Current Pharmaceutical Design, 2003, 8, 99-110 1
1381-6128/03 $35.00+.00 © 2003 Bentham Science Publishers Ltd.
Annelid Neuroimmune System
Christophe Lefebvre and Michel Salzet
*
Laboratoire de Neuroimmunologie des Annélides, UMR CNRS 8017, SN3, Université des
Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq Cedex, France
Abstract : Neuropeptides have been found in nervous central or immune systems of
Annelids. Since these signaling molecules are found free in the hemolymph, they are
considered as hormones. Hormonal processes along with enzymatic processing similar
to that found in vertebrates occur in annelids. Furthermore, amino acid sequence
determination of annelids precursor gene products reveals the presence of the respective
peptides that exhibit high sequence identity to their mammalian counterparts.
Nevertheless, specific neuropeptides to annelids or invertebrates have also been in these
animals. These peptides are flanked by potential proteolytic signal sites for the various
known enzymes confirming that annelids neuropeptide precursors are processed in a
similar manner to that described in mammals i.e. implicating prohormone convertase
enzymes.
1. INTRODUCTION
Neuropeptides are widespread and play a major role in
the animal kingdom, including in protozoa. The similar
amino acid sequences of some of the neuropeptides, i.e.,
oxytocin/vasopressin, angiotensins, in vertebrates and in
invertebrates demonstrate that they are stable and old in
evolutionary terms. These signaling peptides seem to have
appeared before that of a primitive nervous system,
suggesting that they were first implicated in intercellular
communication [1]. Therefore, they may have evolved from
a small number of signaling proteins encoded by ancestral
genes that have been conserved and amplified over time [1].
2. WHAT CONSTITUTES A NEUROENDOCRINE
SYSTEM?
In vertebrates, this system is based on chemical signaling
between neural and endocrine structures. Final outcomes
may be realized via the chemical messengers traveling from
circulatory conduits to their specific target sites. This
process may, in part, rely on neurosecretion of the signaling
molecules [2]. The complexity of this system can be
visualized quickly when one considers its operating
regulations that result from both classical neurotransmitters,
cytokines, growth factors and hormones neuroendocrine,
autocrine and paracrine communications. Apart from a
neuroendocrine system also exists a neuroimmune
communication, which consists to a reciprocal signaling
between neuroendocrine and immune cells which use the
same molecules to coordinate their activity, i.e.,
adrenocorticotropin ACTH [3]. We have recently
*Address correspondence to this author at the Laboratoire de
Neuroimmunologie des Annélides, UMR CNRS 8017, SN3, Université des
Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq Cedex,
France; E-mail: michel.salzet@univ-lillel.fr
demonstrated that neurovascular regulation [4] of
neurosecretion occurs in rat median eminence fragments via a
nitric oxide mediated process [5]. Thus, our concept of a
neuroendocrine system is constantly growing given its
complexity but may be simply summarized as the result of
bi-directional communications between neural and endocrine
structures over a distance greater than that occurring by
synaptic communication.
3. DO ANNELIDS HAVE A NEUROENDOCRINE
SYSTEM?
Annelids neural tissues do not contain anatomical correlates
of hypothalamus or pituitary. However, they possess
localized ganglionic regions rich in mammalian-like
neuroendocrine signaling molecules e.g. angiotensins [6-8],
oxytocin/vasopressin peptide family [7], opioids [9-12]
(tables 1 and 2). Furthermore, these molecules appear free in
the animals’ hemolymph, demonstrating distant signaling
[13-15] via several target tissues [15], including immune
cells [16-20]. Thus, the fact that a classical closed conduit
system to carry signaling molecules does not exist in
Annelids should not detract from an endocrine presence
because the baseline functioning of the system depends on
distance between the origin of a signal molecule and its
target tissue/receptor.
4. ARE NEUROENDOCRINE SIGNALING
MOLECULES IN ANNELIDS AND VERTEBRATES
SIMILAR?
This question represents an important aspect regarding
the existence of an Annelids neuroendocrine system. Among
the 30 neuropeptides isolated, so far, in annelids (Tables 1
and 2), the most part already sequenced are related to the
ones previously isolated in vertebrates. They can be divided
into 4 groups of signaling molecules i.e. the angiotensins,