Descending control of itch transmission by the serotonergic system via 5-HT1A-facilitated GRP-GRPR signaling

Neuron

Volumn 84, Issue 4, 2014, Pages 821-834

  Zhao, Zhong Qiu ^a   Liu, Xian Yu ^a   Jeffry, Joseph ^a   Karunarathne, W K Ajith ^a   Li, Jin Lian ^b   Munanairi, Admire ^a   Zhou, Xuan Yi ^a   Li, Hui ^a,b   Sun, Yan Gang ^a   Wan, Li ^a   Wu, Zhen Yu ^b   Kim, Seungil ^a   Huo, Fu Quan ^a   Mo, Ping ^a,c   Barry, Devin M ^a   Zhang, Chun Kui ^b   Kim, Ji Young ^a   Gautam, N ^a   Renner, Kenneth J ^d   Li, Yun Qing ^b   Chen, Zhou Feng ^a   more..

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c The Second People s Hospital of Nanhai District   (China)

^d University of South Dakota   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GASTRIN RELEASING PEPTIDE; GASTRIN RELEASING PEPTIDE RECEPTOR; SEROTONIN 1A RECEPTOR; BOMBESIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CONTROLLED STUDY; ITCH SENSATION; MALE; MOUSE; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PRURITUS; SCRATCHING; SENSATION; SEROTONINERGIC SYSTEM; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD NERVE CELL; ACTION POTENTIAL; ANIMAL; CALCIUM SIGNALING; DRUG EFFECTS; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; GASTRIN-RELEASING PEPTIDE; MALE; MICE; NEURONS; PRURITUS; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTORS, BOMBESIN; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 84918841467     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.10.003     Document Type: Article

References (65)

1. Abe K., Kato G., Katafuchi T., Tamae A., Furue H., Yoshimura M. Responses to 5-HT in morphologically identified neurons in the rat substantia gelatinosa invitro. Neuroscience 2009, 159:316-324.
2. Akiyama T., Iodi Carstens M., Carstens E. Transmitters and pathways mediating inhibition of spinal itch-signaling neurons by scratching and other counterstimuli. PLoS ONE 2011, 6:e22665.
3. Akiyama T., Tominaga M., Takamori K., Carstens M.I., Carstens E. Roles of glutamate, substance P, and gastrin-releasing peptide as spinal neurotransmitters of histaminergic and nonhistaminergic itch. Pain 2014, 155:80-92.
4. Bardin L. The complex role of serotonin and 5-HT receptors in chronic pain. Behav. Pharmacol. 2011, 22:390-404.
5. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38:1083-1152.
6. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 1984, 7:309-338.
7. Birdsall T.C. 5-Hydroxytryptophan: a clinically-effective serotonin precursor. Altern. Med. Rev. 1998, 3:271-280.
8. Björklund A., Baumgarten H.G., Rensch A. 5,7-Dihydroxytryptamine: improvement of its selectivity for serotonin neurons in the CNS by pretreatment with desipramine. J.Neurochem. 1975, 24:833-835.
9. Bouvier M. Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2001, 2:274-286.
10. Davidson S., Zhang X., Khasabov S.G., Simone D.A., Giesler G.J. Relief of itch by scratching: state-dependent inhibition of primate spinothalamic tract neurons. Nat. Neurosci. 2009, 12:544-546.
11. Dillon S.R., Sprecher C., Hammond A., Bilsborough J., Rosenfeld-Franklin M., Presnell S.R., Haugen H.S., Maurer M., Harder B., Johnston J., et al. Interleukin 31, a cytokine produced by activated Tcells, induces dermatitis in mice. Nat. Immunol. 2004, 5:752-760.
12. Ding Y.Q., Marklund U., Yuan W., Yin J., Wegman L., Ericson J., Deneris E., Johnson R.L., Chen Z.F. Lmx1b is essential for the development of serotonergic neurons. Nat. Neurosci. 2003, 6:933-938.
13. Grudt T.J., Williams J.T., Travagli R.A. Inhibition by 5-hydroxytryptamine and noradrenaline in substantia gelatinosa of guinea-pig spinal trigeminal nucleus. J.Physiol. 1995, 485:113-120.
14. Hampton L.L., Ladenheim E.E., Akeson M., Way J.M., Weber H.C., Sutliff V.E., Jensen R.T., Wine L.J., Arnheiter H., Battey J.F. Loss of bombesin-induced feeding suppression in gastrin-releasing peptide receptor-deficient mice. Proc. Natl. Acad. Sci. USA 1998, 95:3188-3192.
15. Heisler L.K., Chu H.M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., Tecott L.H. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc. Natl. Acad. Sci. USA 1998, 95:15049-15054.
16. Hoyer D., Hannon J.P., Martin G.R. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol. Biochem. Behav. 2002, 71:533-554.
17. Ikoma A., Steinhoff M., Ständer S., Yosipovitch G., Schmelz M. The neurobiology of itch. Nat. Rev. Neurosci. 2006, 7:535-547.
18. Jeffry J.A., Yu S.Q., Sikand P., Parihar A., Evans M.S., Premkumar L.S. Selective targeting of TRPV1 expressing sensory nerve terminals in the spinal cord for long lasting analgesia. PLoS ONE 2009, 4:e7021.
19. Jeffry J., Kim S., Chen Z.F. Itch signaling in the nervous system. Physiology (Bethesda) 2011, 26:286-292.
20. Jensen R.T., Battey J.F., Spindel E.R., Benya R.V. International Union of Pharmacology. LXVIII. Mammalian bombesin receptors: nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol. Rev. 2008, 60:1-42.
21. Julius D., Nathans J. Signaling by sensory receptors. Cold Spring Harb. Perspect. Biol. 2012, 4:a005991.
22. Karunarathne W.K., Giri L., Kalyanaraman V., Gautam N. Optically triggering spatiotemporally confined GPCR activity in a cell and programming neurite initiation and extension. Proc. Natl. Acad. Sci. USA 2013, 110:E1565-E1574.
23. Kim J.Y., Kim A., Zhao Z.Q., Liu X.Y., Chen Z.F. Postnatal maintenance of the 5-Ht1a-Pet1 autoregulatory loop by serotonin in the raphe nuclei of the brainstem. Mol. Brain 2014, 7:48.
24. Kroog G.S., Jensen R.T., Battey J.F. Mammalian bombesin receptors. Med. Res. Rev. 1995, 15:389-417.
25. Lagerström M.C., Rogoz K., Abrahamsen B., Persson E., Reinius B., Nordenankar K., Olund C., Smith C., Mendez J.A., Chen Z.F., et al. VGLUT2-dependent sensory neurons in the TRPV1 population regulate pain and itch. Neuron 2010, 68:529-542.
26. LaMotte R.H., Dong X., Ringkamp M. Sensory neurons and circuits mediating itch. Nat. Rev. Neurosci. 2014, 15:19-31.
27. Li J.L., Kaneko T., Shigemoto R., Mizuno N. Distribution of trigeminohypothalamic and spinohypothalamic tract neurons displaying substance P receptor-like immunoreactivity in the rat. J.Comp. Neurol. 1997, 378:508-521.
28. 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.
29. Liu X.Y., Liu Z.C., Sun Y.G., Ross M., Kim S., Tsai F.F., Li Q.F., Jeffry J., Kim J.Y., Loh H.H., Chen Z.F. Unidirectional cross-activation of GRPR by MOR1D uncouples itch and analgesia induced by opioids. Cell 2011, 147:447-458.
30. Liu X.Y., Wan L., Huo F.Q., Barry D.M., Li H., Zhao Z.Q., Chen Z.F. B-type natriuretic peptide is neither itch-specific nor functions upstream of the GRP-GRPR signaling pathway. Mol. Pain 2014, 10:4.
31. Lu Y., Perl E.R. Selective action of noradrenaline and serotonin on neurones of the spinal superficial dorsal horn in the rat. J.Physiol. 2007, 582:127-136.
32. Ma Q. Labeled lines meet and talk: population coding of somatic sensations. J.Clin. Invest. 2010, 120:3773-3778.
33. Millan M.J. Descending control of pain. Prog. Neurobiol. 2002, 66:355-474.
34. Milligan G. The prevalence, maintenance, and relevance of G protein-coupled receptor oligomerization. Mol. Pharmacol. 2013, 84:158-169.
35. Miyamoto T., Nojima H., Shinkado T., Nakahashi T., Kuraishi Y. Itch-associated response induced by experimental dry skin in mice. Jpn. J. Pharmacol. 2002, 88:285-292.
36. Mochizuki H., Tashiro M., Kano M., Sakurada Y., Itoh M., Yanai K. Imaging of central itch modulation in the human brain using positron emission tomography. Pain 2003, 105:339-346.
37. Moore G.A., McConkey D.J., Kass G.E., O'Brien P.J., Orrenius S. 2,5-Di(tert-butyl)-1,4-benzohydroquinone-a novel inhibitor of liver microsomal Ca2+ sequestration. FEBS Lett. 1987, 224:331-336.
38. Murray F.S., Weaver M.M. Effects of ipsilateral and contralateral counterirritation on experimentally produced itch in human beings. J.Comp. Physiol. Psychol. 1975, 89:819-826.
39. Nattkemper L.A., Zhao Z.Q., Nichols A.J., Papoiu A.D., Shively C.A., Chen Z.F., Yosipovitch G. Overexpression of the gastrin-releasing peptide in cutaneous nerve fibers and its receptor in the spinal cord in primates with chronic itch. J.Invest. Dermatol. 2013, 133:2489-2492.
40. O'Donohue T.L., Massari V.J., Pazoles C.J., Chronwall B.M., Shults C.W., Quirion R., Chase T.N., Moody T.W. A role for bombesin in sensory processing in the spinal cord. J.Neurosci. 1984, 4:2956-2962.
41. Ossipov M.H., Dussor G.O., Porreca F. Central modulation of pain. J.Clin. Invest. 2010, 120:3779-3787.
42. Pang Y.W., Li J.L., Nakamura K., Wu S., Kaneko T., Mizuno N. Expression of vesicular glutamate transporter 1 immunoreactivity in peripheral and central endings of trigeminal mesencephalic nucleus neurons in the rat. J.Comp. Neurol. 2006, 498:129-141.
43. Paus R., Schmelz M., Bíró T., Steinhoff M. Frontiers in pruritus research: scratching the brain for more effective itch therapy. J.Clin. Invest. 2006, 116:1174-1186.
44. Pin J.P., Neubig R., Bouvier M., Devi L., Filizola M., Javitch J.A., Lohse M.J., Milligan G., Palczewski K., Parmentier M., Spedding M. International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol. Rev. 2007, 59:5-13.
45. Prezeau L., Rives M.L., Comps-Agrar L., Maurel D., Kniazeff J., Pin J.P. Functional crosstalk between GPCRs: with or without oligomerization. Curr. Opin. Pharmacol. 2010, 10:6-13.
46. Prinster S.C., Hague C., Hall R.A. Heterodimerization of g protein-coupled receptors: specificity and functional significance. Pharmacol. Rev. 2005, 57:289-298.
47. Sorkin L.S., McAdoo D.J. Amino acids and serotonin are released into the lumbar spinal cord of the anesthetized cat following intradermal capsaicin injections. Brain Res. 1993, 607:89-98.
48. Sun Y.G., Chen Z.F. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature 2007, 448:700-703.
49. Sun Y.G., Zhao Z.Q., Meng X.L., Yin J., Liu X.Y., Chen Z.F. Cellular basis of itch sensation. Science 2009, 325:1531-1534.
50. Suzuki R., Rygh L.J., Dickenson A.H. Bad news from the brain: descending 5-HT pathways that control spinal pain processing. Trends Pharmacol. Sci. 2004, 25:613-617.
51. Takanami K., Sakamoto H., Matsuda K.I., Satoh K., Tanida T., Yamada S., Inoue K., Oti T., Sakamoto T., Kawata M. Distribution of gastrin-releasing peptide in the rat trigeminal and spinal somatosensory systems. J.Comp. Neurol. 2014, 522:1858-1873.
52. Tominaga M., Ogawa H., Takamori K. Histological characterization of cutaneous nerve fibers containing gastrin-releasing peptide in NC/Nga mice: an atopic dermatitis model. J.Invest. Dermatol. 2009, 129:2901-2905.
53. Uchizono K. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 1965, 207:642-643.
54. Walther D.J., Peter J.U., Bashammakh S., Hörtnagl H., Voits M., Fink H., Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003, 299:76.
55. Ward L., Wright E., McMahon S.B. A comparison of the effects of noxious and innocuous counterstimuli on experimentally induced itch and pain. Pain 1996, 64:129-138.
56. Yaksh T.L., Tyce G.M. Release of norepinephrine and serotonin in cat spinal cord: direct invivo evidence for the activation of descending monoamine pathways by somatic stimulation. J.Physiol. (Paris) 1981, 77:483-487.
57. Yoshimura M., Furue H. Mechanisms for the anti-nociceptive actions of the descending noradrenergic and serotonergic systems in the spinal cord. J.Pharmacol. Sci. 2006, 101:107-117.
58. Yosipovitch G., Papoiu A.D.P. What causes itch in atopic dermatitis?. Curr. Allergy Asthma Rep. 2008, 8:306-311.
59. Yosipovitch G., Duque M.I., Fast K., Dawn A.G., Coghill R.C. Scratching and noxious heat stimuli inhibit itch in humans: a psychophysical study. Br. J. Dermatol. 2007, 156:629-634.
60. Zhang Y.Q., Gao X., Ji G.C., Huang Y.L., Wu G.C., Zhao Z.Q. Expression of 5-HT1A receptor mRNA in rat lumbar spinal dorsal horn neurons after peripheral inflammation. Pain 2002, 98:287-295.
61. Zhao Z.Q., Scott M., Chiechio S., Wang J.S., Renner K.J., Gereau R.W., Johnson R.L., Deneris E.S., Chen Z.F. Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J.Neurosci. 2006, 26:12781-12788.
62. Zhao Z.Q., Chiechio S., Sun Y.G., Zhang K.H., Zhao C.S., Scott M., Johnson R.L., Deneris E.S., Renner K.J., Gereau R.W., Chen Z.F. Mice lacking central serotonergic neurons show enhanced inflammatory pain and an impaired analgesic response to antidepressant drugs. J.Neurosci. 2007, 27:6045-6053.
63. Zhao Z.Q., Gao Y.J., Sun Y.G., Zhao C.S., Gereau R.W., Chen Z.F. Central serotonergic neurons are differentially required for opioid analgesia but not for morphine tolerance or morphine reward. Proc. Natl. Acad. Sci. USA 2007, 104:14519-14524.
64. Zhao Z.-Q., Huo F.-Q., Jeffry J., Hampton L., Demehri S., Kim S., Liu X.-Y., Barry D.M., Wan L., Liu Z.-C., et al. Chronic itch development in sensory neurons requires BRAF signaling pathways. J.Clin. Invest. 2013, 123:4769-4780.
65. Zhao Z.Q., Wan L., Liu X.Y., Huo F.Q., Li H., Barry D.M., Krieger S., Kim S., Liu Z.C., Xu J., et al. Cross-Inhibition of NMBR and GRPR Signaling Maintains Normal Histaminergic Itch Transmission. J.Neurosci. 2014, 34:12402-12414.