Literature DB >> 20937891

Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra.

Jung Shan Hwang1, Yasuharu Takaku, Tsuyoshi Momose, Patrizia Adamczyk, Suat Özbek, Kazuho Ikeo, Konstantin Khalturin, Georg Hemmrich, Thomas C G Bosch, Thomas W Holstein, Charles N David, Takashi Gojobori.   

Abstract

Taxonomically restricted genes or lineage-specific genes contribute to morphological diversification in metazoans and provide unique functions for particular taxa in adapting to specific environments. To understand how such genes arise and participate in morphological evolution, we have investigated a gene called nematogalectin in Hydra, which has a structural role in the formation of nematocysts, stinging organelles that are unique to the phylum Cnidaria. Nematogalectin is a 28-kDa protein with an N-terminal GlyXY domain (glycine followed by two hydrophobic amino acids), which can form a collagen triple helix, followed by a galactose-binding lectin domain. Alternative splicing of the nematogalectin transcript allows the gene to encode two proteins, nematogalectin A and nematogalectin B. We demonstrate that expression of nematogalectin A and B is mutually exclusive in different nematocyst types: Desmonemes express nematogalectin B, whereas stenoteles and isorhizas express nematogalectin B early in differentiation, followed by nematogalectin A. Like Hydra, the marine hydrozoan Clytia also has two nematogalectin transcripts, which are expressed in different nematocyte types. By comparison, anthozoans have only one nematogalectin gene. Gene phylogeny indicates that tandem duplication of nematogalectin B exons gave rise to nematogalectin A before the divergence of Anthozoa and Medusozoa and that nematogalectin A was subsequently lost in Anthozoa. The emergence of nematogalectin A may have played a role in the morphological diversification of nematocysts in the medusozoan lineage.

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Year:  2010        PMID: 20937891      PMCID: PMC2972925          DOI: 10.1073/pnas.1003256107

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  27 in total

Review 1.  Alternative splicing: increasing diversity in the proteomic world.

Authors:  B R Graveley
Journal:  Trends Genet       Date:  2001-02       Impact factor: 11.639

2.  Origin of alternative splicing by tandem exon duplication.

Authors:  F A Kondrashov; E V Koonin
Journal:  Hum Mol Genet       Date:  2001-11-01       Impact factor: 6.150

3.  Common exon duplication in animals and its role in alternative splicing.

Authors:  Ivica Letunic; Richard R Copley; Peer Bork
Journal:  Hum Mol Genet       Date:  2002-06-15       Impact factor: 6.150

4.  Structure/function relationships in the minicollagen of Hydra nematocysts.

Authors:  Suat Ozbek; Olivier Pertz; Martine Schwager; Ariel Lustig; Thomas Holstein; Jürgen Engel
Journal:  J Biol Chem       Date:  2002-10-03       Impact factor: 5.157

5.  A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles.

Authors:  Patrizia Adamczyk; Claudia Zenkert; Prakash G Balasubramanian; Shuhei Yamada; Saori Murakoshi; Kazuyuki Sugahara; Jung Shan Hwang; Takashi Gojobori; Thomas W Holstein; Suat Ozbek
Journal:  J Biol Chem       Date:  2010-06-09       Impact factor: 5.157

6.  The morphogenesis of nematocytes in Hydra and Forskålia: an ultrastructural study.

Authors:  T Holstein
Journal:  J Ultrastruct Res       Date:  1981-06

7.  Poly-gamma-glutamate synthesis during formation of nematocyst capsules in Hydra.

Authors:  Susanne Szczepanek; Mihai Cikala; Charles N David
Journal:  J Cell Sci       Date:  2002-02-15       Impact factor: 5.285

8.  The secretion and development of nematocysts in a siphonophore.

Authors:  R J Skaer
Journal:  J Cell Sci       Date:  1973-09       Impact factor: 5.285

9.  Spinalin, a new glycine- and histidine-rich protein in spines of Hydra nematocysts.

Authors:  A W Koch; T W Holstein; C Mala; E Kurz; J Engel; C N David
Journal:  J Cell Sci       Date:  1998-06       Impact factor: 5.285

10.  Mini-collagens in hydra nematocytes.

Authors:  E M Kurz; T W Holstein; B M Petri; J Engel; C N David
Journal:  J Cell Biol       Date:  1991-11       Impact factor: 10.539

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  26 in total

Review 1.  Evolutionary crossroads in developmental biology: Cnidaria.

Authors:  Ulrich Technau; Robert E Steele
Journal:  Development       Date:  2011-03-09       Impact factor: 6.868

2.  Functional and proteomic analysis of Ceratonova shasta (Cnidaria: Myxozoa) polar capsules reveals adaptations to parasitism.

Authors:  Gadi Piriatinskiy; Stephen D Atkinson; Sinwook Park; David Morgenstern; Vera Brekhman; Gilad Yossifon; Jerri L Bartholomew; Tamar Lotan
Journal:  Sci Rep       Date:  2017-08-21       Impact factor: 4.379

3.  Stem cell differentiation trajectories in Hydra resolved at single-cell resolution.

Authors:  Stefan Siebert; Jeffrey A Farrell; Jack F Cazet; Yashodara Abeykoon; Abby S Primack; Christine E Schnitzler; Celina E Juliano
Journal:  Science       Date:  2019-07-26       Impact factor: 47.728

4.  Genomic insights into the evolutionary origin of Myxozoa within Cnidaria.

Authors:  E Sally Chang; Moran Neuhof; Nimrod D Rubinstein; Arik Diamant; Hervé Philippe; Dorothée Huchon; Paulyn Cartwright
Journal:  Proc Natl Acad Sci U S A       Date:  2015-11-16       Impact factor: 11.205

5.  Expression patterns suggest that despite considerable functional redundancy, galectin-4 and -6 play distinct roles in normal and damaged mouse digestive tract.

Authors:  Denis Houzelstein; Edouard Reyes-Gomez; Marie Maurer; Pierre Netter; Dominique Higuet
Journal:  J Histochem Cytochem       Date:  2013-01-28       Impact factor: 2.479

6.  A genome wide survey reveals multiple nematocyst-specific genes in Myxozoa.

Authors:  Erez Shpirer; Arik Diamant; Paulyn Cartwright; Dorothée Huchon
Journal:  BMC Evol Biol       Date:  2018-09-12       Impact factor: 3.260

Review 7.  A genomic view of 500 million years of cnidarian evolution.

Authors:  Robert E Steele; Charles N David; Ulrich Technau
Journal:  Trends Genet       Date:  2010-11-01       Impact factor: 11.639

8.  Venom proteome of the box jellyfish Chironex fleckeri.

Authors:  Diane L Brinkman; Ammar Aziz; Alex Loukas; Jeremy Potriquet; Jamie Seymour; Jason Mulvenna
Journal:  PLoS One       Date:  2012-12-07       Impact factor: 3.240

9.  Diversified carbohydrate-binding lectins from marine resources.

Authors:  Tomohisa Ogawa; Mizuki Watanabe; Takako Naganuma; Koji Muramoto
Journal:  J Amino Acids       Date:  2011-11-15

10.  Analysis of soluble protein contents from the nematocysts of a model sea anemone sheds light on venom evolution.

Authors:  Yehu Moran; Daniela Praher; Ami Schlesinger; Ari Ayalon; Yossi Tal; Ulrich Technau
Journal:  Mar Biotechnol (NY)       Date:  2012-11-15       Impact factor: 3.619

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