HSP90 expression in two migratory cell types during ascidian development: Test cells deposit HSP90 on the larval tunic

International Journal of Developmental Biology

Volumn 54, Issue 8-9, 2010, Pages 1337-1346

  Bishop, Cory D ^a   Hall, Brian K ^b   Bates, William R ^c  

^a ST FRANCIS XAVIER UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Ascidian; Hsp90; Test cells; Tlc

Indexed keywords

ANTIGEN; HEAT SHOCK PROTEIN 90; HUMAN NATURAL KILLER ANTIGEN 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ASCIDIACEA; BOLTENIA VILLOSA; BOTRYLLOIDES VIOLACEUS; CELL MIGRATION; CELL POPULATION; CELL TYPE; CNEMIDOCARPA FINMARKIENSIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR SPACE; HALOCYNTHIA IGABOJA; LARVAL DEVELOPMENT; LARVAL STAGE; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; TISSUE LEVEL;

ANIMALS; BLOTTING, WESTERN; CELL LINEAGE; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; FEMALE; HSP90 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; LARVA; MOLECULAR CHAPERONES; NEURAL CREST; UROCHORDATA;

ANIMALIA; ASCIDIA; BOLTENIA VILLOSA; BOTRYLLOIDES VIOLACEUS; CNEMIDOCARPA FINMARKIENSIS; HALOCYNTHIA IGABOJA; PYURIDAE; STYELIDAE;

EID: 77957693608     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082730cb     Document Type: Article

References (69)

1. ABO T. and BALCH C.M. (1981). A differentiation antigen of NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol 127: 1024-1029.
2. DE BARROS C.M., ANDRADE L.R., ALLODI S., VISKOV C., MOURIER P.A., CAVALCANTE M.C.M., STRAUS A.H., TAKAHASHI H.K., POMIN V.H., CARVALHO V.F., MARTINS M.A., and PAVÃO M.S.G. (2007). The hemolymph of the ascidian Styela plicata (Chordata-Tunicata) contains heparin inside basophil-like cells and a unique sulfated galactoglucan in the plasma. J Biol Chem 282: 1615-1626.
3. BATES W.R. (1988). Development of myoplasm enriched ascidian embryos. Dev Biol 129: 241-252.
4. BATES W.R. (2004). Cellular features of an apoptotic form of programmed cell death during development of the ascidian, Boltenia villosa. Zool Sci 21: 553-563.
5. BATES W.R. and BISHOP C. (1996). Localization of constitutive heat shock proteins in developing ascidians. Devel Growth and Differ 38: 307-314
6. BATES W.R. and JEFFERY W.R. (1987). Alkaline phosphatase expression in ascidian egg fragments and andromerogons. Dev Biol 119: 382-389.
7. BATES W.R. and MALLET J.E. (1991). Ultrastructural and histochemical study of anural development in the ascidian Molgula pacifica (Huntsman). Roux's Arch Dev Biol 200: 193-201.
8. BISHOP C.D., BATES W.R. and BRANDHORST, B.P. (2001). Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 289: 374-384.
9. BISHOP C.D., BATES W.R. and BRANDHORST, B.P. (2002). HSP90 function is required for morphogenesis in ascidian and sea urchin embryos. Dev Genes Evol 212: 70-80.
10. CAVALCANTE M.C., ALLODI S., VALENTE A.P., STRAUS A.H., TAKAHASHI H.K., MOURÃO P.A., PAVÃO M.S. (2000). Occurrence of heparin in the invertebrate Styela plicata (Tunicata) is restricted to cell layers facing the outside environment. An ancient role in defense? J Biol Chem 275: 36189-36196.
11. CAVALCANTE M.C., DE ANDRADE L.R., DU BOCAGE SANTOS-PINTO C., STRAUS A.H., TAKAHASHI H.K., ALLODI S., PAVAO M.S. (2002). Colocalization of heparin and histamine in the intracellular granules of test cells from the invertebrate Styela plicata (Chordata-Tunicata). J Struct Biol 137: 313-321.
12. CAVEY M.J. (1976). Ornamentation of the larval tunic by test cells. J Ultrastructural Res 55: 297-298.
13. CHAHDI A., DAEFFLER L., GIES J.P. and LANDRY Y. (1998). Drugs interacting with G protein a subunits: selectivity and pespectives. Fundam Clin Pharmacol 12: 121-132.
14. CHAHDI A., MOUSLI M. and LANDRY Y. (1998). Substance P-related inhibitors of mast cell exocytosis act on G proteins or on the cell surface. Eur J Pharmacol 341: 329-335.
15. CHAHDI, A., FRAUNDORFER P.F. and BEAVEN M.A. (2000). Compound 48/80 activates mast cell phospholipase D via heterotrimeric GTP-binding proteins. J Pharmacol Exp Ther 292: 122-130.
16. CHEN B., ZHONG, D. and MONTEIRO A. (2006). Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7: 156-175.
17. CLONEY R.A. (1990). Larval tunic and the function of the test cells in ascidians. Acta Zoologica 71: 151-159.
18. CLONEY R.A. (1994). Test cell secretions and their functions in ascidian development. In: Reproduction and Development of Marine Invertebrates. (Eds. Wilson WH, Stricker SA and Shinn GL). Johns Hopkins University Press, Baltimore, USA.
19. CLONEY R.A. and CAVEY M.J. (1982). Ascidian larval tunic: Extraembryonic structures influence morphogenesis. Cell Tissue Res 222: 547-562.
20. CONNOLY M.H. and HALL B.K. (2008). Embryonic heat shock reveals latent hsp90 translation in zebrafish (Danio rerio). Int J Dev Biol 52: 71-79.
21. CUTFORTH T. and RUBIN G.M. (1994). Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 77: 1027-1036.
22. DING D., PARKHURST S.M., HALSELL S.R., and LIPSHITZI H.D. (1993). Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Mol Cel Biol 13: 3773-3781.
23. D'SOUSA S.M. and BROWN I.R. (1998). Constitutive expression of heat shock proteins Hsp90, Hsc70, Hsp70 and Hsp60 in neural and non- neuronal tissues of the rat during postnatal development. Cell Stress Chaperones 3:188-199.
24. EUSTACE B.K., SAKURAI T., STEWART J.K., YIMLAMAI D., UNGER C., ZEHETMEIER C., LAIN B., TORELLA C., HENNING S.W., BESTE G., SCROGGINS B.T., NECKERS L., ILAG L.L. and JAY D.G. (2004). Functional proteomic screens reveal an essential role for extracellular HSP90 alpha in cancer cell invasiveness. Nat Cell Biol 6: 507-514.
25. EUSTACE B.K. and JAY D.G. (2004). Extracellular roles for the molecular chaperone HSP90. Cell Cycle 3: 1098-1100.
26. GUNTER H.M. and DEGNAN M.B. (2007). Developmental expression of Hsp90, Hsp70 and HSF during morphogenesis in the vetigastropod Haliotis asinina Dev Genes Evol 217: 603-612.
27. HIRANO T. and NISHIDA H. (1997). Developmental fates of larval tissues after metamorphosis in ascidian Halocynthia roretzi. I. Origin of mesodermal tissues of the juvenile. Dev Biol 192: 199-210.
28. JEFFERY W.R. (2006). Ascidian Neural Crest-Like Cells: Phylogenetic Distribution, Relationship to Larval Complexity, and Pigment Cell Fate. J Exp Zool (Mol Dev Evol) 306B: 470-480.
29. JEFFERY W.R., CHIBA T., KRAJKA F.R., DEYTS C., SATOH, N. and JOLY J.-S. (2008). Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: Insights into the ancestry and evolution of the neural crest. Dev Biol 324:152-160.
30. KANG B.H., PLESCIA J., DOHI T., ROSA J., DOXSEY S.J. and ALTIERI D.C.(2007). Regulation of Tumor Cell Mitochondrial Homeostasis by an Organelle- Specific Hsp90 Chaperone Network. Cell 131: 257-270.
31. LEE K.J., KIM Y.M., KIM D.Y., JEOUNG D., HAN K., LEE S.T., LEE Y.S. and PARK K.H. (2006). Release of heat shock protein 70 (Hsp70) and the effects of extracellular Hsp70 on matrix metalloproteinase-9 expression in human monocytic U937 cells. Exp Mol Med 38: 364-374.
32. LI W., LI Y., GUAN S., FAN J., CHENG C.-F., BRIGHT A.M., CHINN C., CHEN M. and WOODLEY D.T. (2007). Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. Embo J 26: 1221-33.
33. MAURY B., MARTINAND-MARI C., CHAMBON J.P., SOUL J., DEGOLS G., SAHUQUET A., WEILL M., BERTHOMIEU A., FORT P., MANGEAT P., BAGHDIGUIAN S. (2006). Fertilization regulates apoptosis of Ciona intestinalis extra-embryonic cells through thyroxine (T4)-dependent NF-kappaB pathway activation during early embryonic development. Dev Biol 289: 152-165.
34. MILTON C.C., HUYNH B., BATTERHAM P., RUTHERFORD S.L., HOFFMANN A.A. (2003). Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci USA 100: 13396-13401.
35. MILTON C.C., ULANE C.M. and RUTHERFORD S. (2006). Control of Canalization and Evolvability by Hsp90. PLOS One. 1: 1-12.
36. MONNIOT F., MARTOJA R., TRUCHET M. and FROHLICH F. (1992). Opal in ascidians: A curious bioaccumulation in the ovary. Mar Biol 112: 283-292.
37. MOUSLI M., BUEB J.-L., BRONNER C., BAND R. and LANDRY Y. (1990). Gprotein activation: a receptor-independent mode of action for cationic amphiphilic neuropeptides and venom peptides. Trends Pharmacol Sci 11, 358-362.
38. NISHIDA H. and SATOH N. (1987). Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol 121: 526-541.
39. NISHIDE K., NISHIKATA T. and SATOH N. (1989). A monoclonal antibody specific to embryonic trunk lateral cells of the ascidian Halocynthia roretzi stains coelomic cells of juvenile and adult basophilic blood cells. Develop Growth Differ 13: 595-600.
40. OKADA T., TAKAMURA K., YAMAGUCHI Y. and YAMAMOTO M. (1996). Secretory function of the test cell in larval tunic formation in the ascidian Ciona intestinalis: An immunoelectron study. Zoological Science 13: 253-261.
41. QUEITSCH C., SANGSTER T.A. and LINDQUIST S. (2002). Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
42. ROBERTS S.P. and FEDER M.E. (1999). Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 121: 323-329.
43. ROBINSON W.E., KUSTIN K. and CLONEY R.A. (1986). The influence of tunichrome and other reducing compounds on tunic and fin formation in embryonic Ascidia callosa Stimpson. J Exp Zool 237: 63-72.
44. RUTHERFORD S. and LINDQUIST S. (1998). Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
45. SASS J.B., WEINBERG E.S. and KRONE P.H. (1996). Specific localization of zebrafish hsp90a mRNA to myoD-expressing cells suggests a role for hsp90a during normal muscle development. Mech Dev 54:195-204.
46. SATO Y., TERAKADO K. and MORISAWA M. (1997). Test cell migration and tunic formation during post-hatching development of the larva of the ascidian Ciona intestinalis. Develop Growth Differ 39: 117-126.
47. SATO Y. and MORISAWA M. (1999). Loss of test cells leads to the formation of new tunic surface cells and abnormal metamorphosis in larvae of Ciona intestinalis (Chordata, Ascidiacae). Dev Genes Evol 209: 592-600.
48. SENYSHYN J., BAUMGARTNER R.A. and BEAVEN M.A. (1998). Quercetin sensitizes RBL-2H3 cells to polybasic mast-cell secretagogues through increased expression of Gi GTP-binding proteins linked to a phospholipase C signaling pathway. J Immunol 160, 5136-5144.
49. SIDERA K., SAMIOTAKI M., YFANTI E., PANAYOTOU G., and PATSAVOUDI E. (2004). Involvement of cell surface HSP90 in cell migration reveals a novel role in the developing nervous system J Biol Chem 279: 45379-45388.
50. SIDERA K., GAITANOU M., STELLAS D., MATSAS R. and PATSAVOUDI E. (2008). A critical role for HSP90 in cancer cell invasion involves interaction with the extracellular domain of HER-2. J Biol Chem 283: 2031-2041.
51. SMITH M.J. (1970). The blood cells and tunic of the ascidian Halocynthia aurantium (Pallas). I. Hematology, tunic morphology, and partition of cells between blood and tunic. Biol Bull 138: 354-388.
52. SMITH M.J. and DEHNEL P.A. (1970). The chemical and enzymatic analyses of the tunic of the ascidians Halocynthia aurantium (Pallas) Comp Biochem Physiol 35: 17-30.
53. SONG Y., FEE L., LEE T.H. and WHARTON R.P. (2007). The molecular chaperone Hsp90 is required for mRNA localization in Drosophila melanogaster embryos. Genetics 176: 2213-22.
54. SOTGIA C., FASCIO, U., ORTOLANI G. and DE BERNARDI F. (1993). Behavior of endodermal «button cells» during metamorphosis of ascidian larvae. Int J Dev Biol 37: 547-55.
55. SUZUKI Y. and NIJHOUT H.F. (2006). Evolution of a polyphenism by genetic accommodation. Science 311:650-652.
56. TAKAMURA K., UEDA Y., IRIE U. and YAMAGUCHI Y. (1996). Immunohistology with antibodies specific to test cells in the ascidian Ciona intestinalis suggests their role in larval tunic formation. Zoological Science 13: 241-251.
57. TOKUOKA M., IMAI K.S., SATOU Y. and SATOH N. (2004). Three distinct lineages of mesenchymal cells in Ciona intestinalis embryos demonstrated by specific gene expression. Dev Biol 274: 211-224.
58. TOKUOKA M., SATOH N., SATOU Y. (2005). A bHLH transcription factor gene, Twist-like1, is essential for the formation of mesodermal tissues of Ciona juveniles. Dev Biol 288: 387-396.
59. TUCKER G.C., AOYAMA H., LIPINKSI M., TURSZ T., THIERY J.P. (1984). Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ 14: 223-230.
60. TSUTSUMI S., NECKERS L. (2007). Extracellular heat shock protein 90: A role for a molecular chaperone in cell motility and cancer metastasis. Cancer Sci 98: 1536-39.
61. ULLRICH S.J., ROBINSON E.A., LAW L.W., WILLINGHAM M., APPELLA E. (1986). A mouse tumor-specific transplantation antigen is a heat shock-related protein. Proc Natl Acad Sci USA 83: 3121-5.
62. VINCENT M., THIERY J.P. (1984). A cell surface marker for neural crest and placodal cells: further evolution in peripheral and central nervous system. Dev Biol 103: 468-481.
63. WADA H. (1992). Evolutionary history of free-swimming and sessile lifestyles in urochordates as deduced from 18S rDNA molecular phylogeny. Mol Biol Evol 15: 1189-1194.
64. WADDINGTON C.H. (1953a). Genetic assimilation of an acquired character. Evolution 7: 118-126.
65. WADDINGTON C.H. (1953b). The «Baldwin effect,» «genetic assimilation» and «homeostasis». Evolution 7: 386-387.
66. WARDROP A.B. (1970). The structure and formation of the test of Pyura stolonifera (Tunicata). Protoplasma 70: 73-86.
67. XU Y., LINDQUIST S. (1993). HSP90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci USA. 90: 7074-7078.
68. YEYATI P.L., BANCEWICZ R.M., MAULE J., VAN HEYNINGEN V. (2007). Hsp90 Selectively Modulates Phenotype in Vertebrate Development. PLOS Genetics 3: 431-447.
69. YOUNG C.M., GOWAN R.F., DALBY J., PENNACHETTI C.A., GAGLIARDI D. (1988). Distributional consequences of adhesive eggs and anural development in the ascidian Molgula pacifica (Huntsman, 1912). Biol Bull 174: 39-46.