Neuroprotective and axon growth promoting effects of intraocular inflammation do not depend on oncomodulin or the presence of large numbers of activated macrophages

Experimental Neurology

Volumn 209, Issue 2, 2008, Pages 469-482

  Hauk, Thomas G ^a   Müller, Adrienne ^a   Lee, Jieun ^a   Schwendener, Reto ^b   Fischer, Dietmar ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Axon regeneration; CNS; Macrophages; Oncomodulin; Optic nerve; Retina; Retinal ganglion cells; Zymosan

Indexed keywords

ONCOMODULIN; ZYMOSAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL INVASION; EYE INFLAMMATION; EYE INJURY; FEMALE; LENS; MACROPHAGE ACTIVATION; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; VITREOUS BODY;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; CALCIUM-BINDING PROTEINS; CARBOCYANINES; CELL LINE, TRANSFORMED; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LENS, CRYSTALLINE; MACROPHAGES; NERVE REGENERATION; NERVE TISSUE PROTEINS; OPTIC NERVE DISEASES; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; TIME FACTORS; TRANSFECTION; ZYMOSAN;

EID: 38649110471     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.09.020     Document Type: Article

References (42)

1. Appel E., Kolman O., Kazimirsky G., Blumberg P.M., and Brodie C. Regulation of GDNF expression in cultured astrocytes by inflammatory stimuli. NeuroReport 8 (1997) 3309-3312
2. Ballou S.P., and Lozanski G. Induction of inflammatory cytokine release from cultured human monocytes by C-reactive protein. Cytokine 4 (1992) 361-368
3. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., and Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14 (1994) 4368-4374
4. Biewenga J., van der Ende M.B., Krist L.F., Borst A., Ghufron M., and van Rooijen N. Macrophage depletion in the rat after intraperitoneal administration of liposome-encapsulated clodronate: depletion kinetics and accelerated repopulation of peritoneal and omental macrophages by administration of Freund's adjuvant. Cell Tissue Res. 280 (1995) 189-196
5. Bowman C.C., Rasley A., Tranguch S.L., and Marriott I. Cultured astrocytes express toll-like receptors for bacterial products. Glia 43 (2003) 281-291
6. Brewer L.M., Durkin J.P., and MacManus J.P. Immunocytochemical detection of oncomodulin in tumor tissue. J. Histochem. Cytochem. 32 (1984) 1009-1016
7. Bsibsi M., Ravid R., Gveric D., and van Noort J.M. Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 61 (2002) 1013-1021
8. Checchin D., Sennlaub F., Levavasseur E., Leduc M., and Chemtob S. Potential role of microglia in retinal blood vessel formation. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3595-3602
9. Clayshulte T.M., Taylor D.F., and Henzl M.T. Reactivity of cysteine 18 in oncomodulin. J. Biol. Chem. 265 (1990) 1800-1805
10. Correale J., and Villa A. The neuroprotective role of inflammation in nervous system injuries. J. Neurol. 251 (2004) 1304-1316
11. Dougherty K.D., Dreyfus C.F., and Black I.B. Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol. Dis. 7 (2000) 574-585
12. Esen N., Tanga F.Y., DeLeo J.A., and Kielian T. Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus. J. Neurochem. 88 (2004) 746-758
13. Fischer D., Pavlidis M., and Thanos S. Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest. Ophthalmol. Vis. Sci. 41 (2000) 3943-3954
14. Fischer D., Heiduschka P., and Thanos S. Lens-injury-stimulated axonal regeneration throughout the optic pathway of adult rats. Exp. Neurol. 172 (2001) 257-272
15. Fischer D., He Z., and Benowitz L.I. Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J. Neurosci. 24 (2004) 1646-1651
16. Fischer D., Petkova V., Thanos S., and Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24 (2004) 8726-8740
17. Holmlund U., Cebers G., Dahlfors A.R., Sandstedt B., Bremme K., Ekstrom E.S., and Scheynius A. Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Toll-like receptor-4 in the human placenta. Immunology 107 (2002) 145-151
18. Lazarov-Spiegler O., Solomon A.S., and Schwartz M. Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24 (1998) 329-337
19. Leon S., Yin Y., Nguyen J., Irwin N., and Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 20 (2000) 4615-4626
20. Leskovar A., Moriarty L.J., Turek J.J., Schoenlein I.A., and Borgens R.B. The macrophage in acute neural injury: changes in cell numbers over time and levels of cytokine production in mammalian central and peripheral nervous systems. J. Exp. Biol. 203 (2000) 1783-1795
21. Lorber B., Berry M., Logan A., and Tonge D. Effect of lens lesion on neurite outgrowth of retinal ganglion cells in vitro. Mol. Cell. Neurosci. 21 (2002) 301-311
22. Lorber B., Berry M., and Logan A. Lens injury stimulates adult mouse retinal ganglion cell axon regeneration via both macrophage- and lens-derived factors. Eur. J. Neurosci. 21 (2005) 2029-2034
23. Mey J., and Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res. 602 (1993) 304-317
24. Moghimi S.M. Apoptotic cell death in activated monocytes following incorporation of clodronate-liposomes. J. Leukoc. Biol. 61 (1997) 643-645
25. Naito M., Nagai H., Kawano S., Umezu H., Zhu H., Moriyama H., Yamamoto T., Takatsuka H., and Takei Y. Liposome-encapsulated dichloromethylene diphosphonate induces macrophage apoptosis in vivo and in vitro. J. Leukoc. Biol. 60 (1996) 337-344
26. Nilsen N., Nonstad U., Khan N., Knetter C.F., Akira S., Sundan A., Espevik T., and Lien E. Lipopolysaccharide and double-stranded RNA up-regulate toll-like receptor 2 independently of myeloid differentiation factor 88. J. Biol. Chem. 279 (2004) 39727-39735
27. Pernet V., and Di Polo A. Synergistic action of brain-derived neurotrophic factor and lens injury promotes retinal ganglion cell survival, but leads to optic nerve dystrophy in vivo. Brain 129 (2006) 1014-1026
28. Popovich P.G., Guan Z., Wei P., Huitinga I., van Rooijen N., and Stokes B.T. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158 (1999) 351-365
29. Pouvreau I., Zech J.C., Thillaye-Goldenberg B., Naud M.C., Van Rooijen N., and de Kozak Y. Effect of macrophage depletion by liposomes containing dichloromethylene-diphosphonate on endotoxin-induced uveitis. J. Neuroimmunol. 86 (1998) 171-181
30. Rapalino O., Lazarov-Spiegler O., Agranov E., Velan G.J., Yoles E., Fraidakis M., Solomon A., Gepstein R., Katz A., Belkin M., Hadani M., and Schwartz M. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 4 (1998) 814-821
31. Rudge J.S., Alderson R.F., Pasnikowski E., McClain J., Ip N.Y., and Lindsay R.M. Expression of ciliary neurotrophic factor and the neurotrophins - nerve growth factor, brain-derived neurotrophic factor and neurotrophin 3 - in cultured rat hippocampal astrocytes. Eur. J. Neurosci. 4 (1992) 459-471
32. Rudge J.S., Morrissey D., Lindsay R.M., and Pasnikowski E.M. Regulation of ciliary neurotrophic factor in cultured rat hippocampal astrocytes. Eur. J. Neurosci. 6 (1994) 218-229
33. Selander K.S., Monkkonen J., Karhukorpi E.K., Harkonen P., Hannuniemi R., and Vaananen H.K. Characteristics of clodronate-induced apoptosis in osteoclasts and macrophages. Mol. Pharmacol. 50 (1996) 1127-1138
34. Setzu A., Lathia J.D., Zhao C., Wells K., Rao M.S., Ffrench-Constant C., and Franklin R.J. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54 (2006) 297-303
35. Slegers T.P., Torres P.F., Broersma L., van Rooijen N., van Rij G., and van der Gaag R. Effect of macrophage depletion on immune effector mechanisms during corneal allograft rejection in rats. Invest. Ophthalmol. Vis. Sci. 41 (2000) 2239-2247
36. Steinmetz M.P., Horn K.P., Tom V.J., Miller J.H., Busch S.A., Nair D., Silver D.J., and Silver J. Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J. Neurosci. 25 (2005) 8066-8076
37. Taylor P.R., Brown G.D., Reid D.M., Willment J.A., Martinez-Pomares L., Gordon S., and Wong S.Y. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169 (2002) 3876-3882
38. Underhill D.M., Ozinsky A., Hajjar A.M., Stevens A., Wilson C.B., Bassetti M., and Aderem A. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401 (1999) 811-815
39. van Rooijen N., Sanders A., and van den Berg T.K. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J. Immunol. Methods 193 (1996) 93-99
40. Widenfalk J., Lundstromer K., Jubran M., Brene S., and Olson L. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci. 21 (2001) 3457-3475
41. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., and Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 23 (2003) 2284-2293
42. Yin Y., Henzl M.T., Lorber B., Nakazawa T., Thomas T.T., Jiang F., Langer R., and Benowitz L.I. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat. Neurosci. 9 (2006) 843-852