Colocalization of heparin and histamine in the intracellular granules of test cells from the invertebrate Styela plicata (Chordata-Tunicata)

Cavalcante, Moisés C.M.; Andrade, Leonardo R.; Santos-Pinto, Cláudia Du Bocage; Straus, Anita H.; Takahashi, Hélio K.; Allodi, Silvana; Pavão, Mauro S.G.

doi:10.1016/s1047-8477(02)00007-2

Cited by 55 publications

(45 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Because the nature of the antigens was not characterized in these reports, no specific proteins secreted from test cells have been identified. Test cells in Styela plicata contain and can be induced to release, heparin and histamine (Cavalcante et al, 2000;Cavalcante et al, 2002), supporting an interpretation of immune-like function. The common conclusions derived from these reports are that test cells contain and deposit molecules that modify the external surface of the larval tunic.…”

Section: Abstract: Hsp90 Test Cells Tlc Ascidianmentioning

confidence: 70%

“…Later this antigen was found to be identical to that which generated the antibody NC1 from extracts of quail ciliary ganglion (Vincent and Thiery, 1984). Here in a urochordate we observe that the HNK-1 antigen appears to be present in test cells and trunk lateral cells, two cell types that, respectively, have been homologized with vertebrate mesodermal and neural crest cells (Cavalcante 2002, Jeffery et al, 2008. The implications for current models of neural crest origin and evolution are fascinating indeed.…”

mentioning

confidence: 64%

Section: Test Cells and The Larval Tunicmentioning

confidence: 99%

“…This similarity was further demonstrated by immunolabeling experiments with anti-HNK-1, in which both test cells and trunk lateral cells were stained. A third connection between test cells and trunk lateral cells has been revealed by investigations into the presence of heparin and histamine in ascidians (Cavalcante et al, 2000(Cavalcante et al, , 2002. In vertebrates, these molecules are associated with immunologic function and are secreted exclusively by a subtype of mast cell.…”

Section: A Relationship Between Test Cells and Some Tlc Descendants?mentioning

confidence: 99%

“…The antigens reported in Takamura et al (1996) and Okada et al (1996) have not been characterized and thus, HSP90 is the first identified protein that is deposited from the test cells on to the larval tunic. The mechanism by which test cells release their contents is not known, but test cells of Styela plicata can be induced to release heparin and histamine by the mammalian mast cell secretagogue compound 48/80 (Cavalcante et al, 2002), invoking GTPase and phospholipase C-and D-activity (Chahdi et al., 1998a(Chahdi et al., ,b, 2000Mousli et al, 1990;Senyshyn et al, 1998).Two observations indicate an evolutionary association of test cells and larval tunics: (i) Embryos of larvaceans, the sister taxon to Ascidians + Thalaceans (Wada, 1992), do not contain test cells (Cloney, 1990) and do not have a larval stage, (ii) Embryos of the direct developing ascidian Molgula pacifica do not contain test cells (Young et al, 1988;Bates and Mallet, 1991;Cloney, 1994). For reasons that are still not clear, but are almost certainly related to the deposition of materials by test cells discussed above, this association may be required to render the tunic an adaptive structure.…”

mentioning

confidence: 99%

See 4 more Smart Citations

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

Bishop

Hall²,

Bates³

2010

Int. J. Dev. Biol.

View full text Add to dashboard Cite

Heat shock protein 90 (HSP90) is a ubiquitously expressed molecular chaperone that controls the folding, assembly and activity of proteins, many of which are involved in signal transduction. Recent work has shown that HSP90 is present extracellularly, indicating a heretofore under appreciated requirement for extracellular chaperoning, particularly among migratory cells. We applied immunological and surgical techniques to document the differential expression of HSP90 during ascidian development. Relative to other cell types during development, test cells and trunk lateral cells (TLCs), two migratory cell types in the ascidian Boltenia villosa, express elevated levels of HSP90. Late in embryogenesis, test cells deposit HSP90 onto the tunic, the second report of extracellular HSP90 during animal development. The pyurid ascidian Halocynthia igaboja and the styelids Cnemidocarpa finmarkiensis and Botrylloides violaceus all express HSP90 at elevated levels in larval mesenchyme, suggesting that this pattern of expression is widespread in the Ascidiaceae. We show that HSP90 expression in TLCs and test cells is coincident with the presence of HNK-1. Whereas in B. violaceous, cell populations expressing elevated levels of HSP90 are distinct from those expressing HNK-1, in B. villosa both these antigens are present in the TLCs. We evaluate existing hypotheses about test cell function and, in reference to the similarities between test cells and some of the descendants of TLCs, hypothesize that test cells are TLC descendants. Implications for the proposed evolutionary relationship between TLCs and neural crest are briefly discussed. KEY WORDS: HSP90, test cells, TLC, ascidianAmong marine invertebrates, ascidians are unique in both their mode of larval locomotion and their possession of a protective extracellular matrix, the tunic. The tunic is composed of carbohydrate polymers and proteins that interact extensively (Smith and Dehnel, 1970). In adult and larval stages of ascidians, the tunic is secreted by epidermal cells (Wardrop 1970;Robinson et al., 1986). In embryos and larvae the tunic appears to require the presence of test cells, a third unique characteristic of ascidian embryos.Test cells are extraembryonic migratory cells that reside between the embryo and the follicular envelope of almost all ascidian embryos. The rarity of test cell analogues in the animal kingdom is conspicuous and the ontogenetic origin and function of test cells remains enigmatic. Test cells are thought by some authors to derive from the inner follicular envelope, which, in turn, arises from the germinal epithelium (Cloney, 1994 and references Int. J. Dev. Biol. 54: 1337-1346 (2010) doi: 10.1387/ijdb.082730cb Abbreviations used in this paper: HNK-1, human natural killer antigen 1; HSP90, heat shock protein 90; TLCs, trunk lateral cells. therein). Another hypothesis is that test cells derive from migratory amoeboid or lymphocyte cells that differentiate into test cells and become preferentially associated with developing oocytes (Clon...

show abstract

Section: Abstract: Hsp90 Test Cells Tlc Ascidianmentioning

confidence: 70%

mentioning

confidence: 64%

Section: Test Cells and The Larval Tunicmentioning

confidence: 99%

Section: A Relationship Between Test Cells and Some Tlc Descendants?mentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

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

Bishop

Hall²,

Bates³

2010

Int. J. Dev. Biol.

View full text Add to dashboard Cite

show abstract

Cell Secretion Mediated by Granule‐Associated Vesicle Transport: A Glimpse at Evolution

Crivellato

Nico

Gallo

et al. 2010

The Anatomical Record

View full text Add to dashboard Cite

Regulated secretion allows extrusion of cell products stored in specialized membrane-bound organelles called secretory granules or secretory vesicles. Regulated secretion provides basic functions in living organisms, and in a phylogenetic perspective, it is recognizable in the most primitive eukaryotic forms. This article is an attempt to trace the evolutionary history of a special type of secretory pattern, which has been referred to as vesiclemediated degranulation or piecemeal degranulation (PMD). First described in the early 70s of the last century in inflammatory cells, such as the basophils, mast cells, and eosinophils, this regulated secretory route has subsequently been recognized in endocrine cells, in particular in the chromaffin cells of the adrenal medulla. This vesicle-mediated degranulation is held to mobilize small and specific aliquots of granule-associated material for selective paracrine or endocrine transport to the cell exterior. PMD has been identified in many vertebrate classes. By contrast, no data are available for invertebrates. We speculate that this pattern of cell secretion emerged early in phylogenesis, when the first metazoans appeared. In this review article, we will first revise the concept of vesicle-mediated degranulation in the light of the most recent experimental discoveries and theoretical implications. Then, the distribution of this secretory mode among vertebrates and its molecular basis will be highlighted. Finally, the potential occurrence of PMD in invertebrates, its biological significance from an evolutionary perspective and the future direction of investigations will be briefly sketched. Anat Rec, 293:1115Rec, 293: -1124

show abstract

Ascidian (Chordata-Tunicata) Glycosaminoglycans: Extraction, Purification, Biochemical, and Spectroscopic Analysis

Teixeira

Pavão

2021

Methods in Molecular Biology

View full text Add to dashboard Cite

Colocalization of heparin and histamine in the intracellular granules of test cells from the invertebrate Styela plicata (Chordata-Tunicata)

Cited by 55 publications

References 45 publications

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

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

Cell Secretion Mediated by Granule‐Associated Vesicle Transport: A Glimpse at Evolution

Ascidian (Chordata-Tunicata) Glycosaminoglycans: Extraction, Purification, Biochemical, and Spectroscopic Analysis

Contact Info

Product

Resources

About