Molluscan memory of mnjury: Evolutionary insights into Chronic pain and neurological disorders

Brain, Behavior and Evolution

Volumn 74, Issue 3, 2009, Pages 206-218

  Walters, Edgar T ^a   Moroz, Leonid L ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Aplysia; Evolution; Gene loss; Genome; Injury; Memory; Neurological disorders; Nociceptive sensitization; Pain

Indexed keywords

ANIMAL; CHRONIC DISEASE; EVOLUTION; GENETICS; HUMAN; INJURY; MEMORY; MOLLUSC; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; CHRONIC DISEASE; EVOLUTION; HUMANS; MEMORY; MOLLUSCA; NERVOUS SYSTEM DISEASES; NEURONAL PLASTICITY; PAIN; WOUNDS AND INJURIES;

EID: 73649115646     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000258667     Document Type: Review

References (119)

1. Adams DJ, Smith SJ, Thompson SH (1980) Ionic currents in molluscan soma. Annu Rev Neurosci 3: 141-167.
2. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89: 121-145.
3. Aley KO, McCarter G, Levine JD (1998) Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 18: 7008-7014.
4. Ali Z, Ringkamp M, Hartke TV, Chien HF, Flavahan NA, Campbell JN, Meyer RA (1999) Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J Neurophysiol 81: 455-466.
5. Ambron RT, Walters ET (1996) Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol 13: 61-79.
6. Ambron RT, Zhang XP, Gunstream JD, Povelones M, Walters ET (1996) Intrinsic injury signals enhance growth, survival, and excitability of Aplysia neurons. J Neurosci 16: 7469-7477.
7. Antonov I, Antonova I, Kandel ER, Hawkins RD (2001) The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia . J Neurosci 21: 6413-6422.
8. Antonov I, Ha T, Antonova I, Moroz LL, Hawkins, RD (2007) Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia . J Neurosci 27: 10993-11002
9. Babcock DT, Landry C, Galko MJ (2009) Cytokine signaling mediates UV-induced nociceptive sensitization in Drosophila larvae. Curr Biol 19: 799-806.
10. Bailey CH, Kandel ER (2008) Synaptic remodeling, synaptic growth and the storage of longterm memory in Aplysia . Prog Brain Res 169: 179-198.
11. Balaban PM (1980) Sensitization and habituation in command neurons of the defensive reflex in Helix lucorum . Neurosci Behav Physiol 10: 340-345.
12. Barco A, Bailey CH, Kandel ER (2006) Common molecular mechanisms in explicit and implicit memory. J Neurochem 97: 1520-1533.
13. Bedi SS, Salim A, Chen S, Glanzman DL (1998) Long-term effects of axotomy on excitability and growth of isolated Aplysia sensory neurons in cell culture: Potential role of cAMP. J Neurophysiol 79: 1371-1383.
14. Billy AJ, Walters ET (1989) Long-term expansion and sensitization of mechanosensory receptive fields in Aplysia support an activity-dependent model of whole-cell sensory plasticity. J Neurosci 9: 1254-1262.
15. Bradley J, Finkbeiner S (2002) An evaluation of specificity in activity-dependent gene expression in neurons. Prog Neurobiol 67: 469-477.
16. Breivik H, Collett B, Ventafridda V, Cohen R, Gallacher D (2006) Survey of chronic pain in Europe: Prevalence, impact on daily life, and treatment. Eur J Pain 10: 287-333.
17. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7: 575-590.
18. Byrne J, Castellucci V, Kandel ER (1974) Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia. J Neurophysiol 37: 1041-1064.
19. Carew TJ, Castellucci VF, Kandel ER (1971) An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia . Int J Neurosci 2: 79-98.
20. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99: 221-237.
21. Cash D, Carew TJ (1989) A quantitative analysis of the development of the central nervous system in juvenile Aplysia californica . J Neurobiol 20: 25-47.
22. Chase RB (2002) Behavior and its neural control in gastropod molluscs. Oxford, UK: Oxford University Press.
23. Cheng JK, Ji RR (2008) Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 33: 1970-1978.
24. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N (2009) Translational control of longlasting synaptic plasticity and memory. Neuron 61: 10-26.
25. De Roo M, Klauser P, Garcia PM, Poglia L, Muller D (2008) Spine dynamics and synapse remodeling during LTP and memory processes. Prog Brain Res 169: 199-207.
26. Devor M (2006) Sodium channels and mechanisms of neuropathic pain. J Pain 7:S3-S12.
27. Doucette R, Diamond J (1987) Normal and precocious sprouting of heat nociceptors in the skin of adult rats. J Comp Neurol 261: 592-603.
28. Drake TJ, Jezzini S, Lovell P, Moroz LL, Tan W (2005) Single cell glutamate analysis in Aplysia sensory neurons. J Neurosci Methods 144: 73-77.
29. Dulin MF, Steffensen I, Morris CE, Walters ET (1995) Recovery of function, peripheral sensitization and sensory neurone activation by novel pathways following axonal injury in Aplysia californica . J Exp Biol 198: 2055-2066.
30. Erez H, Spira ME (2008) Local self-assembly mechanisms underlie the differential transformation of the proximal and distal cut axonal ends into functional and aberrant growth cones. J Comp Neurol 507: 1019-1030.
31. Erickson MT, Walters ET (1988) Differential expression of pseudoconditioning and sensitization by siphon responses in Aplysia : Novel response selection after training. J Neurosci 8: 3000-3010.
32. Fantappie MR, Gimba ER, Rumjanek FD (2001) Lack of DNA methylation in Schistosoma mansoni . Exp Parasitol 98: 162-166.
33. Gasull X, Liao X, Dulin MF, Phelps C, Walters ET (2005) Evidence that long-term hyperexcitability of the sensory neuron soma induced by nerve injury in Aplysia is adaptive. J Neurophysiol 94: 2218-2230.
34. Gerhart J, Kirschner M (1997) Cells, Embryos, and Evolution: Toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability. Malden, MA: Blackwell Publishers.
35. Gibbs ME, Hutchinson D, Hertz L (2008) Astrocytic involvement in learning and memory consolidation. Neurosci Biobehav Rev 32: 927-944.
36. Gilbert DL, Adelman WJ, Arnold JM (1990) Squid as experimental animals. New York, NY: Plenum Press.
37. Gitler D, Spira ME (1998) Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 20: 1123-1135.
38. Glanzman DL (2008) New tricks for an old slug: The critical role of postsynaptic mechanisms in learning and memory in Aplysia . Prog Brain Res 169: 277-292.
39. Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514
40. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311: 395-398.
41. Gunstream JD, Castro GA, Walters ET (1995) Retrograde transport of plasticity signals in Aplysia sensory neurons following axonal injury. J Neurosci 15: 439-448.
42. Ha TJ, Kohn AB, Bobkova YV, Moroz LL (2006) Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea : Relevance to memory mechanisms. Biol Bull 210: 255-270.
43. Hosea Blewett HJ (2008) Exploring the mechanisms behind S-adenosylmethionine (SAMe) in the treatment of osteoarthritis. Crit Rev Food Sci Nutr 48: 458-463.
44. Hu JY, Chen Y, Schacher S (2007) Protein kinase C regulates local synthesis and secretion of a neuropeptide required for activity-dependent long-term synaptic plasticity. J Neurosci 27: 8927-8939.
45. Illich PA, Walters ET (1997) Mechanosensory neurons innervating Aplysia siphon encode noxious stimuli and display nociceptive sensitization. J Neurosci 17: 459-469.
46. Jankowsky JL, Patterson PH (1999) Cytokine and growth factor involvement in long-term potentiation. Mol Cell Neurosci 14: 273-286.
47. Jezzini SH, Bodnarova M, Moroz LL (2005) Twocolor in situ hybridization in the CNS of Aplysia californica . J Neurosci Methods 149: 15-25.
48. Ji RR, Kohno T, Moore KA, Woolf CJ (2003) Central sensitization and LTP: Do pain and memory share similar mechanisms? Trends Neurosci 26: 696-705.
49. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36: 57-68.
50. Jimenez-Diaz L, Geranton SM, Passmore GM, Leith JL, Fisher AS, Berliocchi L, Sivasubramaniam AK, Sheasby A, Lumb BM, Hunt SP (2008) Local translation in primary afferent fibers regulates nociception. PLoS ONE 3: E1961.
51. Kandel ER (1976) Cellular Basis of Behavior. San Francisco, CA: W.H. Freeman and Company.
52. Kandel ER (2001) The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
53. Knudsen B, Kohn AB, Nahir B, McFadden CS, Moroz LL (2006) Complete DNA sequence of the mitochondrial genome of the sea-slug, Aplysia californica : Conservation of the gene order in Euthyneura. Mol Phylogenet Evol 38: 459-469.
54. Kunjilwar KK, Fishman HM, Englot DJ, O'Neil RG, Walters ET (2009) Long-lasting hyperexcitability induced by depolarization in the absence of detectable Ca2+ signals. J Neurophysiol 101: 1351-1360.
55. Lai KO, Zhao Y, Ch'ng TH, Martin KC (2008) Importin-mediated retrograde transport of CREB2 from distal processes to the nucleus in neurons. Proc Natl Acad Sci USA, 105: 17175-17180.
56. Lee JA, Lim CS, Lee SH, Kim H, Nukina N, Kaang BK (2003) Aggregate formation and the impairment of long-term synaptic facilitation by ectopic expression of mutant huntingtin in Aplysia neurons. J Neurochem 85: 160-169.
57. Lee YS, Silva AJ (2009) The molecular and cellular biology of enhanced cognition. Nat Rev Neurosci 10: 126-140.
58. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, Malone LM, Sweatt JD (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281: 15763-15773.
59. Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2: 18-23.
60. Lin H, Bao J, Sung YJ, Walters ET, Ambron RT (2003) Rapid electrical and delayed molecular signals regulate the serum response element after nerve injury: Convergence of injury and learning signals. J Neurobiol 57: 204-220.
61. Lovell P, Jezzini SH, Moroz LL (2006) Electroporation of neurons and growth cones in Aplysia californica . J Neurosci Methods 151: 114-120.
62. Lovell P, Moroz LL (2006) The largest growth cones in the animal kingdom and dynamics of neuronal growth in cell culture of Aplysia. Int Comp Biol 46:847-870.
63. Lu X, Richardson PM (1991) Inflammation near the nerve cell body enhances axonal regeneration. J Neurosci 11: 972-978.
64. Lu Y, Christian K, Lu B (2008) BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89: 312-323.
65. Ma C, LaMotte RH (2005) Enhanced excitability of dissociated primary sensory neurons after chronic compression of the dorsal root ganglion in the rat. Pain 113: 106-112. (Pubitemid 40038451)
66. Mannion RJ, Costigan M, Decosterd I, Amaya F, Ma QP, Holstege JC, Ji RR, Acheson A, Lindsay RM, Wilkinson GA, Woolf CJ (1999) Neurotrophins: Peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc Natl Acad Sci USA 96: 9385-9390.
67. Marchand F, Perretti M, McMahon SB (2005) Role of the immune system in chronic pain. Nat Rev Neurosci 6: 521-532.
68. Merskey H, Bogduk N (1994) Part III: Pain terms, a current list with definitions and notes on usage. In: Classification of chronic pain, IASP task force on taxonomy (Merskey H, Bogduk N, eds), pp 209-214. Seattle, WA: IASP Press.
69. Moccia R, Chen D, Lyles V, Kapuya E, E Y, Kalachikov S, Spahn CM, Frank J, Kandel ER, Barad M, Martin KC (2003) An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J Neurosci 23: 9409-9417.
70. Moroz LL, Dahlgren RL, Boudko D, Sweedler JV, Lovell P (2005) Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. J Inorg Biochem 99: 929-939.
71. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, Russo JJ, Ju J, Kandel ER (2006) Neuronal transcriptome of Aplysia : Neuronal compartments and circuitry. Cell 127: 1453-1467.
72. Moroz LL, Gyori J, Salanki J (1993) NMDA-like receptors in the CNS of molluscs. Neuroreport 4: 201-204.
73. Moroz LL, Ju J, Russo JJ, Puthanveetti S, Kohn A, Medina M, Walsh PJ, Birren B, Lander ES, Kandel ER (2004) Sequencing the Aplysia genome: A model for single cell, real-time and comparative genomics. http://www.genome. gov/Pages/Research/Sequencing/SeqProposals/ AplysiaSeq.pdf
74. Nicholls JG, Baylor DA (1968) Specific modalities and receptive fields of sensory neurons in CNS of the leech. J Neurophysiol 31: 740-756.
75. Obata K, Noguchi K (2004) MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci 74: 2643-2653.
76. Ochoa JL, Campero M, Serra J, Bostock H (2005) Hyperexcitable polymodal and insensitive nociceptors in painful human neuropathy. Muscle Nerve 32: 459-472.
77. Ota KT, Pierre VJ, Ploski JE, Queen K, Schafe GE (2008) The NO-cGMP-PKG signaling pathway regulates synaptic plasticity and fear memory consolidation in the lateral amygdala via activation of ERK/MAP kinase. Learn Mem 15: 792-805.
78. Otis KO, Thompson KR, Martin KC (2006) Importin- mediated nuclear transport in neurons. Curr Opin Neurobiol 16: 329-335.
79. Panchin Y, Moroz LL (2008) Molluscan mobile elements similar to the vertebrate recombination- activating genes. Biochem Biophys Res Commun 369: 818-823.
80. Pastor J, Soria B, Belmonte C (1996) Properties of the nociceptive neurons of the leech segmental ganglion. J Neurophysiol 75: 2268-2279.
81. Pezet S, McMahon SB (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538.
82. Price TJ, Rashid MH, Millecamps M, Sanoja R, Entrena JM, Cervero F (2007) Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: Role of mGluR1/5 and mTOR. J Neurosci 27: 13958-13967.
83. Purcell AL, Carew TJ (2003) Tyrosine kinases, synaptic plasticity and memory: Insights from vertebrates and invertebrates. Trends Neurosci 26: 625-630.
84. Rae PM, Steele RE (1979) Absence of cytosine methylation at C-C-G-G and G-C-G-C sites in the rDNA coding regions and intervening sequences of Drosophila and the rDNA of other insects. Nucleic Acids Res 6: 2987-2995.
85. Rao VR, Finkbeiner S (2007) NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 30: 284-291.
86. Saha RN, Dudek SM (2008) Action potentials: To the nucleus and beyond. Exp Biol Med (Maywood) 233: 385-393.
87. Samarova EI, Bravarenko NI, Korshunova TA, Gulyaeva NV, Palotas A, Balaban PM (2005) Effect of beta-amyloid peptide on behavior and synaptic plasticity in terrestrial snail. Brain Res Bull 67: 40-45.
88. Satpute-Krishnan P, DeGiorgis JA, Bearer EL (2003) Fast anterograde transport of herpes simplex virus: Role for the amyloid precursor protein of alzheimer's disease. Aging Cell 2: 305-318.
89. Shea VK, Perl ER (1985) Regeneration of cutaneous afferent unmyelinated (C) fibers after transection. J Neurophysiol 54: 502-512.
90. Shemesh OA, Erez H, Ginzburg I, Spira ME (2008) Tau-induced traffic jams reflect organelles accumulation at points of microtubule polar mismatching. Traffic 9: 458-471.
91. Shim B, Kim DW, Kim BH, Nam TS, Leem JW, Chung JM (2005) Mechanical and heat sensitization of cutaneous nociceptors in rats with experimental peripheral neuropathy. Neuroscience 132: 193-201.
92. Simpson VJ, Johnson TE, Hammen RF (1986) Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res 14: 6711-6719.
93. Smith DS, Skene JH (1997) A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosci 17: 646-658.
94. Sossin WS (2008) Molecular memory traces. Prog Brain Res 169: 3-25.
95. Steffensen I, Dulin MF, Walters ET, Morris CE (1995) Peripheral regeneration and central sprouting of sensory neurone axons in Aplysia californica following nerve injury. J Exp Biol 198: 2067-2078.
96. Sung YJ, Ambron RT (2004) Pathways that elicit long-term changes in gene expression in nociceptive neurons following nerve injury: Contributions to neuropathic pain. Neurol Res 26: 195-203.
97. Sung YJ, Walters ET, Ambron RT (2004) A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24: 7583-7595.
98. Suzuki MM, Bird A (2008) DNA methylation landscapes: Provocative insights from epigenomics. Nat Rev Genet 9: 465-476.
99. Tamura S, Morikawa Y, Senba E (2005) Up-regulated phosphorylation of signal transducer and activator of transcription 3 and cyclic AMP-responsive element binding protein by peripheral inflammation in primary afferent neurons possibly through oncostatin M receptor. Neuroscience 133: 797-806.
100. Teng FY, Tang BL (2006) Axonal regeneration in adult CNS neurons - signaling molecules and pathways. J Neurochem 96: 1501-1508.
101. Tobin DM, Bargmann CI (2004) Invertebrate nociception: Behaviors, neurons and molecules. J Neurobiol 61: 161-174.
102. Tracey WD Jr, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila gene essential for nociception. Cell 113: 261-273.
103. Valentine JW (2004) On the origin of phyla. Chicago, IL: University of Chicago Press.
104. Walters ET (1987a) Multiple sensory neuronal correlates of site-specific sensitization in Aplysia . J Neurosci 7: 408-417.
105. Walters ET (1987b) Site-specific sensitization of defensive reflexes in Aplysia : A simple model of long-term hyperalgesia. J Neurosci 7: 400-407.
106. Walters ET (1991) A functional, cellular, and evolutionary model of nociceptive plasticity in Aplysia . Biol Bull 180: 241-251.
107. Walters ET (1994) Injury-related behavior and neuronal plasticity: An evolutionary perspective on sensitization, hyperalgesia, and analgesia. Int Rev Neurobiol 36: 325-427.
108. Walters ET (2008) Evolutionary aspects of pain. In: The senses: A comprehensive reference, volume 5. Pain (Basbaum A, Bushnell CM, eds), pp 175-184. Burlington, MA: Academic Press/Elsevier.
109. Walters ET, Alizadeh H, Castro GA (1991) Similar neuronal alterations induced by axonal injury and learning in Aplysia . Science 253: 797-799.
110. Walters ET, Bodnarova M, Billy AJ, Dulin MF, Diaz-Rios M, Miller MW, Moroz LL (2004) Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica . J Comp Neurol 471: 219-240.
111. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983) Mechanoafferent neurons innervating tail of Aplysia . I. Response properties and synaptic connections. J Neurophysiol 50: 1522-1542.
112. Walters ET, Fishman HM, Yang Q, Du J, Bedi SS, Carlton SM, Grill RJ (2008) Spontaneous activity in small DRG neurons following spinal cord injury may contribute to chronic neuropathic pain. Soc Neurosci Abstr Viewer/Itinerary Planner, Program 368.21
113. Waxman SG, Kocsis JD, Black JA (1994) Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 72: 466-470.
114. Weragoda RM, Ferrer E, Walters ET (2004) Memory-like alterations in Aplysia axons after nerve injury or localized depolarization. J Neurosci 24: 10393-10401.
115. Weragoda RM, Walters ET (2007) Serotonin induces memory-like, rapamycin-sensitive hyperexcitability in sensory axons of aplysia that contributes to injury responses. J Neurophysiol 98: 1231-1239.
116. Woolf CJ, Costigan M (1999) Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc Natl Acad Sci USA 96: 7723-7730.
117. Woolf CJ, Ma Q (2007) Nociceptors - noxious stimulus detectors. Neuron 55: 353-364.
118. Xu J, Kang J (2005) The mechanisms and functions of activity-dependent long-term potentiation of intrinsic excitability. Rev Neurosci 16: 311-323. (Pubitemid 43185083)
119. Zheng JH, Walters ET, Song XJ (2007) Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J Neurophysiol 97: 15-25.