The molecular dynamics of pain control (original) (raw)
Hunt, S. P. & Rossi, J. Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information . Phil. Trans. R. Soc. Lond. B308, 283– 289 (1985). PubMed ArticleCAS Google Scholar
Willis, W. D. & Westlund, K. N. Neuroanatomy of the pain system and of the pathways that modulate pain. J. Clin. Neurophysiol.14, 2–31 (1997 ). ArticleCASPubMedPubMed Central Google Scholar
Bernard, J. F. & Bandler, R. Parallel circuits for emotional coping behaviour: new pieces in the puzzle. J. Comp. Neurol.401, 429–436 (1998). ArticleCASPubMed Google Scholar
Craig, A. D. in The Emotional Motor System. Progress in Brain Research Vol. 107 (eds Holstege, G., Saper, C. & Bandler, R.) 225– 242 (Elsevier, New York, 1996). Book Google Scholar
Villanueva, L., Bouhassira, D. & Le Bars, D. The medullary subnucleus reticularis dorsalis (SRD) as a key link in both the transmission and modulation of pain signals. Pain67, 231–240 ( 1996). ArticleCASPubMed Google Scholar
Lima, D., Mendes-Ribeiro, J. A. & Coimbra, A. The spino-latero-reticular system of the rat: projections from the superficial dorsal horn and structural characterization of marginal neurons involved. Neuroscience45, 137– 152 (1991). ArticleCASPubMed Google Scholar
Dubner, R. & Ren, K. Endogenous mechanisms of sensory modulation . Pain6, S45–S53 (1999 ). PubMed
Basbaum, A. I. & Fields, H. L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci.7, 309–338 ( 1984). ArticleCASPubMed Google Scholar
Honore, P. et al. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience98, 585– 598 (2000). ArticleCASPubMed Google Scholar
Hokfelt, T., Zhang, X. & Wiesenfeld-Hallin, Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci.17, 22–30 (1994). ArticleCASPubMed Google Scholar
Chizh, B. A., Dickenson, A. H. & Wnendt, S. The race to control pain: more participants, more targets . Trends Pharmacol. Sci.20, 354– 357 (1999). ArticleCASPubMed Google Scholar
Hunt, S. P., Pini, A. & Evan, G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation . Nature328, 632–634 (1987). ArticleCASPubMed Google Scholar
Williams, S., Evan, G. I. & Hunt, S. P. Changing patterns of c-fos induction in spinal neurons following thermal cutaneous stimulation in the rat. Neuroscience36, 73–81 ( 1990). ArticleCASPubMed Google Scholar
Fields, H. in Molecular Neurobiology of Pain (ed. Borsook, D.) 307– 317 (IASP, Seattle, 1997). Google Scholar
Yaksh, T. L. Spinal systems and pain processing: development of novel analgesic drugs with mechanistically defined models. Trends Pharmacol. Sci.20, 329–337 (1999). ArticleCASPubMed Google Scholar
Snider, W. D. & McMahon, S. B. Tackling pain at the source: new ideas about nociceptors. Neuron20, 629–632 (1998). ArticleCASPubMed Google Scholar
Michaelis, M., Habler, H. J. & Jaenig, W. Silent afferents: a separate class of primary afferents? Clin. Exp. Pharmacol. Physiol.23, 99– 105 (1996). ArticleCASPubMed Google Scholar
Xu, G. Y., Huang, L. Y. & Zhao, Z. Q. Activation of silent mechanoreceptive cat C and A sensory neurons and their substance P expression following peripheral inflammation . J. Physiol.528, 339– 348 (2000). ArticleCASPubMedPubMed Central Google Scholar
Nagy, J. I. & Hunt, S. P. Fluoride-resistant acid phosphatase-containing neurons in dorsal root ganglia are separate from those containing substance P or somatostatin. Neuroscience7, 89– 97 (1982). ArticleCASPubMed Google Scholar
Ribeiro-Da-Silva, A., Castro-Lopes, J. M. & Coimbra, A. Distribution of glomeruli with fluoride-resistant acid phosphatase (FRAP)-containing terminals in the substantia gelatinosa of the rat. Brain Res.377, 323– 329 (1986). ArticleCASPubMed Google Scholar
Guo, A., Vulchanova, L., Wang, J., Li, X. & Elde, R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur. J. Neurosci.11, 946–958 (1999). ArticleCASPubMed Google Scholar
Silverman, J. D. & Kruger, L. Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated 'nociceptor' thin axons in rat testis and cornea whole-mount preparations . Somatosens. Res.5, 259– 267 (1988). ArticleCASPubMed Google Scholar
Bennett, D. L. et al. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci.18, 3059–3072 (1998). ArticleCASPubMedPubMed Central Google Scholar
Ribeiro-da-Silva, A. & Coimbra, A. Capsaicin causes selective damage to type I synaptic glomeruli in rat substantia gelatinosa . Brain Res.290, 380–383 (1984). ArticleCASPubMed Google Scholar
Averill, S., McMahon, S. B., Clary, D. O., Reichardt, L. F. & Priestley, J. V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci.7, 1484– 1494 (1995). ArticleCASPubMedPubMed Central Google Scholar
Cuello, A. C., Ribeiro-da-Silva, A., Ma, W., De Koninck, Y. & Henry, J. L. Organization of substance P primary sensory neurons: ultrastructural and physiological correlates. Regul. Pept.46, 155–164 (1993). ArticleCASPubMed Google Scholar
Michael, G. J. & Priestley, J. V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy . J. Neurosci.19, 1844– 1854 (1999). ArticleCASPubMedPubMed Central Google Scholar
Caterina, M. J. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature389, 816– 824 (1997).References29and51imply that there might be pharmacological targets for treating pain that are preferentially expressed by peripheral sensory neurons. ArticleCASPubMed Google Scholar
Bennett, D. L., Koltzenburg, M., Priestley, J. V., Shelton, D. L. & McMahon, S. B. Endogenous nerve growth factor regulates the sensitivity of nociceptors in the adult rat. Eur. J. Neurosci.10, 1282–1291 (1998). ArticleCASPubMed Google Scholar
Oddiah, D., Anand, P., McMahon, S. B. & Rattray, M. Rapid increase of NGF, BDNF and NT-3 mRNAs in inflamed bladder. Neuroreport9, 1455–1458 (1998). ArticleCASPubMed Google Scholar
Koltzenburg, M., Bennett, D. L., Shelton, D. L. & McMahon, S. B. Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin. Eur. J. Neurosci.11, 1698–1704 (1999). ArticleCASPubMed Google Scholar
Csillik, B. Nerve growth factor regulates central terminals of primary sensory neurons . Z. Mikrosk Anat. Forsch.98, 11– 16 (1984). CASPubMed Google Scholar
Fitzgerald, M., Wall, P. D., Goedert, M. & Emson, P. C. Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res.332, 131 –141 (1985). ArticleCASPubMed Google Scholar
Woolf, C. J., Shortland, P. & Coggeshall, R. E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature355, 75– 78 (1992). ArticleCASPubMed Google Scholar
Bennett, D. L., French, J., Priestley, J. V. & McMahon, S. B. NGF but not NT-3 or BDNF prevents the A fiber sprouting into lamina II of the spinal cord that occurs following axotomy. Mol. Cell. Neurosci.8, 211–220 ( 1996). ArticleCASPubMed Google Scholar
Malmberg, A. B., Chen, C., Tonegawa, S. & Basbaum, A. I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCγ. Science278, 279–283 ( 1997).References37and38identify novel targets for treating and understanding the mechanisms that give rise to neuropathic pain. ArticleCASPubMed Google Scholar
Bozic, C. R., Lu, B., Hopken, U. E., Gerard, C. & Gerard, N. P. Neurogenic amplification of immune complex inflammation . Science273, 1722–1725 (1996). ArticleCASPubMed Google Scholar
De Felipe, C. et al. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature392, 394–397 (1998).The first demonstration of the wide-ranging roles of substance P in behaviour using gene knockout. ArticleCASPubMed Google Scholar
McMahon, S. B., Bennett, D. L., Priestley, J. V. & Shelton, D. L. The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA–IgG fusion molecule. Nature Med.1, 774–780 ( 1995). ArticleCASPubMed Google Scholar
Neumann, S., Doubell, T. P., Leslie, T. & Woolf, C. J. Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature384, 360 –364 (1996). ArticleCASPubMed Google Scholar
Swett, J. E. & Woolf, C. J. The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J. Comp. Neurol.231, 66–77 (1985). ArticleCASPubMed Google Scholar
Janig, W. & Koltzenburg, M. On the function of spinal primary afferent fibres supplying colon and urinary bladder. J. Auton. Nerv. Syst.30, S89–S96 (1990). ArticlePubMed Google Scholar
Cervero, F. & Tattersall, J. E. Somatic and visceral inputs to the thoracic spinal cord of the cat: marginal zone (lamina I) of the dorsal horn. J. Physiol. (Lond.)388, 383– 395 (1987). ArticleCAS Google Scholar
Morgan, C., Nadelhaft, I. & deGroat, W. C. The distribution within the spinal cord of visceral primary afferent axons carried by the lumbar colonic nerve of the cat. Brain Res.398, 11–17 ( 1986). ArticleCASPubMed Google Scholar
Tominaga, M. et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron21, 531– 543 (1998). ArticleCASPubMed Google Scholar
Davis, J. B. et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature405, 183– 187 (2000). ArticleCASPubMed Google Scholar
Caterina, M. J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science288, 306– 313 (2000). ArticleCASPubMed Google Scholar
Caterina, M. J., Rosen, T. A., Tominaga, M., Brake, A. J. & Julius, D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature398, 436–441 (1999). ArticleCASPubMed Google Scholar
Akopian, A. N., Sivilotti, L. & Wood, J. N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature379, 257–262 (1996). ArticleCASPubMed Google Scholar
Sangameswaran, L. et al. A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J. Biol. Chem.272, 14805–14809 ( 1997). ArticleCASPubMed Google Scholar
Novakovic, S. D. et al. Distribution of the tetrodotoxin-resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J. Neurosci.18, 2174–2187 (1998). ArticleCASPubMedPubMed Central Google Scholar
Cummins, T. R. et al. A novel persistent tetrodotoxin-resistant sodium current In SNS-null and wild-type small primary sensory neurons. J. Neurosci.19, RC43 (1999). ArticleCASPubMedPubMed Central Google Scholar
Tate, S. et al. Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nature Neurosci.1, 653–655 (1998). ArticleCASPubMed Google Scholar
Coward, K. et al. Immunolocalization of SNS/PN3 and NaN/SNS2 sodium channels in human pain states. Pain85, 41– 50 (2000). ArticleCASPubMed Google Scholar
Okuse, K. et al. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol. Cell. Neurosci.10, 196–207 ( 1997). ArticleCASPubMed Google Scholar
Akopian, A. N. et al. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nature Neurosci.2, 541–548 (1999). ArticleCASPubMed Google Scholar
Calza, L. et al. Peptide plasticity in primary sensory neurons and spinal cord during adjuvant-induced arthritis in the rat: an immunocytochemical and in situ hybridization study. Neuroscience82, 575–589 (1998). ArticleCASPubMed Google Scholar
Zhang, X., Bean, A. J., Wiesenfeld-Hallin, Z., Xu, X. J. & Hokfelt, T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord. III. Effects of peripheral axotomy with special reference to galanin. Neuroscience64, 893–915 (1995). ArticleCASPubMed Google Scholar
Schwei, M. J. et al. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J. Neurosci.19, 10886–10897 (1999). This paper describes a mouse model of bone cancer pain and suggests a mechanism by which bone cancer pain is generated. ArticleCASPubMedPubMed Central Google Scholar
Honore, P. et al. Osteoprotegerin blocks bone cancer-induced skeletal destruction, skeletal pain and pain-related neurochemical reorganization of the spinal cord. Nature Med.6, 521– 528 (2000). ArticleCASPubMed Google Scholar
Meller, S. T., Dykstra, C., Grzybycki, D., Murphy, S. & Gebhart, G. F. The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology33, 1471–1478 (1994). ArticleCASPubMed Google Scholar
Peschanski, M., Mantyh, P. W. & Besson, J. M. Spinal afferents to the ventrobasal thalamic complex in the rat: an anatomical study using wheat-germ agglutinin conjugated to horseradish peroxidase. Brain Res.278, 240–244 (1983). ArticleCASPubMed Google Scholar
Mantyh, P. W. The spinothalamic tract in the primate: a re-examination using wheatgerm agglutinin conjugated to horseradish peroxidase. Neuroscience9, 847–862 (1983). ArticleCASPubMed Google Scholar
Dado, R. J., Katter, J. T. & Giesler, G. J. J. Spinothalamic and spinohypothalamic tract neurons in the cervical enlargement of rats. II. Responses to innocuous and noxious mechanical and thermal stimuli. J. Neurophysiol.71 , 981–1002 (1994). ArticleCASPubMed Google Scholar
Katter, J. T., Dado, R. J., Kostarczyk, E. & Giesler, G. J. J. Spinothalamic and spinohypothalamic tract neurons in the sacral spinal cord of rats. I. Locations of antidromically identified axons in the cervical cord and diencephalon. J. Neurophysiol.75, 2581 –2605 (1996). ArticleCASPubMed Google Scholar
Marshall, G. E., Shehab, S. A., Spike, R. C. & Todd, A. J. Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience72, 255–263 (1996). ArticleCASPubMed Google Scholar
Todd, A. J., McGill, M. M. & Shehab, S. A. Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem . Eur. J. Neurosci.12, 689– 700 (2000). ArticleCASPubMed Google Scholar
Ding, Y. Q., Takada, M., Shigemoto, R. & Mizumo, N. Spinoparabrachial tract neurons showing substance P receptor-like immunoreactivity in the lumbar spinal cord of the rat. Brain Res.674 , 336–340 (1995). References69–71qualitatively identify the spinoparabrachial pathway as the main ascending pain pathway in rodents. It originates largely from lamina I/NK1-positive neurons. ArticleCASPubMed Google Scholar
Bernard, J. F., Bester, H. & Besson, J. M. Involvement of the spino-parabrachio-amygdaloid and hypothalamic pathways in the autonomic and affective emotional aspects of pain. Prog. Brain Res.107, 243– 255 (1996).This paper demonstrates that parabrachial neurons are noci-specific and concerned predominantly with the intensity of pain rather than its location or nature. ArticleCASPubMed Google Scholar
Bester, H., Chapman, V., Besson, J. M. & Bernard, J. F. Physiological properties of the lamina I spinoparabrachial neurons in the rat. J. Neurophysiol.83, 2239– 2259 (2000). ArticleCASPubMed Google Scholar
Doyle, C. A. & Hunt, S. P. Substance P receptor (neurokinin-1)-expressing neurons in lamina I of the spinal cord encode for the intensity of noxious stimulation: a c-Fos study in rat. Neuroscience89, 17–28 (1999). ArticleCASPubMed Google Scholar
Mantyh, P. W. et al. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science278, 275–279 (1997). ArticleCASPubMed Google Scholar
Nichols, M. L. et al. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science286, 1558 –1561 (1999).References75and76describe the use of a suicide-ligand approach to selectively target and destroy cells involved in the ascending conduction of pain. ArticleCASPubMed Google Scholar
Bester, H., De Felipe C. D. & Hunt, S. P. The substance P receptor is essential for the full expression of noxious inhibitory controls in the mouse. J. Neurosci. (in the press).
Hirakawa, N., Tershner S. A., Fields, H. L. & Manning, B. H. Bi-directional changes in affective state elicited by manipulation of medullary pain-modulatory circuitry. Neuroscience100, 861–871 (2000). ArticleCASPubMed Google Scholar
Culman, J. & Unger, T. Central tachykinins: mediators of defence reaction and stress reactions. Can. J. Physiol. Pharmacol.73, 885–891 ( 1995). ArticleCASPubMed Google Scholar
Rupniak, N. M. et al. Pharmacological blockade or genetic deletion of substance P (NK(1)) receptors attenuates neonatal vocalisation in guinea-pigs and mice . Neuropharmacology39, 1413– 1421 (2000). ArticleCASPubMed Google Scholar
Murtra, P., Sheasby, A. M., Hunt, S. P. & De Felipe, C. Rewarding effects of opiates are absent in mice lacking the receptor for substance P. Nature405, 180–183 (2000).The first demonstration that the rewarding and analgesic properties of opiates are separable following knockout of the NK1-receptor gene. ArticleCASPubMed Google Scholar
Laird, J. M. et al. Deficits in visceral pain and hyperalgesia of mice with a disruption of the tachykinin NK1 receptor gene. Neuroscience98, 345–352 (2000). ArticleCASPubMed Google Scholar
Kramer, M. S. et al. Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science281, 1640–1645 (1998). This paper presents both preclinical and clinical data indicating that NK1-receptor antagonists might be useful in the treatment of anxiety and depression. ArticleCASPubMed Google Scholar
Treede, R. D., Kenshalo, D. R., Gracely, R. H. & Jones, A. K. The cortical representation of pain. Pain79, 105–111 (1999). ArticleCASPubMed Google Scholar
Price, D. D. Psychological and neural mechanisms of the affective dimension of pain. Science288, 1769–1772 ( 2000). ArticleCASPubMed Google Scholar
Rainville, P., Carrier, B., Hofbauer, R. K., Bushnell, M. C. & Duncan, G. H. Dissociation of sensory and affective dimensions of pain using hypnotic modulation. Pain82, 159–171 (1999). ArticleCASPubMed Google Scholar
Rainville, P., Duncan, G. H., Price, D. D., Carrier, B. & Bushnell, M. C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science277, 968–971 (1997). References86and87identify the sensory and affective dimensions of pain as being separable and dependent, in part, on different brain circuits. ArticleCASPubMed Google Scholar
Flor, H. et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature375, 482 –484 (1995). ArticleCASPubMed Google Scholar
Larbig, W. et al. Evidence for a change in neural processing in phantom limb pain patients. Pain67, 275– 283 (1996). ArticleCASPubMed Google Scholar
Knecht, S. et al. Reorganizational and perceptional changes after amputation . Brain119, 1213–1219 (1996). ArticlePubMed Google Scholar
Lenz, F. A. et al. Stimulation in the human somatosensory thalamus can reproduce both the affective and sensory dimensions of previously experienced pain. Nature Med.1, 910–913 ( 1995). ArticleCASPubMed Google Scholar
Matthes, H. W. et al. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature383, 819–823 (1996). ArticleCASPubMed Google Scholar
Mitchell, J. M., Basbaum, A. I. & Fields, H. L. A locus and mechanism of action for associative morphine tolerance. Nature Neurosci.3, 47– 53 (2000).This paper shows that the amygdala-dependent mechanism of contextual sensitization to opiates is reversible by local injection of CCK-B-receptor antagonists. ArticleCASPubMed Google Scholar
Robbins, T. W. & Everitt, B. J. Drug addiction: bad habits add up. Nature398, 567– 570 (1999). ArticleCASPubMed Google Scholar
Franklin, K. B. Analgesia and abuse potential: an accidental association or a common substrate? Pharmacol. Biochem. Behav.59, 993– 1002 (1998). ArticleCASPubMed Google Scholar
Lumb, B. M. & Lovick, T. A. The rostral hypothalamus: an area for the integration of autonomic and sensory responsiveness. J. Neurophysiol.70, 1570–1577 (1993). ArticleCASPubMed Google Scholar
Lovick, T. A. Midbrain and medullary regulation of defensive cardiovascular functions. Prog. Brain Res.107, 301–313 (1996). ArticleCASPubMed Google Scholar
Koob, G. F. & Le Moal, M. Drug abuse: hedonic homeostatic dysregulation. Science278, 52– 58 (1997). ArticleCASPubMed Google Scholar