Lipoxin A4 inhibits microglial activation and reduces neuroinflammation and neuropathic pain after spinal cord hemisection

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Martini, Alessandra Cadete ^a,b,d   Berta, Temugin ^b,e   Forner, Stefânia ^a,d   Chen, Gang ^b   Bento, Allisson Freire ^c   Ji, Ru Rong ^b   Rae, Giles Alexander ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Centro de Inova ão e Ensaios Pré Clínicos CIEnP   (Brazil)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

Author keywords

Chronic pain; Lipoxin; Microglia; Neuroinflammation; Spinal cord injury

Indexed keywords

CELL MARKER; FORMYL PEPTIDE RECEPTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; LIPOXIN A; PURINERGIC P2Y12 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LIPOXIN;

ADULT; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CD-1 MOUSE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; MALE; MECHANICAL STIMULATION; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHIC PAIN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; VON FREY TEST; WISTAR RAT; ANIMAL; AXOTOMY; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; INTRASPINAL DRUG ADMINISTRATION; NEURALGIA; PATHOPHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; AXOTOMY; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; INJECTIONS, SPINAL; LIPOXINS; MALE; MICE; MICROGLIA; NEURALGIA; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURIES;

EID: 84962834021     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0540-8     Document Type: Article

References (84)

1. Bickenbach et al. ISCoS-WHO collaboration. International Perspecties of Spinal Cord Injury (IPSCI). 2013.
2. Siddall PJ et al. Pregabalin in central neuropathic pain associated with spinal cord injury: a placebo-controlled trial. Neurology. 2006;67(10):1792-800.
3. Siddall PJ, Finnerup NB. Chapter 46 pain following spinal cord injury. Handb Clin Neurol. 2006;81:689-703.
4. Basbaum AI et al. Cellular and molecular mechanisms of pain. Cell. 2009;139(2):267-84.
5. Dworkin RH et al. Recommendations for the pharmacological management of neuropathic pain: an overview and literature update. Mayo Clin Proc. 2010;85(3 Suppl):S3-14.
6. Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. 2007;10(11):1361-8.
7. Ji RR, Xu ZZ, Gao YJ. Emerging targets in neuroinflammation-driven chronic pain. Nat Rev Drug Discov. 2014;13(7):533-48.
8. Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol. 2008;209(2):378-88.
9. Fenn AM et al. IL-4 signaling drives a unique arginase+/IL-1beta+ microglia phenotype and recruits macrophages to the inflammatory CNS: consequences of age-related deficits in IL-4R alpha after traumatic spinal cord injury. J Neurosci. 2014;34(26):8904-17.
10. McMahon SB, Malcangio M. Current challenges in glia-pain biology. Neuron. 2009;64(1):46-54.
11. Jiang BC et al. CXCL13 drives spinal astrocyte activation and neuropathic pain via CXCR5. J Clin Invest. 2016;126(2):745-61.
12. Inoue K, Tsuda M. Microglia and neuropathic pain. Glia. 2009;57(14):1469-79.
13. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol. 2008;8(5):349-61.
14. Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids. 2005;73(3-4):141-62.
15. Svensson CI, Zattoni M, Serhan CN. Lipoxins and aspirin-triggered lipoxin inhibit inflammatory pain processing. J Exp Med. 2007;204(2):245-52.
16. Lima-Garcia JF et al. The precursor of resolvin D series and aspirin-triggered resolvin D1 display anti-hyperalgesic properties in adjuvant-induced arthritis in rats. Br J Pharmacol. 2011;164(2):278-93.
17. Xu ZZ et al. Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat Med. 2010;16(5):592-7. 1p following 597.
18. Li Q et al. Involvement of the spinal NALP1 inflammasome in neuropathic pain and aspirin-triggered-15-epi-lipoxin A4 induced analgesia. Neuroscience. 2013;254:230-40.
19. Petasis NA et al. Design and synthesis of benzo-lipoxin A4 analogs with enhanced stability and potent anti-inflammatory properties. Bioorg Med Chem Lett. 2008;18(4):1382-7.
20. Hu S et al. Lipoxins and aspirin-triggered lipoxin alleviate bone cancer pain in association with suppressing expression of spinal proinflammatory cytokines. J Neuroinflammation. 2012;9:278.
21. Sun T et al. LipoxinA(4) induced antinociception and decreased expression of NF-kappaB and pro-inflammatory cytokines after chronic dorsal root ganglia compression in rats. Eur J Pain. 2012;16(1):18-27.
22. Christensen MD et al. Mechanical and thermal allodynia in chronic central pain following spinal cord injury. Pain. 1996;68(1):97-107.
23. Chaplan SR et al. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53(1):55-63.
24. Berta T et al. Transcriptional and functional profiles of voltage-gated Na(+) channels in injured and non-injured DRG neurons in the SNI model of neuropathic pain. Mol Cell Neurosci. 2008;37(2):196-208.
25. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-8.
26. Berta T et al. Extracellular caspase-6 drives murine inflammatory pain via microglial TNF-alpha secretion. J Clin Invest. 2014;124(3):1173-86.
27. Gao YJ, Zhang L, Ji RR. Spinal injection of TNF-alpha-activated astrocytes produces persistent pain symptom mechanical allodynia by releasing monocyte chemoattractant protein-1. Glia. 2010;58(15):1871-80.
28. Migeotte I, Communi D, Parmentier M. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 2006;17(6):501-19.
29. Maderna P, Godson C. Lipoxins: resolutionary road. Br J Pharmacol. 2009;158(4):947-59.
30. Bartlett DW, Davis ME. Insights into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent imaging. Nucleic Acids Res. 2006;34(1):322-33.
31. Wang YP et al. Aspirin-triggered lipoxin A4 attenuates LPS-induced pro-inflammatory responses by inhibiting activation of NF-kappaB and MAPKs in BV-2 microglial cells. J Neuroinflammation. 2011;8:95.
32. Wu Y et al. Aspirin-triggered lipoxin A(4) attenuates lipopolysaccharide-induced intracellular ROS in BV2 microglia cells by inhibiting the function of NADPH oxidase. Neurochem Res. 2012;37(8):1690-6.
33. Yao C et al. Aspirin-triggered lipoxin A4 attenuates lipopolysaccharide induced inflammatory response in primary astrocytes. Int Immunopharmacol. 2014;18(1):85-9.
34. Loggia ML et al. Evidence for brain glial activation in chronic pain patients. Brain. 2015;138(Pt 3):604-15.
35. Beggs S, Salter MW. The known knowns of microglia-neuronal signalling in neuropathic pain. Neurosci Lett. 2013;557:37-42.
36. Beggs S, Salter MW. Microglia-neuronal signalling in neuropathic pain hypersensitivity 2.0. Curr Opin Neurobiol. 2010;20(4):474-80.
37. Guo Z et al. Lipoxin A4 reduces inflammation through formyl peptide receptor 2/p38 MAPK signaling pathway in subarachnoid hemorrhage rats. Stroke. 2016;47(2):490-7.
38. Nakajima K et al. Neurotrophins regulate the function of cultured microglia. Glia. 1998;24(3):272-89.
39. Hanisch UK. Microglia as a source and target of cytokines. Glia. 2002;40(2):140-55.
40. Ulmann L et al. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci. 2008;28(44):11263-8.
41. Clark AK et al. P2X7-dependent release of interleukin-1beta and nociception in the spinal cord following lipopolysaccharide. J Neurosci. 2010;30(2):573-82.
42. Tsuda M et al. IFN-gamma receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc Natl Acad Sci U S A. 2009;106(19):8032-7.
43. Jin SX et al. p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci. 2003;23(10):4017-22.
44. Tsuda M et al. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia. 2004;45(1):89-95.
45. Cui Y et al. Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance. Brain Res. 2006;1069(1):235-43.
46. Wen YR et al. Activation of p38 mitogen-activated protein kinase in spinal microglia contributes to incision-induced mechanical allodynia. Anesthesiology. 2009;110(1):155-65.
47. Kobayashi K et al. P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J Neurosci. 2008;28(11):2892-902.
48. Serhan CN, Chiang N, Dalli J. The resolution code of acute inflammation: novel pro-resolving lipid mediators in resolution. Semin Immunol. 2015;27(3):200-15.
49. Serhan CN. Pro-resolving lipid mediators are leads for resolution physiology. Nature. 2014;510(7503):92-101.
50. Recchiuti A, Serhan CN. Pro-resolving lipid mediators (SPMs) and their actions in regulating miRNA in novel resolution circuits in inflammation. Front Immunol. 2012;3:298.
51. Wu SH et al. Efficacy and safety of 15(R/S)-methyl-lipoxin A(4) in topical treatment of infantile eczema. Br J Dermatol. 2013;168(1):172-8.
52. Christie PE, Spur BW, Lee TH. The effects of lipoxin A4 on airway responses in asthmatic subjects. Am Rev Respir Dis. 1992;145(6):1281-4.
53. Basbaum AI. Conduction of the effects of noxious stimulation by short-fiber multisynaptic systems of the spinal cord in the rat. Exp Neurol. 1973;40(3):699-716.
54. Rosenberg LJ, Zai LJ, Wrathall JR. Chronic alterations in the cellular composition of spinal cord white matter following contusion injury. Glia. 2005;49(1):107-20.
55. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci. 1994;6(5):712-24.
56. Mehta S et al. A systematic review of pharmacological treatments of pain after spinal cord injury: an update. Arch Phys Med Rehabil. 2016. doi: 10.1016/j.apmr.2015.12.023.
57. Finnerup NB. Pain in patients with spinal cord injury. Pain. 2013;154 Suppl 1:S71-6.
58. Figueroa JD et al. Docosahexaenoic acid pretreatment confers protection and functional improvements after acute spinal cord injury in adult rats. J Neurotrauma. 2012;29(3):551-66.
59. Figueroa JD et al. Dietary omega-3 polyunsaturated fatty acids improve the neurolipidome and restore the DHA status while promoting functional recovery after experimental spinal cord injury. J Neurotrauma. 2013;30(10):853-68.
60. Ward RE et al. Docosahexaenoic acid prevents white matter damage after spinal cord injury. J Neurotrauma. 2010;27(10):1769-80.
61. King VR et al. Omega-3 fatty acids improve recovery, whereas omega-6 fatty acids worsen outcome, after spinal cord injury in the adult rat. J Neurosci. 2006;26(17):4672-80.
62. Figueroa JD et al. Metabolomics uncovers dietary omega-3 fatty acid-derived metabolites implicated in anti-nociceptive responses after experimental spinal cord injury. Neuroscience. 2013;255:1-18.
63. Xu ZZ et al. Neuroprotectin/protectin D1 protects against neuropathic pain in mice after nerve trauma. Ann Neurol. 2013;74(3):490-5.
64. Ji RR et al. Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 2011;34(11):599-609.
65. Chiang N et al. A novel rat lipoxin A4 receptor that is conserved in structure and function. Br J Pharmacol. 2003;139(1):89-98.
66. Chiang N, Arita M, Serhan CN. Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot Essent Fatty Acids. 2005;73(3-4):163-77.
67. Gronert K et al. Identification of a human enterocyte lipoxin A4 receptor that is regulated by interleukin (IL)-13 and interferon gamma and inhibits tumor necrosis factor alpha-induced IL-8 release. J Exp Med. 1998;187(8):1285-94.
68. Schaldach CM, Riby J, Bjeldanes LF. Lipoxin A4: a new class of ligand for the Ah receptor. Biochemistry. 1999;38(23):7594-600.
69. Pamplona FA et al. Anti-inflammatory lipoxin A4 is an endogenous allosteric enhancer of CB1 cannabinoid receptor. Proc Natl Acad Sci U S A. 2012;109(51):21134-9.
70. Machado FS et al. Anti-inflammatory actions of lipoxin A4 and aspirin-triggered lipoxin are SOCS-2 dependent. Nat Med. 2006;12(3):330-4.
71. Schafers M et al. Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci. 2003;23(7):2517-21.
72. Sweitzer SM et al. Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat. Brain Res. 1999;829(1-2):209-21.
73. Gabay E et al. Chronic blockade of interleukin-1 (IL-1) prevents and attenuates neuropathic pain behavior and spontaneous ectopic neuronal activity following nerve injury. Eur J Pain. 2011;15(3):242-8.
74. Park CK et al. Resolving TRPV1- and TNF-alpha-mediated spinal cord synaptic plasticity and inflammatory pain with neuroprotectin D1. J Neurosci. 2011;31(42):15072-85.
75. Spicarova D, Palecek J. Tumor necrosis factor alpha sensitizes spinal cord TRPV1 receptors to the endogenous agonist N-oleoyldopamine. J Neuroinflammation. 2010;7:49.
76. Choi JI et al. Peripheral inflammation induces tumor necrosis factor dependent AMPA receptor trafficking and Akt phosphorylation in spinal cord in addition to pain behavior. Pain. 2010;149(2):243-53.
77. Zhang L et al. TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2. Pain. 2011;152(2):419-27.
78. Stellwagen D et al. Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci. 2005;25(12):3219-28.
79. Zhang H, Nei H, Dougherty PM. A p38 mitogen-activated protein kinase-dependent mechanism of disinhibition in spinal synaptic transmission induced by tumor necrosis factor-alpha. J Neurosci. 2010;30(38):12844-55.
80. Gruber-Schoffnegger D et al. Induction of thermal hyperalgesia and synaptic long-term potentiation in the spinal cord lamina I by TNF-alpha and IL-1beta is mediated by glial cells. J Neurosci. 2013;33(15):6540-51.
81. Nigam S et al. Lipoxin A4 and lipoxin B4 stimulate the release but not the oxygenation of arachidonic acid in human neutrophils: dissociation between lipid remodeling and adhesion. J Cell Physiol. 1990;143(3):512-23.
82. Pierdomenico AM et al. MicroRNA-181b regulates ALX/FPR2 receptor expression and proresolution signaling in human macrophages. J Biol Chem. 2015;290(6):3592-600.
83. Hains BC, Waxman SG. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci. 2006;26(16):4308-17.
84. Marchand F et al. Effects of etanercept and minocycline in a rat model of spinal cord injury. Eur J Pain. 2009;13(7):673-81.