Sizzled-Tolloid Interactions Maintain Foregut Progenitors by Regulating Fibronectin-Dependent BMP Signaling

Developmental Cell

Volumn 23, Issue 2, 2012, Pages 292-304

  Kenny, Alan P ^a   Rankin, Scott A ^a   Allbee, Andrew W ^a   Prewitt, Allison R ^a   Zhang, Zheng ^a   Tabangin, Meredith E ^a   Shifley, Emily T ^a   Louza, Mariana P ^a   Zorn, Aaron M ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBRONECTIN; METALLOPROTEINASE; SECRETED FRIZZLED RELATED PROTEIN 1; SMAD1 PROTEIN; TOLLOID METALLOPROTEINASE;

AGENESIS; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; ENZYME ACTIVITY; GENE EXPRESSION; INTESTINE; MESODERM; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEM CELL; TISSUE DIFFERENTIATION; XENOPUS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; EMBRYO, MAMMALIAN; FIBRONECTINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTESTINES; PROTEIN BINDING; SIGNAL TRANSDUCTION; STEM CELLS; TOLLOID-LIKE METALLOPROTEINASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84865064551     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.07.002     Document Type: Article

References (54)

1. Blitz I.L., Shimmi O., Wünnenberg-Stapleton K., O'Connor M.B., Cho K.W. Is chordin a long-range- or short-range-acting factor? Roles for BMP1-related metalloproteases in chordin and BMP4 autofeedback loop regulation. Dev. Biol. 2000, 223:120-138.
2. Bovolenta P., Esteve P., Ruiz J.M., Cisneros E., Lopez-Rios J. Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease. J. Cell Sci. 2008, 121:737-746.
3. Chung W.S., Shin C.H., Stainier D.Y. Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev. Cell 2008, 15:738-748.
4. Chung W.S., Andersson O., Row R., Kimelman D., Stainier D.Y. Suppression of Alk8-mediated Bmp signaling cell-autonomously induces pancreatic beta-cells in zebrafish. Proc. Natl. Acad. Sci. USA 2010, 107:1142-1147.
5. Collavin L., Kirschner M.W. The secreted Frizzled-related protein Sizzled functions as a negative feedback regulator of extreme ventral mesoderm. Development 2003, 130:805-816.
6. Dale L., Evans W., Goodman S.A. Xolloid-related: a novel BMP1/Tolloid-related metalloprotease is expressed during early Xenopus development. Mech. Dev. 2002, 119:177-190.
7. Davidson L.A., Keller R., DeSimone D.W. Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis. Dev. Dyn. 2004, 231:888-895.
8. Davidson L.A., Marsden M., Keller R., Desimone D.W. Integrin alpha5beta1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension. Curr. Biol. 2006, 16:833-844.
9. He W., Zhang L., Ni A., Zhang Z., Mirotsou M., Mao L., Pratt R.E., Dzau V.J. Exogenously administered secreted frizzled related protein 2 (Sfrp2) reduces fibrosis and improves cardiac function in a rat model of myocardial infarction. Proc. Natl. Acad. Sci. USA 2010, 107:21110-21115.
10. Hopkins D.R., Keles S., Greenspan D.S. The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol. 2007, 26:508-523.
11. Huang G., Zhang Y., Kim B., Ge G., Annis D.S., Mosher D.F., Greenspan D.S. Fibronectin binds and enhances the activity of bone morphogenetic protein 1. J. Biol. Chem. 2009, 284:25879-25888.
12. Inomata H., Haraguchi T., Sasai Y. Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell 2008, 134:854-865.
13. Jasuja R., Ge G., Voss N.G., Lyman-Gingerich J., Branam A.M., Pelegri F.J., Greenspan D.S. Bone morphogenetic protein 1 prodomain specifically binds and regulates signaling by bone morphogenetic proteins 2 and 4. J. Biol. Chem. 2007, 282:9053-9062.
14. Karaulanov E., Knöchel W., Niehrs C. Transcriptional regulation of BMP4 synexpression in transgenic Xenopus. EMBO J. 2004, 23:844-856.
15. Kobayashi K., Luo M., Zhang Y., Wilkes D.C., Ge G., Grieskamp T., Yamada C., Liu T.C., Huang G., Basson C.T., et al. Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction. Nat. Cell Biol. 2009, 11:46-55.
16. Lee H.X., Ambrosio A.L., Reversade B., De Robertis E.M. Embryonic dorsal-ventral signaling: secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell 2006, 124:147-159.
17. Lee H.X., Mendes F.A., Plouhinec J.L., De Robertis E.M. Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity. Genes Dev. 2009, 23:2551-2562.
18. Lee J.L., Chang C.J., Chueh L.L., Lin C.T. Expression of secreted frizzled-related protein 2 in a primary canine mammary tumor cell line: a candidate tumor marker for mammary tumor cells. In Vitro Cell. Dev. Biol. Anim. 2003, 39:221-227.
19. Lee S.J. Genetic analysis of the role of proteolysis in the activation of latent myostatin. PloS One 2008, 3:e1628.
20. Li Y., Rankin S.A., Sinner D., Kenny A.P., Krieg P.A., Zorn A.M. Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. Genes Dev. 2008, 22:3050-3063.
21. Martino M.M., Hubbell J.A. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 2010, 24:4711-4721.
22. Matsuyama M., Aizawa S., Shimono A. Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet. 2009, 5:e1000427.
23. McLin V.A., Rankin S.A., Zorn A.M. Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 2007, 134:2207-2217.
24. Melkonyan H.S., Chang W.C., Shapiro J.P., Mahadevappa M., Fitzpatrick P.A., Kiefer M.C., Tomei L.D., Umansky S.R. SARPs: a family of secreted apoptosis-related proteins. Proc. Natl. Acad. Sci. USA 1997, 94:13636-13641.
25. Moreno M., Muñoz R., Aroca F., Labarca M., Brandan E., Larraín J. Biglycan is a new extracellular component of the Chordin-BMP4 signaling pathway. EMBO J. 2005, 24:1397-1405.
26. Muir A., Greenspan D.S. Metalloproteinases in Drosophila to humans that are central players in developmental processes. J. Biol. Chem. 2011, 286:41905-41911.
27. Muraoka O., Shimizu T., Yabe T., Nojima H., Bae Y.K., Hashimoto H., Hibi M. Sizzled controls dorso-ventral polarity by repressing cleavage of the Chordin protein. Nat. Cell Biol. 2006, 8:329-338.
28. Nistala H., Lee-Arteaga S., Smaldone S., Siciliano G., Carta L., Ono R.N., Sengle G., Arteaga-Solis E., Levasseur R., Ducy P., et al. Fibrillin-1 and -2 differentially modulate endogenous TGF-β and BMP bioavailability during bone formation. J. Cell Biol. 2010, 190:1107-1121.
29. Ohta K., Lupo G., Kuriyama S., Keynes R., Holt C.E., Harris W.A., Tanaka H., Ohnuma S. Tsukushi functions as an organizer inducer by inhibition of BMP activity in cooperation with chordin. Dev. Cell 2004, 7:347-358.
30. Olivares G.H., Carrasco H., Aroca F., Carvallo L., Segovia F., Larraín J. Syndecan-1 regulates BMP signaling and dorso-ventral patterning of the ectoderm during early Xenopus development. Dev. Biol. 2009, 329:338-349.
31. Petryk A., Anderson R.M., Jarcho M.P., Leaf I., Carlson C.S., Klingensmith J., Shawlot W., O'Connor M.B. The mammalian twisted gastrulation gene functions in foregut and craniofacial development. Dev. Biol. 2004, 267:374-386.
32. Piccolo S., Agius E., Lu B., Goodman S., Dale L., De Robertis E.M. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 1997, 91:407-416.
33. Ploper D., Lee H.X., De Robertis E.M. Dorsal-ventral patterning: Crescent is a dorsally secreted Frizzled-related protein that competitively inhibits Tolloid proteases. Dev. Biol. 2011, 352:317-328.
34. Ramirez F., Rifkin D.B. Extracellular microfibrils: contextual platforms for TGFbeta and BMP signaling. Curr. Opin. Cell Biol. 2009, 21:616-622.
35. Ramos J.W., DeSimone D.W. Xenopus embryonic cell adhesion to fibronectin: position-specific activation of RGD/synergy site-dependent migratory behavior at gastrulation. J. Cell Biol. 1996, 134:227-240.
36. Rankin S.A., Kormish J., Kofron M., Jegga A., Zorn A.M. A gene regulatory network controlling hhex transcription in the anterior endoderm of the organizer. Dev. Biol. 2011, 351:297-310.
37. Reversade B., De Robertis E.M. Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 2005, 123:1147-1160.
38. Reversade B., Kuroda H., Lee H., Mays A., De Robertis E.M. Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos. Development 2005, 132:3381-3392.
39. Rodriguez P., Da Silva S., Oxburgh L., Wang F., Hogan B.L., Que J. BMP signaling in the development of the mouse esophagus and forestomach. Development 2010, 137:4171-4176.
40. Rossi J.M., Dunn N.R., Hogan B.L., Zaret K.S. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev. 2001, 15:1998-2009.
41. Salic A.N., Kroll K.L., Evans L.M., Kirschner M.W. Sizzled: a secreted Xwnt8 antagonist expressed in the ventral marginal zone of Xenopus embryos. Development 1997, 124:4739-4748.
42. Schwarzbauer J.E., DeSimone D.W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 2011, 3. 10.1101/cshperspect.a005041.
43. Shin D., Shin C.H., Tucker J., Ober E.A., Rentzsch F., Poss K.D., Hammerschmidt M., Mullins M.C., Stainier D.Y. Bmp and Fgf signaling are essential for liver specification in zebrafish. Development 2007, 134:2041-2050.
44. Tiso N., Filippi A., Pauls S., Bortolussi M., Argenton F. BMP signalling regulates anteroposterior endoderm patterning in zebrafish. Mech. Dev. 2002, 118:29-37.
45. Trinh L.A., Stainier D.Y. Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev. Cell 2004, 6:371-382.
46. Umulis D.M., Shimmi O., O'Connor M.B., Othmer H.G. Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev. Cell 2010, 18:260-274.
47. von Bubnoff A., Peiffer D.A., Blitz I.L., Hayata T., Ogata S., Zeng Q., Trunnell M., Cho K.W. Phylogenetic footprinting and genome scanning identify vertebrate BMP response elements and new target genes. Dev. Biol. 2005, 281:210-226.
48. Wandzioch E., Zaret K.S. Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. Science 2009, 324:1707-1710.
49. Wang X., Harris R.E., Bayston L.J., Ashe H.L. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008, 455:72-77.
50. Wermter C., Höwel M., Hintze V., Bombosch B., Aufenvenne K., Yiallouros I., Stöcker W. The protease domain of procollagen C-proteinase (BMP1) lacks substrate selectivity, which is conferred by non-proteolytic domains. Biol. Chem. 2007, 388:513-521.
51. Yabe T., Shimizu T., Muraoka O., Bae Y.K., Hirata T., Nojima H., Kawakami A., Hirano T., Hibi M. Ogon/Secreted Frizzled functions as a negative feedback regulator of Bmp signaling. Development 2003, 130:2705-2716.
52. Zakin L., De Robertis E.M. Extracellular regulation of BMP signaling. Curr. Biol. 2010, 20:R89-R92.
53. Zaret K.S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat. Rev. Genet. 2008, 9:329-340.
54. Zorn A.M., Wells J.M. Vertebrate endoderm development and organ formation. Annu. Rev. Cell Dev. Biol. 2009, 25:221-251.