Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crab Cancer productus.
A club-shaped, tachykinin-immunopositive structure first described nearly two decades ago in the commissural ganglion (CoG) of three species of decapod crustaceans has remained enigmatic, as its function is unknown. Here, we use a combination of anatomical, mass spectrometric and electrophysiological techniques to address this issue in the crab Cancer productus. Immunohistochemistry using an antibody to the vertebrate tachykinin substance P shows that a homologous site exists in each CoG of this crab. Confocal microscopy reveals that its structure and organization are similar to those of known neuroendocrine organs. Based on its location in the anterior medial quadrant of the CoG, we have named this structure the anterior commissural organ (ACO). Matrix-assisted laser desorption/ionization Fourier transform mass spectrometry shows that the ACO contains the peptide APSGFLGMRamide, commonly known as Cancer borealis tachykinin-related peptide Ia (CabTRP Ia). Using the same technique, we show that CabTRP Ia is also released into the hemolymph. As no tachykinin-like labeling is seen in any of the other known neuroendocrine sites of this species (i.e. the sinus gland, the pericardial organ and the anterior cardiac plexus), the ACO is a prime candidate to be the source of CabTRP Ia present in the circulatory system. Our electrophysiological studies indicate that one target of hemolymph-borne CabTRP Ia is the foregut musculature. Here, no direct CabTRP Ia innervation is present, yet several gastric mill and pyloric muscles are nonetheless modulated by hormonally relevant concentrations of the peptide. Collectively, our findings show that the C. productus ACO is a neuroendocrine organ providing hormonal CabTRP Ia modulation to the foregut musculature. Homologous structures in other decapods are hypothesized to function similarly.
Messinger
Daniel I
DI
Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA.
Kutz
Kimberly K
KK
Le
Thuc
T
Verley
Derek R
DR
Hsu
Yun-Wei A
YW
Ngo
Christina T
CT
Cain
Shaun D
SD
Birmingham
John T
JT
Li
Lingjun
L
Christie
Andrew E
AE
D000818:Animals; D003386:Brachyura; D004594:Electrophysiology; D005453:Fluorescence; D017952:Ganglia, Invertebrate / Q000166:cytology* / Q000378:metabolism; D041981:Gastrointestinal Tract / Q000378:metabolism; D007150:Immunohistochemistry; D018613:Microscopy, Confocal; D009119:Muscle Contraction / Q000502:physiology; D009132:Muscles / Q000378:metabolism / Q000502:physiology; D009490:Neurosecretory Systems / Q000033:anatomy & histology* / Q000378:metabolism*; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; D015320:Tachykinins / Q000378:metabolism*
D015320:Tachykinins