Polarization of Macrophages/Microglia toward an M2 Phenotype as a Therapeutic Strategy for Stroke Treatment

Rational Basis for Clinical Translation in Stroke Therapy

Volumn , Issue , 2014, Pages 381-392

  Ballesteros, Iván ^a   Cuartero, María I ^a   de la Parra, Juan ^a   Pérez Ruiz, Alberto ^a   Hurtado, Olivia ^a   Lizasoain, Ignacio ^a   Moro, María Angeles ^a  

^a SCHOOL OF MEDICINE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84928652341     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b16285-26     Document Type: Chapter

References (58)

1. Ballesteros I, Cuartero MI, Pradillo JM et al. Rosiglitazone-induced CD36 up-regulation resolves inflammation by PPARγ and 5-LO-dependent pathways2, J Leukoc Biol, 2014;95:587-598.
2. Beatty GL, Chiorean EG, Fishman MP et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011;331:1612-1616.
3. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, Kuchroo VK. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 1998;161:3299-3306.
4. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat Immunol 2010;11:889-896.
5. Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 2008;28:4283-4292.
6. Castellanos M, Castillo J, Garcia MM, Leira R, Serena J, Chamorro A, Davalos A. Inflammation-mediated damage in progressing lacunar infarctions: A potential therapeutic target. Stroke 2002;33:982-987.
7. Colton CA. Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 2009;4:399-418.
8. Couzin J. Clinical research. ALS trial raises questions about promising drug. Science 2007;318:1227.
9. Duluc D, Corvaisier M, Blanchard S, Catala L, Descamps P, Gamelin E, Ponsoda S, Delneste Y, Hebbar M, Jeannin P. Interferon-gamma reverses the immunosuppressive and protumoral properties and prevents the generation of human tumor-associated macrophages. Int J Cancer 2009;125:367-373.
10. Falcone M, Rajan AJ, Bloom BR, Brosnan CF. A critical role for IL-4 in regulating disease severity in experimental allergic encephalomyelitis as demonstrated in IL-4-deficient C57BL/6 mice and BALB/c mice. J Immunol 1998;160:4822-4830.
11. Fitch MT, Silver J. Activated macrophages and the blood-brain barrier: Inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol 1997;148:587-603.
12. Frieler RA, Meng H, Duan SZ, Berger S, Schutz G, He Y, Xi G, Wang MM, Mortensen RM. Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke 2011;42:179-185.
13. Furlan R, Poliani PL, Galbiati F, Bergami A, Grimaldi LM, Comi G, Adorini L, Martino, G. Central nervous system delivery of interleukin 4 by a nonreplicative herpes simplex type 1 viral vector ameliorates autoimmune demyelination. Hum Gene Ther 1998;9:2605-2617.
14. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3:23-35.
15. Gordon S, Martinez FO. Alternative activation of macrophages: Mechanism and functions. Immunity 2010;32:593-604.
16. Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, Thompson RG, Robinson SC, Balkwill FR. “Re-educating” tumor-associated macrophages by targeting NF-kappaB. J Exp Med 2008;205:1261-1268.
17. Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, Gao Y, Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012;43:3063-3070.
18. Iadecola C, Anrather J. The immunology of stroke: From mechanisms to translation. Nat Med 2011;17:796-808.
19. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J. Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer’s disease: Age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 2008;28:11650-11661.
20. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: Role of inflammatory cells. J Leukoc Biol 2010;87:779-789.
21. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009;29:13435-13444.
22. Kim HM, Shin HY, Jeong HJ et al. Reduced IL-2 but elevated IL-4, IL-6, and IgE serum levels in patients with cerebral infarction during the acute stage. J Mol Neurosci 2000;14:191-196.
23. Kobayashi K, Imagama S, Ohgomori T et al. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis 2013;4:e525.
24. London A, Itskovich E, Benhar I, Kalchenko V, Mack M, Jung S, Schwartz M. Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages. J Exp Med 2011;208:23-39.
25. Mandrekar-Colucci S, Karlo JC, Landreth GE. Mechanisms underlying the rapid peroxisome proliferator-activated receptor-gamma-mediated amyloid clearance and reversal of cognitive deficits in a murine model of Alzheimer’s disease. J Neurosci 2012;32:10117-10128.
26. Mandrekar-Colucci S, Landreth GE. Microglia and inflammation in Alzheimer’s disease. CNS Neurol Disord Drug Targets 2010;9:156-167.
27. Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity 2005;23:344-346.
28. Matzinger P. The danger model: A renewed sense of self. Science 2002;296:301-305.
29. McPhail LT, Stirling DP, Tetzlaff W, Kwiecien JM, Ramer MS. The contribution of activated phagocytes and myelin degeneration to axonal retraction/dieback following spinal cord injury. Eur J Neurosci 2004;20:1984-1994.
30. Mikita J, Dubourdieu-Cassagno N, Deloire MS et al. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration. Mult Scler 2011;17:2-15.
31. Mosser DM. The many faces of macrophage activation. J Leukoc Biol 2003;73:209-212.
32. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-969.
33. Perego C, Fumagalli S, De Simoni MG. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation 2011;8:174.
34. Perry VH, Cunningham C, Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 2007;7:161-167.
35. Ponomarev ED, Maresz K, Tan Y, Dittel BN. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci 2007;27:10714-10721.
36. Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat Med 2011;17:64-70.
37. Prewitt CM, Niesman IR, Kane CJ, Houle JD. Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 1997;148:433-443.
38. Puig-Kroger A, Serrano-Gomez D, Caparros E et al. Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J Biol Chem 2004;279:25680-25688.
39. Raes G, Van den Bergh R, De Baetselier P, Ghassabeh GH, Scotton C, Locati M, Mantovani A, Sozzani S. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J Immunol 2005;174:6561, author reply 6561-6562.
40. Rapalino O, Lazarov-Spiegler O, Agranov E et al. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 1998;4:814-821.
41. Serhan CN, Savill J. Resolution of inflammation: The beginning programs the end. Nat Immunol 2005;6:1191-1197.
42. Shaw MK, Lorens JB, Dhawan A et al. Local delivery of interleukin 4 by retrovirus-transduced T lymphocytes ameliorates experimental autoimmune encephalomyelitis. J Exp Med 1997;185:1711-1714.
43. Shechter R, London A, Varol C et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009;6:e1000113.
44. Sica A, Mantovani A. Macrophage plasticity and polarization: In vivo veritas. J Clin Invest 2012;122:787-795.
45. Storkebaum E, Lambrechts D, Dewerchin M et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005;8:85-92.
46. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol 2005;175:342-349.
47. Suzuki Y, Claflin J, Wang X, Lengi A, Kikuchi T. Microglia and macrophages as innate producers of interferon-gamma in the brain following infection with Toxoplasma gondii. Int J Parasitol 2005;35:83-90.
48. Tarkowski E, Rosengren L, Blomstrand C, Wikkelso C, Jensen C, Ekholm S, Tarkowski A. Early intrathecal production of interleukin-6 predicts the size of brain lesion in stroke. Stroke 1995;26:1393-1398.
49. Theodorou GL, Marousi S, Ellul J, Mougiou A, Theodori E, Mouzaki A, Karakantza M. T helper 1 (Th1)/Th2 cytokine expression shift of peripheral blood CD4+ and CD8+ T cells in patients at the post-acute phase of stroke. Clin Exp Immunol 2008;152:456-463.
50. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA 2007;104:19446-19451.
51. Tovar-y-Romo LB, Tapia R. Delayed administration of VEGF rescues spinal motor neurons from death with a short effective time frame in excitotoxic experimental models in vivo. ASN Neuro 2012;4(2):e00081.
52. Vila N, Castillo J, Davalos A, Chamorro A. Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000;31:2325-2329.
53. Xiao Y, Xu J, Wang S, Mao C, Jin M, Ning G, Zhang Y. Genetic ablation of steroid receptor coactivator-3 promotes PPAR-beta-mediated alternative activation of microglia in experimental autoimmune encephalomyelitis. Glia 2010;58:932-942.
54. Xiong X, Barreto GE, Xu L, Ouyang YB, Xie X, Giffard RG. Increased brain injury and worsened neurological outcome in interleukin-4 knockout mice after transient focal cerebral ischemia. Stroke 2011;42:2026-2032.
55. Xu Y, Qian L, Zong G et al. Class A scavenger receptor promotes cerebral ischemic injury by pivoting microglia/macrophage polarization. Neuroscience 2012;218:35-48.
56. Yilmaz G, Granger DN. Leukocyte recruitment and ischemic brain injury. Neuromolecular Med 2010;12:193-204.
57. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI. Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci 2003;23:2284-2293.
58. Zarruk JG, Fernandez-Lopez D, Garcia-Yebenes I et al. Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection. Stroke 2012;43:211-219.