Indomethacin treatment reduces microglia activation and increases numbers of neuroblasts in the subventricular zone and ischaemic striatum after focal ischaemia

Journal of Biosciences

Volumn 41, Issue 3, 2016, Pages 381-394

  Lopes, Rosana S ^a   Cardoso, Marcelo M ^a   Sampaio, Arthur O ^a   Barbosa, Mario Santos ^a   Souza, Celice C ^a   da Silva, Michelle C ^a   Ferreira, Elane Magno N ^a   Freire, Marco Aurelio M ^a,b   Lima, Rafael Rodrigues ^a   Gomes Leal, Walace ^a  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b DEPARTAMENTO DE FÍSICA   (Brazil)

Author keywords

Indomethacin; inflammation; microglia; neuroblasts; striatum; stroke

Indexed keywords

ENDOTHELIN 1; INDOMETACIN;

DISEASE TREATMENT; STROKE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN ISCHEMIA; CELL ACTIVATION; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CORPUS STRIATUM; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MICROGLIA; NEUROBLAST; NEUROMODULATION; NONHUMAN; PRESERVATION; RAT; SUBVENTRICULAR ZONE; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; HUMAN; LATERAL BRAIN VENTRICLE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PATHOLOGY; STROKE;

ANIMALIA; RATTUS;

ANIMALS; BRAIN ISCHEMIA; CELL PROLIFERATION; CORPUS STRIATUM; ENDOTHELIN-1; HUMANS; INDOMETHACIN; LATERAL VENTRICLES; MICROGLIA; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RATS; STROKE;

EID: 84978080550     PISSN: 02505991     EISSN: 09737138     Source Type: Journal    
DOI: 10.1007/s12038-016-9621-1     Document Type: Article

References (61)

1. Aarum J, Sandberg K, Haeberlein SL and Persson MA 2003 Migration and differentiation of neural precursor cells can be directed by microglia. Proc. Natl. Acad. Sci. USA 100 15983–15988
2. Aimone JB, Deng W and Gage FH 2011 Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron. 70 589–596
3. Amiri-Nikpour MR, Nazarbaghi S, Hamdi-Holasou M and Rezaei Y 2015 An open-label evaluator-blinded clinical study of minocycline neuroprotection in ischemic stroke: gender-dependent effect. Acta. Neurol. Scand. 131 45–50
4. Arvidsson A, Collin T, Kirik D, Kokaia Z and Lindvall O 2002 Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 963–970
5. Battista D, Ferrari CC, Gage FH and Pitossi FJ 2006 Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur. J. Neurosci. 23 83–93
6. Breton-Provencher V and Saghatelyan A 2012 Newborn neurons in the adult olfactory bulb: unique properties for specific odor behavior. Behav. Brain Res. 227 480–489
7. Cardoso MM, Franco EC, de Souza CC, da Silva MC, Gouveia A and Gomes-Leal W 2013 Minocycline treatment and bone marrow mononuclear cell transplantation after endothelin-1 induced striatal ischemia. Inflammation 36 197–205
8. Curtis MA, Monzo HJ and Faull RL 2009 The rostral migratory stream and olfactory system: smell, disease and slippery cells. Prog. Brain Res. 175 33–42
9. Das S, Dutta K, Kumawat KL, Ghoshal A, Adhya D and Basu A 2011 Abrogated inflammatory response promotes neurogenesis in a murine model of Japanese encephalitis. Plos One 3 1–15
10. Dijkstra CD, Dopp EA, Joling P and Kraal G 1985 The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in rat recognized by monoclonal antibodies ED1, ED2 and ED3. Adv. Exp. Med. Biol. 186 409–419
11. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM and Alvarez-Buylla A 1999 Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 703–716
12. Doetsch F, Garcia-Verdugo JM and Alvarez-Buylla A 1997 Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17 5046–5061
13. Dos Santos CD, Picanco-Diniz CW and Gomes-Leal W 2007 Differential patterns of inflammatory response, axonal damage and myelin impairment following excitotoxic or ischemic damage to the trigeminal spinal nucleus of adult rats. Brain Res. 1172 130–144
14. Ekdahl CT 2012 Microglial activation - tuning and pruning adult neurogenesis. Front Pharmacol. 3 41
15. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z and Lindvall O 2003 Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100 13632–13637
16. Ekdahl CT, Kokaia Z and Lindvall O 2009 Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158 1021–1029
17. Franco EC, Cardoso MM, Gouveia A, Pereira A and Gomes-Leal W 2012 Modulation of microglial activation enhances neuroprotection and functional recovery derived from bone marrow mononuclear cell transplantation after cortical ischemia. Neurosci. Res. 73 122–132
18. Gage FH, Kempermann G, Palmer TD, Peterson DA and Ray J 1998 Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36 249–266
19. Gleeson JG, Lin PT, Flanagan LA and Walsh CA 1999 Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 257–271
20. Gomes-Leal W 2012 Microglial physiopathology: how to explain the dual role of microglia after acute neural disorders? Brain Behav. 2 345–356
21. Gomes-Leal W, Corkill DJ, Freire MAM, Picanco-Diniz CW and Perry VH 2004 Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp. Neurol. 190 456–467
22. Gresle MM, Jarrott B, Jones NM and Callaway JK 2006 Injury to axons and oligodendrocytes following endothelin-1-induced middle cerebral artery occlusion in conscious rats. Brain Res. 1110 13–22
23. Guimaraes JS, Freire MAM, Lima RR, Picanço-Diniz CW, Pereira A and Gomes-Leal W 2010 Minocycline treatment reduces white matter damage after excitotoxic striatal injury. Brain Res. 1329 182–193
24. Guimaraes JS et al. 2009 Mechanisms of secondary degeneration in the central nervous system during acute neural disorders and white matter damage. Rev. Neurol. 48 304–310
25. Heldmann U, Mine Y, Kokaia Z, Ekdahl CT and Lindvall O 2011 Selective depletion of Mac-1-expressing microglia in rat subventricular zone does not alter neurogenic response early after stroke. Exp. Neurol. 229 391–398
26. Hoehn BD, Palmer TD and Steinberg GK 2005 Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 36 2718–2724
27. Imayoshi I et al. 2008 Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci. 11 1153–1161
28. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y and Kohsaka S 1998 Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 57 1–9
29. Jiang C, Ting AT and Seed B 1998 PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391 82–86
30. Kim BJ et al. 2009 Reduced neurogenesis after suppressed inflammation by minocycline in transient cerebral ischemia in rat. J. Neurol. Sci. 279 70–75
31. Kluska MM, Witte OW, Bolz J and Redecker C 2005 Neurogenesis in the adult dentate gyrus after cortical infarcts: effects of infarct location, N-methyl-D-aspartate receptor blockade and anti-inflammatory treatment. Neuroscience 135 723–735
32. Lalancette-Hebert M, Gowing G, Simard A, Weng YC and Kriz J 2007 Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27 2596–2605
33. Lazarini F, Gabellec MM, Torquet N and Lledo PM 2012 Early activation of microglia triggers long-lasting impairment of adult neurogenesis in the olfactory bulb. J Neurosci. 32 3652–3664
34. Lazarini F and Lledo PM 2011 Is adult neurogenesis essential for olfaction? Trends Neurosci. 34 20–30
35. Li J and McCullough LD 2009 Sex differences in minocycline-induced neuroprotection after experimental stroke. J Cereb Blood Flow Metab. 29 670–674
36. Liu Z et al. 2007 Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38 146–152
37. Ming GL and Song H 2011 Adult neurogenesis in the Mammalian brain: significant answers and significant questions. Neuron 70 687–702
38. Monje ML, Toda H and Palmer TD 2003 Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 1760–1765
39. Morioka T, Kalehua AN and Streit WJ 1993 Characterization of microglial reaction after middle cerebral artery occlusion in rat brain. J. Comp. Neurol. 327 123–132
40. Mullen RJ, Buck CR and Smith AM 1992 NeuN, a neuronal specific nuclear protein in vertebrates. Development 116 201–211
41. Neumann J, Gunzer M, Gutzeit HO, Ullrich O, Reymann KG and Dinkel K 2006 Microglia provide neuroprotection after ischemia. F. J. 20 714–716
42. Neumann J et al. 2008 Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J. Neurosci. 28 5965–5975
43. Nissant A and Pallotto M 2011 Integration and maturation of newborn neurons in the adult olfactory bulb--from synapses to function. Eur. J. Neurosci. 33 1069–1077
44. Parent JM, Vexler ZS, Gong C, Derugin N and Ferriero DM 2002 Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52 802–813
45. Paxinos G, Watson CR and Emson PC 1980 AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J. Neurosci. Methods 3 129–149
46. Rocha EG et al. 2007 Callosal axon arbors in the limb representations of the somatosensory cortex (SI) in the agouti (Dasyprocta primnolopha). J. Comp. Neurol. 500 255–266
47. Sahay A, Wilson DA and Hen R 2011 Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70 582–588
48. Sakata H et al. 2012 Minocycline-preconditioned neural stem cells enhance neuroprotection after ischemic stroke in rats. J. Neurosci. 32 3462–3473
49. Sanai N et al. 2011 Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478 382–386
50. Sasaki T, Nakagomi T, Kirino T, Tamura A, Noguchi M, Saito I and Takakura K 1988 Indomethacin ameliorates ischemic neuronal damage in the gerbil hippocampal CA1 sector. Stroke 19 1399–1403
51. Sierra A et al. 2010 Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7 483–495
52. Souza-Rodrigues RD, Costa AM, Lima RR, Dos Santos CD, Picanco-Diniz CW and Gomes-Leal W 2008 Inflammatory response and white matter damage after microinjections of endothelin-1 into the rat striatum. Brain Res. 1200 78–88
53. Takahashi T, Ogawa Y, Kobayashi T, Sonobe H, Seguchi H, Tani T and Yoshida S 2004 A combination of selective COX-2 inhibitors and hydrogen peroxide increase the reactive oxygen species formation in osteosarcoma cells after X-ray irradiation. Int. J. Mol. Med. 14 405–408
54. Thored P et al. 2006 Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24 739–747
55. Thored P et al. 2009 Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57 835–849
56. Walton NM et al. 2006 Microglia instruct subventricular zone neurogenesis. Glia. 54 815–825
57. Wang Z et al. 2012 Meteorin is a chemokinetic factor in neuroblast migration and promotes stroke-induced striatal neurogenesis. J. Cereb. Blood Flow Metab. 32 387–398
58. Yan YP, Lang BT, Vemuganti R and Dempsey RJ 2009 Osteopontin is a mediator of the lateral migration of neuroblasts from the subventricular zone after focal cerebral ischemia. Neurochem. Int. 55 826–832
59. Yan YP, Sailor KA, Lang BT, Park SW, Vemuganti R and Dempsey RJ 2006a Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 27 1213–1224
60. Yan YP, Sailor KA, Vemuganti R and Dempsey RJ 2006b Insulin-like growth factor-1 is an endogenous mediator of focal ischemia-induced neural progenitor proliferation. Eur. J. Neurosci. 24 45–54
61. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH and Koistinaho J 1999 A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. USA 96 13496–13500