Epigenetic regulation of chronic pain

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Morley S. Psychology of pain. Br. J. Anaesth. 101(1), 25–31 (2008).
  Medline CASGoogle Scholar
• 2 Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 10(9), 895–926 (2009).
  MedlineGoogle Scholar
• 3 Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 52(1), 77–92 (2006).
  Medline CASGoogle Scholar
• 4 Wang W, Gu J, Li YQ, Tao YX. Are voltage-gated sodium channels on the dorsal root ganglion involved in the development of neuropathic pain? Mol. Pain 7, 16 (2011).
  MedlineGoogle Scholar
• 5 Bali P, Im HI, Kenny PJ. Methylation, memory and addiction. Epigenetics 6(6), 671–674 (2011).
  Medline CASGoogle Scholar
• 6 Feng J, Zhou Y, Campbell SL et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 13(4), 423–430 (2010).
  Medline CASGoogle Scholar
• 7 Kramer JM, Kochinke K, Oortveld MA et al. Epigenetic regulation of learning and memory by Drosophila EHMT/G9a. PLoS Biol. 9(1), e1000569 (2011).
  Medline CASGoogle Scholar
• 8 Lutz BM, Bekker A, Tao YX. Noncoding RNAs: new players in chronic pain. Anesthesiology 121(2), 409–417 (2014).•• More updated review regarding the role of noncoding RNAs in chronic pain.
  Medline CASGoogle Scholar
• 9 Wang F, Stefano GB, Kream RM. Epigenetic modification of DRG neuronal gene expression subsequent to nerve injury: etiological contribution to complex regional pain syndromes (Part II). Med. Sci. Monit. 20, 1188–1200 (2014).
  Medline CASGoogle Scholar
• 10 Zovkic IB, Guzman-Karlsson MC, Sweatt JD. Epigenetic regulation of memory formation and maintenance. Learn. Mem. 20(2), 61–74 (2013).
  Medline CASGoogle Scholar
• 11 Mauck M, Van de Ven T, Shaw AD. Epigenetics of chronic pain after thoracic surgery. Curr. Opin. Anaesthesiol. 27(1), 1–5 (2014).
  MedlineGoogle Scholar
• 12 Rahn EJ, Guzman-Karlsson MC, David SJ. Cellular, molecular, and epigenetic mechanisms in non-associative conditioning: implications for pain and memory. Neurobiol. Learn. Mem. 105, 133–150 (2013).
  MedlineGoogle Scholar
• 13 Seo S, Grzenda A, Lomberk G, Ou XM, Cruciani RA, Urrutia R. Epigenetics: a promising paradigm for better understanding and managing pain. J. Pain 14(6), 549–557 (2013).
  Medline CASGoogle Scholar
• 14 Stone LS, Szyf M. The emerging field of pain epigenetics. Pain 154(1), 1–2 (2013).
  MedlineGoogle Scholar
• 15 Kouzarides T. Chromatin modifications and their function. Cell 128(4), 693–705 (2007).
  Medline CASGoogle Scholar
• 16 Kuo MH, Allis CD. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20(8), 615–626 (1998).
  Medline CASGoogle Scholar
• 17 Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 21(3), 381–395 (2011).
  Medline CASGoogle Scholar
• 18 Contestabile A, Sintoni S. Histone acetylation in neurodevelopment. Curr. Pharm. Des. 19(28), 5043–5050 (2013).
  Medline CASGoogle Scholar
• 19 Gong F, Miller KM. Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat. Res. 750(1–2), 23–30 (2013).
  Medline CASGoogle Scholar
• 20 Bai G, Wei D, Zou S, Ren K, Dubner R. Inhibition of class II histone deacetylases in the spinal cord attenuates inflammatory hyperalgesia. Mol. Pain 6, 51 (2010).
  MedlineGoogle Scholar
• 21 Chiechio S, Zammataro M, Morales ME et al. Epigenetic modulation of mGlu2 receptors by histone deacetylase inhibitors in the treatment of inflammatory pain. Mol. Pharmacol. 75(5), 1014–1020 (2009).
  Medline CASGoogle Scholar
• 22 Zhang Z, Cai YQ, Zou F, Bie B, Pan ZZ. Epigenetic suppression of GAD65 expression mediates persistent pain. Nat. Med. 17(11), 1448–1455 (2011).• Recognized the significant role of histone modefication in inflammatory pain
  Medline CASGoogle Scholar
• 23 Tran L, Chaloner A, Sawalha AH, Greenwood Van-Meerveld B. Importance of epigenetic mechanisms in visceral pain induced by chronic water avoidance stress. Psychoneuroendocrinology 38(6), 898–906 (2013).
  Medline CASGoogle Scholar
• 24 Kukkar A, Singh N, Jaggi AS. Attenuation of neuropathic pain by sodium butyrate in an experimental model of chronic constriction injury in rats. J. Formos. Med. Assoc. S0929–S6646(13), 00180 (2013).
  Google Scholar
• 25 Denk F, Huang W, Sidders B et al. HDAC inhibitors attenuate the development of hypersensitivity in models of neuropathic pain. Pain 154(9), 1668–1679 (2013).
  Medline CASGoogle Scholar
• 26 Matsushita Y, Araki K, Omotuyi O, Mukae T, Ueda H. HDAC inhibitors restore C-fibre sensitivity in experimental neuropathic pain model. Br. J. Pharmacol. 170(5), 991–998 (2013).
  Medline CASGoogle Scholar
• 27 Uchida H, Ma L, Ueda H. Epigenetic gene silencing underlies C-fiber dysfunctions in neuropathic pain. J. Neurosci. 30(13), 4806–4814 (2010).•• The first study to identify the role of histone modefication in neuropathic pain.
  Medline CASGoogle Scholar
• 28 Uchida H, Sasaki K, Ma L, Ueda H. Neuron-restrictive silencer factor causes epigenetic silencing of Kv4.3 gene after peripheral nerve injury. Neuroscience 166(1), 1–4 (2010).
  Medline CASGoogle Scholar
• 29 Uchida H, Matsushita Y, Ueda H. Epigenetic regulation of BDNF expression in the primary sensory neurons after peripheral nerve injury: implications in the development of neuropathic pain. Neuroscience 240, 147–154 (2013).
  Medline CASGoogle Scholar
• 30 Li K, Zhao GQ, Li LY, Wu GZ, Cui SS. Epigenetic upregulation of Cdk5 in the dorsal horn contributes to neuropathic pain in rats. Neuroreport 25(14), 1116–1121 (2014).
  Medline CASGoogle Scholar
• 31 Kiguchi N, Kobayashi Y, Maeda T et al. Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J. Pharmacol. Exp. Ther. 340(3), 577–587 (2012).
  Medline CASGoogle Scholar
• 32 Kiguchi N, Kobayashi Y, Saika F, Kishioka S. Epigenetic upregulation of CCL2 and CCL3 via histone modifications in infiltrating macrophages after peripheral nerve injury. Cytokine 64(3), 666–672 (2013).
  Medline CASGoogle Scholar
• 33 Zhu XY, Huang CS, Li Q et al. p300 exerts an epigenetic role in chronic neuropathic pain through its acetyltransferase activity in rats following chronic constriction injury (CCI). Mol. Pain 8, 84 (2012).
  Medline CASGoogle Scholar
• 34 Zhu XY, Huang CS, Li Q et al. Temporal distribution of p300/CBP immunoreactivity in the adult rat spinal dorsal horn following chronic constriction injury (CCI). Cell Mol. Neurobiol. 33(2), 197–204 (2013).
  Medline CASGoogle Scholar
• 35 Yin Q, Lu FF, Zhao Y et al. Resveratrol facilitates pain attenuation in a rat model of neuropathic pain through the activation of spinal Sirt1. Reg. Anesth. Pain Med. 38(2), 93–99 (2013).
  Medline CASGoogle Scholar
• 36 Sun Y, Liang D, Sahbaie P, Clark JD. Effects of methyl donor diets on incisional pain in mice. PLoS One 8(10), e77881 (2013).
  Medline CASGoogle Scholar
• 37 Sun Y, Sahbaie P, Liang DY et al. Epigenetic regulation of spinal CXCR2 signaling in incisional hypersensitivity in mice. Anesthesiology 119(5), 1198–1208 (2013).
  Medline CASGoogle Scholar
• 38 Mayer DJ, Mao J, Holt J, Price DD. Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions. Proc. Natl Acad. Sci. USA 96(14), 7731–7736 (1999).
  Medline CASGoogle Scholar
• 39 Liang DY, Li X, Clark JD. Epigenetic regulation of opioid-induced hyperalgesia, dependence, and tolerance in mice. J. Pain 14(1), 36–47 (2013).
  Medline CASGoogle Scholar
• 40 He X, Ou P, Wu K et al. Resveratrol attenuates morphine antinociceptive tolerance via SIRT1 regulation in the rat spinal cord. Neurosci. Lett. 566, 55–60 (2014).
  Medline CASGoogle Scholar
• 41 Cherng CH, Lee KC, Chien CC et al. Baicalin ameliorates neuropathic pain by suppressing HDAC1 expression in the spinal cord of spinal nerve ligation rats. J. Formos. Med. Assoc. 113(8), 513–520 (2014).
  Medline CASGoogle Scholar
• 42 Klein K, Ospelt C, Gay S. Epigenetic contributions in the development of rheumatoid arthritis. Arthritis Res. Ther. 14(6), 227 (2012).
  Medline CASGoogle Scholar
• 43 Covington HE III, Maze I, Sun H et al. A role for repressive histone methylation in cocaine-induced vulnerability to stress. Neuron 71(4), 656–670 (2011).
  Medline CASGoogle Scholar
• 44 Gupta S, Kim SY, Artis S et al. Histone methylation regulates memory formation. J. Neurosci. 30(10), 3589–3599 (2010).
  Medline CASGoogle Scholar
• 45 Maze I, Covington HE III, Dietz DM et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327(5962), 213–216 (2010).
  Medline CASGoogle Scholar
• 46 Imai S, Ikegami D, Yamashita A et al. Epigenetic transcriptional activation of monocyte chemotactic protein 3 contributes to long-lasting neuropathic pain. Brain 136(Pt 3), 828–843 (2013).
  MedlineGoogle Scholar
• 47 Tsai RY, Shen CH, Feng YP et al. Ultra-low-dose naloxone enhances the antinociceptive effect of morphine in PTX-treated rats: regulation on global histone methylation. Acta Anaesthesiol. Taiwan. 50(3), 106–111 (2012).
  MedlineGoogle Scholar
• 48 Zhang Z, Tao W, Hou YY, Wang W, Kenny PJ, Pan ZZ. MeCP2 repression of G9a in regulation of pain and morphine reward. J. Neurosci 34(27), 9076–9087 (2014).
  Medline CASGoogle Scholar
• 49 Chedin F, Lieber MR, Hsieh CL. The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Proc. Natl Acad. Sci. USA 99(26), 16916–16921 (2002).
  Medline CASGoogle Scholar
• 50 Jeltsch A. Molecular enzymology of mammalian DNA methyltransferases. Curr. Top. Microbiol. Immunol. 301, 203–225 (2006).
  Medline CASGoogle Scholar
• 51 Siedlecki P, Zielenkiewicz P. Mammalian DNA methyltransferases. Acta Biochim. Pol. 53(2), 245–256 (2006).
  Medline CASGoogle Scholar
• 52 Fatemi M, Hermann A, Gowher H, Jeltsch A. Dnmt3a and Dnmt1 functionally cooperate during de novo methylation of DNA. Eur. J. Biochem. 269(20), 4981–4984 (2002).
  Medline CASGoogle Scholar
• 53 Gowher H, Stockdale CJ, Goyal R, Ferreira H, Owen-Hughes T, Jeltsch A. De novo methylation of nucleosomal DNA by the mammalian Dnmt1 and Dnmt3A DNA methyltransferases. Biochemistry 44(29), 9899–9904 (2005).
  Medline CASGoogle Scholar
• 54 Liang G, Chan MF, Tomigahara Y et al. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell Biol. 22(2), 480–491 (2002).
  Medline CASGoogle Scholar
• 55 Lubin FD, Gupta S, Parrish RR, Grissom NM, Davis RL. Epigenetic mechanisms: critical contributors to long-term memory formation. Neuroscientist 17(6), 616–632 (2011).
  Medline CASGoogle Scholar
• 56 Mifsud KR, Gutierrez-Mecinas M, Trollope AF, Collins A, Saunderson EA, Reul JM. Epigenetic mechanisms in stress and adaptation. Brain Behav. Immun. 25(7), 1305–1315 (2011).
  Medline CASGoogle Scholar
• 57 Turek-Plewa J, Jagodzinski PP. The role of mammalian DNA methyltransferases in the regulation of gene expression. Cell Mol. Biol. Lett. 10(4), 631–647 (2005).
  Medline CASGoogle Scholar
• 58 Qi F, Zhou Y, Xiao Y et al. Promoter demethylation of cystathionine-beta-synthetase gene contributes to inflammatory pain in rats. Pain 154(1), 34–45 (2013).
  Medline CASGoogle Scholar
• 59 Pan Z, Zhu LJ, Li YQ et al. Epigenetic modification of spinal miR-219 expression regulates chronic inflammation pain by targeting CaMKIIgamma. J. Neurosci 34(29), 9476–9483 (2014).
  MedlineGoogle Scholar
• 60 Wang Y, Liu C, Guo QL et al. Intrathecal 5-azacytidine inhibits global DNA methylation and methyl-CpG-binding protein 2 expression and alleviates neuropathic pain in rats following chronic constriction injury. Brain Res. 1418, 64–69 (2011).• The first study to demonstrate the role of DNA methylation in neuropathic pain.
  Medline CASGoogle Scholar
• 61 Zhou XL, Yu LN, Wang Y et al. Increased methylation of the MOR gene proximal promoter in primary sensory neurons plays a crucial role in the decreased analgesic effect of opioids in neuropathic pain. Mol. Pain 10, 51 (2014).
  MedlineGoogle Scholar
• 62 Pollema-Mays SL, Centeno MV, Apkarian AV, Martina M. Expression of DNA methyltransferases in adult dorsal root ganglia is cell-type specific and up regulated in a rodent model of neuropathic pain. Front Cell Neurosci. 8, 217 (2014).
  MedlineGoogle Scholar
• 63 Tajerian M, Alvarado S, Millecamps M et al. Peripheral nerve injury is associated with chronic, reversible changes in global DNA methylation in the mouse prefrontal cortex. PLoS One 8(1), e55259 (2013).
  Medline CASGoogle Scholar
• 64 Menzies V, Lyon DE, Archer KJ et al. Epigenetic alterations and an increased frequency of micronuclei in women with fibromyalgia. Nurs. Res. Pract. 2013, 795784 (2013).
  MedlineGoogle Scholar
• 65 Tajerian M, Alvarado S, Millecamps M et al. DNA methylation of SPARC and chronic low back pain. Mol. Pain 7, 65 (2011).
  Medline CASGoogle Scholar
• 66 Viet CT, Ye Y, Dang D et al. Re-expression of the methylated EDNRB gene in oral squamous cell carcinoma attenuates cancer-induced pain. Pain 152(10), 2323–2332 (2011).
  Medline CASGoogle Scholar
• 67 Bell JT, Loomis AK, Butcher LM et al. Differential methylation of the TRPA1 promoter in pain sensitivity. Nat. Commun. 5, 2978 (2014).
  Medline CASGoogle Scholar
• 68 Karouzakis E, Gay RE, Michel BA, Gay S, Neidhart M. DNA hypomethylation in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum. 60(12), 3613–3622 (2009).
  Medline CASGoogle Scholar
• 69 Liu CC, Fang TJ, Ou TT et al. Global DNA methylation, DNMT1, and MBD2 in patients with rheumatoid arthritis. Immunol. Lett. 135(1–2), 96–99 (2011).
  Medline CASGoogle Scholar
• 70 Nakano K, Whitaker JW, Boyle DL, Wang W, Firestein GS. DNA methylome signature in rheumatoid arthritis. Ann. Rheum. Dis. 72(1), 110–117 (2013).
  Medline CASGoogle Scholar
• 71 Karouzakis E, Gay RE, Gay S, Neidhart M. Increased recycling of polyamines is associated with global DNA hypomethylation in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum. 64(6), 1809–1817 (2012).
  Medline CASGoogle Scholar
• 72 Klein K, Gay S. Epigenetic modifications in rheumatoid arthritis, a review. Curr. Opin. Pharmacol. 13(3), 420–425 (2013).
  Medline CASGoogle Scholar
• 73 Sansom OJ, Maddison K, Clarke AR. Mechanisms of disease: methyl-binding domain proteins as potential therapeutic targets in cancer. Nat. Clin Pract. Oncol. 4(5), 305–315 (2007).
  Medline CASGoogle Scholar
• 74 Cuddapah VA, Pillai RB, Shekar KV et al. Methyl-CpG-binding protein 2 (MECP2) mutation type is associated with disease severity in Rett syndrome. J. Med. Genet. 51(3), 152–158 (2014).
  Medline CASGoogle Scholar
• 75 Downs J, Geranton SM, Bebbington A et al. Linking MECP2 and pain sensitivity: the example of Rett syndrome. Am. J. Med. Genet. A 152A(5), 1197–1205 (2010).
  MedlineGoogle Scholar
• 76 Geranton SM, Fratto V, Tochiki KK, Hunt SP. Descending serotonergic controls regulate inflammation-induced mechanical sensitivity and methyl-CpG-binding protein 2 phosphorylation in the rat superficial dorsal horn. Mol. Pain 4, 350 (2008).• First study that demonstrated the involvement of MeCP2 in inflammatory pain.
  Google Scholar
• 77 Tochiki KK, Cunningham J, Hunt SP, Geranton SM. The expression of spinal methyl-CpG-binding protein 2, DNA methyltransferases and histone deacetylases is modulated in persistent pain states. Mol. Pain 8, 14 (2012).
  Medline CASGoogle Scholar
• 78 Chen WG, Chang Q, Lin Y et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302(5646), 885–889 (2003).
  Medline CASGoogle Scholar