Role of heparan sulfate in dextral heart looping in chick

Glycobiology

Volumn 14, Issue 8, 2004, Pages 745-755

  Yue, Xinping ^a,b,c   Schultheiss, Thomas M ^b   McKenzie, Edward A ^d   Rosenberg, Robert D ^b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

6 O sulfation; Chick; Heart looping; Heparan sulfate; Heparanase

Indexed keywords

BETA GLUCURONIDASE; CHONDROITIN SULFATE; DISACCHARIDE; GLUCOSAMINE; HEPARAN SULFATE; HEPARANASE; HEPARIN DERIVATIVE;

ANIMAL TISSUE; ARTICLE; CARBOHYDRATE ANALYSIS; CHICK EMBRYO; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO CULTURE; ENZYME DEGRADATION; HEART DEVELOPMENT; MICROINJECTION; NONHUMAN; PERICARDIUM; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; SULFATION;

ANIMALS; CHICK EMBRYO; CHONDROITIN SULFATES; FIBRONECTINS; GLUCURONIDASE; HEART; HEPARIN; HEPARITIN SULFATE; MICROINJECTIONS; MYOCARDIUM;

EID: 4444281973     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwh083     Document Type: Article

References (55)

1. Allen, B.L. and Rapraeger, A.C. (2003) Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J. Cell Biol., 163, 637-648.
2. Alsan, B.H. and Schultheiss, T.M. (2002) Regulation of avian cardiogenesis by Fgf8 signaling. Development, 129, 1935-1943.
3. Bai, X., Bame, K.J., Habuchi, H., Kimata, K., and Esko, J.D. (1997) Turnover of heparan sulfate depends on 2-O-sulfation of uronic acids. J. Biol. Chem., 272, 23172-23179.
4. Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem., 68, 729-777.
5. Boettger, T., Wittler, L., and Kessel, M. (1999) FGF8 functions in the specification of the right body side of the chick. Curr. Biol., 9, 277-280.
6. Brickman, Y.G., Ford, M.D., Gallagher, J.T., Nurcombe, V., Bartlett, P.P. and Turnbull, J.E. (1998) Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem., 273, 4350-4359.
7. Bullock, S.L., Fletcher, J.M., Beddington, R.S., and Wilson, V.A (1998) Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev., 12, 1894-1906.
8. Capdevila, J., Vogan, K.J., Tabin, C.J., and Izpisua Belmonte, J.C. (2000) Mechanisms of left-right determination in vertebrates. Cell, 101, 9-21.
9. David, G., Bai, X.M., Van der Schueren, B., Cassiman, J.J., and Van den Berghe, H. (1992) Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol., 119, 961-975.
10. Elkin, M., Ilan, N., Ishai-Michaeli, R., Friedmann, Y., Papo, O., Pecker, I., and Vlodavsky, I. (2001) Heparanase as mediator of angiogenesis: mode of action. FASEB J., 15, 1661-1663.
11. Esko, J.D. and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest., 108, 169-173.
12. Fairbanks, M.B., Mildner, A.M., Leone, J.W., Cavey, G.S., Mathews, W.R., Drong, R.F., Slightom, J.L., Bienkowski, M.J., Smith, C.W., Bannow, C.A., and others. (1999) Processing of the human heparanase precursor and evidence that the active enzyme is a heterodimer. J. Biol. Chem., 274, 29587-29590.
13. Forsberg, E. and Kjellen, L. (2001) Heparan sulfate: lessons from knockout mice. J. Clin. Invest., 108, 175-180.
14. Freeman, C. and Parish, C.R. (1998) Human platelet heparanase: purification, characterization and catalytic activity. Biochem. J., 330(pt 3), 1341-1350.
15. Garcia-Martinez, V. and Schoenwolf, G.C. (1993) Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol., 159, 706-719.
16. George, E., Georges-Labouesse, E., Patel-King, R., Rayburn, H., and Hynes, R. (1993) Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development, 119, 1079-1091.
17. Goldshmidt, O., Zcharia, E., Cohen, M., Aingorn, H., Cohen, I., Nadav, L., Katz, B.Z., Geiger, B., and Vlodavsky, I. (2003) Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J., 17, 1015-1025.
18. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002) Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet., 3, 103-113.
19. Hamburger, V. and Hamilton, H.L. (1951) A series of normal stages in the development of the chick embryo. J. Morph., 88, 49-92.
20. Hoyle, C., Brown, N., and Wolpert, L. (1992) Development of left/right handedness in the chick heart. Development, 115, 1071-1078.
21. Hulett, M.D., Freeman, C., Hamdorf, B.J., Baker, R.T., Harris, M.J. and Parish, C.R. (1999) Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat. Med., 5, 803-809.
22. Hulett, M.D., Hornby, J.R., Ohms, S.J., Zuegg, J., Freeman, C., Gready, J.E. and Parish, C.R. (2000) Identification of active-site residues of the pro-metastatic endoglycosidase heparanase. Biochemistry, 39, 15659-15667.
23. Kamimura, K., Fujise, M., Villa, F., Izumi, S., Habuchi, H., Kimata, K., and Nakato, H. (2001) Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) gene. Structure, expression, and function in the formation of the tracheal system. J. Biol. Chem., 276, 17014-17021.
24. Kato, M., Wang, H., Kainulainen, V., Fitzgerald, M.L., Ledbetter, S., Ornitz, D.M., and Bernfield, M. (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat. Med., 4, 691-697.
25. Kjellen, L. (2003) Glucosaminyl N-deacetylase/N-sulphotransferases in heparan sulphate biosynthesis and biology. Biochem. Soc. Trans., 31, 340-342.
26. Kramer, K.L., Barnette, J.E., and Yost, H.J. (2002) PKCgamma regulates syndecan-2 inside-out signaling during xenopus left-right development. Cell, 111, 981-990.
27. Kramer, K.L. and Yost, H.J. (2002) Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell, 2, 115-124.
28. Kuberan, B., Lech, M., Zhang, L., Wu, Z.L., Beeler, D.L., and Rosenberg, R.D. (2002) Analysis of heparan sulfate oligosaccharides with ion pair-reverse phase capillary high performance liquid chromatography-microelectrospray ionization time-of-flight mass spectrometry. J. Am. Chem. Soc., 124, 8707-8718.
29. Kuberan, B., Lech, M.Z., Beeler, D.L., Wu, Z.L., and Rosenberg, R.D. (2003) Enzymatic synthesis of antithrombin III-binding heparan sulfate pentasaccharide. Nat. Biotechnol., 21, 1343-1346.
30. Kussie, P.H., Hulmes, J.D., Ludwig, D.L., Patel, S., Navarro, E.C., Seddon, A.P., Giorgio, N.A., and Bohlen, P. (1999) Cloning and functional expression of a human heparanase gene. Biochem. Biophys. Res. Commun., 261, 183-187.
31. Levin, M., Johnson, R.L., Stern, C. D., Kuehn, M., and Tabin, C. (1995) A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell, 82, 803-814.
32. Linask, K.K. and Lash, J.W. (1986) Precardiac cell migration: fibronectin localization at mesoderm-endoderm interface during directional movement. Dev. Biol., 114, 87-101.
33. Linask, K.K. and Lash, J.W. (1988a) A role for fibronectin in the migration of avian precardiac cells. I. Dose-dependent effects of fibronectin antibody. Dev. Biol., 129, 315-323.
34. Linask, K.K. and Lash, J.W. (1988b) A role for fibronectin in the migration of avian precardiac cells. II. Rotation of the heart-forming region during different stages and its effects. Dev. Biol., 129, 324-329.
35. McKenzie, E., Young, K., Hircock, M., Bennett, J., Bhaman, M., Felix, R., Turner, P., Stamps, A., McMillan, D., Saville, G., and others. (2003) Biochemical characterization of the active heterodimer form of human heparanase (Hpa1) protein expressed in insect cells. Biochem. J., 373, 423-435.
36. Mercola, M. and Levin, M. (2001) Left-right asymmetry determination in vertebrates. Annu. Rev. Cell Dev. Biol., 17, 779-805.
37. Nurcombe, V., Ford, M.D., Wildschut, J.A., and Bartlett, P.F. (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science, 260, 103-106.
38. Okada, Y., Yamada, S., Toyoshima, M., Dong, J., Nakajima, M., and Sugahara, K. (2002) Structural recognition by recombinant human heparanase that plays critical roles in tumor metastasis. Hierarchical sulfate groups with different effects and the essential target disulfated trisaccharide sequence. J. Biol. Chem., 277, 42488-42495.
39. Perrimon, N. and Bernfield, M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature, 404, 725-728.
40. Pikas, D.S., Li, J.-P., Vlodavsky, I., and Lindahl, U. (1998) Substrate specificity of heparanases from human hepatoma and platelets. J. Biol. Chem., 273, 18770-18777.
41. Rapraeger, A.C. (2002) Heparan sulfate-growth factor interactions. Methods Cell Biol., 69, 83-109.
42. Rosenberg, R.D., Shworak, N.W., Liu, J., Schwartz, J.J. and Zhang, L. (1997) Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J. Clin. Invest., 100, S67-S75.
43. Salazar del Rio, J. (1974) Influence of extrinsic factors on the development of the bulboventricular loop of the chick embryo. J. Embryol. Exp. Morphol., 31, 199-206.
44. Schultheiss, T.M. and Lassar, A.B. (1997) Induction of chick cardiac myogenesis by bone morphogenetic proteins. Cold Spring Harb. Symp. Quant. Biol., 62, 413-419.
45. Schultheiss, T.M., Xydas, S., and Lassar, A.B. (1995) Induction of avian cardiac myogenesis by anterior endoderm. Development, 121, 4203-4214.
46. St Amand, T.R., Ra, J., Zhang, Y., Hu, Y., Baber, S.I., Qiu, M., and Chen, Y. (1998) Cloning and expression pattern of chicken Pitx2: a new component in the SHH signaling pathway controlling embryonic heart looping. Biochem. Biophys. Res. Commun., 247, 100-105.
47. Stalsberg, H. and DeHaan, R.L. (1969) The precardiac areas and formation of the tubular heart in the chick embryo. Dev. Biol., 19, 128-159.
48. Toyoshima, M. and Nakajima, M. (1999) Human heparanase. Purification, characterization, cloning, and expression. J. Biol. Chem., 274, 24153-24160.
49. Vlodavsky, I. and Friedmann, Y. (2001) Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J. Clin. Invest., 108, 341-347.
50. Vlodavsky, I., Friedmann, Y., Elkin, M., Aingorn, H., Atzmon, R., Ishai-Michaeli, R., Bitan, M., Pappo, O., Peretz, T., Michal, I., and others. (1999) Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat. Med., 5, 793-802.
51. Walz, A., McFarlane, S., Brickman, Y.G., Nurcombe, V., Bartlett, P.F., and Holt, C.E. (1997) Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development, 124, 2421-2430.
52. Wu, Z.L., Zhang, L., Yabe, T., Kuberan, B., Beeler, D.L., Love, A. and Rosenberg, R.D. (2003) The Involvement of heparan sulfate (HS) in FGF1/HS/FGFR1 signaling complex. J. Biol. Chem., 278, 17121-17129.
53. Yost, H.J. (1990) Inhibition of proteoglycan synthesis eliminates left-right asymmetry in Xenopus laevis cardiac looping. Development, 110, 865-874.
54. Yost, H.J. (1992) Regulation of vertebrate left-right asymmetries by extracellular matrix. Nature, 357, 158-161.
55. Zhang, L., Beeler, D.L., Lawrence, R., Lech, M., Liu, J., Davis, J.C., Shriver, Z., Sasisekharan, R. and Rosenberg, R.D. (2001) 6-O-sulfotransferase-1 represents a critical enzyme in the anticoagulant heparan sulfate biosynthetic pathway. J. Biol. Chem., 276, 42311-42321.