Sea urchin arylsulfatase, an extracellular matrix component, is involved in gastrulation during embryogenesis

Development Genes and Evolution

Volumn 219, Issue 6, 2009, Pages 281-288

  Mitsunaga Nakatsubo, Keiko ^a   Akimoto, Yoshihiro ^b   Kawakami, Hayato ^b   Akasaka, Koji ^c  

^a HIROSHIMA UNIVERSITY   (Japan)

^b KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Arylsulfatase; Extracellular matrix; Gastrulation; Heparin binding; Sea urchin

Indexed keywords

3 AMINOPROPIONITRILE; ARYLSULFATASE; CALCIUM ION; HEPARIN; POLYSACCHARIDE SULFATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME RELEASE; ENZYME REPRESSION; ENZYME SYNTHESIS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GASTRULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; SEA URCHIN;

AMINOPROPIONITRILE; ANIMALS; ARYLSULFATASES; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; EXTRACELLULAR MATRIX; FUCOSE; GASTRULATION; HEPARIN; PROTEIN-LYSINE 6-OXIDASE; SEA URCHINS;

ARSES; ECHINOIDEA; HEMICENTROTUS;

EID: 67650578621     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-009-0289-5     Document Type: Article

References (43)

1. Adelson DL, Humphreys T (1988) Sea urchin morphogenesis and cell-hyalin adhesion are perturbed by a monoclonal antibody specific for hyalin. Development 104:391-402
2. Akasaka K, Terayama H (1983) Sulfated glycan present in the EDTA extract of Hemicentrotus embryos (mid-gastrula). Exp Cell Res 146:177-185
3. Akasaka K, Terayama H (1984) A proteoglycan fraction isolated from the EDTA extract of sea urchin (Hemicentrotus pulcherrimus) gastrulae stimulates reaggregation of dissociated embryonic cells. Exp Cell Res 150:226-233
4. Akasaka K, Akimoto Y, Sato M, Hirano H, Shimada H (1990) Histochemical detection of arylsulfatase activity in sea urchin embryos. Dev Growth Differ 32:293-298
5. Akasaka K, Uemoto H, Wilt F, Mitsunaga-Nakatsubo K, Shimada H (1997) Oral-aboral ectoderm differentiation of sea urchin embryos is disrupted in response to calcium ionophore. Dev Growth Differ 39:373-379
6. Alliegro MC, Ettensohn CA, Burdsal CA, Erickson HP, McClay DR (1988) Echinonectin: A new embryonic substrate adhesion protein. J Cell Biol 107:2319-2327
7. Benson S, Rawson R, Killian C, Wilt F (1991) Role of the extracellular matrix in tissue-specific gene expression in the sea urchin embryo. Mol Reprod Dev 29:220-226
8. Bisgrove BW, Raff RA (1993) The SpEGF III gene encodes a member of the fibropellins: EGF repeat-containing proteins that form the apical lamina of the sea urchin embryo. Dev Biol 157:526-538
9. Burke RD, Myers RL, Sexton TL, Jackson C (1991) Cell movements during the initial phase of gastrulation in the sea urchin embryo. Dev Biol 146:542-557
10. Butler E, Hardin J, Benson S (1987) The role of lysyl oxidase and collagen crosslinking during sea urchin development. Exp Cell Res 173:174-182
11. Coffman JA, McClay DR (1990) A hyaline layer protein that becomes localized to the oral ectoderm and foregut of sea urchin embryos. Dev Biol 140:93-104
12. Csiszar K (2001) Lysyl oxidases: A novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1-32
13. Davidson LA, Koehl MAR, Keller R, Oster GF (1995) How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination. Development 121:2005-2018
14. Davidson LA, Oster GF, Keller RE, Koehl MA (1999) Measurements of mechanical properties of the blastula wall reveal which hypothesized mechanisms of primary invagination are physically plausible in the sea urchin Strongylocentrotus purpuratus. Dev Biol 209:221-238
15. Delehedde M, Lyon M, Sergeant N, Rahmoune H, Fernig DG (2001) Proteoglycans: Pericellular and cell surface multireceptors that integrate external stimuli in the mammary gland. J Mammary Gland Biol Neoplasia 6:253-273
16. Ettensohn CA (1985) Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev Biol 112:383-390
17. Ettensohn CA (1999) Cell movements in the sea urchin embryo. Curr Opin Genet Dev 9:461-465
18. Evers M, Saftig P, Schmidt P, Hafner A, McLoghlin DB, Schmahl W, Hess B, von Figura K, Peters C (1996) Targeted disruption of the arylsulfatase B gene results in mice resembling the phenotype of mucopolysaccharidosis VI. Proc Natl Acad Sci U S A 93:8214-8219
19. Fuchikami T, Mitsunaga-Nakatsubo K, Amemiya S, Hosomi T, Watanabe T, Kurokawa D, Kataoka M, Harada Y, Satoh N, Kusunoki S, Takata K, Shimotori T, Yamamoto T, Sakamoto N, Shimada H, Akasaka K (2002) T-brain homologue (HpTb) is involved in the archenteron induction signals of micromere descendant cells in the sea urchin embryo. Development 129:5205-5216
20. Ghosh D (2007) Human sulfatases: A structural perspective to catalysis. Cell Mol Life Sci 64:2013-2022
21. Hanson SR, Best MD, Wong CH (2004) Sulfatases: Structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed Engl 43:5736-5763
22. Hibino T, Harada Y, Minokawa T, Nonaka M, Amemiya S (2004) Molecular heterotopy in the expression of Brachyury orthologs in order Clypeasteroida (irregular sea urchins) and order Echinoida (regular sea urchins). Dev Genes Evol 214:546-558
23. Kagan HM, Li W (2003) Lysyl oxidase: Properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 88:660-672
24. Kominami T, Takata H (2000) Cellular basis of gastrulation in the sand dollar Scaphechinus mirabilis. Biol Bull 199:287-297
25. Kominami T, Takata H (2004) Gastrulation in the sea urchin embryo: A model system for analyzing the morphogenesis of a monolayered epithelium. Dev Growth Differ 46:309-326
26. McClay DR, Gross JM, Range R, Peterson RE, Bradham C (2004) Sea urchin gastrulation. In: SterF CD (ed) Gastrulation: from cells to embryo. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 123-137
27. Mehl E, Jatzkewitz H (1968) Cerebroside 3-sulfate as a physiological substrate of arylsulfatase A. Biochim Biophys Acta 151:619-627
28. Miller DJ, Macek MB, Shur BD (1992) Complementarity between sperm surface β-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589-593
29. Mitsunaga-Nakatsubo K, Akasaka K, Akimoto Y, Akiba E, Kitajima T, Tomita M, Hirano H, Shimada H (1998) Arylsulfatase exists as non-enzymatic cell surface protein in sea urchin embryos. J Exp Zool 280:220-230
30. Parenti G, Meroni G, Ballabio A (1997) The sulfatase gene family. Curr Opin Genet Dev Cell 7:386-391
31. Pinnell SR, Martin GR (1968) The cross-linking of collagen and elastin: enzymatic conversion of lysine in peptide linkage to alpha-aminoadipic-delta-semialdehyde (allysine) by an extract from bone. Proc Natl Acad Sci U S A 61:708-716
32. Rapraeger AC, Epel D (1981) The appearance of an extracellular arylsulfatase during morphogenesis of the sea urchin Strongylocentrotus purpuratus. Dev Biol 88:269-278
33. Sasaki H, Akasaka K, Shimada H, Shiroya T (1987) Purification and characterization of arylsulfatase from sea urchin embryo. Comp Biochem Biophys 88B:147-152
34. Sasaki H, Yamada K, Akasaka K, Kawasaki H, Suzuki K, Saito A, Sato M, Shimada H (1988) cDNA cloning, nucleotide sequence and expression of the gene for arylsulfatase in the sea urchin (Hemicentrotus pulcherrimus) embryo. Eur J Biochem 177:9-13
35. Scott JE, Orford CR (1981) Dermatan sulphate-rich proteoglycan associates with rat tail-tendon collagen at the d band in the gap region. Biochem J 197:213-216
36. Spiegel E, Spiegel M (1979) The hyaline layer is a collagen-containing extracellular matrix in sea urchin embryos and reaggregating cells. Exp Cell Res 123:434-441
37. Takata H, Kominami T (2001) Ectoderm exerts the driving force for gastrulation in the sand dollar Scaphechinus mirabilis. Dev Growth Differ 43:265-274
38. Tang SS, Trackman PC, Kagan HM (1983) Reaction of aortic lysyl oxidase with β-aminopropionitrile. J Biol Chem 258:4331-4338
39. Wessel GM, McClay DR (1987) Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix. Dev Biol 121:149-165
40. Wessel GM, Wikramanayake A (1999) How to grow a gut: Ontogeny of the endoderm in the sea urchin embryo. Bioessays 21:459-471
41. Wessel GM, Zhang W, Tomlinson CR, Lennarz WJ, Klein WH (1989) Transcription of the Spec 1-like gene of Lytechinus is selectively inhibited in response to disruption of the extracellular matrix. Development 106:355-365
42. Wessel GM, Berg L, Adelson DL, Cannon G, McClay DR (1998) A molecular analysis of hyalin-a substrate for cell adhesion in the hyaline layer of the sea urchin embryo. Dev Biol 193:115-126
43. Yogalingam G, Litjens T, Bielicki J, Crawley AC, Muller V, Anson DS, Hopwood JJ (1996) Feline mucopolysaccharidosis type VI. Characterization of recombinant N-acetylgalactosamine 4-sulfatase and identification of a mutation causing the disease. J Biol Chem 271:27259-27265