Endocannabinoid-Dependent LTD in a Nociceptive Synapse Requires Activation of a Presynaptic TRPV-Like Receptor

Yuan, Sharleen; Burrell, Brian D.

doi:10.1152/jn.00491.2010

Cited by 40 publications

(93 citation statements)

References 81 publications

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“…Finally, presynaptic, but not postsynaptic, intracellular injection of capsazepine blocked both low-frequency stimulation-induced and 2-AG-induced LTD, indicating that presynaptic TRPV-type receptors mediate LTD at the N-to-L synapse. Collectively, these findings indicate that low-frequency stimulation of T neurons stimulates postsynaptic synthesis of 2-AG or a 2-AG-like molecule in L neurons, which then acts in a retrograde manner to inhibit heterosynaptic neurotransmitter release by N neurons via a TRPV-type-receptor-mediated mechanism [127].…”

Section: Review Evolution and Comparative Neurobiology M R Elphickmentioning

confidence: 80%

“…Nevertheless, binding studies using radiolabelled cannabinoids have revealed the presence of putative binding sites in a variety of arthropod species [78], although identification of membrane proteins that bind cannabinoids has yet to be accomplished for any arthropod species. Evidence that TRPV-type ion channels mediate effects of endocannabinoids in the nervous system of the leech H. medicinalis [127] points to these proteins as potential endocannabinoid receptors in arthropods. It is noteworthy that the prototype for the TRP ion channel family was first discovered in Drosophila as a result of molecular analysis of the transient receptor potential (trp) mutant that has a defective phototransduction mechanism [136].…”

Section: Review Evolution and Comparative Neurobiology M R Elphickmentioning

confidence: 99%

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The evolution and comparative neurobiology of endocannabinoid signalling

Elphick

2012

Phil. Trans. R. Soc. B

153

137

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CB 1 -and CB 2 -type cannabinoid receptors mediate effects of the endocannabinoids 2-arachidonoylglycerol (2-AG) and anandamide in mammals. In canonical endocannabinoid-mediated synaptic plasticity, 2-AG is generated postsynaptically by diacylglycerol lipase alpha and acts via presynaptic CB 1 -type cannabinoid receptors to inhibit neurotransmitter release. Electrophysiological studies on lampreys indicate that this retrograde signalling mechanism occurs throughout the vertebrates, whereas system-level studies point to conserved roles for endocannabinoid signalling in neural mechanisms of learning and control of locomotor activity and feeding. CB 1 /CB 2 -type receptors originated in a common ancestor of extant chordates, and in the sea squirt Ciona intestinalis a CB 1 / CB 2 -type receptor is targeted to axons, indicative of an ancient role for cannabinoid receptors as axonal regulators of neuronal signalling. Although CB 1 /CB 2 -type receptors are unique to chordates, enzymes involved in biosynthesis/inactivation of endocannabinoids occur throughout the animal kingdom. Accordingly, non-CB 1 /CB 2 -mediated mechanisms of endocannabinoid signalling have been postulated. For example, there is evidence that 2-AG mediates retrograde signalling at synapses in the nervous system of the leech Hirudo medicinalis by activating presynaptic transient receptor potential vanilloid-type ion channels. Thus, postsynaptic synthesis of 2-AG or anandamide may be a phylogenetically widespread phenomenon, and a variety of proteins may have evolved as presynaptic (or postsynaptic) receptors for endocannabinoids.

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Section: Review Evolution and Comparative Neurobiology M R Elphickmentioning

confidence: 80%

Section: Review Evolution and Comparative Neurobiology M R Elphickmentioning

confidence: 99%

The evolution and comparative neurobiology of endocannabinoid signalling

Elphick

2012

Phil. Trans. R. Soc. B

153

137

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“…CNQX has been successfully used in the leech to block glutamatergic transmission within the CNS (Wessel et al, 1999;Li and Burrell, 2008;Yuan and Burrell, 2010). Unlike the situation with capsaicin, CNQX did not block the AITC-induced activation of the P cells ( Fig.…”

Section: Responses To Aitc In Other Sensory Cellsmentioning

confidence: 92%

Physiological, pharmacological, and behavioral evidence for a TRPA1 channel that can elicit defensive responses in the medicinal leech

Summers

Wang

Hanten

et al. 2015

Journal of Experimental Biology

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Transient receptor potential ankyrin subtype 1 (TRPA1) channels are chemosensitive to compounds such as allyl isothiocyanate (AITC, the active component of mustard oil) and other reactive electrophiles and may also be thermodetectors in many animal phyla. In this study, we provide the first pharmacological evidence of a putative TRPA1-like channel in the medicinal leech. The leech's polymodal nociceptive neuron was activated by both peripheral and central application of the TRPA1 agonist AITC in a concentration-dependent manner. Responses to AITC were inhibited by the selective TRPA1 antagonist HC030031, but also by the TRPV1 antagonist SB366791. Other TRPA1 activators -N-methylmaleimide (NMM) and cinnamaldehyde (CIN) -also activated this nociceptive neuron, although HC030031 only inhibited the effects of NMM. The polymodal nociceptive neurons responded to moderately cold thermal stimuli (<17°C) and these responses were blocked by HC030031. AITC sensitivity was also found in the pressure-sensitive sensory neurons and was blocked by HC030031, but not by SB366791. AITC elicited a nocifensive withdrawal of the posterior sucker in a concentration-dependent manner that could be attenuated with HC030031. Peripheral application of AITC in vivo also produced swimming-like behavior that was attenuated by HC030031. These results suggest the presence of a TRPA1-like channel in the medicinal leech nervous system that responds to cold temperatures and may interact with the leech TRPV-like channel.

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“…To further investigate the activation of the lP cells to peripherally applied capsaicin, the AMPA receptor antagonist CNQX (50 μmol l −1 ) was applied to the CNS through bath application prior to peripheral application of 100 μmol l −1 capsaicin. CNQX has been used previously in the leech to block synaptic transmission in the CNS (Wessel et al, 1999;Li and Burrell, 2008;Yuan and Burrell, 2010). CNQX blocked the capsaicin-induced activation of the lP cell ( Fig.…”

mentioning

confidence: 92%

Physiological and behavioral evidence of a capsaicin sensitive TRPV-like channel in the medicinal leech

Summers

Holec

Burrell

2014

Journal of Experimental Biology

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Transient receptor potential vanilloid (TRPV) channels are found throughout the animal kingdom, where they play an important role in sensory transduction. In this study, we combined physiological studies with in vivo behavioral experiments to examine the presence of a putative TRPV-like receptor in the medicinal leech, building upon earlier studies in this lophotrochozoan invertebrate. The leech polymodal nociceptive neuron was activated by both peripheral and central application of the TRPV1-activator capsaicin in a concentration-dependent manner, with 100 μmol l −1 being the lowest effective concentration. Responses to capsaicin were inhibited by the selective TRPV1 antagonist SB366791. The polymodal nociceptive neuron also responded to noxious thermal stimuli (>40°C), and this response was also blocked by SB366791. Capsaicin sensitivity was selective to the polymodal nociceptor with no direct response being elicited in the mechanical nociceptive neuron or in the nonnociceptive touch-or pressure-sensitive neurons. Capsaicin also elicited nocifensive behavioral responses (withdrawals and locomotion) in a concentration-dependent manner, and these behavioral responses were significantly attenuated with SB366791. These results suggest the presence of a capsaicin-sensitive TRPVlike channel in the medicinal leech central nervous system and are relevant to the evolution of nociceptive signaling. KEY WORDS: Leech, TRPV, Invertebrate, Nociception INTRODUCTIONTransient receptor potential (TRP) channels are a diverse class of non-specific cation channels that are found throughout the animal kingdom (Damann et al., 2008). TRP channels are typically associated with sensory transduction and are often polymodal, such as the mammalian TRP-vanilloid 1 (TRPV1) channel, which responds to noxious thermal (>42°C), mechanical and chemical (low pH, capsaicin) stimuli (Szallasi and Blumberg, 1999). Capsaicin sensitivity varies greatly throughout metazoans, with mammals displaying the greatest response to capsaicin. Birds, once thought to be capsaicin insensitive, have been shown to respond to capsaicin at increased concentrations (30 μmol l −1 ) compared with mammals (Kirifides et al., 2004). Even among mammals, capsaicin sensitivity varies greatly between species, and this variance is further complicated by ontogentic shifts in capsaicin sensitivity within specific strains of mice (Holzer, 1991). Invertebrate sensitivity to capsaicin is no less complicated because ecdysozoans, such as Drosophila (Vriens et al., 2004) and Caenorhabditis elegans (Tobin RESEARCH ARTICLECenter for Brain and Behavior Research, Division of Basic Biomedical Sciences, Sanford, School of Medicine, University of South Dakota, Vermillion, SD 57069, USA. *Author for correspondence (bburrell@usd.edu)Received 23 June 2014; Accepted 7 October 2014 et al., 2002), are reported to be capsaicin insensitive, whereas lophotrochozoans, specifically the gastropod Megalobulimus (KalilGaspar et al., 2007) and the medicinal leech (Hirudo verbana, Carena 1820) (Pasto...

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Endocannabinoid-Dependent LTD in a Nociceptive Synapse Requires Activation of a Presynaptic TRPV-Like Receptor

Cited by 40 publications

References 81 publications

The evolution and comparative neurobiology of endocannabinoid signalling

The evolution and comparative neurobiology of endocannabinoid signalling

Physiological, pharmacological, and behavioral evidence for a TRPA1 channel that can elicit defensive responses in the medicinal leech

Physiological and behavioral evidence of a capsaicin sensitive TRPV-like channel in the medicinal leech

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