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Identification and Expression of Acetylcholinesterase in Octopus vulgaris Arm Development and Regeneration: a Conserved Role for ACHE?

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Abstract

Acetylcholinesterase (ACHE) is a glycoprotein with a key role in terminating synaptic transmission in cholinergic neurons of both vertebrates and invertebrates. ACHE is also involved in the regulation of cell growth and morphogenesis during embryogenesis and regeneration acting through its non-cholinergic sites. The mollusk Octopus vulgaris provides a powerful model for investigating the mechanisms underlying tissue morphogenesis due to its high regenerative power. Here, we performed a comparative investigation of arm morphogenesis during adult arm regeneration and embryonic arm development which may provide insights on the conserved ACHE pathways. In this study, we cloned and characterized O. vulgaris ACHE, finding a single highly conserved ACHE hydrophobic variant, characterized by prototypical catalytic sites and a putative consensus region for a glycosylphosphatidylinositol (GPI)-anchor attachment at the COOH-terminus. We then show that its expression level is correlated to the stage of morphogenesis in both adult and embryonic arm. In particular, ACHE is localized in typical neuronal sites when adult-like arm morphology is established and in differentiating cell locations during the early stages of arm morphogenesis. This possibility is also supported by the presence in the ACHE sequence and model structure of both cholinergic and non-cholinergic sites. This study provides insights into ACHE conserved roles during processes of arm morphogenesis. In addition, our modeling study offers a solid basis for predicting the interaction of the ACHE domains with pharmacological blockers for in vivo investigations. We therefore suggest ACHE as a target for the regulation of tissue morphogenesis.

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Abbreviations

ACHE:

Acetylcholinesterase

ASW:

Artificial sea water

BCHE:

Butyrylcholinesterase

CAS:

Catalytic anionic site

CAT:

Catalytic triad

GPI:

Glycosylphosphatidylinositol

ORF:

Open reading frame

PAS:

Peripheral binding site

RMSD:

Root mean square deviation

RT-qPCR:

Real-time quantitative PCR

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Acknowledgments

We thank Jennifer Helm for the help with data collection and Andrea Contestabile for the technical support. We are also grateful to Prof. Jenny Kien for the suggestions and editorial assistance.

Conflict of Interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Via Morego 30, 16163, Genoa, Italy

    Sara Maria Fossati, Marie-Therese Nödl, Luca Maragliano, Maria Pennuto, Fabio Benfenati & Letizia Zullo

  2. DISTAV, University of Genova, Genoa, Italy

    Simona Candiani & Mario Pestarino

  3. Dulbecco Telethon Institute, Lab of Neurodegenerative Diseases, CIBIO, University of Trento, Trento, Italy

    Maria Pennuto

  4. Centro Oceanográfico de Vigo, Instituto Español de Oceanografía, Vigo, Spain

    Pedro Domingues

  5. Department of Experimental Medicine, University of Genova, Genoa, Italy

    Fabio Benfenati

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  1. Sara Maria Fossati
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  2. Simona Candiani
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  3. Marie-Therese Nödl
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  4. Luca Maragliano
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Correspondence to Sara Maria Fossati.

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Fossati, S.M., Candiani, S., Nödl, MT. et al. Identification and Expression of Acetylcholinesterase in Octopus vulgaris Arm Development and Regeneration: a Conserved Role for ACHE?. Mol Neurobiol 52, 45–56 (2015). https://doi.org/10.1007/s12035-014-8842-2

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