Modulatory role of neuropeptide FF system in nociception and opiate analgesia

Neuropeptides

Volumn 42, Issue 1, 2008, Pages 1-18

  Yang, Hsiu Ying T ^a   Tao, Tao ^b   Iadarola, Michael J ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Asic channels; Nociception; NPFF; Opiate analgesia; RFamide peptides

Indexed keywords

G PROTEIN COUPLED RECEPTOR; MORPHINE; NEUROPEPTIDE FF;

ANALGESIA; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYPOTHALAMUS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; IN VIVO STUDY; ISOTOPE LABELING; MASS SPECTROMETRY; NEUROBLASTOMA; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; RECEPTOR BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SPINAL GANGLION; UPREGULATION;

AMINO ACID SEQUENCE; ANALGESICS, OPIOID; ANIMALS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NOCICEPTORS; OLIGOPEPTIDES; PAIN; RECEPTORS, NEUROPEPTIDE; SODIUM CHANNELS;

BIVALVIA; BOVINAE; MAMMALIA; RATTUS; TETRA; VERTEBRATA;

EID: 38849142011     PISSN: 01434179     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.npep.2007.06.004     Document Type: Review

References (107)

1. Aarnisalo A.A., and Panula P. Neuropeptide FF-containing efferent projections from the medial hypothalamus of rat: a Phaseolus vulgaris leucoagglutinin study. Neuroscience 65 (1995) 175-192
2. Allard M., Geoffre S., Legendre P., Vincent J.D., and Simonnet G. Characterization of rat spinal cord receptors to FLFQPQRFamide, a mammalian morphine modulating peptide: a binding study. Brain Res. 500 (1989) 169-176
3. Allard M., Zajac J.M., and Simonnet G. Autoradiographic distribution of receptors to FLFQPQRFamide, a morphine-modulating peptide, in rat central nervous system. Neuroscience 49 (1992) 101-116
4. Allard M., Jordan D., Zajac J.M., Ries C., Martin D., Monkouanga D., Kopp N., and Simonnet G. Autoradiographic localization of receptors for neuropeptide FF, FLFQPQRFamide, in human spinal sensory system. Brain Res. 633 (1994) 127-132
5. Allard M., Lombard M.C., Besson J.M., and Simonnet G. Preferential post-synaptic localization of F8Fa binding sites in cervical and lumbar rat spinal cord as revealed by extensive unilateral doral rhizotomies. Regul. Peptides 53 S1 (1994) S165-S166
6. Allard M., Rousselot P., Lombard M.C., and Theodosis D.T. Evidence for neuropeptide FF (FLFQRFamide) in rat dorsal root ganglia. Peptides 20 (1999) 327-333
7. Altier N., Dray A., Menard D., and Henry J.L. Neuropeptide FF attenuates allodynia in models of chronic inflammation and neuropathy following intrathecal or intracerebroventricular administration. Eur. J. Pharmacol. 407 (2000) 245-255
8. Anko M.L., and Panula P. Functional modulation of human delta opioid receptor by neuropeptide FF. BMC Neurosci. 6 (2005) 21
9. Anko M.L., and Panula P. Regulation of endogenous human NPFF2 receptor by neuropeptide FF in SK-N-MC neuroblastoma cell line. J. Neurochem. 96 (2006) 573-584
10. Askwith C.C., Cheng C., Ikuma M., Benson C., Price M.P., and Welsh M.J. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 26 (2000) 133-141
11. Ballet S., Mauborgne A., Gouarderes C., Bourgoin A.S., Zajac J.M., Hamon M., and Cesselin F. The neuropeptide FF analogue, 1DME, enhances in vivo met-enkephalin release from the rat spinal cord. Neuropharmacology 38 (1999) 1317-1324
12. Bechtold D.A., and Luckman S.M. The role of RFamide peptides in feeding. J. Endocrinol. 192 (2007) 3-15
13. Boer H.H., Schot L.P., Veenstra J.A., and Reichelt D. Immunocytochemical identification of neural elements in the central nervous systems of a snail, some insects, a fish, and a mammal with an antiserum to the molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell Tissue Res. 213 (1980) 21-27
14. Bonini J.A., Jones K.A., Adham N., Forray C., Artymyshyn R., Durkin M.M., Smith K.E., Tamm J.A., Boteju L.W., Lakhlani P.P., Raddatz R., Yao W.J., Ogozalek K.L., Boyle N., Kouranova E.V., Quan Y., Vaysse P.J., Wetzel J.M., Branchek T.A., Gerald C., and Borowsky B. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J. Biol. Chem. 275 (2000) 39324-39331
15. Bonnard E., Burlet-Schiltz O., Frances B., Mazarguil H., Monsarrat B., Zajac J.M., and Roussin A. Identification of neuropeptide FF-related peptides in rodent spinal cord. Peptides 22 (2001) 1085-1092
16. Bonnard E., Burlet-Schiltz O., Monsarrat B., Girard J.P., and Zajac J.M. Identification of proNeuropeptide FFA peptides processed in neuronal and non-neuronal cells and in nervous tissue. Eur. J. Biochem. 270 (2003) 4187-4199
17. Burlet-Schiltz O., Mazarguil H., Sol J.C., Chaynes P., Monsarrat B., Zajac J.M., and Roussin A. Identification of neuropeptide FF-related peptides in human cerebrospinal fluid by mass spectrometry. FEBS Lett. 532 (2002) 313-318
18. Catarsi S., Babinski K., and Seguela P. Selective modulation of heteromeric ASIC proton-gated channels by neuropeptide FF. Neuropharmacology 41 (2001) 592-600
19. Cesselin F. Opioid and anti-opioid peptides. Fundam. Clin. Pharmacol. 9 (1995) 409-433
20. Chartrel N., Dujardin C., Anouar Y., Leprince J., Decker A., Clerens S., Do-Rego J.C., Vandesande F., Llorens-Cortes C., Costentin J., Beauvillain J.C., and Vaudry H. Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc. Nat. Acad. Sci. USA 100 (2003) 15247-15252
21. Chen C.C., Zimmer A., Sun W.H., Hall J., Brownstein M.J., and Zimmer A. A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc. Nat. Acad. Sci. USA 99 (2002) 8992-8997
22. Chen X., Paukert M., Kadurin I., Pusch M., and Grunder S. Strong modulation by RFamide neuropeptides of the ASIC1b/3 heteromer in competition with extracellular calcium. Neuropharmacology 50 (2006) 964-974
23. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16 (1988) 10881-10890
24. Courteix C., Coudore-Civiale M.A., Privat A.M., Zajac J.M., Eschalier A., and Fialip J. Spinal effect of a neuropeptide FF analogue on hyperalgesia and morphine-induced analgesia in mononeuropathic and diabetic rats. Brit. J. Pharmacol. 127 (1999) 1454-1462
25. Deval E., Baron A., Lingueglia E., Mazarguil H., Zajac J.M., and Lazdunski M. Effects of neuropeptide SF and related peptides on acid sensing ion channel 3 and sensory neuron excitability. Neuropharmacology 44 (2003) 662-671
26. Devillers J.P., Mazarguil H., Allard M., Dickenson A.H., Zajac J.M., and Simonnet G. Characterization of a potent agonist for NPFF receptors: binding study on rat spinal cord membranes. Neuropharmacology 33 (1994) 661-669
27. Devillers J.P., Boisserie F., Laulin J.P., Larcher A., and Simonnet G. Simultaneous activation of spinal antiopioid system (neuropeptide FF) and pain facilitatory circuitry by stimulation of opioid receptors in rats. Brain Res. 700 (1995) 173-181
28. Dockray G.J. The expanding family of -RFamide peptides and their effects on feeding behaviour. Exp. Physiol. 89 (2004) 229-235
29. Dockray G.J., Reeve Jr. J.R., Shively J., Gayton R.J., and Barnard C.S. A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide. Nature 305 (1983) 328-330
30. Draisci G., Kajander K.C., Dubner R., Bennett G.J., and Iadarola M.J. Up-regulation of opioid gene expression in spinal cord evoked by experimental nerve injuries and inflammation. Brain Res. 560 (1991) 186-192
31. 125I][D.Tyr1, (NMe)Phe3]NPFF. Synapse 24 (1996) 282-296
32. Elshourbagy N.A., Ames R.S., Fitzgerald L.R., Foley J.J., Chambers J.K., Szekeres P.G., Evans N.A., Schmidt D.B., Buckley P.T., Dytko G.M., Murdock P.R., Milligan G., Groarke D.A., Tan K.B., Shabon U., Nuthulaganti P., Wang D.Y., Wilson S., Bergsma D.J., and Sarau H.M. Receptor for the pain modulatory neuropeptides FF and AF is an orphan G protein-coupled receptor. J. Biol. Chem. 275 (2000) 25965-25971
33. Fukusumi S., Habata Y., Yoshida H., Iijima N., Kawamata Y., Hosoya M., Fujii R., Hinuma S., Kitada C., Shintani Y., Suenaga M., Onda H., Nishimura O., Tanaka M., Ibata Y., and Fujino M. Characteristics and distribution of endogenous RFamide-related peptide-1. Biochim. Biophys. Acta 1540 (2001) 221-232
34. Gelot A., Mazarguil H., Dupuy P., Frances B., Gouarderes C., Roumy M., and Zajac J.M. Biochemical, cellular and pharmacological activities of a human neuropeptide FF-related peptide. Eur. J. Pharmacol. 354 (1998) 167-172
35. Gibbs, R.A., Rogers, J., Katze, M.G., Bumgarner, R., Weinstock, G.M., Mardis, E.R., Remington, K.A., Strausberg, R.L., Venter, J.C., Wilson, R.K., Batzer, M.A., Bustamante, C.D., Eichler, E.E., Hahn, M.W., Hardison, R.C., Makova, K.D., Miller, W., Milosavljevic, A., Palermo, R.E., Siepel, A., Sikela, J.M., Attaway, T., Bell, S., Bernard, K.E., Buhay, C.J., Chandrabose, M.N., Dao, M., Davis, C., Delehaunty, K.D., Ding, Y., Dinh, H.H., Dugan-Rocha, S., Fulton, L.A., Gabisi, R.A., Garner, T.T., Godfrey, J., Hawes, A.C., Hernandez, J., Hines, S., Holder, M., Hume, J., Jhangiani, S.N., Joshi, V., Khan, Z.M., Kirkness, E.F., Cree, A., Fowler, R.G., Lee, S., Lewis, L.R., Li, Z., Liu, Y.S., Moore, S.M., Muzny, D., Nazareth, L.V., Ngo, D.N., Okwuonu, G.O., Pai, G., Parker, D., Paul, H.A., Pfannkoch, C., Pohl, C.S., Rogers, Y.H., Ruiz, S.J., Sabo, A., Santibanez, J., Schneider, B.W., Smith, S.M., Sodergren, E., Svatek, A.F., Utterback, T.R., Vattathil, S., Warren, W., White, C.S., Chinwalla, A.T., Feng, Y., Halpern, A.L., Hillier, L.W., Huang, X., Minx, P., Nelson, J.O., Pepin, K.H., Qin, X., Sutton, G.G., Venter, E., Walenz, B.P., Wallis, J.W., Worley, K.C., Yang, S.P., Jones, S.M., Marra, M.A., Rocchi, M., Schein, J.E., Baertsch, R., Clarke, L., Csuros, M., Glasscock, J., Harris, R.A., Havlak, P., Jackson, A.R., Jiang, H., Liu, Y., Messina, D.N., Shen, Y., Song, H.X., Wylie, T., Zhang, L., Birney, E., Han, K., Konkel, M.K., Lee, J., Smit, A.F., Ullmer, B., Wang, H., Xing, J., Burhans, R., Cheng, Z., Karro, J.E., Ma, J., Raney, B., She, X., Cox, M.J., Demuth, J.P., Dumas, L.J., Han, S.G., Hopkins, J., Karimpour-Fard, A., Kim, Y.H., Pollack, J.R., Vinar, T., Addo-Quaye, C., Degenhardt, J., Denby, A., Hubisz, M.J., Indap, A., Kosiol, C., Lahn, B.T., Lawson, H.A., Marklein, A., Nielsen, R., Vallender, E.J., Clark, A.G., Ferguson, B., Hernandez, R.D., Hirani, K., Kehrer-Sawatzki, H., Kolb, J., Patil, S., Pu, L.L., Ren, Y., Smith, D.G., Wheeler, D.A., Schenck, I., Ball, E.V., Chen, R., Cooper, D.N., Giardine, B., Hsu, F., Kent, W.J., Lesk, A., Nelson, D.L., O'Brien W, E., Prufer, K., Stenson, P.D., Wallace, J.C., Ke, H., Liu, X.M., Wang, P., Xiang, A.P., Yang, F., Barber, G.P., Haussler, D., Karolchik, D., Kern, A.D., Kuhn, R.M., Smith, K.E. and Zwieg, A.S., 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316, 222-234.
36. Gicquel S., Mazarguil H., Desprat C., Allard M., Devillers J.P., Simonnet G., and Zajac J.M. Structure-activity study of neuropeptide FF: contribution of N-terminal regions to affinity and activity. J. Med. Chem. 37 (1994) 3477-3481
37. Gouarderes C., Sutak M., Zajac J.M., and Jhamandas K. Antinociceptive effects of intrathecally administered F8Famide and FMRFamide in the rat. Eur. J. Pharmacol. 237 (1993) 73-81
38. Gouarderes C., Jhamandas K., Sutak M., and Zajac J.M. Role of opioid receptors in the spinal antinociceptive effects of neuropeptide FF analogues. Brit. J. Pharmacol. 117 (1996) 493-501
39. Gouarderes C., kar S., and Zajac J.M. Presence of neuropeptide FF receptors on primary afferent fibres of the rat spinal cord. Neuroscience 74 (1996) 21-27
40. Gouarderes C., Roumy M., Advokat C., Jhamandas K., and Zajac J.M. Dual localization of neuropeptide FF receptors in the rat dorsal horn. Synapse 35 (2000) 45-52
41. Greenberg M.J., Painter S.D., Doble K.E., Nagle G.T., Price D.A., and Lehman H.K. The molluscan neurosecretory peptide FMRFamide: comparative pharmacology and relationship to the enkephalins. Fed. Proc. 42 (1983) 82-86
42. Harrison L.M., Kastin A.J., and Zadina J.E. Opiate tolerance and dependence: receptors, G-proteins, and antiopiates. Peptides 19 (1998) 1603-1630
43. Hinuma S., Habata Y., Fujii R., Kawamata Y., Hosoya M., Fukusumi S., Kitada C., Masuo Y., Asano T., Matsumoto H., Sekiguchi M., Kurokawa T., Nishimura O., Onda H., and Fujino M. A prolactin-releasing peptide in the brain. Nature 393 (1998) 272-276
44. Hinuma S., Shintani Y., Fukusumi S., Iijima N., Matsumoto Y., Hosoya M., Fujii R., Watanabe T., Kikuchi K., Terao Y., Yano T., Yamamoto T., Kawamata Y., Habata Y., Asada M., Kitada C., Kurokawa T., Onda H., Nishimura O., Tanaka M., Ibata Y., and Fujino M. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat. Cell Biol. 2 (2000) 703-708
45. Huang E.Y., Li J.Y., Tan P.P., Wong C.H., and Chen J.C. The cardiovascular effects of PFRFamide and PFR(Tic)amide, a possible agonist and antagonist of neuropeptide FF (NPFF). Peptides 21 (2000) 205-210
46. Hylden J.L., Thomas D.A., Iadarola M.J., Nahin R.L., and Dubner R. Spinal opioid analgesic effects are enhanced in a model of unilateral inflammation/hyperalgesia: possible involvement of noradrenergic mechanisms. Eur. J. Pharmacol. 194 (1991) 135-143
47. Iadarola M.J., Mannes A.J., Karai L., Mitchell K., O' Donnell B., Wellisch O., and Yang H.-Y.T. Neuropeptide FF receptor 2 up-regulation in dorsal root ganglion and dorsal spinal cord during peripheral inflammation. Soc. Neurosci. (2003) Abstract 437.5
48. Jhamandas J.H., and Mactavish D. Central administration of neuropeptide FF (NPFF) causes increased neuronal activation and up-regulation of NPFF gene expression in the rat brainstem. J. Comp. Neurol. 447 (2002) 300-307
49. Jhamandas K., Milne B., Sutak M., Gouarderes C., Zajac J.M., and Yang H.-Y.T. Facilitation of spinal morphine analgesia in normal and morphine tolerant animals by neuropeptide SF and related peptides. Peptides 27 (2006) 953-963
50. Kalliomaki M.L., and Panula P. Neuropeptide FF, but not prolactin-releasing peptide, mRNA is differentially regulated in the hypothalamic and medullary neurons after salt loading. Neuroscience 124 (2004) 81-87
51. Kersante F., Mollereau C., Zajac J.M., and Roumy M. Anti-opioid activities of NPFF1 receptors in a SH-SY5Y model. Peptides 27 (2006) 980-989
52. Kivipelto L., and Panula P. Comparative distribution of neurons containing FLFQPQRFamide-like (morphine-modulating) peptide and related neuropeptides in the rat brain. Eur. J. Neurosci. 3 (1991) 175-185
53. Kivipelto L., and Panula P. Origin and distribution of neuropeptide-FF-like immunoreactivity in the spinal cord of rats. J. Comp. Neurol. 307 (1991) 107-119
54. Kivipelto L., Majane E.A., Yang H.-Y.T., and Panula P. Immunohistochemical distribution and partial characterization of FLFQPQRFamidelike peptides in the central nervous system of rats. J. Comp. Neurol. 286 (1989) 269-287
55. Kontinen V.K., Aarnisalo A.A., Idanpaan-Heikkila J.J., Panula P., and Kalso E. Neuropeptide FF in the rat spinal cord during carrageenan inflammation. Peptides 18 (1997) 287-292
56. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brezillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., Vassart G., and Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol. Chem. 276 (2001) 34631-34636
57. Kotani M., Mollereau C., Detheux M., Le Poul E., Brezillon S., Vakili J., Mazarguil H., Vassart G., Zajac J.M., and Parmentier M. Functional characterization of a human receptor for neuropeptide FF and related peptides. Brit. J. Pharmacol. 133 (2001) 138-144
58. Laguzzi R., Nosjean A., Mazarguil H., and Allard M. Cardiovascular effects induced by the stimulation of neuropeptide FF receptors in the dorsal vagal complex: an autoradiographic and pharmacological study in the rat. Brain Res. 711 (1996) 193-202
59. Lee C.H., Wasowicz K., Brown R., Majane E.A., Yang H.-Y.T., and Panula P. Distribution and characterization of neuropeptide FF-like immunoreactivity in the rat nervous system with a monoclonal antibody. Eur. J. Neurosci. 5 (1993) 1339-1348
60. Lingueglia E., Deval E., and Lazdunski M. FMRFamide-gated sodium channel and ASIC channels: a new class of ionotropic receptors for FMRFamide and related peptides. Peptides 27 (2006) 1138-1152
61. Liu Q., Guan X.M., Martin W.J., McDonald T.P., Clements M.K., Jiang Q., Zeng Z., Jacobson M., Williams Jr. D.L., Yu H., Bomford D., Figueroa D., Mallee J., Wang R., Evans J., Gould R., and Austin C.P. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J. Biol. Chem. 276 (2001) 36961-36969
62. Lombard M.C., Simonnet G., Zajac J.M., Besson J.M., and Allard M. Distribution of neuropeptide FF (FLFQPQRFamide) receptors in the adult rat spinal cord: effects of dorsal rhizotomy and neonatal capsaicin. Neuroscience 68 (1995) 1229-1235
63. Lombard M.C., Weil-Fugazza J., Ries C., and Allard M. Unilateral joint inflammation induces bilateral and time-dependent changes in neuropeptide FF binding in the superficial dorsal horn of the rat spinal cord: implication of supraspinal descending systems. Brain Res. 816 (1999) 598-608
64. 2-like peptide in rat pituitary: decrease by osmotic stimulus. Peptides 12 (1991) 1303-1308
65. 2-like peptide. Brain Res. 494 (1989) 1-12
66. Majane E.A., Zhu J., Aarnisalo A.A., Panula P., and Yang H.-Y.T. Origin of neurohypophyseal neuropeptide-FF (FLFQPQRF-NH2). Endocrinology 133 (1993) 1578-1584
67. Mamet J., Baron A., Lazdunski M., and Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 22 (2002) 10662-10670
68. Mollereau C., Mazarguil H., Zajac J.M., and Roumy M. Neuropeptide FF (NPFF) analogs functionally antagonize opioid activities in NPFF2 receptor-transfected SH-SY5Y neuroblastoma cells. Mol. Pharmacol. 67 (2005) 965-975
69. Mollereau C., Roumy M., and Zajac J.M. Opioid-modulating peptides: mechanisms of action. Curr. Top. Med. Chem. 5 (2005) 341-355
70. Murase T., Arima H., Kondo K., and Oiso Y. Neuropeptide FF reduces food intake in rats. Peptides 17 (1996) 353-354
71. Nicklous D.M., and Simansky K.J. Neuropeptide FF exerts pro- and anti-opioid actions in the parabrachial nucleus to modulate food intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 (2003) R1046-R1054
72. Nystedt J.M., Brandt A.M., Mandelin J., Vilim F.S., Ziff E.B., and Panula P. Analysis of human neuropeptide FF gene expression. J. Neurochem. 82 (2002) 1330-1342
73. Nystedt J.M., Lemberg K., Lintunen M., Mustonen K., Holma R., Kontinen V.K., Kalso E., and Panula P. Pain- and morphine-associated transcriptional regulation of neuropeptide FF and the G-protein-coupled NPFF2 receptor gene. Neurobiol. Dis. 16 (2004) 254-262
74. Nystedt J.M., Brandt A., Vilim F.S., Ziff E.B., and Panula P. Identification of transcriptional regulators of neuropeptide FF gene expression. Peptides 27 (2006) 1020-1035
75. Osugi T., Ukena K., Sower S.A., Kawauchi H., and Tsutsui K. Evolutionary origin and divergence of PQRFamide peptides and LPXRFamide peptides in the RFamide peptide family. Insights from novel lamprey RFamide peptides. FEBS J. 273 (2006) 1731-1743
76. Ohtaki T., Shintani Y., Honda S., Matsumoto H., Hori A., Kanehashi K., Terao Y., Kumano S., Takatsu Y., Masuda Y., Ishibashi Y., Watanabe T., Asada M., Yamada T., Suenaga M., Kitada C., Usuki S., Kurokawa T., Onda H., Nishimura O., and Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411 (2001) 613-617
77. Panula P., Kivipelto L., Nieminen O., Majane E.A., and Yang H.-Y.T. Neuroanatomy of morphine-modulating peptides. Med. Biol. 65 (1987) 127-135
78. Panula P., Aarnisalo A.A., and Wasowicz K. Neuropeptide FF, a mammalian neuropeptide with multiple functions. Prog. Neurobiol. 48 (1996) 461-487
79. Panula P., Kalso E., Nieminen M., Kontinen V.K., Brandt A., and Pertovaara A. Neuropeptide FF and modulation of pain. Brain Res. 848 (1999) 191-196
80. Payza K., and Yang H.-Y.T. Modulation of neuropeptide FF receptors by guanine nucleotides and cations in membranes of rat brain and spinal cord. J. Neurochem. 60 (1993) 1894-1899
81. Perry S.J., Yi-Kung Huang E., Cronk D., Bagust J., Sharma R., Walker R.J., Wilson S., and Burke J.F. A human gene encoding morphine modulating peptides related to NPFF and FMRFamide. FEBS Lett. 409 (1997) 426-430
82. Price D.A., and Greenberg M.J. Structure of a molluscan cardioexcitatory neuropeptide. Science 197 (1977) 670-671
83. Price M.P., McIlwrath S.L., Xie J., Cheng C., Qiao J., Tarr D.E., Sluka K.A., Brennan T.J., Lewin G.R., and Welsh M.J. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32 (2001) 1071-1083
84. Przewlocki R., and Przewlocka B. Opioids in chronic pain. Eur. J. Pharmacol. 429 (2001) 79-91
85. Raffa R.B., Kim A., Rice K.C., de Costa B.R., Codd E.E., and Rothman R.B. Low affinity of FMRFamide and four FaRPs (FMRFamide-related peptides), including the mammalian-derived FaRPs F-8-Famide (NPFF) and A-18-Famide, for opioid mu, delta, kappa 1, kappa 2a, or kappa 2b receptors. Peptides 15 (1994) 401-404
86. 2+ channels in rat spinal ganglion neurones. Neuroreport 7 (1996) 2979-2981
87. 2+ in mouse spinal ganglion neurons. Eur. J. Pharmacol. 306 (1996) 291-295
88. Roumy M., and Zajac J.M. Neuropeptide FF, pain and analgesia. Eur. J. Pharmacol. 345 (1998) 1-11
89. Roumy M., and Zajac J. Neuropeptide FF selectively attenuates the effects of nociceptin on acutely dissociated neurons of the rat dorsal raphe nucleus. Brain Res. 845 (1999) 208-214
90. Roumy M., Lorenzo C., Mazeres S., Bouchet S., Zajac J.M., and Mollereau C. Physical association between neuropeptide FF and micro-opioid receptors as a possible molecular basis for anti-opioid activity. J. Biol. Chem. 282 (2007) 8332-8342
91. Simonin F., Schmitt M., Laulin J.P., Laboureyras E., Jhamandas J.H., MacTavish D., Matifas A., Mollereau C., Laurent P., Parmentier M., Kieffer B.L., Bourguignon J.J., and Simonnet G. RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc. Nat. Acad. Sci. USA 103 (2006) 466-471
92. Stinus L., Allard M., Gold L., and Simonnet G. Changes in CNS neuropeptide FF-like material, pain sensitivity, and opiate dependence following chronic morphine treatment. Peptides 16 (1995) 1235-1241
93. Sunter D., Hewson A.K., Lynam S., and Dickson S.L. Intracerebroventricular injection of neuropeptide FF, an opioid modulating neuropeptide, acutely reduces food intake and stimulates water intake in the rat. Neurosci. Lett. 313 (2001) 145-148
94. Traub R.J., Iadarola M.J., and Ruda M.A. Effect of multiple dorsal rhizotomies on calcitonin gene-related peptide-like immunoreactivity in the lumbosacral dorsal spinal cord of the cat: a radioimmunoassay analysis. Peptides 10 (1989) 979-983
95. Ukena K., and Tsutsui K. Distribution of novel RFamide-related peptide-like immunoreactivity in the mouse central nervous system. Neurosci. Lett. 300 (2001) 153-156
96. Ukena K., Iwakoshi E., Minakata H., and Tsutsui K. A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett. 512 (2002) 255-258
97. Vilim F.S., Aarnisalo A.A., Nieminen M.L., Lintunen M., Karlstedt K., Kontinen V.K., Kalso E., States B., Panula P., and Ziff E. Gene for pain modulatory neuropeptide NPFF: induction in spinal cord by noxious stimuli. Mol. Pharmacol. 55 (1999) 804-811
98. Voilley N., de Weille J., Mamet J., and Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J. Neurosci. 21 (2001) 8026-8033
99. Vyas N., Mollereau C., Cheve G., and McCurdy C.R. Structure-activity relationships of neuropeptide FF and related peptidic and non-peptidic derivatives. Peptides 27 (2006) 990-996
100. Waldmann R., and Lazdunski M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr. Opin Neurobiol. 8 (1998) 418-424
101. Xie J., Price M.P., Wemmie J.A., Askwith C.C., and Welsh M.J. ASIC3 and ASIC1 mediate FMRFamide-related peptide enhancement of H+-gated currents in cultured dorsal root ganglion neurons. J. Neurophysiol. 89 (2003) 2459-2465
102. Xu M., Kontinen V.K., Panula P., and Kalso E. Effects of (1DMe)NPYF, a synthetic neuropeptide FF analogue, in different pain models. Peptides 20 (1999) 1071-1077
103. Yang H.-Y.T., and Iadarola M.J. Activation of spinal neuropeptide FF and the neuropeptide FF receptor 2 during inflammatory hyperalgesia in rats. Neuroscience 118 (2003) 179-187
104. Yang H.-Y.T., and Iadarola M.J. Modulatory roles of the NPFF system in pain mechanisms at the spinal level. Peptides 27 (2006) 943-952
105. Yang H.-Y.T., Fratta W., Majane E.A., and Costa E. Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc. Nat. Acad. Sci. USA 82 (1985) 7757-7761
106. Yoshida H., Habata Y., Hosoya M., Kawamata Y., Kitada C., and Hinuma S. Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim. Biophys. Acta 1593 (2003) 151-157
107. Zeng Z., McDonald T.P., Wang R., Liu Q., and Austin C.P. Neuropeptide FF receptor 2 (NPFF2) is localized to pain-processing regions in the primate spinal cord and the lower level of the medulla oblongata. J. Chem. Neuroanat. 25 (2003) 269-278