Commonalities between pain and memory mechanisms and their meaning for understanding chronic pain

Progress in Molecular Biology and Translational Science

Volumn 131, Issue , 2015, Pages 409-434

  Price, Theodore J ^a   Inyang, Kufreobong E ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

BDNF Hyperalgesic priming Atypical PKC PKMzeta trkB Opioid LTP eIF4E mTOR Axonal mRNA NGF ERK AMPK CREB IL 6 Reconsolidation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ARTICLE; BRAIN CORTEX; CHRONIC PAIN; DENDRITIC SPINE; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; PAIN MEMORY; PAIN PLASTICITY; PAIN RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SPINAL CORD DORSAL HORN; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN SYNTHESIS;

ANIMALS; CHRONIC PAIN; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NOCICEPTORS; PROTEIN BIOSYNTHESIS; SPINAL CORD DORSAL HORN;

EID: 84924606422     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/bs.pmbts.2014.11.010     Document Type: Chapter

References (122)

1. C.J. Woolf, and E.T. Walters Common patterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia Trends Neurosci 14 1991 74 78
2. F. Cervero Spinal cord mechanisms of hyperalgesia and allodynia: role of peripheral input from nociceptors Prog Brain Res 113 1996 413 422
3. M. Devor, W. Janig, and M. Michaelis Modulation of activity in dorsal root ganglion neurons by sympathetic activation in nerve-injured rats J Neurophysiol 71 1994 38 47
4. S.J. Lisney, and M. Devor Afterdischarge and interactions among fibers in damaged peripheral nerve in the rat Brain Res 415 1987 122 136
5. D.B. Reichling, P.G. Green, and J.D. Levine The fundamental unit of pain is the cell Pain 154 2013 S2 S9
6. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26 2003 696 705
7. A. Latremoliere, and C.J. Woolf Central sensitization: a generator of pain hypersensitivity by central neural plasticity J Pain 10 2009 895 926
8. C.J. Woolf Central sensitization: uncovering the relation between pain and plasticity Anesthesiology 106 2007 864 867
9. R. Ruscheweyh, O. Wilder-Smith, R. Drdla, X.G. Liu, and J. Sandkuhler Long-term potentiation in spinal nociceptive pathways as a novel target for pain therapy Mol Pain 7 2011 20
10. J. Sandkuhler Understanding LTP in pain pathways Mol Pain 3 2007 9
11. T.J. Price, and S. Ghosh ZIPping to pain relief: the role (or not) of PKMzeta in chronic pain Mol Pain 9 2013 6
12. D.B. Reichling, and J.D. Levine Critical role of nociceptor plasticity in chronic pain Trends Neurosci 32 2009 611 618
13. S.G. Dennis, and R. Melzack Self-mutilation after dorsal rhizotomy in rats: effects of prior pain and pattern of root lesions Exp Neurol 65 1979 412 421
14. J. Katz, and R. Melzack Pain 'memories' in phantom limbs: review and clinical observations Pain 43 1990 319 336
15. H. Flor, L. Nikolajsen, and T. Staehelin Jensen Phantom limb pain: a case of maladaptive CNS plasticity? Nat Rev Neurosci 7 2006 873 881
16. A. Vaso, H.M. Adahan, and A. Gjika Peripheral nervous system origin of phantom limb pain Pain 155 2014 1384 1391
17. T.J. Coderre, and R. Melzack Cutaneous hyperalgesia: contributions of the peripheral and central nervous systems to the increase in pain sensitivity after injury Brain Res 404 1987 95 106
18. E.R. Kandel The molecular biology of memory storage: a dialog between genes and synapses Biosci Rep 24 2004 475 522
19. P. De Camilli, and T.J. Carew Nobel celebrates the neurosciences. Modulatory signaling in the brain Cell 103 2000 829 833
20. A.L. Clatworthy, and E.T. Walters Rapid amplification and facilitation of mechanosensory discharge in Aplysia by noxious stimulation J Neurophysiol 70 1993 1181 1194
21. P.A. Illich, and E.T. Walters Mechanosensory neurons innervating Aplysia siphon encode noxious stimuli and display nociceptive sensitization J Neurosci 17 1997 459 469
22. R.M. Weragoda, E. Ferrer, and E.T. Walters Memory-like alterations in Aplysia axons after nerve injury or localized depolarization J Neurosci 24 2004 10393 10401
23. E.T. Walters, and L.L. Moroz Molluscan memory of injury: evolutionary insights into chronic pain and neurological disorders Brain Behav Evol 74 2009 206 218
24. R.J. Crook, K. Dickson, R.T. Hanlon, and E.T. Walters Nociceptive sensitization reduces predation risk Curr Biol 24 2014 1121 1125
25. T.J. Price, and G. Dussor Evolution: the advantage of 'maladaptive' pain plasticity Curr Biol 24 2014 R384 R386
26. O. Steward, and W.B. Levy Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus J Neurosci 2 1982 284 291
27. T.V. Bliss, and T. Lomo Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path J Physiol 232 1973 331 356
28. M. Costa-Mattioli, W.S. Sossin, E. Klann, and N. Sonenberg Translational control of long-lasting synaptic plasticity and memory Neuron 61 2009 10 26
29. G.J. Bassell, and S.T. Warren Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function Neuron 60 2008 201 214
30. W.C. Abraham, and J.M. Williams LTP maintenance and its protein synthesis-dependence Neurobiol Learn Mem 89 2008 260 268
31. T.J. Price, and S.M. Geranton Translating nociceptor sensitivity: the role of axonal protein synthesis in nociceptor physiology Eur J Neurosci 29 2009 2253 2263
32. T.C. Sacktor How does PKMzeta maintain long-term memory? Nat Rev Neurosci 12 2011 9 15
33. V. Brown, P. Jin, and S. Ceman Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome Cell 107 2001 477 487
34. J.C. Darnell, K.B. Jensen, P. Jin, V. Brown, S.T. Warren, and R.B. Darnell Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function Cell 107 2001 489 499
35. D. Willis, K.W. Li, and J.Q. Zheng Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons J Neurosci 25 2005 778 791
36. D.E. Willis, E.A. van Niekerk, and Y. Sasaki Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs J Cell Biol 178 2007 965 980
37. R.J. Weatheritt, T.J. Gibson, and M.M. Babu Asymmetric mRNA localization contributes to fidelity and sensitivity of spatially localized systems Nat Struct Mol Biol 21 2014 833 839
38. A. Tantos, K.H. Han, and P. Tompa Intrinsic disorder in cell signaling and gene transcription Mol Cell Endocrinol 348 2012 457 465
39. L. Boussemart, H. Malka-Mahieu, and I. Girault eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies Nature 513 2014 105 109
40. A.L. Wolfe, K. Singh, and Y. Zhong RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer Nature 513 2014 65 70
41. O. Bogen, N. Alessandri-Haber, C. Chu, R.W. Gear, and J.D. Levine Generation of a pain memory in the primary afferent nociceptor triggered by PKCepsilon activation of CPEB J Neurosci 32 2012 2018 2026
42. O.A. Dina, S.G. Khasar, R.W. Gear, and J.D. Levine Activation of Gi induces mechanical hyperalgesia poststress or inflammation Neuroscience 160 2009 501 507
43. L.F. Ferrari, O. Bogen, N. Alessandri-Haber, E. Levine, R.W. Gear, and J.D. Levine Transient decrease in nociceptor GRK2 expression produces long-term enhancement in inflammatory pain Neuroscience 222 2012 392 403
44. E.K. Joseph, and J.D. Levine Multiple PKCepsilon-dependent mechanisms mediating mechanical hyperalgesia Pain 150 2010 17 21
45. H. Wang, C.J. Heijnen, and C.T. van Velthoven Balancing GRK2 and EPAC1 levels prevents and relieves chronic pain J Clin Invest 123 2013 5023 5034
46. I. Topisirovic, and N. Sonenberg mRNA translation and energy metabolism in cancer: the role of the MAPK and mTORC1 pathways Cold Spring Harb Symp Quant Biol 76 2011 355 367
47. O.K. Melemedjian, G.L. Mejia, T.S. Lepow, O.K. Zoph, and T.J. Price Bidirectional regulation of P body formation mediated by eIF4F complex formation in sensory neurons Neurosci Lett 563 2013 169 174
48. O.K. Melemedjian, M.N. Asiedu, and D.V. Tillu IL-6- and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex J Neurosci 30 2010 15113 15123
49. M.N. Asiedu, D.V. Tillu, and O.K. Melemedjian Spinal protein kinase M zeta underlies the maintenance mechanism of persistent nociceptive sensitization J Neurosci 31 2011 6646 6653
50. D. Carling, C. Thornton, A. Woods, and M.J. Sanders AMP-activated protein kinase: new regulation, new roles? Biochem J 445 2012 11 27
51. K. Inoki, T. Zhu, and K.L. Guan TSC2 mediates cellular energy response to control cell growth and survival Cell 115 2003 577 590
52. S.N. Jakobsen, D.G. Hardie, N. Morrice, and H.E. Tornqvist 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside J Biol Chem 276 2001 46912 46916
53. C.H. Shen, P. Yuan, and R. Perez-Lorenzo Phosphorylation of BRAF by AMPK impairs BRAF-KSR1 association and cell proliferation Mol Cell 52 2013 161 172
54. T.J. Price, and G. Dussor AMPK: an emerging target for modification of injury-induced pain plasticity Neurosci Lett 557 2013 9 18
55. O.K. Melemedjian, M.N. Asiedu, and D.V. Tillu Targeting adenosine monophosphate-activated protein kinase (AMPK) in preclinical models reveals a potential mechanism for the treatment of neuropathic pain Mol Pain 7 2011 70
56. D.V. Tillu, O.K. Melemedjian, and M.N. Asiedu Resveratrol engages AMPK to attenuate ERK and mTOR signaling in sensory neurons and inhibits incision-induced acute and chronic pain Mol Pain 8 2012 5
57. O.Q. Russe, C.V. Moser, and K.L. Kynast Activation of the AMP-activated protein kinase reduces inflammatory nociception J Pain 14 2013 1330 1340
58. T.J. Price, and O.K. Melemedjian Fragile X mental retardation protein (FMRP) and the spinal sensory system Results Probl Cell Differ 54 2012 41 59
59. T.J. Price, M.H. Rashid, M. Millecamps, R. Sanoja, J.M. Entrena, and F. Cervero Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR J Neurosci 27 2007 13958 13967
60. J.D. Richter CPEB: a life in translation Trends Biochem Sci 32 2007 279 285
61. T. Udagawa, S.A. Swanger, and K. Takeuchi Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex Mol Cell 47 2012 253 266
62. L.F. Ferrari, O. Bogen, and J.D. Levine Role of nociceptor alphaCaMKII in transition from acute to chronic pain (hyperalgesic priming) in male and female rats J Neurosci 33 2013 11002 11011
63. 2 +/calmodulin-dependent protein kinase II and protein phosphatase 1 during hippocampal long-term potentiation J Neurosci 25 2005 5604 5610
64. K. Si, S. Lindquist, and E.R. Kandel A neuronal isoform of the aplysia CPEB has prion-like properties Cell 115 2003 879 891
65. K. Si, M. Giustetto, and A. Etkin A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia Cell 115 2003 893 904
66. O.K. Melemedjian, D.V. Tillu, and J.K. Moy Local translation and retrograde axonal transport of CREB regulates IL-6-induced nociceptive plasticity Mol Pain 10 2014 45
67. P.K. Dash, B. Hochner, and E.R. Kandel Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation Nature 345 1990 718 721
68. B.K. Kaang, E.R. Kandel, and S.G. Grant Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons Neuron 10 1993 427 435
69. E.J. Rahn, M.C. Guzman-Karlsson, and J. David Sweatt Cellular, molecular, and epigenetic mechanisms in non-associative conditioning: implications for pain and memory Neurobiol Learn Mem 105 2013 133 150
70. L.J. Cox, U. Hengst, N.G. Gurskaya, K.A. Lukyanov, and S.R. Jaffrey Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival Nat Cell Biol 10 2008 149 159
71. L.F. Ferrari, O. Bogen, C. Chu, and J.D. Levine Peripheral administration of translation inhibitors reverses increased hyperalgesia in a model of chronic pain in the rat J Pain 14 2013 731 738
72. J.R. Whitlock, A.J. Heynen, M.G. Shuler, and M.F. Bear Learning induces long-term potentiation in the hippocampus Science 313 2006 1093 1097
73. M. De Roo, P. Klauser, P.M. Garcia, L. Poglia, and D. Muller Spine dynamics and synapse remodeling during LTP and memory processes Prog Brain Res 169 2008 199 207
74. A.M. Tan, J.S. Choi, S.G. Waxman, and B.C. Hains Dendritic spine remodeling after spinal cord injury alters neuronal signal processing J Neurophysiol 102 2009 2396 2409
75. A.M. Tan, Y.W. Chang, P. Zhao, B.C. Hains, and S.G. Waxman Rac1-regulated dendritic spine remodeling contributes to neuropathic pain after peripheral nerve injury Exp Neurol 232 2011 222 233
76. A.M. Tan, S. Stamboulian, and Y.W. Chang Neuropathic pain memory is maintained by Rac1-regulated dendritic spine remodeling after spinal cord injury J Neurosci 28 2008 13173 13183
77. H. Ikeda, J. Stark, and H. Fischer Synaptic amplifier of inflammatory pain in the spinal dorsal horn Science 312 2006 1659 1662
78. A. Latremoliere, and C.J. Woolf Synaptic plasticity and central sensitization: author reply J Pain 11 2010 801 803
79. J. Sandkuhler Central sensitization versus synaptic long-term potentiation (LTP): a critical comment J Pain 11 2010 798 800
80. H. Fenselau, B. Heinke, and J. Sandkuhler Heterosynaptic long-term potentiation at GABAergic synapses of spinal lamina I neurons J Neurosci 31 2011 17383 17391
81. R. Drdla, M. Gassner, E. Gingl, and J. Sandkuhler Induction of synaptic long-term potentiation after opioid withdrawal Science 325 2009 207 210
82. R. Drdla-Schutting, J. Benrath, G. Wunderbaldinger, and J. Sandkuhler Erasure of a spinal memory trace of pain by a brief, high-dose opioid administration Science 335 2012 235 238
83. W. Ma, A. Ribeiro-da-Silva, Y. De Koninck, V. Radhakrishnan, A.C. Cuello, and J.L. Henry Substance P and enkephalin immunoreactivities in axonal boutons presynaptic to physiologically identified dorsal horn neurons. An ultrastructural multiple-labelling study in the cat Neuroscience 77 1997 793 811
84. A. Ribeiro-da-Silva, Y. De Koninck, A.C. Cuello, and J.L. Henry Enkephalin-immunoreactive nociceptive neurons in the cat spinal cord Neuroreport 3 1992 25 28
85. 2 + currents by a mu-opioid in a defined subset of rat sensory neurons J Neurosci 13 1993 867 873
86. 2 + currents, but spares a sustained current Neuron 6 1991 13 20
87. G. Corder, S. Doolen, and R.R. Donahue Constitutive mu-opioid receptor activity leads to long-term endogenous analgesia and dependence Science 341 2013 1394 1399
88. R.L. Huganir, and R.A. Nicoll AMPARs and synaptic plasticity: the last 25 years Neuron 80 2013 704 717
89. E. Pastalkova, P. Serrano, D. Pinkhasova, E. Wallace, A.A. Fenton, and T.C. Sacktor Storage of spatial information by the maintenance mechanism of LTP Science 313 2006 1141 1144
90. O.K. Melemedjian, D.V. Tillu, and M.N. Asiedu BDNF regulates atypical PKC at spinal synapses to initiate and maintain a centralized chronic pain state Mol Pain 9 2013 12
91. A. Laferriere, M.H. Pitcher, and A. Haldane PKMzeta is essential for spinal plasticity underlying the maintenance of persistent pain Mol Pain 7 2011 99
92. A.M. Lee, B.R. Kanter, and D. Wang Prkcz null mice show normal learning and memory Nature 493 2013 416 419
93. L.J. Volk, J.L. Bachman, R. Johnson, Y. Yu, and R.L. Huganir PKM-zeta is not required for hippocampal synaptic plasticity, learning and memory Nature 493 2013 420 423
94. P.V. Migues, O. Hardt, and D.C. Wu PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking Nat Neurosci 13 2010 630 634
95. Y.X. Tao AMPA receptor trafficking in inflammation-induced dorsal horn central sensitization Neurosci Bull 28 2012 111 120
96. A. Balkowiec, and D.M. Katz Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ J Neurosci 20 2000 7417 7423
97. S. Matayoshi, N. Jiang, and T. Katafuchi Actions of brain-derived neurotrophic factor on spinal nociceptive transmission during inflammation in the rat J Physiol 569 2005 685 695
98. S.M. Garraway, J.C. Petruska, and L.M. Mendell BDNF sensitizes the response of lamina II neurons to high threshold primary afferent inputs Eur J Neurosci 18 2003 2467 2476
99. B.J. Kerr, E.J. Bradbury, and D.L. Bennett Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord J Neurosci 19 1999 5138 5148
100. S. Pezet, M. Malcangio, and I.J. Lever Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn Mol Cell Neurosci 21 2002 684 695
101. R.J. Mannion, M. Costigan, and I. Decosterd Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity Proc Natl Acad Sci U S A 96 1999 9385 9390
102. J. Zhao, A. Seereeram, and M.A. Nassar Nociceptor-derived brain-derived neurotrophic factor regulates acute and inflammatory but not neuropathic pain Mol Cell Neurosci 31 2006 539 548
103. T. Trang, S. Beggs, and M.W. Salter Brain-derived neurotrophic factor from microglia: a molecular substrate for neuropathic pain Neuron Glia Biol 7 2011 99 108
104. Y. Lu, K. Christian, and B. Lu BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89 2008 312 323
105. L.J. Zhou, Y. Zhong, W.J. Ren, Y.Y. Li, T. Zhang, and X.G. Liu BDNF induces late-phase LTP of C-fiber evoked field potentials in rat spinal dorsal horn Exp Neurol 212 2008 507 514
106. K. Nader, and O. Hardt A single standard for memory: the case for reconsolidation Nat Rev Neurosci 10 2009 224 234
107. K. Nader, G.E. Schafe, and J.E. Le Doux Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval Nature 406 2000 722 726
108. R.P. Bonin, and Y. De Koninck A spinal analog of memory reconsolidation enables reversal of hyperalgesia Nat Neurosci 17 2014 1043 1045
109. W. Harris Persistent pain in lesions of the peripheral and central nervous system Br Med J 2 1921 896 900
110. R.B. Lipton Tracing transformation: chronic migraine classification, progression, and epidemiology Neurology 72 2009 S3 S7
111. M.E. Bigal, and R.B. Lipton Clinical course in migraine: conceptualizing migraine transformation Neurology 71 2008 848 855
112. J.D. Bartleson Low back pain Curr Treat Options Neurol 3 2001 159 168
113. J.D. Cassidy, P. Cote, L.J. Carroll, and V. Kristman Incidence and course of low back pain episodes in the general population Spine (Phila Pa 1976) 30 2005 2817 2823
114. T.S. Carey, J.M. Garrett, A. Jackman, and N. Hadler Recurrence and care seeking after acute back pain: results of a long-term follow-up study. North Carolina Back Pain Project Med Care 37 1999 157 164
115. E. Kolb, M. Canjuga, G.F. Bauer, and T. Laubli Course of back pain across 5 years: a retrospective cohort study in the general population of Switzerland Spine (Phila Pa 1976) 36 2011 E268 E273
116. M. Von Korff, and K. Saunders The course of back pain in primary care Spine (Phila Pa 1976) 21 1996 2833 2837 [discussion: 2838-2839]
117. G.B. Andersson Epidemiological features of chronic low-back pain Lancet 354 1999 581 585
118. O. Tamcan, A.F. Mannion, C. Eisenring, B. Horisberger, A. Elfering, and U. Muller The course of chronic and recurrent low back pain in the general population Pain 150 2010 451 457
119. P.R. Croft, M. Lewis, and A.C. Papageorgiou Risk factors for neck pain: a longitudinal study in the general population Pain 93 2001 317 325
120. P.S. Nolet, P. Cote, J.D. Cassidy, and L.J. Carroll The association between a lifetime history of a neck injury in a motor vehicle collision and future neck pain: a population-based cohort study Eur Spine J 19 2010 972 981
121. A. Althaus, A. Hinrichs-Rocker, and R. Chapman Development of a risk index for the prediction of chronic post-surgical pain Eur J Pain 16 2012 901 910
122. P.R. Pinto, T. McIntyre, R. Ferrero, A. Almeida, and V. Araujo-Soares Risk factors for moderate and severe persistent pain in patients undergoing total knee and hip arthroplasty: a prospective predictive study PLoS One 8 2013 e73917