Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages

Journal of Experimental Medicine

Volumn 208, Issue 1, 2011, Pages 23-39

  London, Anat ^a   Itskovich, Elena ^a   Benhar, Inbal ^a   Kalchenko, Vyacheslav ^a   Mack, Matthias ^b   Jung, Steffen ^a   Schwartz, Michal ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL RENEWAL; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; INTOXICATION; MACROPHAGE; MALE; MONOCYTE; MOUSE; NERVE DEGENERATION; NERVE FIBER REGENERATION; NEUROPATHY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA INJURY; STEM CELL;

AGING; ANIMALS; IMMUNITY, INNATE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; RETINAL GANGLION CELLS; STEM CELLS; WOUND HEALING;

EID: 78651473243     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101202     Document Type: Article

References (94)

1. Ahmad, I., L. Tang, and H. Pham. 2000. Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 270:517-521. doi:10.1006/bbrc.2000.2473
2. Alvarado, J.A., L.J. Katz, S. Trivedi, and A.S. Shifera. 2010. Monocyte modulation of aqueous outflow and recruitment to the trabecular meshwork following selective laser trabeculoplasty. Arch. Ophthalmol. 128:731-737. doi:10.1001/archophthalmol.2010.85
3. Anchan, R.M., T.A. Reh, J. Angello, A. Balliet, and M. Walker. 1991. EGF and TGF-alpha stimulate retinal neuroepithelial cell proliferation in vitro. Neuron. 6:923-936. doi:10.1016/0896-6273(91)90233-P
4. Andrews, D.M., V.B. Matthews, L.M. Sammels, A.C. Carrello, and P.C. McMinn. 1999. The severity of murray valley encephalitis in mice is linked to neutrophil infiltration and inducible nitric oxide synthase activity in the central nervous system. J. Virol. 73:8781-8790.
5. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. van Rooijen, A. Plonquet, R.K. Gherardi, and B. Chazaud. 2007. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204:1057-1069. doi:10.1084/jem.20070075
6. Bakalash, S., A. Kessler, T. Mizrahi, R. Nussenblatt, and M. Schwartz. 2003. Antigenic specificity of immunoprotective therapeutic vaccination for glaucoma. Invest. Ophthalmol. Vis. Sci. 44:3374-3381. doi:10.1167/iovs.03-0080
7. Bakalash, S., G.B. Shlomo, E. Aloni, I. Shaked, L. Wheeler, R. Ofri, and M. Schwartz. 2005. T-cell-based vaccination for morphological and functional neuroprotection in a rat model of chronically elevated intraocular pressure. J. Mol. Med. 83:904-916. doi:10.1007/s00109-005-0689-6
8. Balasubramaniam, B., D.A. Carter, E.J. Mayer, and A.D. Dick. 2009. Microglia derived IL-6 suppresses neurosphere generation from adult human retinal cell suspensions. Exp. Eye Res. 89:757-766. doi:10.1016/j.exer.2009.06. 019
9. Barouch, R., and M. Schwartz. 2002. Autoreactive T cells induce neurotrophin production by immune and neural cells in injured rat optic nerve: implications for protective autoimmunity. FASEB J. 16:1304-1306.
10. Battista, D., C.C. Ferrari, F.H. Gage, and F.J. Pitossi. 2006. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur. J. Neurosci. 23:83-93. doi:10.1111/j.1460-9568.2005.04539.x
11. Ben Simon, G.J., S. Bakalash, E. Aloni, and M. Rosner. 2006. A rat model for acute rise in intraocular pressure: immune modulation as a therapeutic strategy. Am. J. Ophthalmol. 141:1105-1111. doi:10.1016/j.ajo.2006.01.073
12. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 441:235-238. doi:10.1038/nature04753
13. Boyd, Z.S., A. Kriatchko, J. Yang, N. Agarwal, M.B. Wax, and R.V. Patil. 2003. Interleukin-10 receptor signaling through STAT-3 regulates the apoptosis of retinal ganglion cells in response to stress. Invest. Ophthalmol. Vis. Sci. 44:5206-5211. doi:10.1167/iovs.03-0534
14. Bystrom, J., I. Evans, J. Newson, M. Stables, I. Toor, N. van Rooijen, M. Crawford, P. Colville-Nash, S. Farrow, and D.W. Gilroy. 2008. Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood. 112:4117-4127. doi:10.1182/blood-2007-12-129767
15. Close, J.L., J. Liu, B. Gumuscu, and T.A. Reh. 2006. Epidermal growth factor receptor expression regulates proliferation in the postnatal rat retina. Glia. 54:94-104. doi:10.1002/glia.20361
16. Cortes, L.M., D. Avichezer, P.B. Silver, D. Luger, M.J. Mattapallil, C.C. Chan, and R.R. Caspi. 2008. Inhibitory peptide analogs derived from a major uveitogenic epitope protect from antiretinal autoimmunity by inducing type 2 and regulatory T cells. J. Leukoc. Biol. 84:577-585. doi:10.1189/jlb.0308189
17. Cui, Q., Y. Yin, and L.I. Benowitz. 2009. The role of macrophages in optic nerve regeneration. Neuroscience. 158:1039-1048. doi:10.1016/j. neuroscience.2008.07.036
18. Da, T., and A.S. Verkman. 2004. Aquaporin-4 gene disruption in mice protects against impaired retinal function and cell death after ischemia. Invest. Ophthalmol. Vis. Sci. 45:4477-4483. doi:10.1167/iovs.04-0940
19. Dimitriu, C., M. Bach, W.A. Lagrèze, and T. Jehle. 2008. Methylprednisolone fails to preserve retinal ganglion cells and visual function after ocular ischemia in rats. Invest. Ophthalmol. Vis. Sci. 49:5003-5007. doi:10.1167/iovs.08-1869
20. Dirnagl, U., C. Iadecola, and M.A. Moskowitz. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22:391-397. doi:10.1016/S0166-2236(99)01401-0
21. Dreyer, E.B., D. Zurakowski, R.A. Schumer, S.M. Podos, and S.A. Lipton. 1996. Elevated glutamate levels in the vitreous body of humans and monkeys with glaucoma. Arch. Ophthalmol. 114:299-305.
22. Einstein, O., and T. Ben-Hur. 2008. The changing face of neural stem cell therapy in neurologic diseases. Arch. Neurol. 65:452-456. doi:10.1001/archneur. 65.4.452
23. Ekdahl, C.T., J.H. Claasen, S. Bonde, Z. Kokaia, and O. Lindvall. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA. 100:13632-13637. doi:10.1073/pnas.2234031100
24. Fisher, J., H. Levkovitch-Verbin, H. Schori, E. Yoles, O. Butovsky, J.F. Kaye, A. Ben-Nun, and M. Schwartz. 2001a. Vaccination for neuroprotection in the mouse optic nerve: implications for optic neuropathies. J. Neurosci. 21:136-142.
25. Fisher, J., T. Mizrahi, H. Schori, E. Yoles, H. Levkovitch-Verbin, S. Haggiag, M. Revel, and M. Schwartz. 2001b. Increased post-traumatic survival of neurons in IL-6-knockout mice on a background of EAE susceptibility. J. Neuroimmunol. 119:1-9. doi:10.1016/S0165-5728(01)00342-3
26. Gamm, D.M., S. Wang, B. Lu, S. Girman, T. Holmes, N. Bischoff, R.L. Shearer, Y. Sauvé, E. Capowski, C.N. Svendsen, and R.D. Lund. 2007. Protection of visual functions by human neural progenitors in a rat model of retinal disease. PLoS One. 2:e338. doi:10.1371/journal.pone.0000338
27. Geissmann, F., M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley. 2010. Development of monocytes, macrophages, and dendritic cells. Science. 327:656-661.
28. Giordano, F., A. De Marzo, F. Vetrini, and V. Marigo. 2007. Fibroblast growth factor and epidermal growth factor differently affect differentiation of murine retinal stem cells in vitro. Mol. Vis. 13:1842-1850.
29. Gordon, S., and P.R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964. doi:10.1038/nri1733
30. Gronert, K. 2010. Resolution, the grail for healthy ocular inflammation. Exp. Eye Res. 91:478-485. doi:10.1016/j.exer.2010.07.004
31. Gupta, N., and Y.H. Yücel. 2007. Glaucoma as a neurodegenerative disease. Curr. Opin. Ophthalmol. 18:110-114.
32. Harwerth, R.S., and H.A. Quigley. 2006. Visual field defects and retinal ganglion cell losses in patients with glaucoma. Arch. Ophthalmol. 124:853-859. doi:10.1001/archopht.124.6.853
33. Howell, G.R., R.T. Libby, and S.W. John. 2008. Mouse genetic models: an ideal system for understanding glaucomatous neurodegeneration and neuroprotection. Prog. Brain Res. 173:303-321. doi:10.1016/S0079-6123(08)01122-9
34. Jo, S.A., E. Wang, and L.I. Benowitz. 1999. Ciliary neurotrophic factor is an axogenesis factor for retinal ganglion cells. Neuroscience. 89:579-591. doi:10.1016/S0306-4522(98)00546-6
35. Johnson, T.V., N.D. Bull, and K.R. Martin. 2009. Transplantation prospects for the inner retina. Eye (Lond). 23:1980-1984.
36. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106-4114. doi:10.1128/MCB.20.11.4106-4114.2000
37. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity. 17:211-220. doi:10.1016/S1074-7613(02)00365-5
38. Kerr, E.C., B.J. Raveney, D.A. Copland, A.D. Dick, and L.B. Nicholson. 2008. Analysis of retinal cellular infiltrate in experimental autoimmune uveoretinitis reveals multiple regulatory cell populations. J. Autoimmun. 31:354-361. doi:10.1016/j.jaut.2008.08.006
39. Kerrigan-Baumrind, L.A., H.A. Quigley, M.E. Pease, D.F. Kerrigan, and R.S. Mitchell. 2000. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest. Ophthalmol. Vis. Sci. 41:741-748.
40. Kiyota, T., S. Okuyama, R.J. Swan, M.T. Jacobsen, H.E. Gendelman, and T. Ikezu. 2010. CNS expression of anti-inflammatory cytokine interleukin-4 attenuates Alzheimer's disease-like pathogenesis in APP+PS1 bigenic mice. FASEB J. 24:3093-3102. doi:10.1096/fj .10-155317
41. Klassen, H.J., T.F. Ng, Y. Kurimoto, I. Kirov, M. Shatos, P. Coffey, and M.J. Young. 2004. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest. Ophthalmol. Vis. Sci. 45:4167-4173. doi:10.1167/iovs.04-0511
42. Koeberle, P.D., J. Gauldie, and A.K. Ball. 2004. Effects of adenoviral-mediated gene transfer of interleukin-10, interleukin-4, and transforming growth factor-beta on the survival of axotomized retinal ganglion cells. Neuroscience. 125:903-920. doi:10.1016/S0306-4522(03)00398-1
43. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75:263-274. doi:10.1016/0092-8674(93)80068-P
44. Levin, L.A. 2003. Retinal ganglion cells and neuroprotection for glaucoma. Surv. Ophthalmol. 48:S21-S24. doi:10.1016/S0039-6257(03)00007-9
45. Levin, L.A., R.W. Beck, M.P. Joseph, S. Seiff, and R. Kraker. 1999. The treatment of traumatic optic neuropathy: the International Optic Nerve Trauma Study. Ophthalmology. 106:1268-1277. doi:10.1016/S0161-6420(99)00707-1
46. Liu, B., and J.S. Hong. 2003. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304:1-7. doi:10.1124/jpet.102.035048
47. Ma, T.C., A. Campana, P.S. Lange, H.H. Lee, K. Banerjee, J.B. Bryson, L. Mahishi, S. Alam, R.J. Giger, S. Barnes, et al. 2010. A large-scale chemical screen for regulators of the arginase 1 promoter identifies the soy iso- flavone daidzeinas a clinically approved small molecule that can promote neuronal protection or regeneration via a cAMP-independent pathway. J. Neurosci. 30:739-748. doi:10.1523/JNEUROSCI.5266-09.2010
48. Mack, M., J. Cihak, C. Simonis, B. Luckow, A.E. Proudfoot, J. Plachý, H. Brühl, M. Frink, H.J. Anders, V. Vielhauer, et al. 2001. Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice. J. Immunol. 166:4697-4704.
49. MacLaren, R.E., R.A. Pearson, A. MacNeil, R.H. Douglas, T.E. Salt, M. Akimoto, A. Swaroop, J.C. Sowden, and R.R. Ali. 2006. Retinal repair by transplantation of photoreceptor precursors. Nature. 444:203-207. doi:10.1038/nature05161
50. Mangan, P.R., L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, R.D. Hatton, S.M. Wahl, T.R. Schoeb, and C.T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature. 441:231-234. doi:10.1038/nature04754
51. Martino, G., and S. Pluchino. 2006. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 7:395-406. doi:10.1038/nrn1908
52. Moalem, G., R. Leibowitz-Amit, E. Yoles, F. Mor, I.R. Cohen, and M. Schwartz. 1999. Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat. Med. 5:49-55. doi:10.1038/4734
53. Molina-Holgado, E., J.M. Vela, A. Arévalo-Martín, and C. Guaza. 2001. LPS/IFN-gamma cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur. J. Neurosci. 13:493-502. doi:10.1046/j.0953-816x.2000.01412.x
54. Monje, M.L., H. Toda, and T.D. Palmer. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 302:1760-1765. doi:10.1126/science.1088417
55. Moore, K.W., R. de Waal Malefyt, R.L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765. doi:10.1146/annurev.immunol.19.1.683
56. Moshiri, A., J. Close, and T.A. Reh. 2004. Retinal stem cells and regeneration. Int. J. Dev. Biol. 48:1003-1014. doi:10.1387/ijdb.041870am
57. Mosser, D.M., and J.P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958-969. doi:10.1038/nri2448
58. Movahedi, K., M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, A. Beschin, P. De Baetselier, and J.A. Van Ginderachter. 2008. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood. 111:4233-4244. doi:10.1182/blood-2007-07-099226
59. Nadal-Nicolás, F.M., M. Jiménez-López, P. Sobrado-Calvo, L. Nieto- López, I. Cánovas-Martínez, M. Salinas-Navarro, M. Vidal-Sanz, and M. Agudo. 2009. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest. Ophthalmol. Vis. Sci. 50:3860-3868. doi:10.1167/iovs.08-3267
60. Nahrendorf, M., F.K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J.L. Figueiredo, P. Libby, R. Weissleder, and M.J. Pittet. 2007. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204:3037-3047. doi:10.1084/jem.20070885
61. Nickerson, P.E., J.G. Emsley, T. Myers, and D.B. Clarke. 2007. Proliferation and expression of progenitor and mature retinal phenotypes in the adult mammalian ciliary body after retinal ganglion cell injury. Invest. Ophthalmol. Vis. Sci. 48:5266-5275. doi:10.1167/iovs.07-0167
62. Nimmerjahn, A., F. Kirchhoff, and F. Helmchen. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 308:1314-1318. doi:10.1126/science.1110647 (Pubitemid 40746128)
63. Ohlsson, M., U. Westerlund, I.A. Langmoen, and M. Svensson. 2004. Methylprednisolone treatment does not influence axonal regeneration or degeneration following optic nerve injury in the adult rat. J. Neuroophthalmol. 24:11-18. (Pubitemid 38381218)
64. Pease, M.E., D.J. Zack, C. Berlinicke, K. Bloom, F. Cone, Y. Wang, R.L. Klein, W.W. Hauswirth, and H.A. Quigley. 2009. Effect of CNTF on retinal ganglion cell survival in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 50:2194-2200. doi:10.1167/iovs.08-3013
65. Pluchino, S., L. Muzio, J. Imitola, M. Deleidi, C. Alfaro-Cervello, G. Salani, C. Porcheri, E. Brambilla, F. Cavasinni, A. Bergamaschi, et al. 2008. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain. 131:2564-2578. doi:10.1093/brain/awn198
66. Reh, T.A., and A.J. Fischer. 2006. Retinal stem cells. Methods Enzymol. 419:52-73. doi:10.1016/S0076-6879(06)19003-5
67. Rolls, A., R. Shechter, A. London, Y. Ziv, A. Ronen, R. Levy, and M. Schwartz. 2007. Toll-like receptors modulate adult hippocampal neurogenesis. Nat. Cell Biol. 9:1081-1088. doi:10.1038/ncb1629
68. Rolls, A., R. Shechter, A. London, Y. Segev, J. Jacob-Hirsch, N. Amariglio, G. Rechavi, and M. Schwartz. 2008. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 5:e171. doi:10.1371/journal.pmed.0050171
69. Schori, H., J. Kipnis, E. Yoles, E. WoldeMussie, G. Ruiz, L.A. Wheeler, and M. Schwartz. 2001. Vaccination for protection of retinal ganglion cells against death from glutamate cytotoxicity and ocular hypertension: implications for glaucoma. Proc. Natl. Acad. Sci. USA. 98:3398-3403. doi:10.1073/pnas. 041609498
70. Schori, H., E. Yoles, L.A. Wheeler, T. Raveh, A. Kimchi, and M. Schwartz. 2002. Immune-related mechanisms participating in resistance and susceptibility to glutamate toxicity. Eur. J. Neurosci. 16:557-564. doi:10.1046/j.1460-9568. 2002.02134.x
71. Schwartz, M. 2004. Vaccination for glaucoma: dream or reality? Brain Res. Bull. 62:481-484. doi:10.1016/S0361-9230(03)00073-X
72. Schwartz, M., and J. Kipnis. 2007. Model of acute injury to study neuroprotection. Methods Mol. Biol. 399:41-53. doi:10.1007/978-1-59745-504-6-4
73. Shaw, P.J., and P.G. Ince. 1997. Glutamate, excitotoxicity and amyotrophic lateral sclerosis. J. Neurol. 244:S3-S14. doi:10.1007/BF03160574
74. Shechter, R., Y. Ziv, and M. Schwartz. 2007. New GABAergic interneurons supported by myelin-specific T cells are formed in intact adult spinal cord. Stem Cells. 25:2277-2282. doi:10.1634/stemcells.2006-0705
75. Shechter, R., A. Ronen, A. Rolls, A. London, S. Bakalash, M.J. Young, and M. Schwartz. 2008. Toll-like receptor 4 restricts retinal progenitor cell proliferation. J. Cell Biol. 183:393-400. doi:10.1083/jcb.200804010
76. Shechter, R., A. London, C. Varol, C. Raposo, M. Cusimano, G. Yovel, A. Rolls, M. Mack, S. Pluchino, G. Martino, et al. 2009. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 6:e1000113. doi:10.1371/journal.pmed. 1000113
77. Solberg, Y., G. Dubinski, M. Tchirkov, M. Belkin, and M. Rosner. 1999. Methylprednisolone therapy for retinal laser injury. Surv. Ophthalmol. 44:S85-S92. doi:10.1016/S0039-6257(99)00093-4
78. Stanke, J.J., and A.J. Fischer. 2010. Embryonic retinal cells and support to mature retinal neurons. Invest. Ophthalmol. Vis. Sci. 51:2208-2218. doi:10.1167/iovs.09-4447
79. Streilein, J.W. 2003. Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat. Rev. Immunol. 3:879-889. doi:10.1038/nri1224
80. Tropepe, V., B.L. Coles, B.J. Chiasson, D.J. Horsford, A.J. Elia, R.R. McInnes, and D. van der Kooy. 2000. Retinal stem cells in the adult mammalian eye. Science. 287:2032-2036. doi:10.1126/science.287.5460.2032
81. Vallières, L., I.L. Campbell, F.H. Gage, and P.E. Sawchenko. 2002. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 22:486-492.
82. Varol, C., L. Landsman, D.K. Fogg, L. Greenshtein, B. Gildor, R. Margalit, V. Kalchenko, F. Geissmann, and S. Jung. 2007. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 204:171-180. doi:10.1084/jem.20061011
83. Veldhoen, M., R.J. Hocking, C.J. Atkins, R.M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 24:179-189. doi:10.1016/j.immuni.2006.01.001
84. Vorwerk, C.K., M.S. Gorla, and E.B. Dreyer. 1999. An experimental basis for implicating excitotoxicity in glaucomatous optic neuropathy. Surv. Ophthalmol. 43:S142-S150. doi:10.1016/S0039-6257(99)00017-X
85. Weber, M.S., T. Prod'homme, S. Youssef, S.E. Dunn, C.D. Rundle, L. Lee, J.C. Patarroyo, O. Stüve, R.A. Sobel, L. Steinman, and S.S. Zamvil. 2007. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat. Med. 13:935-943. doi:10.1038/nm1620
86. Weinreb, R.N. 2007. Glaucoma neuroprotection: What is it? Why is it needed? Can. J. Ophthalmol. 42:396-398. doi:10.3129/i07-045
87. Werner, S., and R. Grose. 2003. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83:835-870.
88. Wohl, S.G., C.W. Schmeer, A. Kretz, O.W. Witte, and S. Isenmann. 2009. Optic nerve lesion increases cell proliferation and nestin expression in the adult mouse eye in vivo. Exp. Neurol. 219:175-186. doi:10.1016/j.expneurol.2009. 05.008
89. Wolf, S.A., B. Steiner, A. Wengner, M. Lipp, T. Kammertoens, and G. Kempermann. 2009. Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J. 23:3121-3128. doi:10.1096/fj.08-113944
90. Yin, Y., M.T. Henzl, B. Lorber, T. Nakazawa, T.T. Thomas, F. Jiang, R. Langer, and L.I. Benowitz. 2006. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat. Neurosci. 9:843-852. doi:10.1038/nn1701
91. Yoles, E., and M. Schwartz. 1998. Elevation of intraocular glutamate levels in rats with partial lesion of the optic nerve. Arch. Ophthalmol. 116:906-910.
92. Zhao, X., A.V. Das, F. Soto-Leon, and I. Ahmad. 2005. Growth factor-responsive progenitors in the postnatal mammalian retina. Dev. Dyn. 232:349-358. doi:10.1002/dvdy.20290
93. Ziv, Y., and M. Schwartz. 2008. Orchestrating brain-cell renewal: the role of immune cells in adult neurogenesis in health and disease. Trends Mol. Med. 14:471-478. doi:10.1016/j.molmed.2008.09.004
94. Ziv, Y., N. Ron, O. Butovsky, G. Landa, E. Sudai, N. Greenberg, H. Cohen, J. Kipnis, and M. Schwartz. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9:268-275. doi:10.1038/nn16299