Growth factor-dependent branching of the ureteric bud is modulated by selective 6-O sulfation of heparan sulfate

Developmental Biology

Volumn 356, Issue 1, 2011, Pages 19-27

  Shah, Mita M ^a   Sakurai, Hiroyuki ^a,f   Gallegos, Thomas F ^a   Sweeney, Derina E ^a   Bush, Kevin T ^b   Esko, Jeffrey D ^c,d   Nigam, Sanjay K ^a,b,c,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d University of California San Diego   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Branching morphogenesis; Growth factor; Heparan sulfate; Kidney development; Ureteric bud

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; GROWTH FACTOR; HEPARAN SULFATE; HEPARIN; NEU DIFFERENTIATION FACTOR; NEURITE PROMOTING FACTOR; PLEIOTROPHIN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; GROWTH REGULATION; KIDNEY CELL CULTURE; MESENCHYME; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; RAT; SULFATION; URETERIC BUD BRANCHING;

MUS;

EID: 79959908429     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.05.004     Document Type: Article

References (55)

1. Akiyama T., Kamimura K., Firkus C., Takeo S., Shimmi O., Nakato H. Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev. Biol. 2008, 313:408-419.
2. al-Awqati Q., Goldberg M.R. Architectural patterns in branching morphogenesis in the kidney. Kidney Int. 1998, 54:1832-1842.
3. Allen B.L., Rapraeger A.C. Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J. Cell Biol. 2003, 163:637-648.
4. Barasch J., Qiao J., McWilliams G., Chen D., Oliver J.A., Herzlinger D. Ureteric bud cells secrete multiple factors, including bFGF, which rescue renal progenitors from apoptosis. Am. J. Physiol. 1997, 273:F757-F767.
5. Brenner B.M., Milford E.L. Nephron underdosing: a programmed cause of chronic renal allograft failure. Am. J. Kidney Dis. 1993, 21:66-72.
6. Brenner B.M., Garcia D.L., Anderson S. Glomeruli and blood pressure. Less of one, more the other?. Am. J. Hypertens. 1988, 1:335-347.
7. Bullock S.L., Fletcher J.M., Beddington R.S., Wilson V.A. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 1998, 12:1894-1906.
8. Bush K.T., Sakurai H., Steer D.L., Leonard M.O., Sampogna R.V., Meyer T.N., Schwesinger C., Qiao J., Nigam S.K. TGF-beta superfamily members modulate growth, branching, shaping, and patterning of the ureteric bud. Dev. Biol. 2004, 266:285-298.
9. Davies J.A., Yates E.A., Turnbull J.E. Structural determinants of heparan sulphate modulation of GDNF signalling. Growth Factors 2003, 21:109-119.
10. Deakin J.A., Blaum B.S., Gallagher J.T., Uhrin D., Lyon M. The binding properties of minimal oligosaccharides reveal a common heparan sulfate/dermatan sulfate-binding site in hepatocyte growth factor/scatter factor that can accommodate a wide variety of sulfation patterns. J. Biol. Chem. 2009, 284:6311-6321.
11. Dische Z. A new specific color reaction of hexuronic acids. J. Biol. Chem. 1947, 167:189-198.
12. Esko J.D., Lindahl U. Molecular diversity of heparan sulfate. J. Clin. Invest. 2001, 108:169-173.
13. Guimond S., Maccarana M., Olwin B.B., Lindahl U., Rapraeger A.C. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 1993, 268:23906-23914.
14. Habuchi H., Kimata K. Mice deficient in heparan sulfate 6-O-sulfotransferase-1. Prog. Mol. Biol. Transl. Sci. 2010, 93:79-111.
15. HajMohammadi S., Enjyoji K., Princivalle M., Christi P., Lech M., Beeler D., Rayburn H., Schwartz J.J., Barzegar S., de Agostini A.I., Post M.J., Rosenberg R.D., Shworak N.W. Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J. Clin. Invest. 2003, 111:989-999.
16. Han C., Belenkaya T.Y., Khodoun M., Tauchi M., Lin X. Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development 2004, 131:1563-1575.
17. Jastrebova N., Vanwildemeersch M., Rapraeger A.C., Gimenez-Gallego G., Lindahl U., Spillmann D. Heparan sulfate-related oligosaccharides in ternary complex formation with fibroblast growth factors 1 and 2 and their receptors. J. Biol. Chem. 2006, 281:26884-26892.
18. Kamimura K., Fujise M., Villa F., Izumi S., Habuchi H., Kimata K., Nakato H. Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) gene. Structure, expression, and function in the formation of the tracheal system. J. Biol. Chem. 2001, 276:17014-17021.
19. Kamimura K., Koyama T., Habuchi H., Ueda R., Masu M., Kimata K., Nakato H. Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J. Cell Biol. 2006, 174:773-778.
20. Karihaloo A., Karumanchi S.A., Barasch J., Jha V., Nickel C.H., Yang J., Grisaru S., Bush K.T., Nigam S., Rosenblum N.D., Sukhatme V.P., Cantley L.G. Endostatin regulates branching morphogenesis of renal epithelial cells and ureteric bud. Proc. Natl Acad. Sci. U. S. A. 2001, 98:12509-12514.
21. Kleinschmit A., Koyama T., Dejima K., Hayashi Y., Kamimura K., Nakato H. Drosophila heparan sulfate 6-O endosulfatase regulates Wingless morphogen gradient formation. Dev. Biol. 2010, 345:204-214.
22. Kreuger J., Spillmann D., Li J.P., Lindahl U. Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 2006, 174:323-327.
23. LaRochelle W.J., Sakaguchi K., Atabey N., Cheon H.G., Takagi Y., Kinaia T., Day R.M., Miki T., Burgess W.H., Bottaro D.P. Heparan sulfate proteoglycan modulates keratinocyte growth factor signaling through interaction with both ligand and receptor. Biochemistry 1999, 38:1765-1771.
24. Merry C.L., Bullock S.L., Swan D.C., Backen A.C., Lyon M., Beddington R.S., Wilson V.A., Gallagher J.T. The molecular phenotype of heparan sulfate in the Hs2st?/? mutant mouse. J. Biol. Chem. 2001, 276:35429-35434.
25. Meyer T.N., Schwesinger C., Bush K.T., Stuart R.O., Rose D.W., Shah M.M., Vaughn D.A., Steer D.L., Nigam S.K. Spatiotemporal regulation of morphogenetic molecules during in vitro branching of the isolated ureteric bud: toward a model of branching through budding in the developing kidney. Dev. Biol. 2004, 275:44-67.
26. Meyer T.N., Schwesinger C., Sampogna R.V., Vaughn D.A., Stuart R.O., Steer D.L., Bush K.T., Nigam S.K. Rho kinase acts at separate steps in ureteric bud and metanephric mesenchyme morphogenesis during kidney development. Differentiation 2006, 74:638-647.
27. Nakato H., Kimata K. Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim. Biophys. Acta 2002, 1573:312-318.
28. Nigam S.K. Determinants of branching tubulogenesis. Curr. Opin. Nephrol. Hypertens. 1995, 4:209-214.
29. Nigam S.K., Shah M.M. How does the ureteric bud branch?. J. Am. Soc. Nephrol. 2009, 20:1465-1469.
30. Ostrovsky O., Berman B., Gallagher J., Mulloy B., Fernig D.G., Delehedde M., Ron D. Differential effects of heparin saccharides on the formation of specific fibroblast growth factor (FGF) and FGF receptor complexes. J. Biol. Chem. 2002, 277:2444-2453.
31. Pan Y., Woodbury A., Esko J.D., Grobe K., Zhang X. Heparan sulfate biosynthetic gene Ndst1 is required for FGF signaling in early lens development. Development 2006, 133:4933-4944.
32. Pan Y., Carbe C., Powers A., Zhang E.E., Esko J.D., Grobe K., Feng G.S., Zhang X. Bud specific N-sulfation of heparan sulfate regulates Shp2-dependent FGF signaling during lacrimal gland induction. Development 2008, 135:301-310.
33. Patel V.N., Knox S.M., Likar K.M., Lathrop C.A., Hossain R., Eftekhari S., Whitelock J.M., Elkin M., Vlodavsky I., Hoffman M.P. Heparanase cleavage of perlecan heparan sulfate modulates FGF10 activity during ex vivo submandibular gland branching morphogenesis. Development 2007, 134:4177-4186.
34. Patel V.N., Likar K.M., Zisman-Rozen S., Cowherd S.N., Lassiter K.S., Sher I., Yates E.A., Turnbull J.E., Ron D., Hoffman M.P. Specific heparan sulfate structures modulate FGF10-mediated submandibular gland epithelial morphogenesis and differentiation. J. Biol. Chem. 2008, 283:9308-9317.
35. Poladia D.P., Kish K., Kutay B., Hains D., Kegg H., Zhao H., Bates C.M. Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev. Biol. 2006, 291:325-339.
36. Qiao J., Sakurai H., Nigam S.K. Branching morphogenesis independent of mesenchymal-epithelial contact in the developing kidney. Proc. Natl Acad. Sci. U. S. A. 1999, 96:7330-7335.
37. Qiao J., Uzzo R., Obara-Ishihara T., Degenstein L., Fuchs E., Herzlinger D. FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 1999, 126:547-554.
38. Qiao J., Bush K.T., Steer D.L., Stuart R.O., Sakurai H., Wachsman W., Nigam S.K. Multiple fibroblast growth factors support growth of the ureteric bud but have different effects on branching morphogenesis. Mech. Dev. 2001, 109:123-135.
39. Qu X., Carbe C., Tao C., Powers A., Lawrence R., van Kuppevelt T.H., Cardoso W.V., Grobe K., Esko J.D., Zhang X. Lacrimal gland development and Fgf10-Fgfr2b signaling are controlled by 2-O- and 6-O-sulfated heparan sulfate. J. Biol. Chem. 2011, 286:14435-14444.
40. Reich-Slotky R., Bonneh-Barkay D., Shaoul E., Bluma B., Svahn C.M., Ron D. Differential effect of cell-associated heparan sulfates on the binding of keratinocyte growth factor (KGF) and acidic fibroblast growth factor to the KGF receptor. J. Biol. Chem. 1994, 269:32279-32285.
41. Sakurai H., Tsukamoto T., Kjelsberg C.A., Cantley L.G., Nigam S.K. EGF receptor ligands are a large fraction of in vitro branching morphogens secreted by embryonic kidney. Am. J. Physiol. 1997, 273:F463-F472.
42. Sakurai H., Bush K.T., Nigam S.K. Identification of pleiotrophin as a mesenchymal factor involved in ureteric bud branching morphogenesis. Development 2001, 128:3283-3293.
43. Sakurai H., Bush K.T., Nigam S.K. Heregulin induces glial cell line-derived neurotrophic growth factor-independent, non-branching growth and differentiation of ureteric bud epithelia. J. Biol. Chem. 2005, 280:42181-42187.
44. Sampogna R.V., Nigam S.K. Implications of gene networks for understanding resilience and vulnerability in the kidney branching program. Physiology (Bethesda) 2004, 19:339-347.
45. Santos O.F., Moura L.A., Rosen E.M., Nigam S.K. Modulation of HGF-induced tubulogenesis and branching by multiple phosphorylation mechanisms. Dev. Biol. 1993, 159:535-548.
46. Shah M.M., Sampogna R.V., Sakurai H., Bush K.T., Nigam S.K. Branching morphogenesis and kidney disease. Development 2004, 131:1449-1462.
47. Shah M.M., Tee J.B., Meyer T., Meyer-Schwesinger C., Choi Y., Sweeney D.E., Gallegos T.F., Johkura K., Rosines E., Kouznetsova V., Rose D.W., Bush K.T., Sakurai H., Nigam S.K. The instructive role of metanephric mesenchyme in ureteric bud patterning, sculpting, and maturation and its potential ability to buffer ureteric bud branching defects. Am. J. Physiol. Renal Physiol. 2009, 297:F1330-F1341.
48. Shah M.M., Sakurai H., Sweeney D.E., Gallegos T.F., Bush K.T., Esko J.D., Nigam S.K. Hs2st mediated kidney mesenchyme induction regulates early ureteric bud branching. Dev. Biol. 2010, 339:354-365.
49. Steer D.L., Shah M.M., Bush K.T., Stuart R.O., Sampogna R.V., Meyer T.N., Schwesinger C., Bai X., Esko J.D., Nigam S.K. Regulation of ureteric bud branching morphogenesis by sulfated proteoglycans in the developing kidney. Dev. Biol. 2004, 272:310-327.
50. Sugaya N., Habuchi H., Nagai N., Ashikari-Hada S., Kimata K. 6-O-sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J. Biol. Chem. 2008, 283:10366-10376.
51. Takei Y., Ozawa Y., Sato M., Watanabe A., Tabata T. Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 2004, 131:73-82.
52. Thompson S.M., Jesudason E.C., Turnbull J.E., Fernig D.G. Heparan sulfate in lung morphogenesis: the elephant in the room. Birth Defects Res. C Embryo Today 2010, 90:32-44.
53. Wilson V.A., Gallagher J.T., Merry C.L. Heparan sulfate 2-O-sulfotransferase (Hs2st) and mouse development. Glycoconj. J. 2002, 19:347-354.
54. Zent R., Bush K.T., Pohl M.L., Quaranta V., Koshikawa N., Wang Z., Kreidberg J.A., Sakurai H., Stuart R.O., Nigam S.K. Involvement of laminin binding integrins and laminin-5 in branching morphogenesis of the ureteric bud during kidney development. Dev. Biol. 2001, 238:289-302.
55. Zhao H., Kegg H., Grady S., Truong H.T., Robinson M.L., Baum M., Bates C.M. Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev. Biol. 2004, 276:403-415.