Excess intracellular ATP causes neuropathic pain following spinal cord injury.
Astrocyte
Microglia
Neuroinflammation
Neuropathic pain
Purinergic receptor
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
16 Aug 2022
16 Aug 2022
Historique:
received:
07
06
2022
accepted:
01
08
2022
revised:
16
07
2022
entrez:
16
8
2022
pubmed:
17
8
2022
medline:
19
8
2022
Statut:
epublish
Résumé
Intractable neuropathic pain following spinal cord injury (NP-SCI) reduces a patient's quality of life. Excessive release of ATP into the extracellular space evokes neuroinflammation via purinergic receptor. Neuroinflammation plays an important role in the initiation and maintenance of NP. However, little is known about whether or not extracellular ATP cause NP-SCI. We found in the present study that excess of intracellular ATP at the lesion site evokes at-level NP-SCI. No significant differences in the body weight, locomotor function, or motor behaviors were found in groups that were negative and positive for at-level allodynia. The intracellular ATP level at the lesion site was significantly higher in the allodynia-positive mice than in the allodynia-negative mice. A metabolome analysis revealed that there were no significant differences in the ATP production or degradation between allodynia-negative and allodynia-positive mice. Dorsal horn neurons in allodynia mice were found to be inactivated in the resting state, suggesting that decreased ATP consumption due to neural inactivity leads to a build-up of intracellular ATP. In contrast to the findings in the resting state, mechanical stimulation increased the neural activity of dorsal horn and extracellular ATP release at lesion site. The forced production of intracellular ATP at the lesion site in non-allodynia mice induced allodynia. The inhibition of P2X4 receptors in allodynia mice reduced allodynia. These results suggest that an excess buildup of intracellular ATP in the resting state causes at-level NP-SCI as a result of the extracellular release of ATP with mechanical stimulation.
Identifiants
pubmed: 35972649
doi: 10.1007/s00018-022-04510-z
pii: 10.1007/s00018-022-04510-z
doi:
Substances chimiques
Adenosine Triphosphate
8L70Q75FXE
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
483Subventions
Organisme : Japan Society for the Promotion of Science
ID : JP19K09527
Organisme : Japan Society for the Promotion of Science
ID : JP22K09248
Organisme : Japan Agency for Medical Research and Development
ID : JP20ek0610017
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
von Hehn CA, Baron R, Woolf CJ (2012) Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73(4):638–652. https://doi.org/10.1016/j.neuron.2012.02.008
doi: 10.1016/j.neuron.2012.02.008
Ravenscroft A, Ahmed YS, Burnside IG (2000) Chronic pain after SCI A patient survey. Spinal cord 38(10):611–614. https://doi.org/10.1038/sj.sc.3101073
doi: 10.1038/sj.sc.3101073
pubmed: 11093322
Siddall PJ, McClelland JM, Rutkowski SB, Cousins MJ (2003) A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 103(3):249–257. https://doi.org/10.1016/S0304-3959(02)00452-9
doi: 10.1016/S0304-3959(02)00452-9
pubmed: 12791431
Rintala DH, Loubser PG, Castro J, Hart KA, Fuhrer MJ (1998) Chronic pain in a community-based sample of men with spinal cord injury: prevalence, severity, and relationship with impairment, disability, handicap, and subjective well-being. Arch Phys Med Rehabil 79(6):604–614. https://doi.org/10.1016/s0003-9993(98)90032-6
doi: 10.1016/s0003-9993(98)90032-6
pubmed: 9630137
Störmer S, Gerner HJ, Grüninger W, Metzmacher K, Föllinger S, Wienke C, Aldinger W, Walker N, Zimmermann M, Paeslack V (1997) Chronic pain/dysaesthesiae in spinal cord injury patients: results of a multicentre study. Spinal cord 35(7):446–455. https://doi.org/10.1038/sj.sc.3100411
doi: 10.1038/sj.sc.3100411
pubmed: 9232750
Siddall PJ, Middleton JW (2015) Spinal cord injury-induced pain: mechanisms and treatments. Pain Manag 5(6):493–507. https://doi.org/10.2217/pmt.15.47
doi: 10.2217/pmt.15.47
pubmed: 26402151
McMahon SB, Malcangio M (2009) Current challenges in glia-pain biology. Neuron 64(1):46–54. https://doi.org/10.1016/j.neuron.2009.09.033
doi: 10.1016/j.neuron.2009.09.033
pubmed: 19840548
Nakagawa T, Kaneko S (2010) Spinal astrocytes as therapeutic targets for pathological pain. J Pharmacol Sci 114(4):347–353. https://doi.org/10.1254/jphs.10r04cp
doi: 10.1254/jphs.10r04cp
pubmed: 21081837
Zhao P, Waxman SG, Hains BC (2007) Extracellular signal-regulated kinase-regulated microglia-neuron signaling by prostaglandin E2 contributes to pain after spinal cord injury. J Neurosci 27(9):2357–2368. https://doi.org/10.1523/JNEUROSCI.0138-07.2007
doi: 10.1523/JNEUROSCI.0138-07.2007
pubmed: 17329433
pmcid: 6673468
Theriault E, Frankenstein UN, Hertzberg EL, Nagy JI (1997) Connexin43 and astrocytic gap junctions in the rat spinal cord after acute compression injury. J Comp Neurol 382(2):199–214
doi: 10.1002/(SICI)1096-9861(19970602)382:2<199::AID-CNE5>3.0.CO;2-Z
Huang C, Han X, Li X, Lam E, Peng W, Lou N, Torres A, Yang M, Garre JM, Tian GF, Bennett MV, Nedergaard M, Takano T (2012) Critical role of connexin 43 in secondary expansion of traumatic spinal cord injury. J Neurosci 32(10):3333–3338. https://doi.org/10.1523/JNEUROSCI.1216-11.2012
doi: 10.1523/JNEUROSCI.1216-11.2012
pubmed: 22399755
pmcid: 3569730
Peng W, Cotrina ML, Han X, Yu H, Bekar L, Blum L, Takano T, Tian GF, Goldman SA, Nedergaard M (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc Natl Acad Sci USA 106(30):12489–12493. https://doi.org/10.1073/pnas.0902531106
doi: 10.1073/pnas.0902531106
pubmed: 19666625
pmcid: 2718350
Chen MJ, Kress B, Han X, Moll K, Peng W, Ji RR, Nedergaard M (2012) Astrocytic CX43 hemichannels and gap junctions play a crucial role in development of chronic neuropathic pain following spinal cord injury. Glia 60(11):1660–1670. https://doi.org/10.1002/glia.22384
doi: 10.1002/glia.22384
pubmed: 22951907
pmcid: 3604747
Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8(6):752–758. https://doi.org/10.1038/nn1472
doi: 10.1038/nn1472
pubmed: 15895084
Zhang ZJ, Jiang BC, Gao YJ (2017) Chemokines in neuron-glial cell interaction and pathogenesis of neuropathic pain. Cell Mol Life Sci 74(18):3275–3291. https://doi.org/10.1007/s00018-017-2513-1
doi: 10.1007/s00018-017-2513-1
pubmed: 28389721
Pfyffer D, Wyss PO, Huber E, Curt A, Henning A, Freund P (2020) Metabolites of neuroinflammation relate to neuropathic pain after spinal cord injury. Neurology 95(7):e805–e814. https://doi.org/10.1212/WNL.0000000000010003
doi: 10.1212/WNL.0000000000010003
pubmed: 32591473
pmcid: 7605501
Trang T, Salter MW (2012) P2X4 purinoceptor signaling in chronic pain. Purinergic Signal 8(3):621–628. https://doi.org/10.1007/s11302-012-9306-7
doi: 10.1007/s11302-012-9306-7
pubmed: 22528681
pmcid: 3360095
Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424(6950):778–783. https://doi.org/10.1038/nature01786
doi: 10.1038/nature01786
pubmed: 12917686
Schwab JM, Guo L, Schluesener HJ (2005) Spinal cord injury induces early and persistent lesional P2X4 receptor expression. J Neuroimmunol 163(1–2):185–189. https://doi.org/10.1016/j.jneuroim.2005.02.016
doi: 10.1016/j.jneuroim.2005.02.016
pubmed: 15885321
de Rivero Vaccari JP, Bastien D, Yurcisin G, Pineau I, Dietrich WD, De Koninck Y, Keane RW, Lacroix S (2012) P2X4 receptors influence inflammasome activation after spinal cord injury. J Neurosci 32(9):3058–3066. https://doi.org/10.1523/JNEUROSCI.4930-11.2012
doi: 10.1523/JNEUROSCI.4930-11.2012
pubmed: 22378878
pmcid: 6622016
Crown ED, Gwak YS, Ye Z, Johnson KM, Hulsebosch CE (2008) Activation of p38 MAP kinase is involved in central neuropathic pain following spinal cord injury. Exp Neurol 213(2):257–267. https://doi.org/10.1016/j.expneurol.2008.05.025
doi: 10.1016/j.expneurol.2008.05.025
pubmed: 18590729
pmcid: 2580737
Hains BC, Waxman SG (2006) Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26(16):4308–4317. https://doi.org/10.1523/JNEUROSCI.0003-06.2006
doi: 10.1523/JNEUROSCI.0003-06.2006
pubmed: 16624951
pmcid: 6674010
Inoue K, Tsuda M (2018) Microglia in neuropathic pain: cellular and molecular mechanisms and therapeutic potential. Nat Rev Neurosci 19(3):138–152. https://doi.org/10.1038/nrn.2018.2
doi: 10.1038/nrn.2018.2
pubmed: 29416128
Tsuda M, Masuda T, Tozaki-Saitoh H, Inoue K (2013) P2X4 receptors and neuropathic pain. Front Cell Neurosci 7:191. https://doi.org/10.3389/fncel.2013.00191
doi: 10.3389/fncel.2013.00191
pubmed: 24191146
pmcid: 3808787
Nakano M, Imamura H, Nagai T, Noji H (2011) Ca
doi: 10.1021/cb100313n
pubmed: 21488691
Yamamoto M, Kim M, Imai H, Itakura Y, Ohtsuki G (2019) Microglia-triggered plasticity of intrinsic excitability modulates psychomotor behaviors in acute cerebellar inflammation. Cell Rep 28(11):2923-2938.e8. https://doi.org/10.1016/j.celrep.2019.07.078
doi: 10.1016/j.celrep.2019.07.078
pubmed: 31509752
Long T, He W, Pan Q, Zhang S, Zhang Y, Liu C, Liu Q, Qin G, Chen L, Zhou J (2018) Microglia P2X4 receptor contributes to central sensitization following recurrent nitroglycerin stimulation. J Neuroinflammation 15(1):245. https://doi.org/10.1186/s12974-018-1285-3
doi: 10.1186/s12974-018-1285-3
pubmed: 30165876
pmcid: 6117935
Minett MS, Eijkelkamp N, Wood JN (2014) Significant determinants of mouse pain behaviour. PLoS ONE 9(8):e104458. https://doi.org/10.1371/journal.pone.0104458
doi: 10.1371/journal.pone.0104458
pubmed: 25101983
pmcid: 4125188
Lei BH, Chen JH, Yin HS (2014) Repeated amphetamine treatment alters spinal magnetic resonance signals and pain sensitivity in mice. Neurosci Lett 583:70–75. https://doi.org/10.1016/j.neulet.2014.09.031
doi: 10.1016/j.neulet.2014.09.031
pubmed: 25246351
Kikuta S, Nakamura Y, Yamamura Y, Tamura A, Homma N, Yanagawa Y, Tamura H, Kasahara J, Osanai M (2015) Quantitative activation-induced manganese-enhanced MRI reveals severity of Parkinson’s disease in mice. Sci Rep 5:12800. https://doi.org/10.1038/srep12800
doi: 10.1038/srep12800
pubmed: 26255701
pmcid: 4530460
Furue H, Narikawa K, Kumamoto E, Yoshimura M (1999) Responsiveness of rat substantia gelatinosa neurones to mechanical but not thermal stimuli revealed by in vivo patch-clamp recording. J Physiol 521(Pt 2):529–535. https://doi.org/10.1111/j.1469-7793.1999.00529.x
doi: 10.1111/j.1469-7793.1999.00529.x
pubmed: 10581321
pmcid: 2269671
Furue H, Sonohata M, Yoshimura M (2003) Nihon seirigaku zasshi. J Physiol Soc Jpn 65(10):315–321
Sugiyama D, Hur SW, Pickering AE, Kase D, Kim SJ, Kawamata M, Imoto K, Furue H (2012) In vivo patch-clamp recording from locus coeruleus neurones in the rat brainstem. J Physiol 590(10):2225–2231. https://doi.org/10.1113/jphysiol.2011.226407
doi: 10.1113/jphysiol.2011.226407
pubmed: 22371480
pmcid: 3424748
Funai Y, Pickering AE, Uta D, Nishikawa K, Mori T, Asada A, Imoto K, Furue H (2014) Systemic dexmedetomidine augments inhibitory synaptic transmission in the superficial dorsal horn through activation of descending noradrenergic control: an in vivo patch-clamp analysis of analgesic mechanisms. Pain 155(3):617–628. https://doi.org/10.1016/j.pain.2013.12.018
doi: 10.1016/j.pain.2013.12.018
pubmed: 24355412
Wong-Riley MT, Liang HL, Eells JT, Chance B, Henry MM, Buchmann E, Kane M, Whelan HT (2005) Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J Biol Chem 280(6):4761–4771. https://doi.org/10.1074/jbc.M409650200
doi: 10.1074/jbc.M409650200
pubmed: 15557336
Ying R, Liang HL, Whelan HT, Eells JT, Wong-Riley MT (2008) Pretreatment with near-infrared light via light-emitting diode provides added benefit against rotenone- and MPP+-induced neurotoxicity. Brain Res 1243:167–173. https://doi.org/10.1016/j.brainres.2008.09.057
doi: 10.1016/j.brainres.2008.09.057
pubmed: 18848925
pmcid: 3706077
Yu Z, Liu N, Zhao J, Li Y, McCarthy TJ, Tedford CE, Lo EH, Wang X (2015) Near infrared radiation rescues mitochondrial dysfunction in cortical neurons after oxygen-glucose deprivation. Metab Brain Dis 30(2):491–496. https://doi.org/10.1007/s11011-014-9515-6
doi: 10.1007/s11011-014-9515-6
pubmed: 24599760
Mochizuki-Oda N, Kataoka Y, Cui Y, Yamada H, Heya M, Awazu K (2002) Effects of near-infra-red laser irradiation on adenosine triphosphate and adenosine diphosphate contents of rat brain tissue. Neurosci Lett 323(3):207–210. https://doi.org/10.1016/s0304-3940(02)00159-3
doi: 10.1016/s0304-3940(02)00159-3
pubmed: 11959421
Ohnishi Y, Yamamoto M, Sugiura Y, Setoyama D, Kishima H (2021) Rostro-caudal different energy metabolism leading to differences in degeneration in spinal cord injury. Brain communications 3(2):fcab058. https://doi.org/10.1093/braincomms/fcab058
doi: 10.1093/braincomms/fcab058
pubmed: 33928249
pmcid: 8066884
Brambilla D, Chapman D, Greene R (2005) Adenosine mediation of presynaptic feedback inhibition of glutamate release. Neuron 46(2):275–283. https://doi.org/10.1016/j.neuron.2005.03.016
doi: 10.1016/j.neuron.2005.03.016
pubmed: 15848805
Manzoni OJ, Manabe T, Nicoll RA (1994) Release of adenosine by activation of NMDA receptors in the hippocampus. Science (New York, NY) 265(5181):2098–2101. https://doi.org/10.1126/science.7916485
doi: 10.1126/science.7916485
Lovatt D, Xu Q, Liu W, Takano T, Smith NA, Schnermann J, Tieu K, Nedergaard M (2012) Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci USA 109(16):6265–6270. https://doi.org/10.1073/pnas.1120997109
doi: 10.1073/pnas.1120997109
pubmed: 22421436
pmcid: 3341061
Badimon A, Strasburger HJ, Ayata P, Chen X, Nair A, Ikegami A, Hwang P, Chan AT, Graves SM, Uweru JO, Ledderose C, Kutlu MG, Wheeler MA, Kahan A, Ishikawa M, Wang YC, Loh YE, Jiang JX, Surmeier DJ, Robson SC, Schaefer A (2020) Negative feedback control of neuronal activity by microglia. Nature 586(7829):417–423. https://doi.org/10.1038/s41586-020-2777-8
doi: 10.1038/s41586-020-2777-8
pubmed: 32999463
pmcid: 7577179
Harris JJ, Jolivet R, Attwell D (2012) Synaptic energy use and supply. Neuron 75(5):762–777. https://doi.org/10.1016/j.neuron.2012.08.019
doi: 10.1016/j.neuron.2012.08.019
pubmed: 22958818
Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science (New York, NY) 263(5154):1768–1771. https://doi.org/10.1126/science.8134839
doi: 10.1126/science.8134839
Roh DH, Yoon SY, Seo HS, Kang SY, Han HJ, Beitz AJ, Lee JH (2010) Intrathecal injection of carbenoxolone, a gap junction decoupler, attenuates the induction of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 224(1):123–132. https://doi.org/10.1016/j.expneurol.2010.03.002
doi: 10.1016/j.expneurol.2010.03.002
pubmed: 20226782
Zündorf G, Kahlert S, Reiser G (2007) Gap-junction blocker carbenoxolone differentially enhances NMDA-induced cell death in hippocampal neurons and astrocytes in co-culture. J Neurochem 102(2):508–521. https://doi.org/10.1111/j.1471-4159.2007.04509.x
doi: 10.1111/j.1471-4159.2007.04509.x
pubmed: 17403140
Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26(35):8881–8891. https://doi.org/10.1523/JNEUROSCI.1302-06.2006
doi: 10.1523/JNEUROSCI.1302-06.2006
pubmed: 16943543
pmcid: 6675342
Oliet SH, Panatier A, Piet R, Mothet JP, Poulain DA, Theodosis DT (2008) Neuron-glia interactions in the rat supraoptic nucleus. Prog Brain Res 170:109–117. https://doi.org/10.1016/S0079-6123(08)00410-X
doi: 10.1016/S0079-6123(08)00410-X
pubmed: 18655876
Eroglu C, Barres BA (2010) Regulation of synaptic connectivity by glia. Nature 468(7321):223–231. https://doi.org/10.1038/nature09612
doi: 10.1038/nature09612
pubmed: 21068831
pmcid: 4431554
Pannasch U, Freche D, Dallérac G, Ghézali G, Escartin C, Ezan P, Cohen-Salmon M, Benchenane K, Abudara V, Dufour A, Lübke JH, Déglon N, Knott G, Holcman D, Rouach N (2014) Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 17(4):549–558. https://doi.org/10.1038/nn.3662
doi: 10.1038/nn.3662
pubmed: 24584052
Ullian EM, Christopherson KS, Barres BA (2004) Role for glia in synaptogenesis. Glia 47(3):209–216. https://doi.org/10.1002/glia.20082
doi: 10.1002/glia.20082
pubmed: 15252809
Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science (New York, NY) 291(5504):657–661. https://doi.org/10.1126/science.291.5504.657
doi: 10.1126/science.291.5504.657
Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29(10):3276–3287. https://doi.org/10.1523/JNEUROSCI.4707-08.2009
doi: 10.1523/JNEUROSCI.4707-08.2009
pubmed: 19279265
pmcid: 2819812
Wilhelmsson U, Li L, Pekna M, Berthold CH, Blom S, Eliasson C, Renner O, Bushong E, Ellisman M, Morgan TE, Pekny M (2004) Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J Neurosci 24(21):5016–5021. https://doi.org/10.1523/JNEUROSCI.0820-04.2004
doi: 10.1523/JNEUROSCI.0820-04.2004
pubmed: 15163694
pmcid: 6729371
Pekny M, Pekna M (2014) Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol Rev 94(4):1077–1098. https://doi.org/10.1152/physrev.00041.2013
doi: 10.1152/physrev.00041.2013
pubmed: 25287860
Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ, Haydon PG, Coulter DA (2010) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13(5):584–591. https://doi.org/10.1038/nn.2535
doi: 10.1038/nn.2535
pubmed: 20418874
pmcid: 3225960
Pósfai B, Cserép C, Orsolits B, Dénes Á (2019) New insights into microglia-neuron interactions: a neuron’s perspective. Neuroscience 405:103–117. https://doi.org/10.1016/j.neuroscience.2018.04.046
doi: 10.1016/j.neuroscience.2018.04.046
pubmed: 29753862
Fu H, Zhao Y, Hu D, Wang S, Yu T, Zhang L (2020) Depletion of microglia exacerbates injury and impairs function recovery after spinal cord injury in mice. Cell Death Dis 11(7):528. https://doi.org/10.1038/s41419-020-2733-4
doi: 10.1038/s41419-020-2733-4
pubmed: 32661227
pmcid: 7359318
Bellver-Landete V, Bretheau F, Mailhot B, Vallières N, Lessard M, Janelle ME, Vernoux N, Tremblay MÈ, Fuehrmann T, Shoichet MS, Lacroix S (2019) Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury. Nat Commun 10(1):518. https://doi.org/10.1038/s41467-019-08446-0
doi: 10.1038/s41467-019-08446-0
pubmed: 30705270
pmcid: 6355913
Freria CM, Hall JC, Wei P, Guan Z, McTigue DM, Popovich PG (2017) Deletion of the Fractalkine Receptor, CX3CR1, Improves Endogenous Repair, Axon Sprouting, and Synaptogenesis after Spinal Cord Injury in Mice. J Neurosci 37(13):3568–3587. https://doi.org/10.1523/JNEUROSCI.2841-16.2017
doi: 10.1523/JNEUROSCI.2841-16.2017
pubmed: 28264978
pmcid: 5373135
Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22(2):73–86. https://doi.org/10.1016/j.ijdevneu.2003.12.008
doi: 10.1016/j.ijdevneu.2003.12.008
pubmed: 15036382
Witcher MR, Kirov SA, Harris KM (2007) Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55(1):13–23. https://doi.org/10.1002/glia.20415
doi: 10.1002/glia.20415
pubmed: 17001633
Allen NJ, Eroglu C (2017) Cell biology of astrocyte-synapse interactions. Neuron 96(3):697–708. https://doi.org/10.1016/j.neuron.2017.09.056
doi: 10.1016/j.neuron.2017.09.056
pubmed: 29096081
pmcid: 5687890
Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22(1):183–192. https://doi.org/10.1523/JNEUROSCI.22-01-00183.2002
doi: 10.1523/JNEUROSCI.22-01-00183.2002
pubmed: 11756501
pmcid: 6757596
Wong ST, Atkinson BA, Weaver LC (2000) Confocal microscopic analysis reveals sprouting of primary afferent fibres in rat dorsal horn after spinal cord injury. Neurosci Lett 296(2–3):65–68. https://doi.org/10.1016/s0304-3940(00)01601-3
doi: 10.1016/s0304-3940(00)01601-3
pubmed: 11108982
O’Shea TM, Burda JE, Sofroniew MV (2017) Cell biology of spinal cord injury and repair. J Clin Investig 127(9):3259–3270. https://doi.org/10.1172/JCI90608
doi: 10.1172/JCI90608
pubmed: 28737515
pmcid: 5669582
Siddall PJ, Xu CL, Floyd N, Keay KA (1999) C-fos expression in the spinal cord of rats exhibiting allodynia following contusive spinal cord injury. Brain Res 851(1–2):281–286. https://doi.org/10.1016/s0006-8993(99)02173-3
doi: 10.1016/s0006-8993(99)02173-3
pubmed: 10642858
Anderson AJ, Cummings BJ, Cotman CW (1994) Increased immunoreactivity for Jun- and Fos-related proteins in Alzheimer’s disease: association with pathology. Exp Neurol 125(2):286–295. https://doi.org/10.1006/exnr.1994.1031
doi: 10.1006/exnr.1994.1031
pubmed: 8313943
Morishita T, Yamashita A, Katayama Y, Oshima H, Nishizaki Y, Shijo K, Fukaya C, Yamamoto T (2011) Chronological changes in astrocytes induced by chronic electrical sensorimotor cortex stimulation in rats. Neurol Med Chir 51(7):496–502. https://doi.org/10.2176/nmc.51.496
doi: 10.2176/nmc.51.496
Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7(6):423–436. https://doi.org/10.1038/nrn1928
doi: 10.1038/nrn1928
pubmed: 16715052
pmcid: 2062484
Fields RD, Ni Y (2010) Nonsynaptic communication through ATP release from volume-activated anion channels in axons. Sci Signal 3(142):ra73. https://doi.org/10.1126/scisignal.2001128
doi: 10.1126/scisignal.2001128
pubmed: 20923934
pmcid: 5023281
Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M, Fang YY, Zhang J, Li SJ, Xiong WC, Yan HC, Gao YB, Liu JH, Li XW, Sun LR, Zeng YN, Zhu XH, Gao TM (2013) Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med 19(6):773–777. https://doi.org/10.1038/nm.3162
doi: 10.1038/nm.3162
pubmed: 23644515
Turovsky EA, Braga A, Yu Y, Esteras N, Korsak A, Theparambil SM, Hadjihambi A, Hosford PS, Teschemacher AG, Marina N, Lythgoe MF, Haydon PG, Gourine AV (2020) Mechanosensory signaling in astrocytes. J Neurosci 40(49):9364–9371. https://doi.org/10.1523/JNEUROSCI.1249-20.2020
doi: 10.1523/JNEUROSCI.1249-20.2020
pubmed: 33122390
pmcid: 7724146
Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278(2):1354–1362. https://doi.org/10.1074/jbc.M209454200
doi: 10.1074/jbc.M209454200
pubmed: 12414798
Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40(5):971–982. https://doi.org/10.1016/s0896-6273(03)00717-7
doi: 10.1016/s0896-6273(03)00717-7
pubmed: 14659095
Fields RD (2011) Nonsynaptic and nonvesicular ATP release from neurons and relevance to neuron-glia signaling. Semin Cell Dev Biol 22(2):214–219. https://doi.org/10.1016/j.semcdb.2011.02.009
doi: 10.1016/j.semcdb.2011.02.009
pubmed: 21320624
pmcid: 3163842
Imura Y, Morizawa Y, Komatsu R, Shibata K, Shinozaki Y, Kasai H, Moriishi K, Moriyama Y, Koizumi S (2013) Microglia release ATP by exocytosis. Glia 61(8):1320–1330. https://doi.org/10.1002/glia.22517
doi: 10.1002/glia.22517
pubmed: 23832620
Tashima R, Koga K, Sekine M, Kanehisa K, Kohro Y, Tominaga K, Matsushita K, Tozaki-Saitoh H, Fukazawa Y, Inoue K, Yawo H, Furue H, Tsuda M (2018) Optogenetic activation of non-nociceptive Aβ fibers induces neuropathic pain-like sensory and emotional behaviors after nerve injury in rats. eNeuro. https://doi.org/10.1523/ENEURO.0450-17.2018
doi: 10.1523/ENEURO.0450-17.2018
pubmed: 29468190
pmcid: 5819669
Hildebrand ME, Xu J, Dedek A, Li Y, Sengar AS, Beggs S, Lombroso PJ, Salter MW (2016) Potentiation of synaptic GluN2B NMDAR currents by fyn kinase is gated through BDNF-mediated disinhibition in spinal pain processing. Cell Rep 17(10):2753–2765. https://doi.org/10.1016/j.celrep.2016.11.024
doi: 10.1016/j.celrep.2016.11.024
pubmed: 27926876
Inoue K, Tsuda M (2009) Microglia and neuropathic pain. Glia 57(14):1469–1479. https://doi.org/10.1002/glia.20871
doi: 10.1002/glia.20871
pubmed: 19306358
Ji RR, Xu ZZ, Gao YJ (2014) Emerging targets in neuroinflammation-driven chronic pain. Nat Rev Drug Discov 13(7):533–548. https://doi.org/10.1038/nrd4334
doi: 10.1038/nrd4334
pubmed: 24948120
pmcid: 4228377
Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F, Buell GN, Reeve AJ, Chessell IP, Rassendren F (2008) Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28(44):11263–11268. https://doi.org/10.1523/JNEUROSCI.2308-08.2008
doi: 10.1523/JNEUROSCI.2308-08.2008
pubmed: 18971468
pmcid: 6671487
Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438(7070):1017–1021. https://doi.org/10.1038/nature04223
doi: 10.1038/nature04223
pubmed: 16355225
Keller AF, Beggs S, Salter MW, De Koninck Y (2007) Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol Pain 3:27. https://doi.org/10.1186/1744-8069-3-27
doi: 10.1186/1744-8069-3-27
pubmed: 17900333
pmcid: 2093929
Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sík A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424(6951):938–942. https://doi.org/10.1038/nature01868
doi: 10.1038/nature01868
pubmed: 12931188
Tsuda M (2016) Microglia in the spinal cord and neuropathic pain. J Diabetes Investig 7(1):17–26. https://doi.org/10.1111/jdi.12379
doi: 10.1111/jdi.12379
pubmed: 26813032
Teng Y, Zhang Y, Yue S, Chen H, Qu Y, Wei H, Jia X (2019) Intrathecal injection of bone marrow stromal cells attenuates neuropathic pain via inhibition of P2X
doi: 10.1186/s12974-019-1631-0
Karu TI, Kolyakov SF (2005) Exact action spectra for cellular responses relevant to phototherapy. Photomed Laser Surg 23(4):355–361. https://doi.org/10.1089/pho.2005.23.355
doi: 10.1089/pho.2005.23.355
pubmed: 16144476
Karu TI (2010) Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62(8):607–610. https://doi.org/10.1002/iub.359
doi: 10.1002/iub.359
pubmed: 20681024
Yu W, Naim JO, McGowan M, Ippolito K, Lanzafame RJ (1997) Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochem Photobiol 66(6):866–871. https://doi.org/10.1111/j.1751-1097.1997.tb03239.x
doi: 10.1111/j.1751-1097.1997.tb03239.x
pubmed: 9421973
Passarella S (1989) He-Ne laser irradiation of isolated mitochondria. J Photochem Photobiol B 3(4):642–643. https://doi.org/10.1016/1011-1344(89)80090-9
doi: 10.1016/1011-1344(89)80090-9
pubmed: 2507765
Wu S, Zhou F, Wei Y, Chen WR, Chen Q, Xing D (2014) Cancer phototherapy via selective photoinactivation of respiratory chain oxidase to trigger a fatal superoxide anion burst. Antioxid Redox Signal 20(5):733–746. https://doi.org/10.1089/ars.2013.5229
doi: 10.1089/ars.2013.5229
pubmed: 23992126
pmcid: 3910666
Zupin L, Barbi E, Sagredini R, Ottaviani G, Crovella S, Celsi F (2021) In vitro effects of photobiomodulation therapy on 50B11 sensory neurons: evaluation of cell metabolism, oxidative stress, mitochondrial membrane potential (MMP), and capsaicin-induced calcium flow. J Biophotonics 14(2):e202000347. https://doi.org/10.1002/jbio.202000347
doi: 10.1002/jbio.202000347
pubmed: 33128434
Cho H, Jeon HJ, Park S, Park CS, Chung E (2020) Neurite growth of trigeminal ganglion neurons in vitro with near-infrared light irradiation. J Photochem Photobiol 210:111959. https://doi.org/10.1016/j.jphotobiol.2020.111959
doi: 10.1016/j.jphotobiol.2020.111959