173
Views
2
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

The Role of Bone Morphogenetic Protein 4 in Microglial Polarization in the Process of Neuropathic Pain

, , , , & ORCID Icon
Pages 2803-2817 | Published online: 03 May 2022

References

  • Finnerup NB, Kuner R, Jensen TS. Neuropathic pain: from mechanisms to treatment. Physiol Rev. 2021;101(1):259–301. doi:10.1152/physrev.00045.2019
  • Tiwari V, Guan Y, Raja SN. Modulating the delicate glial-neuronal interactions in neuropathic pain: promises and potential caveats. Neurosci Biobehav Rev. 2014;45:19–27. doi:10.1016/j.neubiorev.2014.05.002
  • Pinho-Ribeiro FA, Verri WA, Chiu IM. Nociceptor sensory neuron-immune interactions in pain and inflammation. Trends Immunol. 2017;38(1):5–19. doi:10.1016/j.it.2016.10.001
  • Calvo M, Bennett DL. The mechanisms of microgliosis and pain following peripheral nerve injury. Exp Neurol. 2012;234(2):271–282. doi:10.1016/j.expneurol.2011.08.018
  • Clark AK, Old EA, Malcangio M. Neuropathic pain and cytokines: current perspectives. J Pain Res. 2013;6:803–814. doi:10.2147/JPR.S53660
  • Xu F, Huang J, He Z, et al. Microglial polarization dynamics in dorsal spinal cord in the early stages following chronic sciatic nerve damage. Neurosci Lett. 2016;617:6–13. doi:10.1016/j.neulet.2016.01.038
  • Gong X, Chen Y, Fu B, Jiang J, Zhang M. Infant nerve injury induces delayed microglial polarization to the M1 phenotype, and exercise reduces delayed neuropathic pain by modulating microglial activity. Neuroscience. 2017;349:76–86. doi:10.1016/j.neuroscience.2017.02.051
  • Xu N, Tang XH, Pan W, et al. Spared nerve injury increases the expression of microglia M1 markers in the prefrontal cortex of rats and provokes depression-like behaviors. Front Neurosci. 2017;11:209. doi:10.3389/fnins.2017.00209
  • Lowery JW, Rosen V. Bone morphogenetic protein-based therapeutic approaches. Cold Spring Harb Perspect Biol. 2018;10(4):a022327. doi:10.1101/cshperspect.a022327
  • Wang Y, Cheng X, He Q, et al. Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci. 2011;31(16):6053–6058. doi:10.1523/JNEUROSCI.5524-09.2011
  • Cole AE, Murray SS, Xiao J. Bone morphogenetic protein 4 signalling in neural stem and progenitor cells during development and after injury. Stem Cells Int. 2016;2016:9260592. doi:10.1155/2016/9260592
  • Miyagi M, Mikawa S, Sato T, et al. BMP2, BMP4, noggin, BMPRIA, BMPRIB, and BMPRII are differentially expressed in the adult rat spinal cord. Neuroscience. 2012;203:12–26. doi:10.1016/j.neuroscience.2011.12.022
  • Yang L, Liu S, Wang Y. Role of bone morphogenetic protein-2/4 in astrocyte activation in neuropathic pain. Mol Pain. 2019;15:1744806919892100. doi:10.1177/17448069.19892100
  • Hashimoto M, Koda M, Furuya T, Murata A, Yamazaki M, Takahashi K. Intrathecal Noggin administration in rats temporally ameliorates mechanical allodynia induced by a chronic constriction injury. eNeurologicalSci. 2016;4:4–9. doi:10.1016/j.ensci.2016.03.001
  • Westin BD, Walker SM, Deumens R, Grafe M, Yaksh TL. Validation of a preclinical spinal safety model: effects of intrathecal morphine in the neonatal rat. Anesthesiology. 2010;113(1):183–199. doi:10.1097/ALN.0b013e3181dcd6ec
  • Chung JM, Kim HK, Chung K. Segmental spinal nerve ligation model of neuropathic pain. Methods Mol Med. 2004;99:35–45. doi:10.1385/1-59259-770-X:035
  • Helbing T, Arnold L, Wiltgen G, et al. Endothelial BMP4 regulates leukocyte diapedesis and promotes inflammation. Inflammation. 2017;40(6):1862–1874. doi:10.1007/s10753-017-0627-0
  • Sorescu GP, Song H, Tressel SL, et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress induces monocyte adhesion by stimulating reactive oxygen species production from a nox1-based NADPH oxidase. Circ Res. 2004;95(8):773–779. doi:10.1161/01.RES.0000145728.22878.45
  • Jo H, Song H, Mowbray A. Role of NADPH oxidases in disturbed flow- and BMP4- induced inflammation and atherosclerosis. Antioxid Redox Signal. 2006;8(9–10):1609–1619. doi:10.1089/ars.2006.8.1609
  • Wong WT, Tian XY, Chen Y, et al. Bone morphogenic protein-4 impairs endothelial function through oxidative stress-dependent cyclooxygenase-2 upregulation: implications on hypertension. Circ Res. 2010;107(8):984–991. doi:10.1161/CIRCRESAHA.110.222794
  • Helbing T, Wiltgen G, Hornstein A, et al. Bone morphogenetic protein-modulator BMPER regulates endothelial barrier function. Inflammation. 2017;40(2):442–453. doi:10.1007/s10753-016-0490-4
  • Youn JY, Zhou J, Cai H. Bone morphogenic protein 4 mediates NOX1-dependent eNOS uncoupling, endothelial dysfunction, and COX2 induction in type 2 diabetes mellitus. Mol Endocrinol. 2015;29(8):1123–1133. doi:10.1210/ME.2014-1313
  • Hanna A, Frangogiannis NG. The role of the TGF-β superfamily in myocardial infarction. Front Cardiovasc Med. 2019;6:140. doi:10.3389/fcvm.2019.00140
  • Pallotta I, Sun B, Wrona EA, Freytes DO. BMP protein-mediated crosstalk between inflammatory cells and human pluripotent stem cell-derived cardiomyocytes. J Tissue Eng Regen Med. 2017;11(5):1466–1478. doi:10.1002/term.2045
  • Wu T, Ling QY, Zhong C, et al. Expression of BMP4 in myocardium and vascular tissue of obese mice. J Inflamm. 2015;12:8. doi:10.1186/s12950-015-0047-6
  • Sun B, Huo R, Sheng Y, et al. Bone morphogenetic protein-4 mediates cardiac hypertrophy, apoptosis, and fibrosis in experimentally pathological cardiac hypertrophy. Hypertension. 2013;61(2):352–360. doi:10.1161/HYPERTENSIONAHA.111.00562
  • Kercheva M, Gusakova AM, Ryabova TR, Suslova TE, Kzhyshkowska J, Ryabov VV. Serum levels of bone morphogenetic proteins 2 and 4 in patients with acute myocardial infarction. Cells. 2020;9(10):2179. doi:10.3390/cells9102179
  • Zhao X, Zhang J, Zhang W, et al. the relationship between circulating bone morphogenetic protein-4 and inflammation cytokines in patients undergoing thoracic surgery: a prospective randomized study. J Inflamm Res. 2021;14:4069–4077. doi:10.2147/JIR.S324775
  • Csiszar A, Labinskyy N, Jo H, Ballabh P, Ungvari Z. Differential proinflammatory and prooxidant effects of bone morphogenetic protein-4 in coronary and pulmonary arterial endothelial cells. Am J Physiol Heart Circ Physiol. 2008;295(2):H569–77. doi:10.1152/ajpheart.00180.2008
  • Kariyawasam HH, Xanthou G, Barkans J, Aizen M, Kay AB, Robinson DS. Basal expression of bone morphogenetic protein receptor is reduced in mild asthma. Am J Respir Crit Care Med. 2008;177(10):1074–1081. doi:10.1164/rccm.200709-1376OC
  • Martínez VG, Rubio C, Martínez-Fernández M, et al. BMP4 induces M2 macrophage polarization and favors tumor progression in bladder cancer. Clin Cancer Res. 2017;23(23):7388–7399. doi:10.1158/1078-043.2.CCR-17-1004
  • Valencia J, Fernández-Sevilla L, Fraile-Ramos A, et al. Acute lymphoblastic leukaemia cells impair dendritic cell and macrophage differentiation: role of BMP4. Cells. 2019;8(7):722. doi:10.3390/cells8070722
  • Qian SW, Wu MY, Wang YN, et al. BMP4 facilitates beige fat biogenesis via regulating adipose tissue macrophages. J Mol Cell Biol. 2019;11(1):14–25. doi:10.1093/jmcb/mjy011
  • Li Q, Barres BA. Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol. 2018;18(4):225–242. doi:10.1038/nri.2017.125
  • Haage V, Semtner M, Vidal RO, et al. Comprehensive gene expression meta-analysis identifies signature genes that distinguish microglia from peripheral monocytes/macrophages in health and glioma. Acta Neuropathol Commun. 2019;7(1):20. doi:10.1186/s40478-019-0665-y
  • Ara J, See J, Mamontov P, et al. Bone morphogenetic proteins 4, 6, and 7 are up-regulated in mouse spinal cord during experimental autoimmune encephalomyelitis. J Neurosci Res. 2008;86(1):125–135. doi:10.1002/jnr.21462
  • Costa C, Eixarch H, Martínez-Sáez E, et al. Expression of bone morphogenetic proteins in multiple sclerosis lesions. Am J Pathol. 2019;189(3):665–676. doi:10.1016/j.ajpath.2018.11.007
  • Shijo T, Warita H, Suzuki N, et al. Antagonizing bone morphogenetic protein 4 attenuates disease progression in a rat model of amyotrophic lateral sclerosis. Exp Neurol. 2018;307:164–179. doi:10.1016/j.expneurol.2018.06.009
  • Gomez-Puerto MC, Iyengar PV, García de Vinuesa A, Ten Dijke P, Sanchez-Duffhues G. Bone morphogenetic protein receptor signal transduction in human disease. J Pathol. 2019;247(1):9–20. doi:10.1002/path.5170
  • Sahni V, Mukhopadhyay A, Tysseling V, et al. BMPR1a and BMPR1b signaling exert opposing effects on gliosis after spinal cord injury. J Neurosci. 2010;30(5):1839–1855. doi:10.1523/JNEUROSCI.4459-09.2010
  • Wang D, Prakash J, Nguyen P, et al. Bone morphogenetic protein signaling in vascular disease: anti-inflammatory action through myocardin-related transcription factor A. J Biol Chem. 2012;287(33):28067–28077. doi:10.1074/jbc.M112.379487
  • Kim CW, Song H, Kumar S, et al. Anti-inflammatory and antiatherogenic role of BMP receptor II in endothelial cells. Arterioscler Thromb Vasc Biol. 2013;33(6):1350–1359. doi:10.1161/ATVBAHA.112.300287
  • Maric I, Kucic N, Turk Wensveen T, et al. BMP signaling in rats with TNBS-induced colitis following BMP7 therapy. Am J Physiol Gastrointest Liver Physiol. 2012;302(10):G1151–62. doi:10.1152/ajpgi.00244.2011
  • Rosendahl A, Pardali E, Speletas M, Ten Dijke P, Heldin CH, Sideras P. Activation of bone morphogenetic protein/Smad signaling in bronchial epithelial cells during airway inflammation. Am J Respir Cell Mol Biol. 2002;27(2):160–169. doi:10.1165/ajrcmb.27.2.4779
  • Jin GL, Hong LM, Liu HP, et al. Koumine modulates spinal microglial M1 polarization and the inflammatory response through the Notch-RBP-Jκ signaling pathway, ameliorating diabetic neuropathic pain in rats. Phytomedicine. 2021;90:153640. doi:10.1016/j.phymed.2021.153640
  • Guo A, Li J, Luo L, et al. Valproic acid mitigates spinal nerve ligation-induced neuropathic pain in rats by modulating microglial function and inhibiting neuroinflammatory response. Int Immunopharmacol. 2021;92:107332. doi:10.1016/j.intimp.2020.107332
  • Piotrowska A, Kwiatkowski K, Rojewska E, Makuch W, Mika J. Maraviroc reduces neuropathic pain through polarization of microglia and astroglia - evidence from in vivo and in vitro studies. Neuropharmacology. 2016;108:207–219. doi:10.1016/j.neuropharm.2016.04.024
  • Popiolek-Barczyk K, Kolosowska N, Piotrowska A, et al. Parthenolide relieves pain and promotes M2 microglia/macrophage polarization in rat model of neuropathy. Neural Plast. 2015;2015:676473. doi:10.1155/2015/676473
  • Li H, Wang P, Tang L, et al. Distinct polarization dynamics of microglia and infiltrating macrophages: a novel mechanism of spinal cord ischemia/reperfusion injury. J Inflamm Res. 2021;14:5227–5239. doi:10.2147/JIR.S335382
  • Phan-Everson T, Etoc F, Li S, et al. Differential compartmentalization of BMP4/NOGGIN requires NOGGIN trans-epithelial transport. Dev Cell. 2021;56(13):1930–1944.e5. doi:10.1016/j.devcel.2021.05.003
  • Harnisch K, Teuber-Hanselmann S, Macha N, et al. Myelination in multiple sclerosis lesions is associated with regulation of bone morphogenetic protein 4 and its antagonist Noggin. Int J Mol Sci. 2019;20(1):154. doi:10.3390/ijms20010154
  • Matsuura I, Taniguchi J, Hata K, Saeki N, Yamashita T. BMP inhibition enhances axonal growth and functional recovery after spinal cord injury. J Neurochem. 2008;105(4):1471–1479. doi:10.1111/j.1471-4159.2008.05251.x
  • Lei ZN, Liu F, Zhang LM, Huang YL, Sun FY. Bcl-2 increases stroke-induced striatal neurogenesis in adult brains by inhibiting BMP-4 function via activation of β-catenin signaling. Neurochem Int. 2012;61(1):34–42. doi:10.1016/j.neuint.2012.04.004
  • Shin JA, Kim YA, Kim HW, et al. Iron released from reactive microglia by noggin improves myelin repair in the ischemic brain. Neuropharmacology. 2018;133:202–215. doi:10.1016/j.neuropharm.2018.01.038
  • Shin JA, Lim SM, Jeong SI, Kang JL, Park EM. Noggin improves ischemic brain tissue repair and promotes alternative activation of microglia in mice. Brain Behav Immun. 2014;40:143–154. doi:10.1016/j.bbi.2014.03.013