Thrombospondins in early Xenopus embryos: Dynamic patterns of expression suggest diverse roles in nervous system, notochord, and muscle development

Developmental Dynamics

Volumn 211, Issue 4, 1998, Pages 390-407

  Urry, Lisa A ^a   Whittaker, Charles A ^b   Duquette, Mark ^c   Lawler, Jack ^c   DeSimone, Douglas W ^b,d  

^a MILLS COLLEGE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Expression; Thrombospondin; Xenopus embryo

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; SCLEROPROTEIN; THROMBOSPONDIN 1; THROMBOSPONDIN 3; THROMBOSPONDIN 4; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPENDYMA; EPIDERMIS; GASTRULATION; GENE EXPRESSION; MOLECULAR CLONING; MUSCLE DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEUROEPITHELIUM; NEUROMERE; NONHUMAN; NOTOCHORD; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SOMITE; TADPOLE; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; MUSCLES; NERVOUS SYSTEM; NOTOCHORD; THROMBOSPONDINS; TIME FACTORS; TISSUE DISTRIBUTION; XENOPUS LAEVIS;

EID: 0031900176     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199804)211:4<390::AID-AJA10>3.0.CO;2-8     Document Type: Article

References (105)

1. Adams JC, Lawler J. Diverse mechanisms for cell attachment to platelet thrombospondin. J. Cell Sci. 1993a;104:1061-1071.
2. Adams JC, Lawler J. The thrombospondin family. Curr. Biol. 1993b; 3:188-190.
3. Adams JC, Lawler J. Cell-type specific adhesive interactions of skeletal myoblasts with thrombospondin-1. Mol. Biol. Cell. 1994; 5:423-437.
4. Adams JC, Tucker RP, Lawler J. The thrombospondin gene family. Austin: R.G. Landes Company, 1995.
5. v, subunit is expressed on mesodermal cell surfaces during amphibian gastrulation. Dev. Biol. 1995;70:249-261.
6. Arber S, Caroni P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neunte outgrowth. J. Cell Biol. 1995;131:1083-1094.
7. Asch AS, Barnwell J, Silverstein RL, Nachman RL. Isolation of the thrombospondin membrane receptor. J. Clin. Invest. 1987;79:1054-1061.
8. Asch AS, Silbiger S, Heimer E, Nachman RL. Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem. Biophys. Res. Commun. 1992;182:1208-1217.
9. Bieker JJ, Yazdani-Buicky M. Distribution of type II collagen mRNA in Xenopus embryos visualized by whole-mount in situ hybridization. J. Histochem. Cytochem. 1992;40:1117-1120.
10. Bornstein P, O'Rourke K, Wikstrom K, Wolf FW, Katz R, Li P, Dixit VM. A second, expressed thrombospondin gene (Thbs2) exists in the mouse genome. J. Biol. Chem. 1991;266:12821-12824.
11. Bornstein P. Thrombospondins: Structure and regulation of expression. Faseb J. 1992;6:3290-3299.
12. Bornstein P. Diversity of function is inherent in matricellular proteins: An appraisal of thrombospondin 1. J. Cell Biol. 1995;130:503-506.
13. Bradley LC, Snape A, Bhatt S, Wilkinson DG. The structure and expression of the Xenopus Krox-20 gene: Conserved and divergent patterns of expression in rhombomeres and neural crest. Mech. Dev. 1993;40:73-84.
14. Brown E, Hooper L, Ho T, Gresham H. Integrin-associated protein: A 50-kD plasma membrane antigen physically and functionally associated with integrins. J. Cell Biol. 1990;111:2785-2794.
15. Corless CL, Mendoza A, Collins T, Lawler J. Colocalization of thrombospondin and syndecan during murine development. Dev. Dyn. 1992;193:346-358.
16. 1 as a neuronal thrombospondin receptor mediating neurite outgrowth. Neuron 1995;15:333-343.
17. Frank D, Harland RM. Localized expression of a Xenopus POU gene depends on cell-autonomous transcriptional activation and induction-dependent inactivation. Development 1992;115:439-448.
18. Gao AG, Lindberg FP, Finn MB, Blystone SD, Brown EJ, Frazier WA. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J. Biol. Chem. 1996;271:21-24.
19. 1-integrin associated α-chain is differentially expressed during Xenopus embryogenesis. Development. 1994;47:199-211.
20. Gobron S, Monnerie H, Meiniel R, Creveaux I, Lehmann W, Lamalle D, Dastaque B, Meiniel A. SCO-spondin: A new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. J. Cell Sci. 1996;109:1053-1061.
21. Gurdon JB. Methods for nuclear transplantation in amphibia. Meth. Cell Biol. 1977;16:125-139.
22. Guthrie S, Lumsden A. Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 1991;112: 221-229.
23. Guthrie S, Prince V, Lumsden A. Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. Development 1993; 118:527-538.
24. Guthrie S. The status of the neural segment. Trends Neurosci. 1995;18:74-79.
25. Hamilton L. The formation of somites in Xenopus. J. Emb. Exp. Morphol. 1969;22:253-264.
26. Hantai D, Rao JS, Reddy BR, Festoff BW. Developmental appearance of thrombospondin in neonatal mouse skeletal muscle. Eur. J. Cell Biol. 1991;55:286-294.
27. Hedbom E, Antonsson P, Hjerpe A, Aeschlimann D, Paulsson M, Rosa-Pimentel E, Sommarin Y, Wendel M, Oldberg A, Heinegard D. Cartilage matrix proteins. An acidic oligomeric protein (COMP) detected only in cartilage. J. Biol. Chem. 1992;267:6132-6136.
28. Hemmati-Brivanlou A, Harland R. Expression of an engrailed-related protein is induced in the anterior neural ectoderm of early Xenopus embryos. Development 1989;106:611-617.
29. Hemmati-Brivanlou A, Frank D, Bolce ME, Brown BD, Sive HL, Harland RM. Localization of specific mRNAs in Xenopus embryos by whole-mount in situ hybridization. Development 1990;110:325-330.
30. Hemmati-Brivanlou A, Mann RW, Harland RM. A protein expressed in the growth cones of embryonic vertebrate neurons defines a new class of intermediate filament protein. Neuron 1992;9:417-428.
31. Hogg PJ, Stenflo J, Mosher DF. Thrombospondin is a slow tight-binding inhibitor of plasmin. Biochemistry 1992;31:265-269.
32. Hogg PJ, Owensby DA, Chesterman CN. Thrombospondin 1 is a tight-binding competitive inhibitor of neutrophil cathepsin G. Determination of the kinetic mechanism of inhibition and localization of cathepsin G binding to the thrombospondin 1 type 3 repeats. J. Biol. Chem. 1993;268:21811-21818.
33. Iruela-Arispe ML, Liska DJ, Sage EH, Bornstein P. Differential expression of thrombospondin 1, 2, and 3 during muring development. Dev. Dyn. 1993;197:40-56.
34. 5 during early development of Xenopus laevis. Mech. Dev. 1995;50:187-199.
35. Karczewski J, Knudsen KA, Smith L, Murphy A, Rothman VL, Tuszynski GP. The interaction of thrombospondin with platelet glycoprotein GPIIb-IIIa. J. Biol. Chem. 1989;264:21322-21326.
36. Kenney MC, Carlson E. Ultrastructural identification of collagen and glycosaminoglycans in notochordal extracellular matrix in vivo and in vitro. Anat. Rec. 1978;190:827-850.
37. Kieffer N, Nurden AT, Hasitz M, Titeux M, Breton-Gorius J. Identification of platelet membrane thrombospondin binding molecules using an anti-thrombospondin antibody. Biochim. Biophys. Acta. 1988;967: 408-415.
38. Klar A, Baldassare M, Jessell TM. F-spondin: A gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neunte extension. Cell 1992;69:95-110.
39. Krieg PA, Varnum SM, Wormington WM, Melton DA. The mRNA encoding elongation factor 1-α (EF-Iα) is a major transcript at the midblastula transition in Xenopus. Dev. Biol. 1989;133:93-100.
40. Laherty CD, O'Rourke K, Wolf FW, Katz R, Seldin MF, Dixit VM. Characterization of mouse thrombospondin 2 sequence and expression during cell growth and development. J. Biol. Chem. 1992;267: 3274-3281.
41. Lawler J, Derick LH, Connolly JE, Chen JH, Chao FC. The structure of human platelet thrombospondin. J. Biol. Chem. 1985;260:3762-3772.
42. Lawler J, Connolly JE, Ferro P, Derick LH. Thrombin and chymotrypsin interactions with thrombospondin. Ann. NY Acad. Sci. 1986;485: 273-287.
43. Lawler J, Hynes RO. The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J. Cell Biol. 1986;103: 1635-1648.
44. Lawler J, Weinstein R, Hynes RO. Cell attachment to thrombospondin: the role of ARG-GLY-ASP, calcium, and integrin receptors. J. Cell Biol. 1988;107:2351-2361.
45. Lawler J, Duquette M, Ferro P. Cloning and sequencing of chicken thrombospondin. J. Biol. Chem. 1991;266:8039-8043.
46. Lawler J, Ferro P, Duquette M. Expression and mutagenesis of thrombospondin. Biochemistry 1992;31:1173-1180.
47. Lawler J, Duquette M, Urry L, McHenry K, Smith TF. The evolution of the thrombospondin gene family. J. Mol. Evol. 1993a;36:509-516.
48. Lawler J, Duquette M, Whittaker CA, Adams JC, McHenry K, DeSimone DW. Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J. Cell Biol. 1993b;120:1059-1067.
49. Lemaire P, Gurdon JB. A role for cytoplasmic determinants in mesoderm patterning: cell-autonomous activation of the goosecoid and Xwnt-8 genes along the dorsoventral axis of early Xenopus embryos. Development 1994;120:1191-1199.
50. Leung-Hagesteijn C, Spence AM, Stern BD, Zhou Y, Su MW, Hedgecock EM, Culotti JG. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 1992;71:289-299.
51. Li WX, Howard RJ, Leung LLK. Identification of a SVTCG in thrombospondin as the conformation-dependent, high affinity binding site for its receptor, CD36. J. Biol. Chem. 1993;268:16179-16184.
52. Lumsden A. The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 1990;13:329-335.
53. Lumsden A, Keynes R. Segmental patterns of neuronal development in the chick hindbrain. Nature 1989;337:424-428.
54. Lumsden A, Krumlauf R. Patterning the vertibrate neuraxis. Science 1996;274:1109-1115.
55. Lumsden A, Sprawson N, Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 1991;113:1281-1291.
56. Marinides GN, Suchard SJ, Mookerjee BK. Role of thrombospondin in mesangial cell growth: Possible existence of an autocrine feedback growth circuit. Kidney Int. 1994;46:350-357.
57. McKeown-Longo PJ, Hanning R, Mosher DF. Binding and degradation of platelet thrombospondin by cultured fibroblasts. J. Cell Biol. 1984;98:22-28.
58. Morgelin M, Heinegard D, Engel J, Paulsson M. Electron microscopy of native cartilage oligomeric matrix protein purified from the Swarm rat chondrosarcoma reveals a five-armed structure. J. Biol. Chem. 1992;267:6137-6141.
59. Mosher DF. Physiology of thrombospondin. Annu. Rev. Med. 1990;41: 85-97.
60. Murphy-Ullrich JE, Hook M. Thrombospondin modulates focal adhesions in endothelial cells. J. Cell Biol. 1989;109:1309-1319.
61. Murphy-Ullrich JE, Gurusiddippa S, Frazier WA, Hook M. Heparinbinding peptides from thrombospondin-1 and -2 contain focal adhesion labeling activity. J. Biol. Chem. 1993;268:26784-26789.
62. Neugebauer KM, Emmett CJ, Venstrom KA, Reichardt LF. Vitronectin and thrombospondin promote retinal neurite outgrowth: developmental regulation and role of integrins. Neuron 1991;6:345-358.
63. Newport J, Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 1982;30:687-696.
64. Newton G, Weremowicz S, Morton CC, Copeland NG, Gilbert DJ, Jenkins NA, Lawler J. Characterization of human and mouse cartilage oligomeric matrix protein. Genomics 1994;24:435-439.
65. Nieuwkoop PD, Faber J. Normal Table of Xenopus laevis. New York: Garland Publishing, Inc., 1967.
66. Oldberg A, Antonsson P, Lindblom K, Heinegard D. COMP (cartilage oligomeric matrix protein) is structurally related to the thrombospondins. J. Biol. Chem. 1992;267:22346-22350.
67. O'Shea KS, Dixit VM. Unique distribution of the extracellular matrix component thrombospondin in the developing mouse embryo. J. Cell Biol. 1988;107:2737-2748.
68. O'Shea KS, Rheinheimer JST, Dixit VM. Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J. Cell Biol. 1990;110:1275-1283.
69. O'Shea KS, Liu LH, Dixit VM. Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 cells. Neuron 1991;7:231-237.
70. Osterhaut DJ, Frazier WA, Higgins D. Thrombospondin promotes process outgrowth in neurons from the peripheral and central nervous systems. Dev. Biol. 1992;150:256-265.
71. Placzek M, Jessell TM, Dodd J. Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 1993;117: 205-218.
72. Prater CA, Plotkin J, Jaye D, Frazier WA. The properdin-like type I repeats of human thrombospondin contain a cell attachment site. J. Cell Biol. 1991;112:1031-1040.
73. Qabar AN, Lin Z, Wolf FW, O'Shea KS, Lawler J, Dixit VM. Thrombospondin 3 is a developmentally regulated heparin binding protein. J. Biol. Chem. 1994;269:1262-1269.
74. Ramos JW, Whittaker CA, DeSimone DW. Integrin adhesive activity is spatially controlled by inductive signals at gastrulation. Development 1996;122:2873-2883.
75. 6 subunits. Dev. Biol. 1993;160:265-275.
76. Redies C. Cadherin expression in the developing vertebrate CNS: From neuromeres to brain nuclei and neural circuits. Exp. Cell Res. 1995;220:243-256.
77. Rosenblum ND, Botelho BB, Bernfield M. Expression of a Xenopus counterpart of mammalian syndecan 2 during embryogenesis. Biochem. J. 1995;309:69-76.
78. Ruiz i Altaba A, Jessell T. Retinoic acid modifies mesodermal patterning in early Xenopus embryos. Genes Dev. 1991;5:175-187.
79. Ruiz i Altaba A, Cox C, Jessell TM, Klar A. Ectopic neural expression of a floor plate maker in frog embryos injected with the midline transcription factor Pintallavis. Proc. Natl. Acad. Sci. USA 1993;90: 8268-8272.
80. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 1977;74:5463-5467.
81. Schultz-Cherry S, Murphy-Ullrich JE. Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J. Cell Biol. 1993;122:923-932.
82. Schultz-Cherry S, Lawler J, Murphy-Ullrich JE. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 1994;269:26783-26788.
83. Schultz-Cherry S, Chen H, Mosher DF, Misenheimer TM, Krutzsch HC, Roberts DD, Murphy-Ullrich JE. Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J. Biol. Chem. 1995;270:7304-7310.
84. Sechrist J, Serbedzija GN, Scherson T, Fraser SE, Bronner-Fraser M. Segmental migration of the hind brain neural crest does not arise from its segmental generation. Development 1993;118:691-703.
85. Slane JM, Mosher DF, Lai CS. Conformational change in thrombospondin induced by removal of bound Ca2+. A spin label approach. FEBS Lett. 1988;229:363-366.
86. Spencer-Adams D, Keller R, Koehl MAR. The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. Development 1990;110:115-130.
87. Speziale MV, Detwiler TC. Reduction of a disulfide bond of thrombospondin in the supernatant solution of activated platelets. Arch. Biochem. Biophys. 1991;286:546-550.
88. Sun X, Mosher DF, Rapraeger A. Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J. Biol. Chem. 1989;264:2885-2889.
89. Taraboletti G, Roberts D, Liotta LA, Giavazzi R. Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor. J. Cell Biol. 1990;111:765-772.
90. Tessier-Lavigne M, Placzek M. Target attraction: are developing neurons guided by chemotropism? Trends Neurosci. 1991;14:303-310.
91. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J. Cell Biol. 1993; 122:497-511.
92. Tucker RP. The in situ localization of tenascin splice variants and thrombospondin 2 mRNA in the avian embryo. Development 1993; 117:347-358.
93. Tucker RP, Adams JC, Lawler J. Thrombospondin-4 is expressed by early osteogenic tissues in the chick embryo. Dev. Dyn. 1995;203:477-490.
94. Tucker RP, Hagios C, Chiquet-Ehrismann R, Lawler J. In situ localization of thrombospondin-1 and thrombospondin-3 transcripts in the avian embryo. Dev. Dyn. 1997;208:326-337.
95. Tuszynski GP, Kowalska MA. Thrombospondin-induced adhesion of human platelets. J. Clin. Invest. 1991;87:1387-1394.
96. Tuszynski GP, Rothman VL, Papale M, Hamilton BK, Eyal J. Identification and characterization of a tumor cell receptor for CSVTCG, a thrombospondin adhesive domain. J. Cell Biol. 1993;120:513-521.
97. von Heijne G. Signal sequences. The limits of variation. J. Mol. Biol. 1985;184:99-105.
98. Vos HL, Devarayalu S, de Vries Y, Bornstein P. Thrombospondin 3 (Thbs3), a new member of the thrombospondin gene family. J. Biol. Chem. 1992;267:12192-12196.
99. Wassersug RJ. Locomotion in amphibian larvae (or 'why aren't tadboles built like fishes?') Am. Zool. 1989;29:65-84.
100. Watkins SC, Lynch GW, Kane LP, Slayter HS. Thrombospondin expression in traumatized skeletal muscle. Cell Tissue Res. 1990;261: 73-84.
101. Whittaker CA, DeSimone DW. Integrin α subunit mRNAs are differentially expressed in early Xenopus embryos. Development 1993;117: 1239-1249.
102. Yabkowitz R, Dixit VM. Human carcinoma cells bind thrombospondin through a Mr 80,000/105,000 receptor. Cancer Res. 1991;51:3648-3656.
103. 1 (VLA-5) integrins. J. Immunol. 1993;151:149-158.
104. Yamada T, Placzek M, Tanaka H, Dodd J, Jessell TM. Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 1991;64:635-647.
105. Youn BW, Malacinski GM. Axial structure development in UV-irradiated (notochord-defective) amphibian embryos. Dev. Biol. 1981; 83:339-352.