A Review on the Role of Microglia in Diabetic Neuropathic Pain

doi:10.3969/j.issn.2095-1396.2016.03.008

Abstract

Abstract: Diabetic neuropathic pain （DNP） is one of the common chronic complications in patients with diabetes mellitus. Because of the complexity of its pathogenesis，the e xact causes of DNP are still unclear. In recent years，the role of microglia in DNP is concerned by researchers. In this review，we discussed the physiological and pathological characteristics of microglia. In addition，the related receptors and signaling pathways of microglia under DNP
condition were also reviewed. These insights provide a basis for new therapeutic approaches.

Key words: microglia, diabetic neuropathic pain, receptor, activation, polarization

HONG Li-mian, JIN Gui-lin, CHU Mei-mei, YU Chang-xi. A Review on the Role of Microglia in Diabetic Neuropathic Pain[J]. ACTA NEUROPHARMACOLOGICA, 2016, 6(3): 56-64.

References

[1] Caroline A Abbott, Rayaz A Malik, Ernest R E van Ross, et al. Prevalence and characteristics of painful diabetic neuropathy in a large community-based diabetic population in the U.K [J]. Diabetes care, 2011, 34(10): 2220-2224.

[2] Nicodemus J M, Enriquez C, Marquez A, et al. Murine model and mechanisms of treatment-induced painful diabetic neuropathy [J]. Neuroscience, 2017, 354:136-145.

[3] Niu Le, Dai Guang-hai, He Gao-le, et al. Decreased spinal endomorphin-2 contributes to mechanical allodynia in streptozotocin-induced diabetic rats [J]. Neurochemistry International, 2017, doi: 10.1016/j.neuint.2017.05.014.

[4] Nadia Zghoul, Edger L Ross, Robert R Edwards, et al. Prevalence of chronic pain with neuropathic characteristics: a randomized telephone survey among medical center patients in Kuwait [J]. J Pain Research, 2017, 10:679-87.

[5] Treede R D, Troels S Jensen, J N Campbell, et al. Neuropathic pain: redefinition and a grading system for clinical and research purposes [J]. Neurology, 2008, 70(18): 1630-1635.

[6] Andrei l Veresiu, Cosmina I Bondor, Bogdan Florea, et al. Detection of undisclosed neuropathy and assessment of its impact on quality of life: a survey in 25,000 Romanian patients with diabetes [J]. J Diabetes Complications, 2015, 29(5): 644-649.

[7] Irina G Obrosova. Diabetes and the peripheral nerve [J]. Biochimica et Biophysica Acta, 2009, 1792(10): 931-940.

[8] Mustafa Naziroglu, Dondu Merve Dikici, Seyda Dursun. Role of oxidative stress and Ca(2)(+) signaling on molecular pathways of neuropathic pain in diabetes: focus on TRP channels [J]. Neurochemical Research, 2012, 37(10): 2065-2075.

[9] Tanya Z Fischer, Stephen G Waxman. Neuropathic pain in diabetes-evidence for a central mechanism [J]. Nature Reviews Neurology, 2010, 6(8): 462-466.

[10] Wang Dong-mei, Rejean Couture, Hong Yan-guo. Activated microglia in the spinal cord underlies diabetic neuropathic pain [J]. J European Pharmacology, 2014, 728(1): 59-66.

[11] Joshua A Smith, Arabinda Das, Swapan K Ray, et al. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases [J]. Brain Research Bulletin, 2012, 87(1): 10-20.

[12] Marco Colonna, Oleg Butovsky. Microglia function in the central nervous system during health and neurodegeneration [J]. Annual Review Immunology, 2017, 35: 441-468.

[13] Francoise Alliot, Isabelle Godin, Bernard Pessac. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain [J]. Brain Research Developmental Brain Research, 1999, 117(2): 145-152.

[14] Florent Ginhoux, Melanie Greter, Marylene Leboeuf, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages [J]. Science, 2010, 330(6005): 841-845.

[15] Sheng Jian-peng, Christiane Ruedl, Klaus Karjalainen. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells [J]. Immunity, 2015, 43(2): 382-393.

[16] Kaoru Saijo, Christopher K Glass. Microglial cell origin and phenotypes in health and disease [J]. Nature Reviews Immunology, 2011, 11(11): 775-787.

[17] Ukpong B Eyo, Michael E Dailey. Microglia: key elements in neural development, plasticity, and pathology [J]. J Neuroimmune Pharmacology, 2013, 8(3): 494-509.

[18] Carol A Colton, Donna M Wilcock. Assessing activation states in microglia [J]. CNS & Neurological Disorders Drug Targets, 2010, 9(2): 174-191.

[19] Manuel B Graeber, Wolfgang J Streit. Microglia: biology and pathology [J]. Acta Neuropathologica, 2010, 119(1): 89-105.

[20] Zuzana Siskova, Marie-Eva Tremblay. Microglia and synapse: interactions in health and neurodegeneration [J]. Neural Plasticity, 2013, 2013(2013): 425845.

[21] Magadalena Zychowska, Ewelina Rojewska, Grzegorz Kreiner, et al. Minocycline influences the anti-inflammatory interleukins and enhances the effectiveness of morphine under mice diabetic neuropathy [J]. J Neuroimmunology, 2013, 262(1-2): 35-45.

[22] Magdalena Zychowska, Ewelina Rojewska, Anna Piotrowska, et al. Microglial inhibition influences XCL1/XCR1 expression and causes analgesic effects in a mouse model of diabetic neuropathy [J]. Anesthesiology, 2016, 125(3): 573-589.

[23] Sun Jin-shan, Yang Yu-jie, Zhang Yong-zhen, et al. Minocycline attenuates pain by inhibiting spinal microglia activation in diabetic rats [J]. Molecular Medicine Reports, 2015, 12(2): 2677-2682.

[24] Cheng K I, Wang H C, Chuang Y T, et al. Persistent mechanical allodynia positively correlates with an increase in activated microglia and increased P-p38 mitogen-activated protein kinase activation in streptozotocin-induced diabetic rats [J]. European journal of pain, 2014, 18(2): 162-173.

[25] Suzuki Naoko, Hasegawa-Moriyama Maiko, Takahashi Yoshika, et al. Lidocaine attenuates the development of diabetic-induced tactile allodynia by inhibiting microglial activation [J]. Anesthesia Analgesia, 2011, 113(4): 941-946.

[26] 张锦华, 杨承祥, 仲吉英, 等. 腰交感神经节射频对糖尿病神经病理性疼痛大鼠小胶质细胞活化的影响 [J]. 中华医学杂志, 2016, 96(24): 1934-1938.

[27] Makoto Tsuda. Microglia in the spinal cord and neuropathic pain [J]. J Diabetes Investigation, 2016, 7(1): 17-26.

[28] Giuliano F, Rampin O, Jardin A, et al. Electrophysiological study of relations between the dorsal nerve of the penis and the lumbar sympathetic chain in the rat [J]. J Urology, 1993, 150(6): 1960-1964.

[29] Starlee Lively, Lyanne C Schlichter. The microglial activation state regulates migration and roles of matrix-dissolving enzymes for invasion [J]. J Neuroinflammation, 2013, 10(1): 75.

[30] Samuel David, Antje Kroner. Repertoire of microglial and macrophage responses after spinal cord injury [J]. Nature Reviews Neuroscience, 2011, 12(7): 388-399.

[31] Li Cao, Cheng He. Polarization of macrophages and microglia in inflammatory demyelination [J]. Neuroscience Bulletin, 2013, 29(2): 189-198.

[32] Kristina A Kigerl, John C Gensel, Daniel P Ankeny, et al. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord [J]. J Neurosci, 2009, 29(43): 13435-13444.

[33] Antje Kroner, Andrew D Greenhalgh, Juan G Zarruk, et al. TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord [J]. Neuron, 2014, 83(5): 1098-1116.

[34] Kavita Pabreja, Kamal Dua, Saurabh Sharma, et al. Minocycline attenuates the development of diabetic neuropathic pain: possible anti-inflammatory and anti-oxidant mechanisms [J]. J European Pharmacology, 2011, 661(1-3): 15-21.

[35] Kazuyoshi Kobayashi, Shiro Imagama, T Ohgomori, et al. Minocycline selectively inhibits M1 polarization of microglia [J]. Cell Death & Disease, 2013, 4(3): e525.

[36] Ashit Syngle, Inderjeet Verma, Pawan Krishan, et al. Minocycline improves peripheral and autonomic neuropathy in type 2 diabetes: MIND study [J]. Neurological Sciences, 2014, 35(7): 1067-1073.

[37] 张昕. ATP调控小胶质细胞极化状态进而参与神经病理性疼痛的研究 [D]. 上海: 上海交通大学, 2015.

[38] Laurence Daulhac, Violette Maffre, Christophe Mallet, et al. Phosphorylation of spinal N-methyl-d-aspartate receptor NR1 subunits by extracellular signal-regulated kinase in dorsal horn neurons and microglia contributes to diabetes-induced painful neuropathy [J]. J European Pain, 2011, 15(2): 169 e1- e12.

[39] Zhou Hong-yi, Chen Shao-rui, Pan Hui-lin. Targeting N-methyl-D-aspartate receptors for treatment of neuropathic pain [J]. Expert Review Clinical Pharmacology, 2011, 4(3): 379-388.

[40] Young S Gwak, Jonghoon Kang, Geda C Unabia, et al. Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats [J]. Experimental Neurology, 2012, 234(2): 362-372.

[41] Ji Ru-rong, Temugin Berta, Maiken Nedergaard. Glia and pain: is chronic pain a gliopathy? [J]. Pain, 2013, 154 (Suppl 1):S10-28.

[42] Ji Ru-rong, Xu Zhen-zhong, Gao Yong-jing. Emerging targets in neuroinflammation-driven chronic pain [J]. Nature Reviews Drug Discovery, 2014, 13(7): 533-548.

[43]Anna K Clark, Doris Gruber-Schoffnegger, Ruth Drdla-Schutting, et al. Selective activation of microglia facilitates synaptic strength [J]. J Neuroscience, 2015, 35(11): 4552-4570.

[44] Qi Mao-song, Elaine A Elion. MAP kinase pathways [J]. J Cell Science, 2005, 118(Pt 16): 3569-3572.

[45] Liang Huang, Gao Yong-Jing, Jeffrey Wang, et al. Shifts in cell-type expression accompany a diminishing role of spinal p38-mapkinase activation over time during prolonged postoperative pain [J]. Anesthesiology, 2011, 115(6): 1281-1290.

[46] Laurence Daulhac, Christophe Mallet, Christine Courteix, et al. Diabetes-induced mechanical hyperalgesia involves spinal mitogen-activated protein kinase activation in neurons and microglia via N-methyl-D-aspartate-dependent mechanisms [J]. Molecular Pharmacology, 2006, 70(4): 1246-1254.

[47] Rachel Wodarski, Anna K Clark, John Grist, et al. Gabapentin reverses microglial activation in the spinal cord of streptozotocin-induced diabetic rats [J]. J European Pain, 2009, 13(8): 807-811.

[48] Cory C Toth, Nicole M Jedrzejewski, Connie L Ellis, et al. Cannabinoid-mediated modulation of neuropathic pain and microglial accumulation in a model of murine type I diabetic peripheral neuropathic pain [J]. Molecular Pain, 2010, 6(1):16.

[49] Li Yu-ying, Wei Xu-hong, Lu Zhen-he, et al. Src/p38 MAPK pathway in spinal microglia is involved in mechanical allodynia induced by peri-sciatic administration of recombinant rat TNF-alpha [J]. Brain Research Bulletin, 2013, 96(1):54-61.

[50] Zhuo Cheng-hua, Zhang Ming-xing, Zhou Sha-sha, et al. SIRT1 attenuates neuropathic pain by epigenetic regulation of mGluR1/5 expressions in type 2 diabetic rats [J]. Pain, 2017, 158(1): 130-139.

[51] Jae Sik Nam, Yu Seon Cheong, Myong Hwan Karm, et al. Effects of nefopam on streptozotocin-induced diabetic neuropathic pain in rats [J]. J Korean Pain, 2014, 27(4): 326-333.

[52] Tufan Mert, Hafize Oksuz, Berin Tugtag, et al. Modulating actions of NMDA receptors on pronociceptive effects of locally injected remifentanil in diabetic rats [J]. Pharmacological Reports, 2014, 66(6): 1065-1072.

[53] Hye Suk Hwang, Eun Jin Yang, Sang Min Lee, et al. Antiallodynic effects of electroacupuncture combined with MK-801 treatment through the regulation of p35/p25 in experimental diabetic neuropathy [J]. Experimental Neurobiology, 2011, 20(3): 144-152.

[54] Sebastien Talbot, Emma Chahmi, Jenny Pena Dias, et al. Key role for spinal dorsal horn microglial kinin B1 receptor in early diabetic pain neuropathy [J]. J Neuroinflammation, 2010, 7(1): 36.

[55] Sebastien Talbot, Rejean Couture. Emerging role of microglial kinin B1 receptor in diabetic pain neuropathy [J]. Experimental Neurology, 2012, 234(2): 373-381.

[56] 史蕾, 张弘弘, 胡吉, et al. 糖尿病神经病理性疼痛与嘌呤受体P2X(英文) [J]. 生理学报, 2012,(05): 531-542.

[57] Xu Guang-yin, Huang Li-Yen Mae. Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons [J]. J Neuroscience, 2002, 22(1): 93-102.

[58] Chen Yi-guang, Felix Scheupein, John P Driver, et al. Testing the role of P2X7 receptors in the development of type 1 diabetes in nonobese diabetic mice [J]. Journal of immunology, 2011, 186(7): 4278-84.

[59] 纳仁高娃, 塔娜, 米炎. P2X4受体在糖尿病神经病理性疼痛模型中的作用 [J]. 疾病监测与控制, 2015, 9(02): 63-65.

[60] 郭艳娇, 王高霞, 刘培雯, 等. MRS2211对糖尿病神经病理性疼痛大鼠的镇痛作用及可能的机制 [J]. 神经解剖学杂志, 2015,31(04): 465-469.

[61] 郭艳娇. 脊髓背角P2Y_（13）受体参与糖尿病大鼠神经病理性疼痛的实验研究 [D]遵义: 遵义医学院, 2016.

[62] Devi Rani Sager, James J Burston, Stephen G Woodhams, et al. Dynamic changes to the endocannabinoid system in models of chronic pain [J]. Philos Trans R Soc Lond B Biol Sci, 2012, 367(1607): 3300-3311.

[63] Gin C Hsieh, Madhavi Pai, Prasant Chandran, et al. Central and peripheral sites of action for CB(2) receptor mediated analgesic activity in chronic inflammatory and neuropathic pain models in rats [J]. J British Pharmacology, 2011, 162(2): 428-440.

[64]H Ikeda, M Ikegami, M Kai, et al. Activation of spinal cannabinoid CB2 receptors inhibits neuropathic pain in streptozotocin-induced diabetic mice [J]. Neuroscience, 2013, 250(8):446-54.

[65] Anne Schreiber, Manuele Neufeld, Carlos Jesus, et al. Peripheral antinociceptive effect of anandamide and drugs that affect the endocannabinoid system on the formalin test in normal and streptozotocin-diabetic rats [J]. Neuropharmacology, 2012, 63(8): 1286-1297.

[66] Donato Calabrese, Silvia Giatti, Simone Romano, et al. Diabetic neuropathic pain: a role for testosterone metabolites [J]. J Endocrinology, 2014, 221(1): 1-13.

[67] Nico Mitro, Gaia Cermenati, Silvia Giatti, et al. LXR and TSPO as new therapeutic targets to increase the levels of neuroactive steroids in the central nervous system of diabetic animals [J]. Neurochemistry international, 2012, 60(6): 616-21.

[68] Silvia Giatti, Marzia Pesaresi, Guido Cavaletti, et al. Neuroprotective effects of a ligand of translocator protein-18 kDa (Ro5-4864) in experimental diabetic neuropathy [J]. Neuroscience, 2009, 164(2): 520-529.