakis G. Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 2010;12:611-617.
24. Dreieicher E, Beck KF, Lazaroski S, Boosen M, Tsalastra-Greul W, Beck M, Fleming I, Schaefer L, Pfeilschifter J. Nitric oxide inhibits glomerular TGF-b signaling via SMOC-1. J Am Soc Nephrol 2009;20:1963-1974.
25. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, Brummelkamp TR, Fleming MD, Camargo FD. Regulation ofprogenitorcell proliferation and granulocyte function by microRNA-223. Nature 2008;451:1125-1129.
26. Fleming I, Fisslthaler B, Dixit M, Busse R. Role of PECAM-1 in the shear-stress-induced activation of Akt and the endothelial nitric oxide synthase (eNOS) in endothelial cells. J Cell Sci 2005;118:4103-4111.
27. Popp R, Bauersachs J, Hecker M, Fleming I, Busse R. A transferable, b-naphthoflavone-inducible, hyperpolarizing factor is synthesized by native and cultured porcine coronary endothelial cells. J Physiol (Lond) 1996;497:699-709.
28. Shi L, Fisslthaler B, Zippel N, Frömel T, Hu J, Elgheznawy A, Heide H, Popp R, Fleming I. MicroRNA-223 antagonizes angiogenesis by targeting b1 integrinand preventing growth factor signaling in endothelial cells. Circ Res 2013;113:1320-1330.
29. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, Ten DP. Balancing the; activation state of the endothelium via two distinct TGF-b type I receptors. EMBO J 2002;21:1743-1753.
30. Ota T, Fujii M, Sugizaki T, Ishii M, Miyazawa K, Aburatani H, Miyazono K. Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-beta in human umbilical vein endothelial cells.J Cell Physiol 2002;193:299-318.
31. Heino J, Massagué J. Transforming growth factor-b switches the pattern of integrins expressed in MG-63 human osteosarcoma cells and causes a selective loss of cell adhesion to laminin.J Biol Chem 1989;264:21806-21811.
32. Castañares C, Redondo-Horcajo M, Magan-Marchal N, Ten DP, Lamas S, Rodriguez-Pascual F. Signaling by ALK5 mediates TGF-b-induced ET-1 expression in endothelial cells: a role for migration and proliferation. J Cell Sci 2007;120:1256-1266.
33. Wang X, McLennan SV, Allen TJ, Twigg SM. Regulation of pro-inflammatory and pro-fibrotic factors by CCN2/CTGF in H9c2cardiomyocytes.J Cell Commun Signal 2010;4:15-23.
34. Liu Z, Kobayashi K, van DM, van Heiningen SH, Valdimarsdottir G, van LT, Scharpfenecker M, Lowik CW, Goumans MJ, Ten DP, Pardali E. VEGF and inhibitors of TGFb type-I receptor kinase synergistically promote blood-vessel formation by inducing a5-integrin expression. J Cell Sci 2009;122:3294-3302.
35. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB, Roberts AB. Transforming growth factor b1 positively regulates its own expression in normal and transformed cells.J Biol Chem 1988;263:7741-7746.
36. Duff SE, Li C, Garland JM, Kumar S. CD105 is important for angiogenesis: evidence and potential applications. FASEBJ 2003;17:984-992.
37. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, Ten DP. Endoglin promotes endothelial cell proliferation and TGF-b/ALK1 signal transduction. EMBO J 2004;23:4018-4028.
38. Chan SY, Loscalzo J. MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle 2010;9:1072-1083.
39. Greco S, Gaetano C, Martelli F. HypoxamiR regulation and function in ischemic cardiovascular diseases. Antioxid Redox Signal 2013;21:1202-1219.
40. Fukao T, Fukuda Y, Kiga K, Sharif J, Hino K, Enomoto Y, Kawamura A, Nakamura K, Takeuchi T, Tanabe M. An evolutionary conserved mechanism for microRNA-223 expression revealed by microRNAgene profiling. Cell 2007;129:617-631.
41. Seifeddine R, Dreiem A, Blanc E, Fulchignoni-Lataud MC, Belda M-ALF, Lecuru F, Mayi TH, Mazure N, Favaudon V, Massaad C, Barouki R, Massaad-Massade L. Hypoxia down-regulates CCAAT/enhancer binding protein-a expression in breast cancer cells. Cancer Res 2008;68:2158-2165.
42. Janardhan HP. The HIF-1a-C/EBPa axis. Sci Signal 2008;1:jc2.
43. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011;146:873-887.
44. Klemencic M, Novinec M, Maier S, Hartmann U, Lenarcic B. The heparin-binding activity of secreted modular calcium-binding protein 1 (SMOC-1) modulates its cell adhesion properties. PLoS ONE 2013;8:e56839.
45. Slavotinek AM. Eye development genes and known syndromes. Mol Genet Metab 2011; 104:448-456.
46. Merkerova M, Belickova M, Bruchova H. Differential expression of microRNAs in hem-atopoietic cell lineages. Eur J Haematol 2008;81:304-310.
47. Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. Existence of a micro-RNA pathway in anucleate platelets. Nat Struct Mol Biol 2009;16:961-966.
48. Basque J-R, Chailler P, Ménard D. Laminins and TGF-b maintain cell polarity and functionality of human gastric glandular epithelium. Am J Physiol Cell Physiol 2002;282: C873-C884.
49. Rivera LB, Brekken RA. SPARC promotes pericyte recruitment via inhibitionofendoglin-dependent TGF-b1 activity. J Cell Biol 2011;193:1305-1319.
50. Kapur NK, Morine KJ, Letarte M. Endoglin: a critical mediator of cardiovascular health. Vasc Health Risk Man 2013;9:195-206.
51. Barnett JM, Suarez S, McCollum GW, Penn JS. Endoglin promotes angiogenesis in cell-and animal-based models of retinal neovascularization. Invest Ophthalmol Vis Sci 2014; 55:6490-6498.
52. Mahmoud M, Allinson KR, Zhai Z, Oakenfull R, Ghandi P, Adams RH, Fruttiger M, Arthur HM. Pathogenesis of arteriovenous malformations in the absence of endoglin. Circ Res 2010;106:1425-1433.
53. Li C, Hampson IN, Hampson L, Kumar P, Bernabeu C, Kumar S. CD105 antagonizes the inhibitory signaling of transforming growth factor beta1 on human vascular endothelial cells. FASEB J 2000;14:55-64.
54. Motamed K, Funk SE, Koyama H, Ross R, Raines EW, Sage EH. Inhibition of PDGF-stimulated and matrix-mediated proliferation of human vascular smooth muscle cells by SPARC is independent of changes in cell shape or cyclin-dependent kinase inhibitors. J Cell Biochem 2002;84:759-771.
55. Zhang JL, Chen GW, Liu YC, Wang PY, Wang X, Wan YL, Zhu J, Gao HQ, Yin J, Wang W, Tian ML. Secreted protein acidic and rich in cysteine (SPARC) suppresses angiogenesis by down-regulating the expression of VEGF and MMP-7 in gastric cancer. PLoS ONE 2012;7:e44618.
56. Gorantla B, Bhoopathi P, Chetty C, Gogineni VR, Sailaja GS, Gondi CS, Rao JS. Notch signaling regulates tumor-induced angiogenesis in SPARC-overexpressed neuroblast-oma. Angiogenesis 2013;16:85-100.