Neuroligin 2 regulates spinal GABAergic plasticity in hyperalgesic priming, a model of the transition from acute to chronic pain

Pain

Volumn 157, Issue 6, 2016, Pages 1314-1324

  Kim, Ji Young V ^a,b   Megat, Salim ^b   Moy, Jamie K ^a,b   Asiedu, Marina N ^b   Mejia, Galo L ^b   Vagner, Josef ^c   Price, Theodore J ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

BDNF; Dorsal horn; GABA; Hyperalgesic priming; Neuroligin 2

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; GABOXADOL; MESSENGER RNA; MIDAZOLAM; MUSCIMOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLIDE 2; NEUROLIGIN; NEUROLIGIN 1; NEUROLIGIN 2; PEPTIDE; POTASSIUM CHLORIDE COTRANSPORTER 2; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POLARITY; CHRONIC PAIN; CONTROLLED STUDY; DISEASE COURSE; DRUG TARGETING; GABAERGIC SYSTEM; HYPERALGESIA; HYPERSENSITIVITY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SPINAL CORD; SPINAL CORD DORSAL HORN; SYNAPTOGENESIS; ANIMAL; DISEASE MODEL; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACUTE PAIN; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULES, NEURONAL; CHRONIC PAIN; DISEASE MODELS, ANIMAL; GABAERGIC NEURONS; HYPERALGESIA; MICE; MICE, INBRED ICR; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PAIN THRESHOLD; SPINAL CORD;

EID: 84971216410     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000513     Document Type: Article

References (53)

1. Anseloni VCZ, Gold MS. Inflammation-induced shift in the valence of spinal GABA-A receptor-mediated modulation of nociception in the adult rat. J Pain 2008; 9: 732-8
2. Asiedu M, Ossipov MH, Kaila K, Price TJ. Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. PAIN 2010; 148: 302-8
3. Asiedu MN, Mejia G, Ossipov MK, Malan TP, Kaila K, Price TJ. Modulation of spinal GABAergic analgesia by inhibition of chloride extrusion capacity in mice. J Pain 2012; 13: 546-54
4. Asiedu MN, Mejia GL, Hubner CA, Kaila K, Price TJ. Inhibition of carbonic anhydrase augments GABAA receptor-mediated analgesia via a spinal mechanism of action. J Pain 2014; 15: 395-406
5. Asiedu MN, Tillu DV, Melemedjian OK, Shy A, Sanoja R, Bodell B, Ghosh S, Porreca F, Price TJ. Spinal protein kinase M zeta underlies the maintenance mechanism of persistent nociceptive sensitization. J Neurosci 2011; 31: 6646-53
6. Blundell J, Tabuchi K, Bolliger MF, Blaiss CA, Brose N, Liu X, Südhof TC, Powell CM. Increased anxiety-like behavior in mice lacking the inhibitory synapse cell adhesion molecule neuroligin 2. Genes Brain Behav 2009; 8: 114-26
7. Budreck EC, Kwon OB, Jung JH, Baudouin S, Thommen A, Kim HS, Fukazawa Y, Harada H, Tabuchi K, Shigemoto R, Scheiffele P, Kim JH. Neuroligin-1 controls synaptic abundance of NMDA-Type glutamate receptors through extracellular coupling. Proc Natl Acad Sci U S A 2013; 110: 725-30
8. Chapman CR, Casey KL, Dubner R, Foley KM, Gracely RH, Reading AE. Pain measurement: an overview. PAIN 1985; 22: 1-31
9. Chih B, Engelman H, Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005; 307: 1324-8
10. Chih B, Gollan L, Scheiffele P. Alternative splicing controls selective transsynaptic interactions of the neuroligin-neurexin complex. Neuron 2006; 51: 171-8
11. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, Südhof TC. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007; 54: 919-31
12. Corder G, Doolen S, Donahue RR, Winter MK, Jutras BL, He Y, Hu X, Wieskopf JS, Mogil JS, Storm DR, Wang ZJ, McCarson KE, Taylor BK. Constitutive mu-opioid receptor activity leads to long-Term endogenous analgesia and dependence. Science 2013; 341: 1394-9
13. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005; 438: 1017-21
14. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 2003; 424: 938-42
15. Dolique T, Favereaux A, Roca-Lapirot O, Roques V, Léger C, Landry M, Nagy F. Unexpected association of the inhibitory neuroligin 2 with excitatory PSD95 in neuropathic pain. PAIN 2013; 154: 2529-46
16. Doyon N, Prescott SA, Castonguay A, Godin AG, Kroger H, De Koninck Y. Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. PLoS Comput Biol 2011; 7: e1002149
17. Eaton MJ, Plunkett JA, Karmally S, Martinez MA, Montanez K. Changes in GAD-And GABA-immunoreactivity in the spinal dorsal horn after peripheral nerve injury and promotion of recovery by lumbar transplant of immortalized serotonergic precursors. J Chem Neuroanat 1998; 16: 57-72
18. Gagnon M, Bergeron MJ, Lavertu G, Castonguay A, Tripathy S, Bonin RP, Perez-Sanchez J, Boudreau D, Wang B, Dumas L, Valade I, Bachand K, Jacob-Wagner M, Tardif C, Kianicka I, Isenring P, Attardo G, Coull JA, De Koninck Y. Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat Med 2013; 19: 1524-8
19. Ibuki T, Hama AT, Wang XT, Pappas GD, Sagen J. Loss of GABAimmunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1996; 76: 845-58
20. Ichtchenko K, Nguyen T, Südhof TC. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 1996; 271: 2676-82
21. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW, Sudhof TC. Binding of neuroligins to PSD-95. Science 1997; 277: 1511-15
22. Josan JS, Vagner J, Handl HL, Sankaranarayanan R, Gillies RJ, Hruby VJ. Solid-phase synthesis of heterobivalent ligands targeted to melanocortin and cholecystokinin receptors. Int J Pept Res Ther 2008; 14: 293-300
23. Kaila K, Price TJ, Payne JA, Puskarjov M, Voipio J. Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat Rev Neurosci 2014; 15: 637-54
24. Kandasamy R, Price TJ. The pharmacology of nociceptor priming. Handb Exp Pharmacol 2015; 227: 15-37
25. Kerr BJ, Bradbury EJ, Bennett DL, Trivedi PM, Dassan P, French J, Shelton DB, McMahon SB, Thompson SW. Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci 1999; 19: 5138-48
26. Khirug S, Ahmad F, Puskarjov M, Afzalov R, Kaila K, Blaesse P. A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J Neurosci 2010; 30: 12028-35
27. Kim HY, Jun J, Wang J, Bittar A, Chung K, Chung JM. Induction of longterm potentiation and long-Term depression is cell-Type specific in the spinal cord. PAIN 2015; 156: 618-25
28. Kim JY, Tillu DV, Quinn TL, Mejia GL, Shy A, Asiedu MN, Murad E, Schumann AP, Totsch SK, Sorge RE, Mantyh PW, Dussor G, Price TJ. Spinal dopaminergic projections control the transition to pathological pain plasticity via a d1/d5-mediated mechanism. J Neurosci 2015; 35: 6307-17
29. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, Glick S, Ingrao J, Klassen-Ross T, Lacroix-Fralish ML, Matsumiya L, Sorge RE, Sotocinal SG, Tabaka JM, Wong D, van den Maagdenberg AM, Ferrari MD, Craig KD, Mogil JS. Coding of facial expressions of pain in the laboratory mouse. Nat Methods 2010; 7: 447-9
30. Lavertu G, Cote SL, De Koninck Y. Enhancing K-Cl co-Transport restores normal spinothalamic sensory coding in a neuropathic pain model. Brain 2014; 137(pt 3): 724-38
31. Lee KY, Prescott SA. Chloride dysregulation and inhibitory receptor blockade yield equivalent disinhibition of spinal neurons yet are differentially reversed by carbonic anhydrase blockade. PAIN 2015; 156: 2431-7
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-Time quantitative PCR and the 2-DDCT method. Methods 2001; 25: 402-8
33. Marvizon JC, Walwyn W, Minasyan A, Chen W, Taylor BK. Latent sensitization: a model for stress-sensitive chronic pain. Curr Protoc Neurosci 2015; 71: 9.50.1-9.50.14
34. Melemedjian OK, Tillu DV, Asiedu MN, Mandell EK, Moy JK, Blute VM, Taylor CJ, Ghosh S, Price TJ. BDNF regulates atypical PKC at spinal synapses to initiate and maintain a centralized chronic pain state. Mol Pain 2013; 9: 12
35. Nijs J, Meeus M, Versijpt J, Moens M, Bos I, Knaepen K, Meeusen R. Brain-derived neurotrophic factor as a driving force behind neuroplasticity in neuropathic and central sensitization pain: a new therapeutic target? Expert Opin Ther Targets 2015; 19: 565-76
36. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 2009; 63: 628-42
37. Prescott SA. Synaptic inhibition and disinhibition in the spinal dorsal horn. Prog Mol Biol Transl Sci 2015; 131: 359-83
38. Price TJ, Cervero F, De Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr Top Med Chem 2005; 5: 547-55
39. Price TJ, Cervero F, Gold MS, Hammond DL, Prescott SA. Chloride regulation in the pain pathway. Brain Res Rev 2009; 60: 149-70
40. Price TJ, Inyang KE. Commonalities between pain and memory mechanisms and their meaning for understanding chronic pain. Prog Mol Biol Transl Sci 2015; 131: 409-34
41. Price TJ, Prescott SA. Inhibitory regulation of the pain gate and how its failure causes pathological pain. PAIN 2015; 156: 789-92
42. Reichling DB, Green PG, Levine JD. The fundamental unit of pain is the cell. PAIN 2013; 154(suppl 1): S2-9
43. Reichling DB, Levine JD. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 2009; 32: 611-18
44. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 1991; 253: 872-9
45. Taylor BK, Corder G. Endogenous analgesia, dependence, and latent pain sensitization. Curr Top Behav Neurosci 2014; 20: 283-325
46. Tillu DV, Hassler SN, Burgos-Vega CC, Quinn TL, Sorge RE, Dussor G, Boitano S, Vagner J, Price TJ. Protease-Activated receptor 2 activation is sufficient to induce the transition to a chronic pain state. PAIN 2015; 156: 859-67
47. Vagner J, Xu L, Handl HL, Josan JS, Morse DL, Mash EA, Gillies RJ, Hruby VJ. Heterobivalent ligands crosslink multiple cell-surface receptors: the human melanocortin-4 and delta-opioid receptors. Angew Chem Int Ed Engl 2008; 47: 1685-8
48. van der Kooij MA, Fantin M, Kraev I, Korshunova I, Grosse J, Zanoletti O, Guirado R, Garcia-Mompo C, Nacher J, Stewart MG, Berezin V, Sandi C. Impaired hippocampal neuroligin-2 function by chronic stress or synthetic peptide treatment is linked to social deficits and increased aggression. Neuropsychopharmacology 2014; 39: 1148-58
49. Varoqueaux F, Jamain S, Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 2004; 83: 449-56
50. Vitureira N, Goda Y. Cell biology in neuroscience: the interplay between Hebbian and homeostatic synaptic plasticity. J Cell Biol 2013; 203: 175-86
51. Wang H, Yu SW, Koh DW, Lew J, Coombs C, Bowers W, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. Apoptosis-inducing factor substitutes for caspase executioners in NMDA-Triggered excitotoxic neuronal death. J Neurosci 2004; 24: 10963-73
52. Yowtak J, Wang J, Kim HY, Lu Y, Chung K, Chung JM. Effect of antioxidant treatment on spinal GABA neurons in a neuropathic pain model in the mouse. PAIN 2013; 154: 2469-76
53. Zhou LJ, Zhong Y, Ren WJ, Li YY, Zhang T, Liu XG. BDNF induces latephase LTP of C-fiber evoked field potentials in rat spinal dorsal horn. Exp Neurol 2008; 212: 507-14