Tension sensitivity of the heart pacemaker neurons in the isopod crustacean<i>Ligia pallasii</i>

Sakurai, Akira; Wilkens, J. L.

doi:10.1242/jeb.00050

Cited by 20 publications

(18 citation statements)

References 48 publications

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“…Thus, if the major target of CLDH is peripheral, we must postulate that feedback from the periphery is activated or modulated to trigger the observed increases in contraction frequency. That such changes in contraction frequency could result from peripheral modulation and the consequent activation of stretch feedback pathways is strongly supported by a study showing that induced stretch is able to alter contraction frequency in the isopod Ligia pallasii (Sakurai and Wilkens, 2003). Alternatively, it is possible that intrinsically released CLDH has effects different from those recorded here in response to perfusion of the peptide through the whole heart.…”

Section: Cldh Is a Powerful Cardioactive Peptide In H Americanussupporting

confidence: 64%

Identification of a calcitonin-like diuretic hormone that functions as an intrinsic modulator of the American lobster,Homarus americanus, cardiac neuromuscular system

Christie

Stevens

Bowers

et al. 2010

Journal of Experimental Biology

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SUMMARYIn insects, a family of peptides with sequence homology to the vertebrate calcitonins has been implicated in the control of diuresis, a process that includes mixing of the hemolymph. Here, we show that a member of the insect calcitonin-like diuretic hormone (CLDH) family is present in the American lobster, Homarus americanus, serving, at least in part, as a powerful modulator of cardiac output. Specifically, during an ongoing EST project, a transcript encoding a putative H. americanus CLDH precursor was identified; a full-length cDNA was subsequently cloned. In silico analyses of the deduced prepro-hormone predicted the mature structure of the encoded CLDH to be GLDLGLGRGFSGSQAAKHLMGLAAANFAGGPamide (Homam-CLDH), which is identical to a known Tribolium castaneum peptide. RT-PCR tissue profiling suggests that Homam-CLDH is broadly distributed within the lobster nervous system, including the cardiac ganglion (CG), which controls the movement of the neurogenic heart. RT-PCR analysis conducted on pacemaker neuron-and motor neuron-specific cDNAs suggests that the motor neurons are the source of the CLDH message in the CG. Perfusion of Homam-CLDH through the isolated lobster heart produced dose-dependent increases in both contraction frequency and amplitude and a dose-dependent decrease in contraction duration, with threshold concentrations for all parameters in the range 10 -11 to 10 -10 moll -1 or less, among the lowest for any peptide on this system. This report is the first documentation of a decapod CLDH, the first demonstration of CLDH bioactivity outside the Insecta, and the first detection of an intrinsic neuropeptide transcript in the crustacean CG.

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Section: Cldh Is a Powerful Cardioactive Peptide In H Americanussupporting

confidence: 64%

Identification of a calcitonin-like diuretic hormone that functions as an intrinsic modulator of the American lobster,Homarus americanus, cardiac neuromuscular system

Christie

Stevens

Bowers

et al. 2010

Journal of Experimental Biology

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“…However, at least in its simplest form, this mechanism would provide purely central feedback, operating within the CG itself. More interestingly, Sakurai and Wilkens (2003) recently reported that increasing tension of the cardiac musculature [i.e., contraction amplitude ( Fig. 12B)] exerts negative feedback effects on parameters of the motor pattern produced by the CG.…”

Section: Cardioactive Actions Of Dopaminementioning

confidence: 93%

“…Mechanistically, this kind of negative feedback from the periphery to the center could be implemented by direct mechanosensitive hyperpolarization of the motor neuron dendrites that extend into the muscle surrounding the CG ( Fig. 2B; Sakurai and Wilkens 2003;see Cooke 2002) or by a retrograde diffusible messenger (e.g., NO: see Mahadevan et al 2004). …”

Section: Cardioactive Actions Of Dopaminementioning

confidence: 99%

Modulation of an Integrated Central Pattern Generator–Effector System: Dopaminergic Regulation of Cardiac Activity in the Blue CrabCallinectes sapidus

Fort

Březina²,

Miller³

2004

Journal of Neurophysiology

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Fort, Timothy J., Vladimir Brezina, and Mark W. Miller. Modulation of an integrated central pattern generator-effector system: dopaminergic regulation of cardiac activity in the blue crab Callinectes sapidus. J Neurophysiol 92: 3455-3470, 2004; doi:10.1152/ jn.00550.2004. Theoretical studies have suggested that the output of a central pattern generator (CPG) must be matched to the properties of its peripheral effector system to ensure production of functional behavior. One way that such matching could be achieved is through coordinated central and peripheral modulation. In this study, morphological and physiological methods were used to examine the sources and actions of dopaminergic modulation in the cardiac system of the blue crab, Callinectes sapidus. Immunohistochemical localization of tyrosine hydroxylase (TH) revealed a prominent neuron in the commissural ganglion, the L-cell, that projected a large-diameter axon to the pericardial organ (PO) by an indirect and circuitous route. Within the PO, the L-cell axon gave rise to fine varicose fibers, suggesting that it releases dopamine in a neurohormonal fashion onto the heart musculature. In addition, one branch of the axon continued beyond the PO to the heart, where it innervated the anterior motor neurons and the posterior pacemaker region of the cardiac ganglion (CG). In physiological experiments, exogenous dopamine produced multiple effects on contraction and motor neuron burst parameters that corresponded to the dual central-peripheral modulation suggested by the L-cell morphology. Interestingly, parameters of the ganglionic motor output were modulated differently in the isolated CG and in a novel semiintact system where the CG remained embedded within the heart musculature. These observations suggest a critical role of feedback from the periphery to the CG and underscore the requirement for integration of peripheral (neurohormonal) actions and direct ganglionic modulation in the regulation of this exceptionally simple system.

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“…Because the heart was perfused at a constant rate, the increased delay between beats as the heart rate slowed would be expected to result in an increased stretch of the heart itself. This could in turn, via the stretch-sensitive dendrites of CG neurons (Alexandrowicz, 1932;Sakurai and Wilkens, 2003), lead to enhanced ganglionic activity and thus increased contraction amplitude. Alternatively, increased stretch might directly, via a Frank-Starling type mechanism, lead to increased contraction force.…”

Section: Modulation Of Contraction Amplitude and Durationmentioning

confidence: 99%

The peptide hormone pQDLDHVFLRFamide (crustacean myosuppressin) modulates theHomarus americanuscardiac neuromuscular system at multiple sites

Stevens

Cashman

Smith

et al. 2009

Journal of Experimental Biology

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SUMMARY pQDLDHVFLRFamide is a highly conserved crustacean neuropeptide with a structure that places it within the myosuppressin subfamily of the FMRFamide-like peptides. Despite its apparent ubiquitous conservation in decapod crustaceans, the paracrine and/or endocrine roles played by pQDLDHVFLRFamide remain largely unknown. We have examined the actions of this peptide on the cardiac neuromuscular system of the American lobster Homarus americanus using four preparations: the intact animal, the heart in vitro, the isolated cardiac ganglion (CG), and a stimulated heart muscle preparation. In the intact animal, injection of myosuppressin caused a decrease in heartbeat frequency. Perfusion of the in vitro heart with pQDLDHVFLRFamide elicited a decrease in the frequency and an increase in the amplitude of heart contractions. In the isolated CG, myosuppressin induced a hyperpolarization of the resting membrane potential of cardiac motor neurons and a decrease in the cycle frequency of their bursting. In the stimulated heart muscle preparation, pQDLDHVFLRFamide increased the amplitude of the induced contractions, suggesting that myosuppressin modulates not only the CG, but also peripheral sites. For at least the in vitro heart and the isolated CG, the effects of myosuppressin were dose-dependent (10 -9 to 10 ) consistent with the peptide serving as a circulating hormone. Although cycle frequency, a parameter directly determined by the CG, consistently decreased when pQDLDHVFLRFamide was applied to all preparation types, the magnitudes of this decrease differed, suggesting the possibility that, because myosuppressin modulates the CG and the periphery, it also alters peripheral feedback to the CG.

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Tension sensitivity of the heart pacemaker neurons in the isopod crustaceanLigia pallasii

Cited by 20 publications

References 48 publications

Identification of a calcitonin-like diuretic hormone that functions as an intrinsic modulator of the American lobster,Homarus americanus, cardiac neuromuscular system

Identification of a calcitonin-like diuretic hormone that functions as an intrinsic modulator of the American lobster,Homarus americanus, cardiac neuromuscular system

Modulation of an Integrated Central Pattern Generator–Effector System: Dopaminergic Regulation of Cardiac Activity in the Blue CrabCallinectes sapidus

The peptide hormone pQDLDHVFLRFamide (crustacean myosuppressin) modulates theHomarus americanuscardiac neuromuscular system at multiple sites

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