Extracellular mutant SOD1 induces microglial-mediated motoneuron injury

GLIA

Volumn 58, Issue 2, 2010, Pages 231-243

  Zhao, Weihua ^a   Beers, David R ^a   Henkel, Jenny S ^a   Zhang, Wei ^a   Urushitani, Makoto ^b,c   Julien, Jean Pierre ^b   Appel, Stanley H ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

^b LAVAL UNIVERSITY   (Canada)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

CD14; Microglia; Motoneurons; Mutant SOD1; Toll like receptors

Indexed keywords

ALANINE; ARGININE; CD14 ANTIGEN; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOKINE; FREE RADICAL; GLYCINE; MUTANT PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CELL KILLING; CONTROLLED STUDY; CYTOKINE RELEASE; EXTRACELLULAR SPACE; INNATE IMMUNITY; MICROGLIA; MOTONEURON; MOUSE; NERVE CELL CULTURE; NERVE CELL LESION; NERVE FUNCTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD14; CELL DEATH; CELLS, CULTURED; COCULTURE TECHNIQUES; EXTRACELLULAR SPACE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROGLIA; MOTOR NEURONS; MUTATION, MISSENSE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPINAL CORD; SUPEROXIDE DISMUTASE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 73149105494     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20919     Document Type: Article

References (51)

1. Arce V, Garces A, de Bovis B, Filippi P, Henderson C, Pettmann B, deLapeyrière O. 1999. Cardiotrophin-1 requires LIFRbeta to promote survival of mouse motoneurons purified by a novel technique. J Neurosci Res 55:119-126.
2. Bate C, Veerhuis R, Eikelenboom P, Williams A. 2004. Microglia kill amyloid-beta1-42 damaged neurons by a CD14-dependent process. Neuroreport 15:1427-1430.
3. Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, Yen AA, Siklos L, McKercher SR, Appel SH. 2006. Wild-type microglia extend survival in PU. 1 Knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 103:16021-16026.
4. Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. 2008. CD4+ T-cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci USA 105:15558-15563.
5. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. 2006. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
6. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, Brown RH Jr, Price DL, Sisodia SS, Cleveland DW. 1994. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 91:8292-8296.
7. Carriedo SG, Yin HZ, Weiss JH. 1996. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 16:4069-4079.
8. Cleveland DW, Rothstein JD. 2001. From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819.
9. Echchannaoui H, Frei K, Letiembre M, Strieter RM, Adachi Y, Landmann R. 2005. CD14 deficiency leads to increased MIP-2 production, CXCR2 expression, neutrophil transmigration, and early death in pneumococcal infection. J Leukoc Biol 78:705-715.
10. Eikelenboom P, Veerhuis R. 1996. The role of complement and activated microglia in the pathogenesis of Alzheimer's disease. Neurobiol Aging 17:673-680.
11. El Khoury JB, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD. 1996. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382:716-719.
12. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, Luster AD. 2003. CD36 mediates the innate host response to beta-amyloid. J Exp Med 197:1657-1666.
13. Ezzi SA, Urushitani M, Julien JP. 2007. Wild-type superoxide dismutase acquires binding and toxic properties of ALS-linked mutant forms through oxidation. J Neurochem 102:170-178.
14. Fassbender K, Walter S, Kühl S, Landmann R, Ishii K, Bertsch T, Stalder AK, Muehlhauser F, Liu Y, Ulmer AJ, Rivest S, Lentschat A, Gulbins E, Jucker M, Staufenbiel M, Brechtel K, Walter J, Multhaup G, Penke B, Adachi Y, Hartmann T, Beyreuther K. 2004. The LPS receptor (CD14) links innate immunity with Alzheimer's disease. FASEB J 18:203-205.
15. Furukawa Y, O'Halloran TV. 2005. Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo- and reduced form of SOD1, leading to unfolding and oxidative aggregation. J Biol Chem 280:17266-17274.
16. Furukawa Y, Fu R, Deng HX, Siddique T, O'Halloran TV. 2006. Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc Natl Acad Sci USA 103:7148-7153.
17. Gruzman A, Wood WL, Alpert E, Prasad MD, Miller RG, Rothstein JD, Bowser R, Hamilton R, Wood TD, Cleveland DW, Lingappa VR, Liu J. 2007. Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 104:12524-12529.
18. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Chen W, Zhai P, Sufit RL, Siddique T. 1994. Motor neuron degeneration in mice that express a human Cu/Zn superoxide dismutase mutation. Science 264:1772-1775.
19. Harraz MM, Marden JJ, Zhou W, Zhang Y, Williams A, Sharov VS, Nelson K, Luo M, Paulson H, Schöneich C, Engelhardt JF. 2008. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J Clin Invest 118:659-670.
20. Henkel JS, Engelhardt JI, Siklos L, Simpson EP, Kim SH, Pan T, Goodman JC, Siddique T, Beers DR, Appel SH. 2004. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55:221-235.
21. Henkel JS, Beers DR, Siklós L, Appel SH. 2006. The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol Cell Neurosci 31:427-437.
22. Jaarsma D, Teuling E, Haasdijk ED, De Zeeuw CI, Hoogenraad CC. 2008. Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci 28:2075-2088.
23. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. 2005. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 175:4320-4330.
24. Kabashi E, Valdmanis PN, Dion P, Rouleau GA. 2007. Oxidized/misfolded superoxide dismutase-1: The cause of all amyotrophic lateral sclerosis? Ann Neurol 62:553-559.
25. Kang J, Rivest S. 2007. MyD88-deficient bone marrow cells accelerate onset and reduce survival in a mouse model of amyotrophic lateral sclerosis. J Cell Biol 179:1219-1230.
26. Letiembre M, Liu Y, Walter S, Hao W, Pfander T, Wrede A, Schulz-Schaeffer W, Fassbender K. 2009. Screening of innate immune receptors in neurodegenerative diseases: A similar pattern. Neurobiol Aging 30:759-768.
27. Leung TF, Tang NLS, Wong GWK, Fok TF. 2005. CD14 and toll-like receptors: Potential contribution of genetic factors and mechanisms to inflammation and allergy. Curr Drug Targets Inflamm Allergy 4:169-175.
28. Lino MM, Schneider C, Caroni P. 2002. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 22:4825-4832.
29. Lobsiger CS, Cleveland DW. 2007. Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci 10:1355-1360.
30. Lomen-Hoerth C. 2008. Amyotrophic lateral sclerosis from bench to bedside. Semin Neurol 28:205-211.
31. Marden JJ, Harraz MM, Williams AJ, Nelson K, Luo M, Paulson H, Engelhardt JF. 2007. Redox modifier genes in amyotrophic lateral sclerosis in mice. J Clin Invest 117:2913-2919.
32. McGeer PL, McGeer EG. 2002. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26:459-470.
33. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S. 2007. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622.
34. Nguyen MD, D'Aigle T, Gowing G, Julien JP, Rivest S. 2004. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J Neurosci 24:1340-1349.
35. Olson JK, Miller SD. 2004. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173:3916-3924.
36. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA. 2001. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 21:3369-3374.
37. Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DF, Wilcox HM, Flood DG, Beal MF, Brown RH Jr, Scott RW, Snider WD. 1996. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 13:43-47.
38. Takeuchi H, Mizuno T, Zhang G, Wang J, Kawanokuchi J, Kuno R, Suzumura A. 2005. Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport. J Biol Chem 280:10444-10454.
39. Tan AS, Berridge MV. 2000. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: A simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents. J Immunol Methods 238:59-68.
40. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP. 2007. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 104:13798-13803.
41. Townsend KP, Town T, Mori T, Lue LF, Shytle D, Sanberg PR, Morgan D, Fernandez F, Flavell RA, Tan J. 2005. CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide. Eur J Immunol 35:901-910.
42. Urushitani M, Kurisu J, Tateno M, Hatakeyama S, Nakayama K, Kato S, Takahashi R. 2004. CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J Neurochem 90:231-244.
43. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. 2006. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9:108-118.
44. Wang J, Xu G, Gonzales V, Coonfield M, Fromholt D, Copeland NG, Jenkins NA, Borchelt DR. 2002. Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Neurobiol Dis 10:128-138.
45. Watters TM, Kenny EF, O'Neill LA. 2007. Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunol Cell Biol 85:411-419.
46. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL. 1995. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.
47. G93A microglia are more neurotoxic relative to wild-type microglia. J Neurochem 102:2008-2019.
48. Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis-Downes M, Mikse OR, Cleveland DW, Goldstein LS. 2008a. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci USA 105:7594-7599.
49. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW. 2008b. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11:251-253.
50. Zhao W, Xie W, Le W, Beers DR, He Y, Henkel JS, Simpson EP, Yen AA, Xiao Q, Appel SH. 2004. Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. J Neuropathol Exp Neurol 63:964-977.
51. Zhao W, Xie W, Xiao Q, Beers DR, Appel SH. 2006. Protective effects of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J Neurochem 99:1176-1187.