Minocycline Attenuates Neonatal Germinal-Matrix-Hemorrhage-Induced Neuroinflammation and Brain Edema by Activating Cannabinoid Receptor 2

Molecular Neurobiology

Volumn 53, Issue 3, 2016, Pages 1935-1948

  Tang, Jun ^a   Chen, Qianwei ^a   Guo, Jing ^a   Yang, Liming ^a   Tao, Yihao ^a   Li, Lin ^a   Miao, Hongping ^a   Feng, Hua ^a   Chen, Zhi ^a   Zhu, Gang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Cannabinoid receptor 2; Germinal matrix hemorrhage; Microglia; Minocycline; Neuroinflammation

Indexed keywords

CANNABINOID 2 RECEPTOR; MESSENGER RNA; MINOCYCLINE; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; CALCIUM BINDING PROTEIN; CANNABINOID; CYTOKINE; INDOLE DERIVATIVE; IODOPRAVADOLINE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN EDEMA; CB2R GENE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); CYTOKINE RELEASE; DRUG EFFECT; FEMALE; GENE EXPRESSION; HEART VENTRICLE VOLUME; MALE; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN VENTRICLE; COMPLICATION; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLAMMATION; INTRACRANIAL HEMORRHAGES; METABOLISM; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN EDEMA; CALCIUM-BINDING PROTEINS; CANNABINOIDS; CEREBRAL VENTRICLES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; INDOLES; INFLAMMATION; INTRACRANIAL HEMORRHAGES; MAGNETIC RESONANCE IMAGING; MALE; MICROFILAMENT PROTEINS; MICROGLIA; MINOCYCLINE; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB2; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84961195897     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9154-x     Document Type: Article

References (51)

1. Heron M et al (2010) Annual summary of vital statistics: 2007. Pediatrics 125(1):4–15
2. Shennan AH, Bewley S (2006) Why should preterm births be rising? BMJ 332(7547):924–5
3. Ballabh P (2010) Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr Res 67(1):1–8
4. Ballabh P, Braun A, Nedergaard M (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 16(1):1–13
5. Murphy BP et al (2002) Posthaemorrhagic ventricular dilatation in the premature infant: natural history and predictors of outcome. Arch Dis Child Fetal Neonatal Ed 87(1):F37–41
6. Xi G, Keep RF, Hoff JT (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5(1):53–63
7. Chen Z et al (2011) Role of iron in brain injury after intraventricular hemorrhage. Stroke 42(2):465–70
8. Lekic T et al (2012) Rodent neonatal germinal matrix hemorrhage mimics the human brain injury, neurological consequences, and post-hemorrhagic hydrocephalus. Exp Neurol 236(1):69–78
9. Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57(6):563–81
10. Supramaniam V et al (2013) Microglia activation in the extremely preterm human brain. Pediatr Res 73(3):301–9
11. Yang S et al (2006) The role of complement C3 in intracerebral hemorrhage-induced brain injury. J Cereb Blood Flow Metab 26(12):1490–5
12. Aronson AL (1980) Pharmacotherapeutics of the newer tetracyclines. J Am Vet Med Assoc 176(10 Spec No):1061–8
13. Tikka T et al (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21(8):2580–8
14. Wasserman JK, Schlichter LC (2007) Minocycline protects the blood-brain barrier and reduces edema following intracerebral hemorrhage in the rat. Exp Neurol 207(2):227–37
15. Wu J et al (2010) Minocycline attenuates brain edema, brain atrophy and neurological deficits after intracerebral hemorrhage. Acta Neurochir Suppl 106:147–50
16. Chu LS et al (2010) Minocycline inhibits 5-lipoxygenase expression and accelerates functional recovery in chronic phase of focal cerebral ischemia in rats. Life Sci 86(5–6):170–7
17. Plane JM et al (2010) Prospects for minocycline neuroprotection. Arch Neurol 67(12):1442–8
18. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166(12):7527–33
19. Markovic DS et al (2011) Minocycline reduces glioma expansion and invasion by attenuating microglial MT1-MMP expression. Brain Behav Immun 25(4):624–8
20. Mackie K (2006) Cannabinoid receptors as therapeutic targets. Annu Rev Pharmacol Toxicol 46:101–22
21. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4(11):873–84
22. Chin CL et al (2008) Differential effects of cannabinoid receptor agonists on regional brain activity using pharmacological MRI. Br J Pharmacol 153(2):367–79
23. Fernandez-Lopez D et al (2012) Reduced infarct size and accumulation of microglia in rats treated with WIN 55,212-2 after neonatal stroke. Neuroscience 207:307–15
24. Choi IY et al (2013) Activation of cannabinoid CB2 receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury. Am J Pathol 182(3):928–39
25. Eljaschewitsch E et al (2006) The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49(1):67–79
26. Sarne Y et al (2011) The dual neuroprotective-neurotoxic profile of cannabinoid drugs. Br J Pharmacol 163(7):1391–401
27. Chen Y, Buck J (2000) Cannabinoids protect cells from oxidative cell death: a receptor-independent mechanism. J Pharmacol Exp Ther 293(3):807–12
28. Sarker KP et al (2000) Anandamide induces apoptosis of PC-12 cells: involvement of superoxide and caspase-3. FEBS Lett 472(1):39–44
29. Kozela E et al (2010) Cannabinoids Delta(9)-tetrahydrocannabinol and cannabidiol differentially inhibit the lipopolysaccharide-activated NF-kappaB and interferon-beta/STAT proinflammatory pathways in BV-2 microglial cells. J Biol Chem 285(3):1616–26
30. Lopez Rodriguez AB et al (2011) Estradiol decreases cortical reactive astrogliosis after brain injury by a mechanism involving cannabinoid receptors. Cereb Cortex 21(9):2046–55
31. Wu J et al (2009) Minocycline reduces intracerebral hemorrhage-induced brain injury. Neurol Res 31(2):183–8
32. Huffman JW et al (1999) 3-(1',1'-Dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 7(12):2905–14
33. Zarruk JG et al (2012) Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection. Stroke 43(1):211–9
34. Diz-Chaves Y et al (2012) Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. J Neuroinflammation 9:71
35. Ashton JC et al (2007) Cerebral hypoxia-ischemia and middle cerebral artery occlusion induce expression of the cannabinoid CB2 receptor in the brain. Neurosci Lett 412(2):114–7
36. Tang J et al (2005) Role of NADPH oxidase in the brain injury of intracerebral hemorrhage. J Neurochem 94(5):1342–50
37. Newson P et al (2005) Intrinsic sensory deprivation induced by neonatal capsaicin treatment induces changes in rat brain and behaviour of possible relevance to schizophrenia. Br J Pharmacol 146(3):408–18
38. Homsi S et al (2009) Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Res 1291:122–32
39. Lopez-Rodriguez, A.B.., et al. (2013) CB1 and CB2 Cannabinoid Receptor Antagonists Prevent Minocycline-Induced Neuroprotection Following Traumatic Brain Injury in Mice. Cereb Cortex
40. Sun J et al (2013) WIN55,212-2 protects oligodendrocyte precursor cells in stroke penumbra following permanent focal cerebral ischemia in rats. Acta Pharmacol Sin 34(1):119–28
41. Fujii M et al (2014) Cannabinoid receptor type 2 agonist attenuates apoptosis by activation of phosphorylated CREB-Bcl-2 pathway after subarachnoid hemorrhage in rats. Exp Neurol 261:396–403
42. Rivest S (2006) Cannabinoids in microglia: a new trick for immune surveillance and neuroprotection. Neuron 49(1):4–8
43. Moller T, Hanisch UK, Ransom BR (2000) Thrombin-induced activation of cultured rodent microglia. J Neurochem 75(4):1539–47
44. Lazovic J et al (2005) Neuroinflammation and both cytotoxic and vasogenic edema are reduced in interleukin-1 type 1 receptor-deficient mice conferring neuroprotection. Stroke 36(10):2226–31
45. Strahle J et al (2012) Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage. Transl Stroke Res 3(Suppl 1):25–38
46. Grainger DJ et al (1995) Release and activation of platelet latent TGF-beta in blood clots during dissolution with plasmin. Nat Med 1(9):932–7
47. Bottner M, Krieglstein K, Unsicker K (2000) The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem 75(6):2227–40
48. Romero-Sandoval EA et al (2009) Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation. Mol Pain 5:25
49. Hua Y et al (2006) Tumor necrosis factor-alpha increases in the brain after intracerebral hemorrhage and thrombin stimulation. Neurosurgery 58(3):542–50, discussion 542-50
50. Wasserman JK, Zhu X, Schlichter LC (2007) Evolution of the inflammatory response in the brain following intracerebral hemorrhage and effects of delayed minocycline treatment. Brain Res 1180:140–54
51. Poralla C et al (2012) Elevated interleukin-6 concentration and alterations of the coagulation system are associated with the development of intraventricular hemorrhage in extremely preterm infants. Neonatology 102(4):270–5