Elsevier

Tissue and Cell

Volume 43, Issue 6, December 2011, Pages 377-383
Tissue and Cell

Expression of a neuropeptide similar to allatotropin in free living turbellaria (platyhelminthes)

https://doi.org/10.1016/j.tice.2011.07.005Get rights and content

Abstract

Mechanisms coordinating cell–cell interaction have appeared early in evolution. Allatotropin (AT), a neuropeptide isolated based on its ability to stimulate the synthesis of juvenile hormones (JHs) in insects has also been found in other invertebrate phyla. Despite this function, AT has proved to be myotropic. In the present study we analyze its expression in two groups of Turbellaria (Catenulida, Macrostomida), and its probable relationship with muscle tissue. The results show the presence of an AT-like peptide in the free living turbellaria analyzed. The analysis of the expression of the peptide together with phalloidin, suggests a functional relationship between the peptide and muscle tissue, showing that it could be acting as a myoregulator. The finding of immunoreactive fibers associated with sensory organs like ciliated pits in Catenulida and eyes in Macrostomida makes probable that AT could play a role in the physiological mechanisms controlling circadian activities. Furthermore, the existence of AT in several phyla of Protostomata suggests that this peptide could be a synapomorphic feature of this group. Indeed, the presence in organisms that do not undergo metamorphosis, could be signaling that it was first involved in myotropic activities, being the stimulation of the synthesis of JHs a secondary function acquired by the phylum Arthropoda.

Introduction

Cell–cell integration is a basic feature to coordinate functions in all living organisms. Then, mechanisms coordinating functions locally as well as systemically are likely to have appeared early in evolution. This is achieved by mean of different ways (e.g. paracrine, endocrine, synaptic) but always involves chemical messengers including molecules with different chemical natures as mineral ions, lipids, aminoacids and peptides. Even in protists (Le Roith et al., 1980), sponges (Lentz, 1966, Weyrer et al., 1999) and cnidarians (Grimmelikhuijzen et al., 1991, Grimmelikhuijzen et al., 1996, Grimmelikhuijzen et al., 2002, Hansen et al., 2002), the existence of cellular mediators was documented, and several native neuropeptides were isolated and characterized.

In Turbellaria, neuropeptides seem to be particularly important as myoregulators, controlling the activity of muscles at the level of both digestive and reproductive organs (Gustafsson et al., 2002). In fact, several neuropeptides have been detected and characterized in Plathyelminthes and Acoela (Gustafsson et al., 2002, Johnston et al., 1995, Johnston et al., 1996, Kreshchenko, 2008, Kreshchenko et al., 2008, McVeigh et al., 2009, Mousley et al., 2004, Reuter et al., 1998, Reuter et al., 2001, Wikgren and Reuter, 1985).

Allatotropin (AT), a neuropeptide originally isolated from the brain of the Lepidoptera Manduca sexta based on its ability to stimulate the synthesis of juvenile hormones (JHs) (Kataoka et al., 1989), has also been isolated and characterized in several other insect species (Abdel-latief et al., 2003, Paemen et al., 1991, Park et al., 2002, Scheng et al., 2007, Truesdell et al., 2000, Veenstra and Costes, 1999) and even in some other invertebrate groups (Elekonich and Horodyski, 2003, Veenstra, 2010), both in nervous as well as in epithelial tissues (Riccillo and Ronderos, 2010, Santini and Ronderos, 2009a, Santini and Ronderos, 2009b, Sterkel et al., 2010). Despite the function as a JHs regulator, as other many peptides, AT has proved to be pleiotropic acting as a cardioaccelerator (Koladich et al., 2002, Rudwall et al., 2000, Sterkel et al., 2010, Veenstra et al., 1994), inhibiting ion transport throughout epithelia (Lee et al., 1998), and also acting as a myoestimulator at the level of the digestive system in several insect species (Duve et al., 1999, Duve et al., 2000, Matthews et al., 2007, Santini and Ronderos, 2007, Sterkel et al., 2010). Indeed, a new activity controlling the release of digestive enzymes was recently described in insects (Lwalaba et al., 2009).

On the basis of the multiplicity of functions described for this peptide, including a so specific one for insects (JHs synthesis regulation), and the probability of that this function could not be primitive, we decide to analyze the expression of AT in two groups of Turbellaria (Catenulida, Macrostomida), and its probable functional relationship with muscle tissues.

Section snippets

Animals

Specimens of free-living turbellarian Macrostomum sp. (Macrostomida) were collected at a rainwater pond in Pereyra Iraola Park (34°51′S; 58°03′W), while specimens of Stenostomum sp. (Catenulida) were collected at another rainwater pond at Berisso (34°57′S; 57°48′W), both localities situated near to the city of La Plata (Buenos Aires Province, Argentina). The specimens were obtained during summer and autumn 2010 and were maintained in the water of origin under a 12:12 h light/dark period until

Results

The analysis reveals the presence of immunoreactive cells in both groups of free living flatworms under study: Catenulida (Stenostomum sp.) and Macrostomida (Macrostomum sp.). The omission of the primary antibody against A. aegypti AT abolished the labeling, and the preadsorption of the primary antibody with the immunizing peptide clearly diminished the staining (data not shown).

Discussion

Our results show the expression of an AT-like peptide in both groups of free living Turbellaria analyzed. The peptide is present in cells resembling neurons, and distributed in different regions of the body of the flatworms. The simultaneous analysis of the expression of the peptide with phalloidin, suggests that the neurons producing this peptide have a functional relationship with muscle fibers, particularly at the level of the pharynx in the two turbellarian groups. Indeed, in Catenulida, in

Acknowledgements

The authors wish to thank Dr. Fernando G. Noriega (Florida International University Florida, USA) for generously supplying us with Allatotropin and Allatotropin-antibody and Mr. J. Alonso for the assistance in the field work. This study was financed with founds from the PICT 01287 (SECyT – Argentina).

References (46)

  • M. Reuter et al.

    An endocrine brain? The pattern of FMRF-amide immunoreactivity in Acoela (Plathelminthes)

    Tissue Cell

    (1998)
  • M. Reuter et al.

    Organization of the nervous system in the Acoela: an immunocytochemical study

    Tissue Cell

    (2001)
  • F.L. Riccillo et al.

    Allatotropin expression during the development of the fourth instar larvae of the kissing-bug Triatoma infestans (Klüg)

    Tissue Cell

    (2010)
  • M.S. Santini et al.

    Allatotropin-like peptide in Malpighian tubules: Insect renal tubules as an autonomous endocrine organ

    Gen. Comp. Endocrinol.

    (2009)
  • M. Sterkel et al.

    Cardioacceleratory and myostimulatory activity of allatotropin in Triatoma infestans (Klüg)

    Comp. Biochem. Physiol. A

    (2010)
  • P.F. Truesdell et al.

    Molecular characterization of a cDNA from the true armyworm Pseudaletia unipuncta encoding Manduca sexta allatotropin peptide

    Insect Biochem. Mol. Biol.

    (2000)
  • K. Ukena et al.

    A novel gut tetradecapeptide isolated from the earthworm, Eisenia foetida

    Peptides

    (1995)
  • J.A. Veenstra

    Neurohormones and neuropeptides encoded by the genome of Lottia gigantea, with reference to other mollusks and insects

    Gen. Comp. Endocrinol.

    (2010)
  • J.A. Veenstra et al.

    Isolation and characterization of a peptide and its cDNA from the mosquito Aedes aegypti related to Manduca sexta allatotropin

    Peptides

    (1999)
  • M.C. Wikgren et al.

    Neuropeptides in a microturbellarian whole mount immunocytochemistry

    Peptides

    (1985)
  • H. Duve et al.

    Regulation of lepidopteran foregut movement by allatostatins and allatotropin from the frontal ganglion

    J. Comp. Neurol.

    (1999)
  • H. Duve et al.

    Triple co-localisation of two types of allatostatin and an allatotropin in the frontal ganglion of the lepidopteran Lacanobia oleracea (Noctuidae): innervation and action on the foregut

    Cell Tissue Res.

    (2000)
  • B. Egger et al.

    To be or not to be a flatworm: the acoel controversy

    PLoS ONE

    (2009)
  • Cited by (0)

    View full text