Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates
In humans, intradermal administration of β-alanine (ALA) and bovine adrenal medulla peptide 8–22 (BAM8-22) evokes the sensation of itch. Currently, it is unknown which human dorsal root ganglion (DRG) neurons express the receptors of these pruritogens, MRGPRD and MRGPRX1, respectively, and which cut...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/64506 |
| _version_ | 1811202670880358400 |
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| author | Amanda Klein Hans Jürgen Solinski Nathalie M Malewicz Hada Fong-ha Ieong Elizabeth I Sypek Steven G Shimada Timothy V Hartke Matthew Wooten Gang Wu Xinzhong Dong Mark A Hoon Robert H LaMotte Matthias Ringkamp |
| author_facet | Amanda Klein Hans Jürgen Solinski Nathalie M Malewicz Hada Fong-ha Ieong Elizabeth I Sypek Steven G Shimada Timothy V Hartke Matthew Wooten Gang Wu Xinzhong Dong Mark A Hoon Robert H LaMotte Matthias Ringkamp |
| author_sort | Amanda Klein |
| collection | DOAJ |
| description | In humans, intradermal administration of β-alanine (ALA) and bovine adrenal medulla peptide 8–22 (BAM8-22) evokes the sensation of itch. Currently, it is unknown which human dorsal root ganglion (DRG) neurons express the receptors of these pruritogens, MRGPRD and MRGPRX1, respectively, and which cutaneous afferents these pruritogens activate in primate. In situ hybridization studies revealed that MRGPRD and MRGPRX1 are co-expressed in a subpopulation of TRPV1+ human DRG neurons. In electrophysiological recordings in nonhuman primates (Macaca nemestrina), subtypes of polymodal C-fiber nociceptors are preferentially activated by ALA and BAM8-22, with significant overlap. When pruritogens ALA, BAM8-22, and histamine, which activate different subclasses of C-fiber afferents, are administered in combination, human volunteers report itch and nociceptive sensations similar to those induced by a single pruritogen. Our results provide evidence for differences in pruriceptive processing between primates and rodents, and do not support the spatial contrast theory of coding of itch and pain. |
| first_indexed | 2024-04-12T02:42:33Z |
| format | Article |
| id | doaj.art-e6aba7ebcd4b4ee18d4d4f7f6c1487b1 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:42:33Z |
| publishDate | 2021-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e6aba7ebcd4b4ee18d4d4f7f6c1487b12022-12-22T03:51:16ZengeLife Sciences Publications LtdeLife2050-084X2021-04-011010.7554/eLife.64506Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primatesAmanda Klein0https://orcid.org/0000-0002-3433-2180Hans Jürgen Solinski1https://orcid.org/0000-0001-6606-3731Nathalie M Malewicz2https://orcid.org/0000-0002-9045-203XHada Fong-ha Ieong3https://orcid.org/0000-0002-3550-8408Elizabeth I Sypek4https://orcid.org/0000-0001-6904-2426Steven G Shimada5https://orcid.org/0000-0001-6357-0017Timothy V Hartke6https://orcid.org/0000-0002-1329-3418Matthew Wooten7https://orcid.org/0000-0001-8629-9899Gang Wu8https://orcid.org/0000-0002-6540-4407Xinzhong Dong9https://orcid.org/0000-0002-9750-7718Mark A Hoon10https://orcid.org/0000-0002-8794-1684Robert H LaMotte11https://orcid.org/0000-0002-9079-8639Matthias Ringkamp12https://orcid.org/0000-0001-6327-0225Department of Neurosurgery, Neurosurgery Pain Research Institute, School of Medicine, Johns Hopkins University, Baltimore, United States; Department of Pharmacy Practice and Pharmaceutical Sciences, University of Minnesota, Duluth, United StatesMolecular Genetics Section, National Institute of Dental and Craniofacial Research, Bethesda, United States; Department of Experimental Pain Research, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Anesthesiology, School of Medicine, Yale University, New Haven, United States; Department of Anesthesiology, Intensive Care Medicine and Pain Management, Medical Faculty of Ruhr-University Bochum, BG University Hospital Bergmannsheil, Bochum, GermanyDepartment of Anesthesiology, School of Medicine, Yale University, New Haven, United StatesThe Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, United StatesDepartment of Anesthesiology, School of Medicine, Yale University, New Haven, United StatesDepartment of Neurosurgery, Neurosurgery Pain Research Institute, School of Medicine, Johns Hopkins University, Baltimore, United StatesDepartment of Neurosurgery, Neurosurgery Pain Research Institute, School of Medicine, Johns Hopkins University, Baltimore, United StatesDepartment of Neurosurgery, Neurosurgery Pain Research Institute, School of Medicine, Johns Hopkins University, Baltimore, United StatesThe Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, United States; Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, United StatesMolecular Genetics Section, National Institute of Dental and Craniofacial Research, Bethesda, United StatesDepartment of Anesthesiology, School of Medicine, Yale University, New Haven, United StatesDepartment of Neurosurgery, Neurosurgery Pain Research Institute, School of Medicine, Johns Hopkins University, Baltimore, United StatesIn humans, intradermal administration of β-alanine (ALA) and bovine adrenal medulla peptide 8–22 (BAM8-22) evokes the sensation of itch. Currently, it is unknown which human dorsal root ganglion (DRG) neurons express the receptors of these pruritogens, MRGPRD and MRGPRX1, respectively, and which cutaneous afferents these pruritogens activate in primate. In situ hybridization studies revealed that MRGPRD and MRGPRX1 are co-expressed in a subpopulation of TRPV1+ human DRG neurons. In electrophysiological recordings in nonhuman primates (Macaca nemestrina), subtypes of polymodal C-fiber nociceptors are preferentially activated by ALA and BAM8-22, with significant overlap. When pruritogens ALA, BAM8-22, and histamine, which activate different subclasses of C-fiber afferents, are administered in combination, human volunteers report itch and nociceptive sensations similar to those induced by a single pruritogen. Our results provide evidence for differences in pruriceptive processing between primates and rodents, and do not support the spatial contrast theory of coding of itch and pain.https://elifesciences.org/articles/64506in situ hybridizationelectrophysiologypsychophysicsitchpaincutaneous nociceptor |
| spellingShingle | Amanda Klein Hans Jürgen Solinski Nathalie M Malewicz Hada Fong-ha Ieong Elizabeth I Sypek Steven G Shimada Timothy V Hartke Matthew Wooten Gang Wu Xinzhong Dong Mark A Hoon Robert H LaMotte Matthias Ringkamp Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates eLife in situ hybridization electrophysiology psychophysics itch pain cutaneous nociceptor |
| title | Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| title_full | Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| title_fullStr | Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| title_full_unstemmed | Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| title_short | Pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| title_sort | pruriception and neuronal coding in nociceptor subtypes in human and nonhuman primates |
| topic | in situ hybridization electrophysiology psychophysics itch pain cutaneous nociceptor |
| url | https://elifesciences.org/articles/64506 |
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