Abstract
Peptides are not only hormones in endocrine and in hypothalamic neurosecretory cells; they are also present in many neurons in the central and peripheral nervous system. Whereas their role in the two former systems seems to be well established, their function in the nervous system proper is more uncertain. Over the last 25 years or so, extensive studies using various methodologies have been carried out to improve our understanding of neuropeptides. Their distribution has been mapped, their intracellular localization has been defined, and results from functional experiments demonstrating pronounced effects in various models have been reported. More recently, at least one receptor of the seven transmembrane-spanning, G-protein-coupled type has been identified for almost every peptide, strongly supporting a role of neuropeptides in nervous system function. We have studied dorsal root ganglion neurons as a model system to probe peptide functions, with particular focus on their possible role in pain mechanisms. These neurons express robust levels of several peptides and peptide receptors. Moreover, peripheral nerve injury (axotomy) causes dramatic changes in peptide and peptide receptor expression, resulting in a virtually new phenotype with regard to these molecules. Some mechanisms which possibly underlie these phenotypic changes, as well as their functional significance are discussed in this article. Various growth factors as well as the neuroimmune molecule leukemia inhibitory factor may be important for the regulation of peptide synthesis in dorsal root ganglion neurons. Moreover, we have hypothesized that galanin can be an endogenous analgesic compound, which is recruited especially after nerve injury (neuropathic pain). In fact, our and others’ studies suggest the existence of two defense systems against pain, one localized at the level of the dorsal horn, where local neurons release inhibitory peptides including opioid peptides. This system responds to inflammatory pain. The second defense system is within the primary sensory neurons themselves and reacts towards neuropathic pain, for example by upregulating galanin. Another important aspect of peptide function is their involvement in trophic events, and there is now evidence that, for example, galanin and neuropeptide Y can influence regeneration and neurite out-growth. Thus, neuropeptides may exert manifold actions, but their roles in most cases still have to be defined and established as being physiologically and/or pathophysiological significant.
Keywords
- Nerve Growth Factor
- Dorsal Root Ganglion
- Dorsal Horn
- Dorsal Root Ganglion Neuron
- Leukemia Inhibitory Factor
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References
Arvidsson U, Ulfhake B, Cullheim S, Bergstrand A, Theodorsson E, Hökfelt T (1991) Distribution of 125I-galanin and its coexistence with 5-hydroxytryptamine in the cat spinal cord: biochemical, histochemical and experimental studies at the light and electron microscopic level. J Comp Neurol 308: 115–138
Banner LR, Patterson PH (1994) Major changes in the expression of the mRNAs for cholinergic differentiation factor/leukemia inhibitory factor and its receptor after injury to adult peripheral nerves and ganglia. Proc Natl Acad Sci USA 91: 7109–7113
Bargmann W (1949) Über die neurosekretorische Verknüpfung von Hypothalamus und Neurohypophyse. Z Zellforsch 34: 610–634
Bleakman D, Colmers WF, Fournier A, Miller RJ (1991) Neuropeptide Y inhibits Ca2+ influx into cultured dorsal root ganglion neurons of the rat via a Y2 receptor. Br J Pharmacol 103: 1781–1789
Brownstein MJ, Mezey E (1986) Multiple chemical messengers in hypothalamic magnocellular neurons. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in brain research, vol 68. Elsevier, Amsterdam, pp 161–168
Burgevin M-C, Loquet I, Quarteronet D, Habert-Ortoli E (1995) Cloning, pharmacological characterization, and anatomical distribution of a rat cDNA encoding for a galanin receptor. J Mol Neurosci 6: 33–41
Coderre TJ, Grimes RW, Melzack R (1986) Deafferentation and chronic pain in animals. An evaluation of evidence suggesting autotomy is related to pain. Pain 26: 61–84
Corness J, Shi T-J, Xu Z-Q, Brulet P, Hökfelt T (1996) Influence of leukemia inhibitory factor on galanin/GMAP and neuropeptide Y expression in mouse primary sensory neurons after axotomy. Exp Brain Res 112: 79–88
Dalsgaard C-J (1988) The sensory system. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy, vol 6. The peripheral nervous system. Elsevier Science, Amsterdam, pp 599–667
Devor M (1991) Sensory basis of autotomy in rats. Pain 45: 109–110
Du Vigneaud V (1956) Hormones of the posterior pituitary gland: oxytocin and vasopressin. In: The Harvey lectures 1954–55. Academic Press, New York, pp 1–26
Dubner R, Ruda MA (1992) Activity-dependent neuronal plasticity following tissue injury and inflammation. TINS 15: 96–103
Duggan AW, Hope PJ, Lang CW (1991) Microinjection of neuropeptide Y into the superficial dorsal horn reduces stimulus-evoked release of immunoreactive substance P in the anesthetized cat. Neuroscience 44: 733–740
Erspamer V (1991) The tachykinin peptide family. TINS 4: 267–269
Ewald DA, Matthies HJG, Perney TM, Walker MW, Miller RJ (1988) The effect of down regulation of protein kinase C on the inhibitory modulation of dorsal root ganglion neuron Ca2+ currents by neuropeptide Y. J Neurosci 8: 2447–2451
Farkas-Szallasi T, Lundberg JM, Wiesenfeld-Hallin Z, Hökfelt T, Szallasi A (1995) Increased levels of GMAP, VIP, and nitric oxide synthase, and their mRNAs, in lumbar dorsal root ganglia of the rat following systemic resiniferatoxin treatment. NeuroReport 6: 2230–2234
Fitzgerald M, Wall PD, Goedert M, Emson PC (1985) Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res 332: 131–141
Fukada K (1985) Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc Natl Acad Sci USA 82: 8795–8799
Fuxe K, Goldstein M, Hökfelt T, Jonsson G, Lidbrink P (1974) Dopaminergic involvement in hypothalamic function: extrahypothalamic and hypothalamic control. A neuroanatomical analysis. Adv Neurol, vol 5. Raven Press, New York, pp 405–419
Gehlert DR, Beavers LS, Johnson D, Gackenheimer SL, Schober DA, Gadski RA (1996) Expression cloning of human brain neuropeptide Y Y2 receptor. Mol Pharmacol 49: 224–228
Gerald C, Walker MW, Vaysse PJ-J, He C, Branchek TA, Weinshank RL (1995) Expression cloning and pharmacological characterization of a human hippocampal neuropeptide Y/peptide YY Y2 receptor subtype. J Biol Chem 270: 26758–26761
Ghilardi JR, Allen CJ, Vigna SR, McVey DC, Mantyh PW (1994) Cholecystokinin and neuropeptide Y receptors on single rabbit vagal afferent ganglion neurons: site of prejunctional modulation of visceral sensory neurons. Brain Res 633: 33–40
Gibson SJ, Polak JM, Allen JM, Adrian TE, Kelly JS, Bloom SR, (1984) The distribution and origin of a novel brain peptide, neuropeptide Y, in the spinal cord of several mammals. J Comp Neurol 227: 78–91
Gozes I, Brenneman DE (1990) VIP: molecular biology and neurobiological function. Mol Neurobiol 3: 201–236
Guillemin R (1978) Peptides in the brain: the new endocrinology of the neuron. Science 202: 390–402
Gustafson EL, Smith KE, Durkin MM, Gerald C, Branchek TA (1996) Distribution of a rat galanin receptor mRNA in rat brain. NeuroReport 7: 953–957
Gustafson EL, Smith KE, Durkin MM, Walker MW, Gerald C, Weinshank R, Branchek TA (1997) Distribution of the neuropeptide Y Y2 receptor mRNA in rat central nervous system. Mol Brain Res 46: 223–235
Harris GW (1955) Neuronal control of the pituitary gland. Edward Arnold Ltd, London
Henken DB, Martin JR (1992a) Herpes simplex virus infection induces a selective increase in the proportion of galanin-positive neurons in mouse sensory ganglia. Exp Neurol 118: 195–203
Henken DB, Martin JR (1992) The proportion of galanin-immunoreactive neurons in mouse trigeminal ganglia is transiently increased following corneal inoculation of herpes simplex virus type-1. Neurosci Lett 140: 177–180
Hökfelt T (1991) Neuropeptides in perspective: the last ten years. Neuron 7: 867–879
Hökfelt T, Mutt V (1997) Neuropeptides. In: Adelman G, Smith B (eds) Encyclopedia of neuroscience, 2nd edn. CD-ROM version. Elsevier, Amsterdam
Hökfelt T, Elfvin LG, Eide R, Schultzberg M, Goldstein M, Luft R (1977) Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci USA 74: 3587–3591
Hökfelt T, Wiesenfeld-Hallin Z, Villar MJ, Melander T (1987) Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83: 217–220
Hökfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. TINS 17: 22–30
Ji R-R, Zhang Q, Pettersson RF, Hökfelt T (1996) aFGF, bFGF and NGF differentially regulate neuropeptide expression in dorsal root ganglia after axotomy and induce autotomy. Reg Pep 66: 179–189
Ji RR, Zhang Q, Bedecs K, Arvidsson J, Zhang X, Xu XJ, Wiesenfeld-Hallin Z, Bartfai T, Hökfelt T (1994) Galanin antisense oligonucleotides reduce galanin levels in dorsal root ganglia and induce autotomy in rats after axotomy. Proc Natl Acad Sci USA 91: 12540–12543
Kashiba H, Senba E, Kawai Y, Ueda Y, Tohyama M (1992) Axonal blockade induces the expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons. Brain Res 577: 19–28
Kashiba H, Senba E, Ueda Y, Tohyama M (1992) Co-localized but target-unrelated expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons after peripheral nerve crush injury. Brain Research 582: 47–57
Kerekes N, Landry M, Rydh-Rinder M, Hökfelt T, (1997) The effect of NGF, BDNF and bFGF on expression of galanin in cultured rat dorsal root ganglia. Brain Res 754: 131–141
Kessler JA, Black IB, (1980) Nerve growth factor stimulates the development of substance P in sensory ganglia. Proc Natl Acad Sci USA 77: 649–652
Kopin AS, Lee YM, McBride EW, Miller LJ, Lu M, Lin HY, L.F. K, Beiborn M (1992) Expression cloning and characterization of the canine parietal cell gastrin receptor. Proc Natl Acad Sci USA 89: 3605–3609
Lindsay RM, Harmar A J, (1989) Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337: 362–364
Lindsay RM, Lockett C, Sternberg J, Winter J (1989) Neuropeptide expression in cultures of adult sensory neurons: modulation of substance P and calcitonin gene-related peptide levels by nerve growth factor. Neuroscience 33: 53–65
Masu Y, Nakayama K, Tamaki H, Harada Y, Kuno M, Nakanishi S, (1987) cDNA cloning of bovine substance-K receptor through oocyte expression system. Nature 329: 836–838
Meister B, Broberger C, Villar MJ, Hökfelt T (1994) Cholecystokinin B receptor gene expression in hypothalamic neurosecretory neurons after experimental manipulations. Neuroendocrinology 60: 458–469
Meister B, Hökfelt T, Geffard M, Oertel W (1988) Glutamic acid decarboxylase- and y-aminobutyric acid-like immunoreacitivites in corticotropin-releasing factor-containing parvocellular neurons of the hypothalamic paraventricular nucleus. Neuroendocrinology 48: 516–526
Melander T, Köhler C, Nilsson S, Hökfelt T, Brodin E, Theodorsson E, Bartfai T (1988) Autoradiographic quantification and anatomical mapping of 125I-galanin binding in the rat central nervous system. J Chem Neuroanat 1: 213–233
Meunier J-C, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour J-L, Guillemot J-C, Ferrare P, Monsarrat B, Mazaguil H, Vassart G, Parmentier M, Costentin J (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL receptor. Nature 377: 532–535
Meyerhof W, Darlison MG, Richter D (1993) The elucidation of neuropeptide receptors and their subtypes through the application of molecular biology. In: Hucho F (ed) New comprehensive biochemistry, Volume 25. Elsevier, Amsterdam, pp 335–353
Mulderry PK (1994) Neuropeptide expression by newborn and adult rat sensory neurons in culture: effects of nerve growth factor and other neurotrophic factors. Neuroscience 59: 673–688
Mutt V (1987) Chemical properties of some polypeptides affecting vascular function. In: Nobin A, Owman C, Arneklo-Nobin B (eds) Neuronal messengers in vascular function. Elsevier, Amsterdam, pp 125–198
Nahin RL, Marino De León KR, Ruda M (1994) Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain 58: 95–108
Otten U, Goedert M, Mayer N, Lembeck F (1980) Requirement of nerve growth factor for development of substance P-containing sensory neurons. Nature 287: 158–159
Parker EM, Izzarelli DG, Nowak HP, Mahle CD, Iben LG, Wang J, Goldstein ME (1995) Cloning and characterization of rat GALR1 galanin receptor from RIN14B insulinoma cells. Mol Brain Res 34: 179–189
Patterson PH (1994) Leukemia inhibitory factor, a cytokine at the interface between neurobiology and immunology. Proc Natl Acad Sci USA 91: 7833–7835
Puttick RM, Pinnock RD, Woodruff GN (1994) Galanin-induced membrane depolarization of neonatal rat cultured dorsal root ganglion cells. Eur J Pharmacol 254: 303–306
Rao MS, Sun Y, Escary JL, Perreau J, Tresser S, Patterson PH, Zigmond RE, Brulet P, Landis SC (1993) Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11: 1175–1185
Reinscheid RK, Nothacker H-P, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma JFJ, Civelli O (1995) A neuropeptide that activates an opioid like G protein coupled receptor. Science 270: 792–794
Rose PM, Fernandes P, Lynch JS, Fraxier ST, Fisher SM, Kodukula K, Kienzle B, Seethala R (1995) Cloning and functional expression of a cDNA encoding a human type 2 neuropeptide Y receptor. J Biol Chem 270: 22661–22664
Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Proc Natl Acad Sci USA 304: 129–135
Rustioni A, Weinberg RJ (1989) The somatosensory system. In: Bjórklund A, Hókfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, vol 7. Intergrated systems of the CNS, Part II. Central visual, auditory, somatosensory, gustatory. Elsevier, Amsterdam, pp 219–321
Rydh-Rinder M, Holmberg K, Elfvin L-G, Wiesenfeld-Hallin Z, Hókfelt T (1996) Effects of peripheral axotomy on neuropeptides and nitric oxide synthase in dorsal root ganglia and spinal cord of the guinea pig: an immunohistochemical study. Brain Res 707: 180–188
Salt TE, Hill RG (1983) Neurotransmitter candidates of somatosensory primary afferent fibers. Neuroscience 10: 1083–1103
Schally AV (1978) Aspects of hypothalamic regulation of the pituitary gland. Its implications for the control of reproductive processes. Science 202: 18–28
Scharrer B (1990) The neuropeptide saga. Am Zool 30: 887–895
Scharrer E (1928) Die Lichtempfindlichkeit blinder Elritzen. Untersuchungen über das Zwischenhirn der Fische. Z Vergl Physiol 7: 1–38
Scharrer E (1952) The general significance of the neurosecretory cell. Scientia 46: 177–183
Scharrer E, Scharrer B (1963) Neuroendocrinology. Columbia University Press, New York
Schwartz TW, U. G, Schambye HT, Hjorth SA (1995) Molecular mechanism of action of non-peptide ligands for peptide receptors. Current Pharm Design 1: 325–342
Shehab SA, Atkinson ME (1986) Vasoactive intestinal polypeptide (VIP) increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons. Brain Res 372: 37–44
Strand FL, Rose KJ, Zuccarelli LA, Kume J (1991) Neuropeptide hormones as neurotrophic factors. Physiol Rev 71: 1017–1037
Sun Y, Zigmond RE (1996) Leukaemia inhibitory factor induced in the sciatic nerve after axotomy is involved in the induction of galanin in sensory neurons. Eur J Neurosci 8: 2213–2220
Tanaka K, Masu M, Nakanishi S (1990) Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4: 847–854
Tatemoto K, Mutt V (1981) Isolation and characterization of the intestinal peptide porcine PHI (PHI 127), a new member of the glucagon-secretion family. Proc Natl Acad Sci USA 78: 6603–6607
Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y, a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296: 659–660
Tohyama M (1992) An overview of the ontogeny of neurotransmitters and neuromodulators in the central nervous system. In: Björklund A, Hökfelt T, Tohyama M (eds) Handbook of chemical neuroanatomy. Ontogeny of transmitters and peptides in the CNS, vol 10. Elsevier, Amsterdam, pp 647–650
Verge VMK, Richardson PM, Wiesenfeld-Hallin Z, Hökfelt T (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J Neurosci 15: 2081–2096
Verge VMK, Xu X-J, Langel Ü, Hökfelt T, Wiesenfeld-Hallin Z, Bartfai T (1993) Evidence for an endogenous inhibitory control on autotomy, a behavioral sign of neuropathic pain, by galanin in the rat after sciatic nerve section: demonstrated by chronic intrathecal infusion of M-35, a newly developed high affinity galanin receptor antagonist. Neurosci Lett 149: 193–197
Villar MJ, Cortés R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33: 587–604
Villar MJ, Meister B, Cortés R, Schalling M, Morris M, Hökfelt T (1990) Neuropeptide gene expression in hypothalamic magnocellular neurons of normal and hypophysectomized rats: a combined immunohistochemical and in situ hybridization study. Neuroscience 36: 181–99
Villar MJ, Wiesenfeld-Hallin Z, Xu XJ, Theodorsson E, Emson PC, Hökfelt T (1991) Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol 112: 29–39
Wahlestedt C, Yanaihara N, Hákanson R (1986) Evidence for different pre- and post-junctional receptors for neuropeptide Y and related peptides. Reg Pep 13: 307–318
Wakisaka S, Kajander KC, Bennett GJ (1991) Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124: 200–203
Walker ME, Ewald DA, Perney TM, Miller RG (1988) Neuropeptide Y modulates neurotransmitter release and Ca2+ currents in rat sensory neurons. J Neurosci 8: 2438–2446
Wall PD, Devor M, Inbal R, Scadding JW, Schonfield D, Seltzer Z, Tomkiewiocz MM (1979) Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 7: 103–113
Weihe E, Schäfer MK-H, Nohr D, Persson S (1994) Expression of neuropeptides, neuropeptide receptors and neuropeptide processing enzymes in spinal neurons and peripheral non-neural cells and plasticity in models of inflammatory pain. In: Hökfelt T, Schaible H-G, Schmidt RF (eds) Neuropeptides, nociception and pain. Chapman & Hall, London, pp 43–69
White DM, Mansfield K (1996) Vasoactive intestinal polypeptide and neuropeptide Y act indirectly to increase neurite outgrowth of dissociated dorsal root ganglion cells. Neuroscience 73: 881–887
Wiesenfeld-Hallin Z (1984) The effect of intrathecal morphine and naltrexone on autotomy in sciatic nerve sectioned rats. Pain 18: 267–278
Wiesenfeld-Hallin Z, Bartfai T, Hökfelt T (1992) Galanin in sensory neurons in the spinal cord. Front Neuroendocrinol 13: 319–343
Xu X-J, Wiesenfeld-Hallin Z, Villar MJ, Fahrenkrug J, Hökfelt T (1990) On the role of galanin, substance P and other neuropeptides in primary sensory neurons of the rat: studies on spinal reflex excitability and peripheral axotomy. Eur J Neurosci 2: 733–743
Xu Z-Q, Shi T-J, Hökfelt T (1996) Expression of galanin and a galanin receptor in several sensory systems and bone anlage of rat embryos. Proc Natl Acad Sci USA 93: 14901–14905
Xu Z-Q, Shi T-J, Landry M, Hökfelt T, (1996) Evidence for galanin receptors in primary sensory neurons and effect of axotomy and inflammation. Neuro Report 8: 237–242
Yamamori T, Fukada K, Aebersold R, Korsching S, Fann MJ, Patterson PH (1989) The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246: 1412–1416
Zhang X, Dagerlind Å, Eide RP, Castel M-N, Broberger C, Wiesenfeld-Halin Z, Hökfelt T (1993a) Marked increase in cholecystokinin B receptor messenger RNA levels in rat dorsal root ganglia after peripheral axotomy. Neuroscience 57: 227–233
Zhang X, Ju G, Eide R, Hökfelt T (1993b) Effect of peripheral nerve cut on neuropeptides in dorsal root ganglia and the spinal cord of monkey with special reference to galanin. J Neurocytol 22: 342–381
Zhang X, Bao L, Xu Z-Q, Kopp J, Arvidsson U, Eide R, Hökfelt T (1994) Localization of neuropeptide Y Y1 receptors in the rat nervous system with special reference to somatic receptors on small dorsal root ganglion neurons. Proc Natl Acad Sci USA 91: 11738–11742
Zhang X, Wiesenfeld-Hallin Z, Hökfelt T (1994) Effect of peripheral axotomy on expression of neuropeptide Y receptor mRNA in rat lumbar dorsal root ganglia. Eur J Neurosci 6: 43–57
Zhang Q, Shi T-J, Ji R-R, Zhang Y-T, Sundler F, Hannibal J, Fahrenkrug J, Hökfelt T (1995) Expression of pituitary adenylate cyclase-activating polypeptide in dorsal root ganglia following axotomy: time course and coexistence. Brain Res 705: 149–155
Zhang X, Ji R-R, Nilsson S, Villar M, Ubink R, Ju G, Wiesenfeld-Hallin Z, Hökfelt T (1995) Neuropeptide Y and galanin binding sites in rat and monkey lumbar dorsal root ganglia and spinal cord and effect of peripheral axotomy. Eur J Neurosci 7: 367–380
Zhang X, Xu Z-Q, Bao L, Dagerlind Å, Hökfelt T (1995) Complementary distribution of receptors for neurotensin and NPY in small neurons in rat lumbar DRGs and regulation of the receptors and peptides after peripheral axotomy. J Neurosci 15: 2733–2747
Zhang Y-Z, Hannibal J, Zhao Q, Moller K, Danielsen N, Fahrenkrug J, Sundler F (1996) Pituitary adenylate cyclase activating peptide (PACA”P) expression in the rat dorsal root ganglia: up-regulation after peripheral nerve injury. Neuroscience 74: 1099–1110
Zhang X, Shi T-J, Holmberg K, Landry M, Huan W, Xiao H, Ju G, Hökfelt T (1997) Expression and regulation of the neuropeptide Y Y2 receptor in sensory and autonomic ganglia. Proc Natl Acad Sci USA 94: 729–734
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Hökfelt, T. et al. (1997). The Ups and Downs of Neuropeptides. In: Korf, HW., Usadel, KH. (eds) Neuroendocrinology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60915-2_2
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