HTR7 Mediates Serotonergic Acute and Chronic Itch

Neuron

Volumn 87, Issue 1, 2015, Pages 124-138

  Morita, Takeshi ^a   McClain, Shannan P ^a   Batia, Lyn M ^a   Pellegrino, Maurizio ^a   Wilson, Sarah R ^a   Kienzler, Michael A ^b   Lyman, Kyle ^b   Olsen, Anne Sofie Braun ^b   Wong, Justin F ^a   Stucky, Cheryl L ^c   Brem, Rachel B ^d,e   Bautista, Diana M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; PROTEIN HTR7; SEROTONIN RECEPTOR; SEROTONIN UPTAKE INHIBITOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; MESSENGER RNA; SEROTONIN; SEROTONIN 7 RECEPTOR; SEROTONIN AGONIST; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPA1 PROTEIN, MOUSE;

ACUTE ITCH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOPIC DERMATITIS; CAUSAL ATTRIBUTION; CHRONIC ITCH; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE SEVERITY; EXCITATION; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PRURITUS; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; SKIN NERVE; ACUTE DISEASE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHRONIC DISEASE; DBA MOUSE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL GANGLION;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; DERMATITIS, ATOPIC; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; GENE EXPRESSION PROFILING; HUMANS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; PRURITUS; RECEPTORS, SEROTONIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; SEROTONIN UPTAKE INHIBITORS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84937516283     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.05.044     Document Type: Article

References (89)

1. Abbott F.V., Hong Y., Blier P. Activation of 5-HT2A receptors potentiates pain produced by inflammatory mediators. Neuropharmacology 1996, 35:99-110.
2. Adham N., Zgombick J.M., Bard J., Branchek T.A. Functional characterization of the recombinant human 5-hydroxytryptamine7(a) receptor isoform coupled to adenylate cyclase stimulation. J. Pharmacol. Exp. Ther. 1998, 287:508-514.
3. Ahn A.H., Basbaum A.I. Tissue injury regulates serotonin 1D receptor expression: implications for the control of migraine and inflammatory pain. J. Neurosci. 2006, 26:8332-8338.
4. Akiyama T., Carstens M.I., Carstens E. Facial injections of pruritogens and algogens excite partly overlapping populations of primary and second-order trigeminal neurons in mice. J. Neurophysiol. 2010, 104:2442-2450.
5. Anjaneyulu M., Chopra K. Fluoxetine attenuates thermal hyperalgesia through 5-HT1/2 receptors in streptozotocin-induced diabetic mice. Eur. J. Pharmacol. 2004, 497:285-292.
6. Bardin L. The complex role of serotonin and 5-HT receptors in chronic pain. Behav. Pharmacol. 2011, 22:390-404.
7. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006, 124:1269-1282.
8. Bautista D.M., Wilson S.R., Hoon M.A. Why we scratch an itch: the molecules, cells and circuits of itch. Nat. Neurosci. 2014, 17:175-182.
9. Bayer H., Müller T., Myrtek D., Sorichter S., Ziegenhagen M., Norgauer J., Zissel G., Idzko M. Serotoninergic receptors on human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2007, 36:85-93.
10. Blardi P., De Lalla A., Leo A., Auteri A., Iapichino S., Di Muro A., Dell'Erba A., Castrogiovanni P. Serotonin and fluoxetine levels in plasma and platelets after fluoxetine treatment in depressive patients. J. Clin. Psychopharmacol. 2002, 22:131-136.
11. Bonnet M.-P., Marret E., Josserand J., Mercier F.J. Effect of prophylactic 5-HT3 receptor antagonists on pruritus induced by neuraxial opioids: a quantitative systematic review. Br. J. Anaesth. 2008, 101:311-319.
12. Brandt E.B., Sivaprasad U. Th2 cytokines and atopic dermatitis. J Clin Cell Immunol 2011, 2:110.
13. Brenchat A., Romero L., García M., Pujol M., Burgueño J., Torrens A., Hamon M., Baeyens J.M., Buschmann H., Zamanillo D., Vela J.M. 5-HT7 receptor activation inhibits mechanical hypersensitivity secondary to capsaicin sensitization in mice. Pain 2009, 141:239-247.
14. Brenchat A., Rocasalbas M., Zamanillo D., Hamon M., Vela J.M., Romer L. Assessment of 5-HT7 receptor agonists selectivity using nociceptive and thermoregulation tests in knockout versus wild-type mice. Adv. Pharmacol. Sci. 2012, 2012:312041.
15. Browning J., Combes B., Mayo M.J. Long-term efficacy of sertraline as a treatment for cholestatic pruritus in patients with primary biliary cirrhosis. Am. J. Gastroenterol. 2003, 98:2736-2741.
16. Brueggemann A., George M., Klau M., Beckler M., Steindl J., Behrends J.C., Fertig N. Ion channel drug discovery and research: the automated Nano-Patch-Clamp technology. Curr. Drug Discov. Technol. 2004, 1:91-96.
17. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313.
18. Cederberg J., Knight S., Svenson S., Melhus H. Itch and skin rash from chocolate during fluoxetine and sertraline treatment: case report. BMC Psychiatry 2004, 4:36.
19. Cevikbas F., Wang X., Akiyama T., Kempkes C., Savinko T., Antal A., Kukova G., Buhl T., Ikoma A., Buddenkotte J., et al. A sensory neuron-expressed IL-31 receptor mediates T helper cell-dependent itch: Involvement of TRPV1 and TRPA1. J. Allergy Clin. Immunol. 2014, 133:448-460.
20. Cho H., Yang Y.D., Lee J., Lee B., Kim T., Jang Y., Back S.K., Na H.S., Harfe B.D., Wang F., et al. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat. Neurosci. 2012, 15:1015-1021.
21. Cookson W., Liang L., Abecasis G., Moffatt M., Lathrop M. Mapping complex disease traits with global gene expression. Nat. Rev. Genet. 2009, 10:184-194.
22. FDA (2014). U.S. Food and Drug Administration/FDA Adverse Event Reporting System (2009-2014). FAERS Quarterly Data Files. Washington, DC. http://www.fda.gov/Drugs/GuidanceComplianceRegulatoryInformation/Surveillance/AdverseDrugEffects/default.htm.
23. Garibyan L., Rheingold C.G., Lerner E.A. Understanding the pathophysiology of itch. Dermatol. Ther. 2013, 26:84-91.
24. Gerhold K.A., Pellegrino M., Tsunozaki M., Morita T., Leitch D.B., Tsuruda P.R., Brem R.B., Catania K.C., Bautista D.M. The star-nosed mole reveals clues to the molecular basis of mammalian touch. PLoS ONE 2013, 8:e55001.
25. Giaever G., Nislow C. The yeast deletion collection: a decade of functional genomics. Genetics 2014, 197:451-465.
26. Glass J.D., Grossman G.H., Farnbauch L., DiNardo L. Midbrain raphe modulation of nonphotic circadian clock resetting and 5-HT release in the mammalian suprachiasmatic nucleus. J. Neurosci. 2003, 23:7451-7460.
27. Green A.D., Young K.K., Lehto S.G., Smith S.B., Mogil J.S. Influence of genotype, dose and sex on pruritogen-induced scratching behavior in the mouse. Pain 2006, 124:50-58.
28. Hampton A.L., Hish G.A., Aslam M.N., Rothman E.D., Bergin I.L., Patterson K.A., Naik M., Paruchuri T., Varani J., Rush H.G. Progression of ulcerative dermatitis lesions in C57BL/6Crl mice and the development of a scoring system for dermatitis lesions. J. Am. Assoc. Lab. Anim. Sci. 2012, 51:586-593.
29. Han L., Ma C., Liu Q., Weng H.J., Cui Y., Tang Z., Kim Y., Nie H., Qu L., Patel K.N., et al. A subpopulation of nociceptors specifically linked to itch. Nat. Neurosci. 2013, 16:174-182.
30. Hedlund P.B. The 5-HT7 receptor and disorders of the nervous system: an overview. Psychopharmacology (Berl.) 2009, 206:345-354.
31. Hedlund P.B., Danielson P.E., Thomas E.A., Slanina K., Carson M.J., Sutcliffe J.G. No hypothermic response to serotonin in 5-HT7 receptor knockout mice. Proc. Natl. Acad. Sci. USA 2003, 100:1375-1380.
32. Hoon M.A. Molecular dissection of itch. Curr. Opin. Neurobiol. 2015, 34C:61-66.
33. Huang J., Li G., Xiang J., Yin D., Chi R. Immunohistochemical study of serotonin in lesions of chronic eczema. Int. J. Dermatol. 2004, 43:723-726.
34. Idzko M., Panther E., Stratz C., Müller T., Bayer H., Zissel G., Dürk T., Sorichter S., Di Virgilio F., Geissler M., et al. The serotoninergic receptors of human dendritic cells: identification and coupling to cytokine release. J. Immunol. 2004, 172:6011-6019.
35. Imamachi N., Park G.H., Lee H., Anderson D.J., Simon M.I., Basbaum A.I., Han S.K. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc. Natl. Acad. Sci. USA 2009, 106:11330-11335.
36. Jørgensen H.S. Studies on the neuroendocrine role of serotonin. Dan. Med. Bull. 2007, 54:266-288.
37. Julius D., Basbaum A.I. Molecular mechanisms of nociception. Nature 2001, 413:203-210.
38. Kalz F., Fekete Z. Studies on the mechanism of the white response and of the delayed blanch phenomenon in atopic subjects by means of Coomassie blue. J. Invest. Dermatol. 1960, 35:135-140.
39. Karai L., Brown D.C., Mannes A.J., Connelly S.T., Brown J., Gandal M., Wellisch O.M., Neubert J.K., Olah Z., Iadarola M.J. Deletion of vanilloid receptor 1-expressing primary afferent neurons for pain control. J. Clin. Invest. 2004, 113:1344-1352.
40. Kayser V., Elfassi I.E., Aubel B., Melfort M., Julius D., Gingrich J.A., Hamon M., Bourgoin S. Mechanical, thermal and formalin-induced nociception is differentially altered in 5-HT1A-/-, 5-HT1B-/-, 5-HT2A-/-, 5-HT3A-/- and 5-HTT-/- knock-out male mice. Pain 2007, 130:235-248.
41. Kerr P.G., Argiles A., Mion C. Whole blood serotonin levels are markedly elevated in patients on dialytic therapy. Am. J. Nephrol. 1992, 12:14-18.
42. Kim J.J., Bridle B.W., Ghia J.E., Wang H., Syed S.N., Manocha M.M., Rengasamy P., Shajib M.S., Wan Y., Hedlund P.B., Khan W.I. Targeted inhibition of serotonin type 7 (5-HT7) receptor function modulates immune responses and reduces the severity of intestinal inflammation. J. Immunol. 2013, 190:4795-4804.
43. Kuraishi Y., Nagasawa T., Hayashi K., Satoh M. Scratching behavior induced by pruritogenic but not algesiogenic agents in mice. Eur. J. Pharmacol. 1995, 275:229-233.
44. Kuraishi Y., Yamaguchi T., Miyamoto T. Itch-scratch responses induced by opioids through central mu opioid receptors in mice. J. Biomed. Sci. 2000, 7:248-252.
45. Kwan K.Y., Glazer J.M., Corey D.P., Rice F.L., Stucky C.L. TRPA1 modulates mechanotransduction in cutaneous sensory neurons. J. Neurosci. 2009, 29:4808-4819.
46. Kyriakides K., Hussain S.K., Hobbs G.J. Management of opioid-induced pruritus: a role for 5-HT3 antagonists?. Br. J. Anaesth. 1999, 82:439-441.
47. LaMotte R.H., Dong X., Ringkamp M. Sensory neurons and circuits mediating itch. Nat. Rev. Neurosci. 2014, 15:19-31.
48. Li M., Hener P., Zhang Z., Kato S., Metzger D., Chambon P. Topical vitamin D3 and low-calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proc. Natl. Acad. Sci. USA 2006, 103:11736-11741.
49. Lin S.Y., Chang W.J., Lin C.S., Huang C.Y., Wang H.F., Sun W.H. Serotonin receptor 5-HT2B mediates serotonin-induced mechanical hyperalgesia. J. Neurosci. 2011, 31:1410-1418.
50. Liu Q., Tang Z., Surdenikova L., Kim S., Patel K.N., Kim A., Ru F., Guan Y., Weng H.J., Geng Y., et al. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 2009, 139:1353-1365.
51. Liu Q., Sikand P., Ma C., Tang Z., Han L., Li Z., Sun S., LaMotte R.H., Dong X. Mechanisms of itch evoked by β-alanine. J. Neurosci. 2012, 32:14532-14537.
52. Liu B., Escalera J., Balakrishna S., Fan L., Caceres A.I., Robinson E., Sui A., McKay M.C., McAlexander M.A., Herrick C.A., Jordt S.E. TRPA1 controls inflammation and pruritogen responses in allergic contact dermatitis. FASEB J. 2013, 27:3549-3563.
53. Lovenberg T.W., Baron B.M., de Lecea L., Miller J.D., Prosser R.A., Rea M.A., Foye P.E., Racke M., Slone A.L., Siegel B.W., et al. A novel adenylyl cyclase-activating serotonin receptor (5-HT7) implicated in the regulation of mammalian circadian rhythms. Neuron 1993, 11:449-458.
54. Lundeberg L., Liang Y., Sundström E., Nordlind K., Verhofstad A., Lidén S., Johansson O. Serotonin in human allergic contact dermatitis. An immunohistochemical and high-performance liquid chromatographic study. Arch. Dermatol. Res. 1999, 291:269-274.
55. Manteniotis S., Lehmann R., Flegel C., Vogel F., Hofreuter A., Schreiner B.S., Altmüller J., Becker C., Schöbel N., Hatt H., Gisselmann G. Comprehensive RNA-Seq expression analysis of sensory ganglia with a focus on ion channels and GPCRs in Trigeminal ganglia. PLoS ONE 2013, 8:e79523.
56. Matterne U., Apfelbacher C.J., Loerbroks A., Schwarzer T., Büttner M., Ofenloch R., Diepgen T.L., Weisshaar E. Prevalence, correlates and characteristics of chronic pruritus: a population-based cross-sectional study. Acta Derm. Venereol. 2011, 91:674-679.
57. Metz M., Ständer S. Chronic pruritus-pathogenesis, clinical aspects and treatment. J. Eur. Acad. Dermatol. Venereol. 2010, 24:1249-1260.
58. Mishra S.K., Hoon M.A. The cells and circuitry for itch responses in mice. Science 2013, 340:968-971.
59. Mollanazar N.K., Smith P.K., Yosipovitch G. Mediators of chronic pruritus in atopic dermatitis: getting the itch out?. Clin. Rev. Allergy Immunol. 2015, Published online May 1, 2015. 10.1007/s12016-015-8488-5.
60. Moser H.R., Giesler G.J. Itch elicited by intradermal injection of serotonin, intracisternal injection of morphine, and their synergistic interactions in rats. Neuroscience 2014, 274:119-127.
61. Nair H.K., Hain H., Quock R.M., Philip V.M., Chesler E.J., Belknap J.K., Lariviere W.R. Genomic loci and candidate genes underlying inflammatory nociception. Pain 2011, 152:599-606.
62. Nascimento E.B., Seniuk J.G., Godin A.M., Ferreira W.C., Dutra M.B., Oliveira A.C., Bastos L.F., Fiebich B.L., Coelho M.M. Peripheral 5-HT1B and 5-HT2A receptors mediate the nociceptive response induced by 5-hydroxytryptamine in mice. Pharmacol. Biochem. Behav. 2011, 99:598-603.
63. Nojima H., Carstens E. 5-Hydroxytryptamine (5-HT)2 receptor involvement in acute 5-HT-evoked scratching but not in allergic pruritus induced by dinitrofluorobenzene in rats. J. Pharmacol. Exp. Ther. 2003, 306:245-252.
64. Nordlind K., Thorslund K., Lonne-Rahm S., Mohabbati S., Berki T., Morales M., Azmitia E.C. Expression of serotonergic receptors in psoriatic skin. Arch. Dermatol. Res. 2006, 298:99-106.
65. Oh M.H., Oh S.Y., Lu J., Lou H., Myers A.C., Zhu Z., Zheng T. TRPA1-dependent pruritus in IL-13-induced chronic atopic dermatitis. J. Immunol. 2013, 191:5371-5382.
66. Rausl A., Nordlind K., Wahlgren C.F. Pruritic and vascular responses induced by serotonin in patients with atopic dermatitis and in healthy controls. Acta Derm. Venereol. 2013, 93:277-280.
67. Roberts A.J., Krucker T., Levy C.L., Slanina K.A., Sutcliffe J.G., Hedlund P.B. Mice lacking 5-HT receptors show specific impairments in contextual learning. Eur. J. Neurosci. 2004, 19:1913-1922.
68. Ross S.E. Pain and itch: insights into the neural circuits of aversive somatosensation in health and disease. Curr. Opin. Neurobiol. 2011, 21:880-887.
69. Sannicandro T.J., Farrar M.C., Markowitz J.S. Selective serotonin reuptake inhibitor-induced rash: case report and review of the literature. Pharmacotherapy 2002, 22:516-518.
70. Santello M., Nevian T. Dysfunction of cortical dendritic integration in neuropathic pain reversed by serotoninergic neuromodulation. Neuron 2015, 86:233-246.
71. Schadt E.E. Exploiting naturally occurring DNA variation and molecular profiling data to dissect disease and drug response traits. Curr. Opin. Biotechnol. 2005, 16:647-654.
72. Schmidt M., Dubin A.E., Petrus M.J., Earley T.J., Patapoutian A. Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 2009, 64:498-509.
73. Schwörer H., Hartmann H., Ramadori G. Relief of cholestatic pruritus by a novel class of drugs: 5-hydroxytryptamine type 3 (5-HT3) receptor antagonists: effectiveness of ondansetron. Pain 1995, 61:33-37.
74. Soga F., Katoh N., Inoue T., Kishimoto S. Serotonin activates human monocytes and prevents apoptosis. J. Invest. Dermatol. 2007, 127:1947-1955.
75. Spergel J.M., Paller A.S. Atopic dermatitis and the atopic march. J. Allergy Clin. Immunol. 2003, 112:S118-S127.
76. Tang W.J., Gilman A.G. Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. Science 1991, 254:1500-1503.
77. Taylor B.A., Heiniger H.J., Meier H. Genetic analysis of resistance to cadmium-induced testicular damage in mice. Proc. Soc. Exp. Biol. Med. 1973, 143:629-633.
78. Tepper S.J., Rapoport A.M., Sheftell F.D. Mechanisms of action of the 5-HT1B/1D receptor agonists. Arch. Neurol. 2002, 59:1084-1088.
79. Van Steenwinckel J., Brisorgueil M.J., Fischer J., Vergé D., Gingrich J.A., Bourgoin S., Hamon M., Bernard R., Conrath M. Role of spinal serotonin 5-HT2A receptor in 2',3'-dideoxycytidine-induced neuropathic pain in the rat and the mouse. Pain 2008, 137:66-80.
80. Vanhoenacker P., Haegeman G., Leysen J.E. 5-HT7 receptors: current knowledge and future prospects. Trends Pharmacol. Sci. 2000, 21:70-77.
81. Warnock J.K., Morris D.W. Adverse cutaneous reactions to antidepressants. Am. J. Clin. Dermatol. 2002, 3:329-339.
82. Wilson S.R., Gerhold K.A., Bifolck-Fisher A., Liu Q., Patel K.N., Dong X., Bautista D.M. TRPA1 is required for histamine-independent, Mas-related G protein-coupled receptor-mediated itch. Nat. Neurosci. 2011, 14:595-602.
83. Wilson S.R., Nelson A.M., Batia L., Morita T., Estandian D., Owens D.M., Lumpkin E.A., Bautista D.M. The ion channel TRPA1 is required for chronic itch. J. Neurosci. 2013, 33:9283-9294.
84. Wilson S.R., Thé L., Batia L.M., Beattie K., Katibah G.E., McClain S.P., Pellegrino M., Estandian D.M., Bautista D.M. The epithelial cell-derived atopic dermatitis cytokine TSLP activates neurons to induce itch. Cell 2013, 155:285-295.
85. Xie W., Strong J.A., Ye L., Mao J.X., Zhang J.M. Knockdown of sodium channel NaV1.6 blocks mechanical pain and abnormal bursting activity of afferent neurons in inflamed sensory ganglia. Pain 2013, 154:1170-1180.
86. Yun J.W., Seo J.A., Jeong Y.S., Bae I.H., Jang W.H., Lee J., Kim S.Y., Shin S.S., Woo B.Y., Lee K.W., et al. TRPV1 antagonist can suppress the atopic dermatitis-like symptoms by accelerating skin barrier recovery. J. Dermatol. Sci. 2011, 62:8-15.
87. Zeitz K.P., Guy N., Malmberg A.B., Dirajlal S., Martin W.J., Sun L., Bonhaus D.W., Stucky C.L., Julius D., Basbaum A.I. The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J. Neurosci. 2002, 22:1010-1019.
88. Zhao Z.Q., Liu X.Y., Jeffry J., Karunarathne W.K., Li J.L., Munanairi A., Zhou X.Y., Li H., Sun Y.G., Wan L., et al. Descending control of itch transmission by the serotonergic system via 5-HT1A-facilitated GRP-GRPR signaling. Neuron 2014, 84:821-834.
89. Zylicz Z., Krajnik M., Sorge A.A., Costantini M. Paroxetine in the treatment of severe non-dermatological pruritus: a randomized, controlled trial. J. Pain Symptom Manage. 2003, 26:1105-1112.