Smooth muscle relaxation in vertebrates is regulated by a variety of neuronal signalling molecules, including neuropeptides and nitric oxide (NO). The physiology of muscle relaxation in echinoderms is of particular interest because these animals are evolutionarily more closely related to the vertebrates than to the majority of invertebrate phyla. However, whilst in vertebrates there is a clear structural and functional distinction between visceral smooth muscle and skeletal striated muscle, this does not apply to echinoderms, in which the majority of muscles, whether associated with the body wall skeleton and its appendages or with visceral organs, are made up of non-striated fibres. The mechanisms by which the nervous system controls muscle relaxation in echinoderms were, until recently, unknown. Using the cardiac stomach of the starfish Asterias rubens as a model, it has been established that the NO-cGMP signalling pathway mediates relaxation. NO also causes relaxation of sea urchin tube feet, and NO may therefore function as a ‘universal’ muscle relaxant in echinoderms. The first neuropeptides to be identified in echinoderms were two related peptides isolated from Asterias rubens known as SALMFamide-1 (S1) and SALMFamide-2 (S2). Both S1 and S2 cause relaxation of the starfish cardiac stomach, but with S2 being approximately ten times more potent than S1. SALMFamide neuropeptides have also been isolated from sea cucumbers, in which they cause relaxation of both gut and body wall muscle. Therefore, like NO, SALMFamides may also function as ‘universal’ muscle relaxants in echinoderms. The mechanisms by which SALMFamides cause relaxation of echinoderm muscle are not known, but several candidate signal transduction pathways are discussed here. The SALMFamides do not, however, appear to act by promoting release of NO, and muscle relaxation in echinoderms is therefore probably regulated by at least two neuronal signalling systems acting in parallel. Recently, other neuropeptides that influence muscle tone have been isolated from the sea cucumber Stichopus japonicus using body wall muscle as a bioassay, but at present SALMFamide peptides are the only ones that have been found to have a direct relaxing action on echinoderm muscle. One of the Stichopus japonicus peptides (holothurin 1), however, causes a reduction in the magnitude of electrically evoked muscle contraction in Stichopus japonicus and also causes ‘softening’ of the body wall dermis, a ‘mutable connective tissue’. It seems most likely that this effect of holothurin 1 on body wall dermis is mediated by constituent muscle cells, and the concept of ‘mutable connective tissue’ in echinoderms may therefore need to be re-evaluated to incorporate the involvement of muscle, as proposed recently for the spine ligament in sea urchins.

REFERENCES

Billack
B.
,
Laskin
J. D.
,
Heck
P. T.
,
Troll
W.
,
Gallo
M. A.
,
Heck
D. E.
(
1998
).
Alterations in cholinergic signaling modulate contraction of isolated sea urchin tube feet: potential role of nitric oxide.
Biol. Bull
195
,
196
–.
Birenheide
R.
,
Tamori
M.
,
Motokawa
T.
,
Ohtani
M.
,
Iwakoshi
E.
,
Muneoka
Y.
,
Fujita
T.
,
Minakata
H.
,
Nomoto
K.
(
1998
).
Peptides controlling stiffness of connective tissue in sea cucumbers.
Biol. Bull
194
,
253
–.
Boeckxstaens
G. E.
,
Pelckmans
P. A.
(
1997
).
Nitric oxide and the non-adrenergic non-cholinergic neurotransmission.
Comp. Biochem. Physiol
118
,
925
–.
Brenner
B. M.
,
Ballermann
B. J.
,
Gunning
M. E.
,
Zeidel
M. L.
(
1990
).
Diverse biological actions of atrial natriuretic peptide.
Physiol. Rev
70
,
665
–.
Bult
H.
,
Boeckxstaens
G. E.
,
Pelckmans
P. A.
,
Jordaens
F. H.
,
Van maercke
Y. M.
,
Herman
A. G.
(
1990
).
Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter.
Nature
345
,
346
–.
Del Castillo
J.
,
Smith
D. S.
,
Vidal
A. M.
,
Sierra
C.
(
1995
).
Catch in the primary spines of the sea urchin Eucidaris tribuloides: A brief review and a new interpretation.
Biol. Bull
188
,
120
–.
Devlin
C. L.
(
2001
).
The pharmacology of-aminobutyric acid and acetylcholine receptors at the echinoderm neuromuscular junction.
J. Exp. Biol
204
,
887
–.
Díaz-Miranda
L.
,
Blanco
R. E.
,
García-Arrarás
J. E.
(
1995
).
Localization of the heptapeptide GFSKLYFamide in the seacucumber Holothuria glaberrima (Echinodermata): A light and electron microscopic study.
J. Comp. Neurol
352
,
626
–.
Díaz-Miranda
L.
,
García-Arrarás
J. E.
(
1995
).
Pharmacological action of the heptapeptide GFSKLYFamide in the muscle of the sea cucumber Holothuria glaberrima (Echinodermata).
Comp. Biochem. Physiol
110
,
171
–.
Elphick
M. R.
,
Emson
R. H.
,
Thorndyke
M. C.
(
1989
).
FMRFamide-like immunoreactivity in the nervous system of the starfish Asterias rubens.
Biol. Bull
177
,
141
–.
Elphick
M. R.
,
Green
I. C.
,
O'Shea
M.
(
1993
).
Nitric oxide synthesis and action in an invertebrate brain.
Brain Res
619
,
344
–.
Elphick
M. R.
,
Melarange
R.
(
1998
).
Nitric oxide function in an echinoderm.
Biol. Bull
194
,
260
–.
Elphick
M. R.
,
Parker
K.
,
Thorndyke
M. C.
(
1992
).
Neuropeptides in sea urchins.
Regul. Peptides
39
,
265
–.
Elphick
M. R.
,
Price
D. A.
,
Lee
T. D.
,
Thorndyke
M. C.
(
1991
).
The SALMFamides: a new family of neuropeptides isolated from an echinoderm.
Proc. R. Soc. Lond. B
243
,
121
–.
Elphick
M. R.
,
Reeve
J. R.
,
Burke
R. D.
,
Thorndyke
M. C.
(
1991
).
Isolation of the neuropeptide SALMFamide-1 from starfish using a new antiserum.
Peptides
12
,
455
–.
Florey
E.
,
Cahill
M. A.
(
1980
).
Cholineric motor control of sea urchin tube feet: evidence for chemical transmission without synapses.
J. Exp. Biol
88
,
281
–.
Florey
E.
,
Cahill
M. A.
,
Rathmayer
M.
(
1975
).
Excitatory actions of GABA and of acetylcholine in sea urchin tube feet.
Comp. Biochem. Physiol
51
,
5
–.
Garthwaite
J.
,
Southam
E.
,
Boulton
C. L.
,
Nielsen
E. B.
,
Schmidt
K.
,
Mayer
B.
(
1995
).
Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one.
Mol. Pharmac
48
,
184
–.
Goldsmith
B. A.
,
Abrams
T. W.
(
1991
).
Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase.
Proc. Natl. Acad. Sci. USA
88
,
9021
–.
Gudermann
T.
,
Schöneberg
T.
,
Schultz
G.
(
1997
).
Functional and structural complexity of signal transduction via G-protein-coupled receptors.
Annu. Rev. Neurosci
20
,
399
–.
MacFarland
R. T.
(
1995
).
Molecular aspects of cyclic GMP signalling.
Zool. Sci
12
,
151
–.
Martinez
A.
,
Riveros-Moreno
V.
,
Polak
J. M.
,
Moncada
S.
,
Seesma
P.
(
1994
).
Nitric oxide (NO) synthase immunoreactivity in the starfish Marthasterias glacialis.
Cell Tissue Res
275
,
599
–.
Melarange
R.
,
Potton
D. J.
,
Thorndyke
M. C.
,
Elphick
M. R.
(
1999
).
SALMFamide neuropeptides cause relaxation and eversion of the cardiac stomach in starfish.
Proc. R. Soc. Lond. B
266
,
1785
–.
Moncada
S.
,
Palmer
R. M. J.
,
Higgs
E. A.
(
1991
).
Nitric oxide — physiology, pathophysiology and pharmacology.
Pharmac. Rev
43
,
109
–.
Motokawa
T.
(
1984
).
Connective tissue catch in echinoderms.
Biol. Rev
59
,
255
–.
Newman
S. J.
,
Elphick
M. R.
,
Thorndyke
M. C.
(
1995
).
Tissue distribution of the SALMFamide neuropeptides S1 and S2 in the starfish Asterias rubens using novel monoclonal and polyclonal antibodies. I. Nervous and locomotory systems.
Proc. R. Soc. Lond. B
261
,
139
–.
Newman
S. J.
,
Elphick
M. R.
,
Thorndyke
M. C.
(
1995
).
Tissue distribution of the SALMFamide neuropeptides S1 and S2 in the starfish Asterias rubens using novel monoclonal and polyclonal antibodies. II. Digestive system.
Proc. R. Soc. Lond. B
261
,
187
–.
Nilsson
G. E.
,
Söderström
V.
(
1997
).
Comparative aspects on nitric oxide in brain and its role as a cerebral vasodilator.
Comp. Biochem. Physiol
118
,
949
–.
Olsson
C.
,
Holmgren
S.
(
1997
).
Nitric oxide in fish gut.
Comp. Biochem. Physiol
118
,
959
–.
O'Neill
P.
(
1989
).
Structure and mechanics of starfish body wall.
J. Exp. Biol
147
,
53
–.
Palmer
R. M. J.
,
Ferrige
A. G.
,
Moncada
S.
(
1987
).
Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor.
Nature
327
,
524
–.
Ruth
P.
,
Wang
G. X.
,
Boekhoff
I.
,
May
B.
,
Pfeifer
A.
,
Penner
R.
,
Korth
M.
,
Breer
H.
,
Hofmann
F.
(
1993
).
Transfected cGMP-dependent protein kinase suppresses calcium transients by inhibition of inositol 1,4,5-trisphosphate production.
Proc. Natl. Acad. Sci. USA
90
,
2623
–.
Schlossmann
J.
,
Ammendola
A.
,
Ashman
K.
,
Zong
X.
,
Huber
A.
,
Neubauer
G.
,
Wang
G.-X.
,
Allescher
H.-D.
,
Korth
M.
,
Wilm
M.
,
Hofmann
F.
,
Ruth
P.
(
2000
).
Regulation of intracellular calcium by a signalling complex of IRAG IP3receptor and cGMP kinase 1.
Nature
404
,
197
–.
Schrammel
A.
,
Behrends
S.
,
Schmidt
K.
,
Koesling
D.
,
Mayer
B.
(
1996
).
Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase.
Mol. Pharmac
50
,
1
–.
Singh
S.
,
Lowe
D. G.
,
Thorpe
D. S.
,
Rodriguez
H.
,
Kuang
W.-J.
,
Dangott
L. J.
,
Chinkers
M.
,
Goeddel
D. V.
,
Garbers
D. L.
(
1988
).
Membrane guanylate cyclase is a cell-surface receptor with homology to protein kinases.
Nature
334
,
708
–.
Sunahara
R. K.
,
Dessauer
C. W.
,
Gilman
A. G.
(
1996
).
Complexity and diversity of mammalian adenylyl cyclases.
Annu. Rev. Pharmac. Toxicol
36
,
461
–.
Surks
H. K.
,
Mochizuki
N.
,
Kasai
Y.
,
Georgescu
S. P.
,
Tang
M. K.
,
Ito
M.
,
Lincoln
T. M.
,
Mendelsohn
M. E.
(
1999
).
Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase I.
Science
286
,
1583
–.
Suzuki
K.
,
Satoh
Y.-I.
,
Suzuki
N.
(
1999
).
Molecular phylogenetic analysis of diverse forms of echinoderm guanylyl cyclases.
Zool. Sci
16
,
515
–.
Turcato
S.
,
Clapp
L. H.
(
1999
).
Effects of the adenylyl cyclase inhibitor SQ22536 on iloprost-induced vasorelaxation and cAMP elevation in isolated guinea-pig aorta.
Br. J. Pharmac
126
,
845
–.
Von Uexkull
J.
(
1900
).
Die Physiologie des Seeigelstachels.
Z. Biol
37
,
334
–.
Zamponi
G. W.
,
Snutch
T. P.
(
1998
).
Modulation of voltage-dependent calcium channels by G proteins.
Current Opin. Neurobiol
8
,
351
–.
This content is only available via PDF.