A Zebrafish and Mouse Model for Selective Pruritus Via Direct Activation of TRPA1

Overview

Journal Elife

Specialty Biology

Date 2018 Mar 22

PMID 29561265

Citations 26

Authors

Kali Esancy

Logan Condon

Jing Feng

Corinna Kimball

Andrew Curtright

Ajay Dhaka

Affiliations

Soon will be listed here.

Abstract

Little is known about the capacity of lower vertebrates to experience itch. A screen of itch-inducing compounds (pruritogens) in zebrafish larvae yielded a single pruritogen, the TLR7 agonist imiquimod, that elicited a somatosensory neuron response. Imiquimod induced itch-like behaviors in zebrafish distinct from those induced by the noxious TRPA1 agonist, allyl isothiocyanate. In the zebrafish, imiquimod-evoked somatosensory neuronal responses and behaviors were entirely dependent upon TRPA1, while in the mouse TRPA1 was required for the direct activation of somatosensory neurons and partially responsible for behaviors elicited by this pruritogen. Imiquimod was found to be a direct but weak TRPA1 agonist that activated a subset of TRPA1 expressing neurons. Imiquimod-responsive TRPA1 expressing neurons were significantly more sensitive to noxious stimuli than other TRPA1 expressing neurons. Together, these results suggest a model for selective itch via activation of a specialized subpopulation of somatosensory neurons with a heightened sensitivity to noxious stimuli.

Citing Articles

Position-independent functional refinement within the vagus motor topographic map.

Kaneko T, Boulanger-Weill J, Isabella A, Moens C Cell Rep. 2024; 43(10):114740.

PMID: 39325616 PMC: 11676005. DOI: 10.1016/j.celrep.2024.114740.

Single-Cell Analysis of Rohon-Beard Neurons Implicates Fgf Signaling in Axon Maintenance and Cell Survival.

Tuttle A, Miller L, Royer L, Wen H, Kelly J, Calistri N J Neurosci. 2024; 44(16).

PMID: 38423763 PMC: 11026351. DOI: 10.1523/JNEUROSCI.1600-23.2024.

Site-Specific Transient Receptor Potential Channel Mechanisms and Their Characteristics for Targeted Chronic Itch Treatment.

Go E, Lee J, Kim Y, Park C Biomolecules. 2024; 14(1).

PMID: 38254707 PMC: 10813675. DOI: 10.3390/biom14010107.

Position-independent functional refinement within the vagus motor topographic map.

Kaneko T, Boulanger-Weill J, Isabella A, Moens C bioRxiv. 2023; .

PMID: 37745606 PMC: 10515832. DOI: 10.1101/2023.09.11.557289.

Heterocyclic chalcone ()-1-(2-hydroxy-3,4,6-trimethoxyphenyl)-3-(thiophen-2-yl) prop-2-en-1-one derived from a natural product with antinociceptive, anti-inflammatory, and hypoglycemic effect in adult zebrafish.

Kueirislene Amancio Ferreira M, Freitas W, Barbosa I, da Rocha M, Wlisses da Silva A, de Lima Reboucas E 3 Biotech. 2023; 13(8):276.

PMID: 37457871 PMC: 10349009. DOI: 10.1007/s13205-023-03696-8.

References

Cruz-Orengo L, Dhaka A, Heuermann R, Young T, Montana M, Cavanaugh E . Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1. Mol Pain. 2008; 4:30. PMC: 2515828. DOI: 10.1186/1744-8069-4-30. View

Hojland C, Andersen H, Poulsen J, Arendt-Nielsen L, Gazerani P . A human surrogate model of itch utilizing the TRPA1 agonist trans-cinnamaldehyde. Acta Derm Venereol. 2015; 95(7):798-803. DOI: 10.2340/00015555-2103. View

Delius J . Preening and associated comfort behavior in birds. Ann N Y Acad Sci. 1988; 525:40-55. DOI: 10.1111/j.1749-6632.1988.tb38594.x. View

Usoskin D, Furlan A, Islam S, Abdo H, Lonnerberg P, Lou D . Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci. 2014; 18(1):145-53. DOI: 10.1038/nn.3881. View

Hornung V, Guenthner-Biller M, Bourquin C, Ablasser A, Schlee M, Uematsu S . Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med. 2005; 11(3):263-70. DOI: 10.1038/nm1191. View

Bautista D, Wilson S, Hoon M . Why we scratch an itch: the molecules, cells and circuits of itch. Nat Neurosci. 2014; 17(2):175-82. PMC: 4364402. DOI: 10.1038/nn.3619. View

Roberson D, Gudes S, Sprague J, Patoski H, Robson V, Blasl F . Activity-dependent silencing reveals functionally distinct itch-generating sensory neurons. Nat Neurosci. 2013; 16(7):910-8. PMC: 3695070. DOI: 10.1038/nn.3404. View

Shimada S, LaMotte R . Behavioral differentiation between itch and pain in mouse. Pain. 2008; 139(3):681-687. PMC: 2723192. DOI: 10.1016/j.pain.2008.08.002. View

Kimura Y, Hisano Y, Kawahara A, Higashijima S . Efficient generation of knock-in transgenic zebrafish carrying reporter/driver genes by CRISPR/Cas9-mediated genome engineering. Sci Rep. 2014; 4:6545. PMC: 4189020. DOI: 10.1038/srep06545. View

10.

Kim S, Park G, Kim D, Lee J, Min H, Wall E . Analysis of cellular and behavioral responses to imiquimod reveals a unique itch pathway in transient receptor potential vanilloid 1 (TRPV1)-expressing neurons. Proc Natl Acad Sci U S A. 2011; 108(8):3371-6. PMC: 3044410. DOI: 10.1073/pnas.1019755108. View

11.

Peitsaro N, Sundvik M, Anichtchik O, Kaslin J, Panula P . Identification of zebrafish histamine H1, H2 and H3 receptors and effects of histaminergic ligands on behavior. Biochem Pharmacol. 2007; 73(8):1205-14. DOI: 10.1016/j.bcp.2007.01.014. View

12.

Akiyama T, Carstens M, Carstens E . Differential itch- and pain-related behavioral responses and µ-opoid modulation in mice. Acta Derm Venereol. 2010; 90(6):575-81. DOI: 10.2340/00015555-0962. View

13.

Pei S, Liu L, Zhong Z, Wang H, Lin S, Shang J . Risk of prenatal depression and stress treatment: alteration on serotonin system of offspring through exposure to Fluoxetine. Sci Rep. 2016; 6:33822. PMC: 5050550. DOI: 10.1038/srep33822. View

14.

Tsujii K, Andoh T, Ui H, Lee J, Kuraishi Y . Involvement of Tryptase and Proteinase-Activated Receptor-2 in Spontaneous Itch-Associated Response in Mice With Atopy-like Dermatitis. J Pharmacol Sci. 2009; 109(3):388-95. DOI: 10.1254/jphs.08332fp. View

15.

Sikand P, Shimada S, Green B, LaMotte R . Similar itch and nociceptive sensations evoked by punctate cutaneous application of capsaicin, histamine and cowhage. Pain. 2009; 144(1-2):66-75. PMC: 2694489. DOI: 10.1016/j.pain.2009.03.001. View

16.

Gau P, Poon J, Ufret-Vincenty C, Snelson C, Gordon S, Raible D . The zebrafish ortholog of TRPV1 is required for heat-induced locomotion. J Neurosci. 2013; 33(12):5249-60. PMC: 3893356. DOI: 10.1523/JNEUROSCI.5403-12.2013. View

17.

Schon M, Schon M . Imiquimod: mode of action. Br J Dermatol. 2007; 157 Suppl 2:8-13. DOI: 10.1111/j.1365-2133.2007.08265.x. View

18.

Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T . Stages of embryonic development of the zebrafish. Dev Dyn. 1995; 203(3):253-310. DOI: 10.1002/aja.1002030302. View

19.

Liu S, Feng J, Luo J, Yang P, Brett T, Hu H . Eact, a small molecule activator of TMEM16A, activates TRPV1 and elicits pain- and itch-related behaviours. Br J Pharmacol. 2016; 173(7):1208-18. PMC: 4941126. DOI: 10.1111/bph.13420. View

20.

Liu Q, Tang Z, Surdenikova L, Kim S, Patel K, Kim A . Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009; 139(7):1353-65. PMC: 2989405. DOI: 10.1016/j.cell.2009.11.034. View