A thrombospondin in the anthozoan Nematostella vectensis is associated with the nervous system and upregulated during regeneration

Richard P Tucker, John F. Hess, Qizhi Gong, Katrina Garvey, Bradley Shibata, Josephine C. Adams

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Thrombospondins are multimeric extracellular matrix glycoproteins that play important roles in development, synaptogenesis and wound healing in mammals. We previously identified four putative thrombospondins in the genome of the starlet sea anemone Nematostella vectensis. This study presents the first analysis of these thrombospondins, with the goals of understanding fundamental roles of thrombospondins in the Eumetazoa. Reverse transcriptase PCR showed that each of the N. vectensis thrombospondins (Nv85341, Nv22035, Nv168100 and Nv30790) is transcribed. Three of the four thrombospondins include an RGD or KGD motif in their thrombospondin type 3 repeats at sites equivalent to mammalian thrombospondins, suggesting ancient roles as RGD integrin ligands. Phylogenetic analysis based on the Cterminal regions demonstrated a high level of sequence diversity between N. vectensis thrombospondins. A full-length cDNA sequence was obtained for Nv168100 (NvTSP168100), which has an unusual domain organization. Immunohistochemistry with an antibody to NvTSP168100 revealed labeling of neuron-like cells in the mesoglea of the retractor muscles and the pharynx. In situ hybridization and quantitative PCR showed that NvTSP168100 is upregulated during regeneration. Immunohistochemistry of the area of regeneration identified strong immunostaining of the glycocalyx, the carbohydrate-rich matrix coating the epidermis, and electron microscopy identified changes in glycocalyx organization during regeneration. Thus, N. vectensis thrombospondins share structural features with thrombospondins from mammals and may have roles in the nervous system and in matrix reorganization during regeneration.

Original languageEnglish (US)
Pages (from-to)217-226
Number of pages10
JournalBiology Open
Volume2
Issue number2
DOIs
StatePublished - Feb 15 2013

Fingerprint

Thrombospondins
Neurology
nervous system
Nervous System
immunohistochemistry
Regeneration
mammals
pharynx
Anthozoa
epidermis (animal)
integrins
tissue repair
extracellular matrix
in situ hybridization
coatings
glycoproteins
electron microscopy
quantitative polymerase chain reaction
neurons
reverse transcriptase polymerase chain reaction

Keywords

  • Cnidaria
  • Extracellular matrix
  • Glycocalyx
  • Mesoglea
  • Nervous system
  • Regeneration

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

A thrombospondin in the anthozoan Nematostella vectensis is associated with the nervous system and upregulated during regeneration. / Tucker, Richard P; Hess, John F.; Gong, Qizhi; Garvey, Katrina; Shibata, Bradley; Adams, Josephine C.

In: Biology Open, Vol. 2, No. 2, 15.02.2013, p. 217-226.

Research output: Contribution to journalArticle

Tucker, Richard P ; Hess, John F. ; Gong, Qizhi ; Garvey, Katrina ; Shibata, Bradley ; Adams, Josephine C. / A thrombospondin in the anthozoan Nematostella vectensis is associated with the nervous system and upregulated during regeneration. In: Biology Open. 2013 ; Vol. 2, No. 2. pp. 217-226.
@article{701a28f2c62442409c3e1604c1c524bb,
title = "A thrombospondin in the anthozoan Nematostella vectensis is associated with the nervous system and upregulated during regeneration",
abstract = "Thrombospondins are multimeric extracellular matrix glycoproteins that play important roles in development, synaptogenesis and wound healing in mammals. We previously identified four putative thrombospondins in the genome of the starlet sea anemone Nematostella vectensis. This study presents the first analysis of these thrombospondins, with the goals of understanding fundamental roles of thrombospondins in the Eumetazoa. Reverse transcriptase PCR showed that each of the N. vectensis thrombospondins (Nv85341, Nv22035, Nv168100 and Nv30790) is transcribed. Three of the four thrombospondins include an RGD or KGD motif in their thrombospondin type 3 repeats at sites equivalent to mammalian thrombospondins, suggesting ancient roles as RGD integrin ligands. Phylogenetic analysis based on the Cterminal regions demonstrated a high level of sequence diversity between N. vectensis thrombospondins. A full-length cDNA sequence was obtained for Nv168100 (NvTSP168100), which has an unusual domain organization. Immunohistochemistry with an antibody to NvTSP168100 revealed labeling of neuron-like cells in the mesoglea of the retractor muscles and the pharynx. In situ hybridization and quantitative PCR showed that NvTSP168100 is upregulated during regeneration. Immunohistochemistry of the area of regeneration identified strong immunostaining of the glycocalyx, the carbohydrate-rich matrix coating the epidermis, and electron microscopy identified changes in glycocalyx organization during regeneration. Thus, N. vectensis thrombospondins share structural features with thrombospondins from mammals and may have roles in the nervous system and in matrix reorganization during regeneration.",
keywords = "Cnidaria, Extracellular matrix, Glycocalyx, Mesoglea, Nervous system, Regeneration",
author = "Tucker, {Richard P} and Hess, {John F.} and Qizhi Gong and Katrina Garvey and Bradley Shibata and Adams, {Josephine C.}",
year = "2013",
month = "2",
day = "15",
doi = "10.1242/bio.20123103",
language = "English (US)",
volume = "2",
pages = "217--226",
journal = "Biology Open",
issn = "2046-6390",
publisher = "Company of Biologists Ltd",
number = "2",

}

TY - JOUR

T1 - A thrombospondin in the anthozoan Nematostella vectensis is associated with the nervous system and upregulated during regeneration

AU - Tucker, Richard P

AU - Hess, John F.

AU - Gong, Qizhi

AU - Garvey, Katrina

AU - Shibata, Bradley

AU - Adams, Josephine C.

PY - 2013/2/15

Y1 - 2013/2/15

N2 - Thrombospondins are multimeric extracellular matrix glycoproteins that play important roles in development, synaptogenesis and wound healing in mammals. We previously identified four putative thrombospondins in the genome of the starlet sea anemone Nematostella vectensis. This study presents the first analysis of these thrombospondins, with the goals of understanding fundamental roles of thrombospondins in the Eumetazoa. Reverse transcriptase PCR showed that each of the N. vectensis thrombospondins (Nv85341, Nv22035, Nv168100 and Nv30790) is transcribed. Three of the four thrombospondins include an RGD or KGD motif in their thrombospondin type 3 repeats at sites equivalent to mammalian thrombospondins, suggesting ancient roles as RGD integrin ligands. Phylogenetic analysis based on the Cterminal regions demonstrated a high level of sequence diversity between N. vectensis thrombospondins. A full-length cDNA sequence was obtained for Nv168100 (NvTSP168100), which has an unusual domain organization. Immunohistochemistry with an antibody to NvTSP168100 revealed labeling of neuron-like cells in the mesoglea of the retractor muscles and the pharynx. In situ hybridization and quantitative PCR showed that NvTSP168100 is upregulated during regeneration. Immunohistochemistry of the area of regeneration identified strong immunostaining of the glycocalyx, the carbohydrate-rich matrix coating the epidermis, and electron microscopy identified changes in glycocalyx organization during regeneration. Thus, N. vectensis thrombospondins share structural features with thrombospondins from mammals and may have roles in the nervous system and in matrix reorganization during regeneration.

AB - Thrombospondins are multimeric extracellular matrix glycoproteins that play important roles in development, synaptogenesis and wound healing in mammals. We previously identified four putative thrombospondins in the genome of the starlet sea anemone Nematostella vectensis. This study presents the first analysis of these thrombospondins, with the goals of understanding fundamental roles of thrombospondins in the Eumetazoa. Reverse transcriptase PCR showed that each of the N. vectensis thrombospondins (Nv85341, Nv22035, Nv168100 and Nv30790) is transcribed. Three of the four thrombospondins include an RGD or KGD motif in their thrombospondin type 3 repeats at sites equivalent to mammalian thrombospondins, suggesting ancient roles as RGD integrin ligands. Phylogenetic analysis based on the Cterminal regions demonstrated a high level of sequence diversity between N. vectensis thrombospondins. A full-length cDNA sequence was obtained for Nv168100 (NvTSP168100), which has an unusual domain organization. Immunohistochemistry with an antibody to NvTSP168100 revealed labeling of neuron-like cells in the mesoglea of the retractor muscles and the pharynx. In situ hybridization and quantitative PCR showed that NvTSP168100 is upregulated during regeneration. Immunohistochemistry of the area of regeneration identified strong immunostaining of the glycocalyx, the carbohydrate-rich matrix coating the epidermis, and electron microscopy identified changes in glycocalyx organization during regeneration. Thus, N. vectensis thrombospondins share structural features with thrombospondins from mammals and may have roles in the nervous system and in matrix reorganization during regeneration.

KW - Cnidaria

KW - Extracellular matrix

KW - Glycocalyx

KW - Mesoglea

KW - Nervous system

KW - Regeneration

UR - http://www.scopus.com/inward/record.url?scp=84965014024&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84965014024&partnerID=8YFLogxK

U2 - 10.1242/bio.20123103

DO - 10.1242/bio.20123103

M3 - Article

VL - 2

SP - 217

EP - 226

JO - Biology Open

JF - Biology Open

SN - 2046-6390

IS - 2

ER -