MCP-1/CCR2 signaling-mediated astrocytosis is accelerated in a transgenic mouse model of SOD1-mutated familial ALS

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Kawaguchi Niida, Motoko ^a   Yamamoto, Tomoko ^a   Kato, Yoichiro ^a   Inose, Yuri ^a   Shibata, Noriyuki ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Astrocyte; CCR2; MCP 1; Motor neuron; SOD1

Indexed keywords

EID: 85005914652     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-1-21     Document Type: Article

References (62)

1. Ince PG, Highley JR, Kirby J, Wharton SB, Takahashi H, Strong MJ, Shaw PJ: Molecular pathology and genetic advances in amyotrophic lateral sclerosis: an emerging molecular pathway and the significance of glial pathology. Acta Neuropathol 2011, 122: 657-671. 10.1007/s00401-011-0913-0
2. Rowland LP, Shneider NA: Amyotrophic lateral sclerosis. N Engl J Med 2001, 344: 1688-1700. 10.1056/NEJM200105313442207
3. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon Y, Deng HX: Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264: 1772-1775. 10.1126/science.8209258
4. McCombe PA, Henderson RD: The Role of immune and inflammatory mechanisms in ALS. Curr Mol Med 2011, 11: 246-254. 10.2174/156652411795243450
5. Shibata N, Kawaguchi-Niida M, Yamamoto T, Toi S, Hirano A, Kobayashi M: Effects of the PPARγ activator pioglitazone on p38 MAP kinase and IΚBα in the spinal cord of a transgenic mouse model of amyotrophic lateral sclerosis. Neuropathology 2008, 28: 387-398. 10.1111/j.1440-1789.2008.00890.x
6. Conductier G, Blondeau N, Guyon A, Nahon JL, Rovère C: The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J Neuroimmunol 2010, 224: 93-100. 10.1016/j.jneuroim.2010.05.010
7. Gu L, Tseng SC, Rollins BJ: Monocyte chemoattractant protein-1. Chem Immunol 1999, 72: 7-29.
8. Li MQ, Li HP, Meng YH, Wang XQ, Zhu XY, Mei J, Li DJ: Chemokine CCL2 enhances survival and invasiveness of endometrial stromal cells in an autocrine manner by activating Akt and MAPK/Erk1/2 signal pathway. Fertil Steril 2012,97(4):919-929. 10.1016/j.fertnstert.2011.12.049
9. Loberg RD, Day LL, Harwood J, Ying C, St John LN, Giles R, Neeley CK, Pienta KJ: CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia 2006, 8: 578-586. 10.1593/neo.06280
10. Lu Y, Cai Z, Galson DL, Xiao G, Liu Y, George DE, Melhem MF, Yao Z, Zhang J: Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate 2006, 66: 1311-1318. 10.1002/pros.20464
11. El Khoury J, Luster AD: Mechanisms of microglia accumulation in Alzheimer's disease: therapeutic implications. Trends Pharmacol Sci 2008, 29: 626-632. 10.1016/j.tips.2008.08.004
12. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM: Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 2001, 193: 713-726. 10.1084/jem.193.6.713
13. Hughes PM, Allegrini PR, Rudin M, Perry VH, Mir AK, Wiessner C: Monocyte chemoattractant protein-1 deficiency is protective in a murine stroke model. J Cereb Blood Flow Metab 2002, 22: 308-317.
14. Baron P, Bussini S, Cardin V, Corbo M, Conti G, Galimberti D, Scarpini E, Bresolin N, Wharton S, Shaw PJ, Silani V: Production of monocyte chemoattractant protein-1 in amyotrophic lateral sclerosis. Muscle Nerve 2005, 32: 541-544. 10.1002/mus.20376
15. Gupta PK, Prabhakar S, Sharma S, Anand A: A predictive model for amyotrophic lateral sclerosis (ALS) diagnosis. J Neurol Sci 2012, 312: 68-72. 10.1016/j.jns.2011.08.021
16. Henkel JS, Engelhardt JI, Siklós L, Simpson EP, Kim SH, Pan T, Goodman JC, Siddique T, Beers DR, Appel SH: Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 2004, 55: 221-235. 10.1002/ana.10805
17. Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH: Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden. Neurology 2004, 62: 1758-1765. 10.1212/WNL.62.10.1758
18. Wilms H, Sievers J, Dengler R, Bufler J, Deuschl G, Lucius R: Intrathecal synthesis of monocyte chemoattractant protein-1 (MCP-1) in amyotrophic lateral sclerosis: further evidence for microglial activation in neurodegeneration. J Neuroimmunol 2003, 144: 139-142. 10.1016/j.jneuroim.2003.08.042
19. Beers DR, Zhao W, Liao B, Kano O, Wang J, Huang A, Appel SH, Henkel JS: Neuroinflammation modulates distinct regional and temporal clinical responses in ALS mice. Brain Behav Immun 2011, 25: 1025-1035. 10.1016/j.bbi.2010.12.008
20. Henkel JS, Beers DR, Siklós L, Appel SH: The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol Cell Neurosci 2006, 31: 427-437. 10.1016/j.mcn.2005.10.016
21. Mantovani S, Garbelli S, Pasini A, Alimonti D, Perotti C, Melazzini M, et al.: Immune system alterations in sporadic amyotrophic lateral sclerosis patients suggest an ongoing neuroinflammatory process. J Neuroimmunol 2009, 210: 73-79. 10.1016/j.jneuroim.2009.02.012
22. Zhang R, Gascon R, Miller RG, Gelinas DF, Mass J, Lancero M, Narvaez A, McGrath MS: MCP-1 chemokine receptor CCR2 is decreased on circulating monocytes in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol 2006, 179: 87-93. 10.1016/j.jneuroim.2006.06.008
23. Dawson J, Miltz W, Mir AK, Wiessner C: Targeting monocyte chemoattractant protein-1 signalling in disease. Expert Opin Ther Targets 2003, 7: 35-48. 10.1517/14728222.7.1.35
24. Roebuck KA, Carpenter LR, Lakshminarayanan V, Page SM, Moy JN, Thomas LL: Stimulus-specific regulation of chemokine expression involves differential activation of the redox-responsive transcription factors AP-1 and NF-ΚB. J Leukoc Biol 1999, 65: 291-298.
25. Allavena P, Bianchi G, Zhou D, van Damme J, Jílek P, Sozzani S, Mantovani A: Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3. Eur J Immunol 1994, 24: 3233-3236. 10.1002/eji.1830241249
26. Amantea D, Nappi G, Bernardi G, Bagetta G, Corasaniti MT: Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 2009, 276: 13-26. 10.1111/j.1742-4658.2008.06766.x
27. Hinojosa AE, Garcia-Bueno B, Leza JC, Madrigal JL: CCL2/MCP-1 modulation of microglial activation and proliferation. J Neuroinflammation 2011, 8: 77. 10.1186/1742-2094-8-77
28. Lee EO, Park HJ, Kang JL, Kim HS, Chong YH: Resveratrol reduces glutamate-mediated monocyte chemotactic protein-1 expression via inhibition of extracellular signal-regulated kinase 1/2 pathway in rat hippocampal slice cultures. J Neurochem 2010, 112: 1477-1487. 10.1111/j.1471-4159.2009.06564.x
29. Mahad D, Callahan MK, Williams KA, Ubogu EE, Kivisäkk P, Tucky B, et al.: Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain 2006, 129: 212-223.
30. Semple BD, Bye N, Rancan M, Ziebell JM, Morganti-Kossmann MC: Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL2-/- mice. J Cereb Blood Flow Metab 2010, 30: 769-782. 10.1038/jcbfm.2009.262
31. Tanabe S, Heesen M, Berman MA, Fischer MB, Yoshizawa I, Luo Y, Dorf ME: Murine astrocytes express a functional chemokine receptor. J Neurosci 1997, 17: 6522-6528.
32. Kuhle J, Lindberg RL, Regeniter A, Mehling M, Steck AJ, Kappos L, Czaplinski A: Increased levels of inflammatory chemokines in amyotrophic lateral sclerosis. Eur J Neurol 2009, 16: 771-774. 10.1111/j.1468-1331.2009.02560.x
33. Philips T, Robberecht W: Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol 2011, 10: 253-263. 10.1016/S1474-4422(11)70015-1
34. Tateishi T, Yamasaki R, Tanaka M, Matsushita T, Kikuchi H, Isobe N, Ohyagi Y, Kira J: CSF chemokine alterations related to the clinical course of amyotrophic lateral sclerosis. J uroimmunol 2010, 222: 76-81.
35. Coughlan CM, McManus CM, Sharron M, Gao Z, Murphy D, Jaffer S, et al.: Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons. Neuroscience 2000, 97: 591-600. 10.1016/S0306-4522(00)00024-5
36. Meng SZ, Oka A, Takashima S: Developmental expressison of monocyte chemoattractant protein-1 in the human cerebellum and brainstem. Brain Dev 1999, 21: 30-35. 10.1016/S0387-7604(98)00065-5
37. Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyanf G, et al.: Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J Clin Invest 2012, 122: 3063-3087. 10.1172/JCI62636
38. Sargsyan SA, Blackburn DJ, Barber SC, Monk PN, Shaw PJ: Mutant SOD1 G93A microglia have an inflammatory phenotype and elevated production of MCP-1. NeuroReport 2009, 20: 1450-1455. 10.1097/WNR.0b013e328331e8fa
39. Semple BD, Kossmann T, Morganti-Kossmann MC: Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J Cereb Blood Flow Metab 2010, 30: 459-473. 10.1038/jcbfm.2009.240
40. Croitoru-Lamoury J, Guillemin GJ, Boussin FD, Mognetti B, Gigout LI, Chéret A, Vaslin B, Le Grand R, Brew BJ, Dormont D: Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNFα and IFNγ in CXCR4 and CCR5 modulation. Glia 2003, 41: 354-370. 10.1002/glia.10181
41. Hickman SE, El Khoury J: Mechanisms of mononuclear phagocyte recruitment in Alzheimer's disease. CNS Neurol Disord Drug Targets 2010, 9: 168-173. 10.2174/187152710791011982
42. Tanuma N, Sakuma H, Sasaki A, Matsumoto Y: Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis. Acta Neuropathol 2006, 112: 195-204. 10.1007/s00401-006-0083-7
43. Jee Y, Yoon WK, Okura Y, Tanuma N, Matsumoto Y: Upregulation of monocyte chemotactic protein-1 and CC chemokine receptor 2 in the central nervous system is closely associated with relapse of autoimmune encephalomyelitis in Lewis rats. J Neuroimmunol 2002, 128: 49-57. 10.1016/S0165-5728(02)00147-9
44. Quinones MP, Kalkonde Y, Estrada CA, Jimenez F, Ramirez R, Mahimainathan L, et al.: Role of astrocytes and chemokine systems in acute TNFalpha induced demyelinating syndrome: CCR2-dependent signals promote astrocyte activation and survival via NF-kappaB and Akt. Mol Cell Neurosci 2008, 37: 96-109. 10.1016/j.mcn.2007.08.017
45. Andjelkovic AV, Song L, Dzenko KA, Cong H, Pachter JS: Functional expression of CCR2 by human fetal astrocytes. J Neurosci Res 2002, 70: 219-231. 10.1002/jnr.10372
46. Sofroniew MV, Vinters HV: Astrocytes: biology and pathology. Acta Neuropathol 2010, 119: 7-35. 10.1007/s00401-009-0619-8
47. Xia MQ, Hyman BT: Chemokines/chemokine receptors in the central nervous system and Alzheimer's disease. J Neurovirol 1999, 5: 32-41. 10.3109/13550289909029743
48. Rappold PM, Tieu K: Astrocytes and therapeutics for Parkinson's disease. Neurotherapeutics 2010, 7: 413-423. 10.1016/j.nurt.2010.07.001
49. Ferraiuolo L, Higginbottom A, Heath PR, Barber S, Greenald D, Kirby J, Shaw PJ: Dysregulation of astrocyte-motoneuron cross-talk in mutant superoxide dismutase 1-related amyotrophic lateral sclerosis. Brain 2011, 134: 2627-2641. 10.1093/brain/awr193
50. Papadeas ST, Kraig SE, O'Banion C, Lepore AC, Maragakis NJ: Astrocytes carrying the superoxide dismutase 1 (SOD1G93A) mutation induce wild-type motor neuron degeneration in vivo. Proc Natl Acad Sci USA 2011, 108: 17803-17808. 10.1073/pnas.1103141108
51. van Der Voorn P, Tekstra J, Beelen RH, Tensen CP, Van Der Valk P, De Groot CJ: Expression of MCP-1 by reactive astrocytes in demyelinating multiple sclerosis lesions. Am J Pathol 1999, 154: 45-51. 10.1016/S0002-9440(10)65249-2
52. Takano T, Oberheim N, Cotrina ML, Nedergaard M: Astrocytes and ischemic injury. Stroke 2009, 40: S8-12. 10.1161/STROKEAHA.108.533166
53. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleaveland DW: Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008, 11: 251-253. 10.1038/nn2047
54. Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS: Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor. PLoS One 2008, 3: e2097. 10.1371/journal.pone.0002097
55. Kabashi E, Durham HD: Failure of protein quality control in amyotrophic lateral sclerosis. Biochim Biophys Acta 2006, 1762: 1038-1050. 10.1016/j.bbadis.2006.06.006
56. Sica A, Saccani A, Borsatti A, Power CA, Wells TN, Luini W, Polentarutti N, Sozzani S, Mantovani A: Bacterial lipopolysaccharide rapidly inhibits expression of C-C chemokine receptors in human monocytes. J Exp Med 1997, 185: 969-974. 10.1084/jem.185.5.969
57. Saccani A, Saccani S, Orlando S, Sironi M, Bernasconi S, Ghezzi P, Mantovani A, Sica A: Redox regulation of chemokine receptor expression. Proc Natl Acad Sci USA 2000, 97: 2761-2766. 10.1073/pnas.97.6.2761
58. Limoli CL, Giedzinski E, Baure J, Rola R, Fike JR: Redox changes induced in hippocampal precursor cells by heavy ion irradiation. Radiat Environ Biophys 2007, 46: 167-172. 10.1007/s00411-006-0077-9
59. Díaz-Amarilla P, Olivera-Bravo S, Trias E, Cragnolini A, Martínez-Palma L, Cassina P, Beckman J, Barbeito L: Phenotypically aberrant astrocytes that promote motoneuron damage in a model of inherited amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2011, 108: 18126-18131. 10.1073/pnas.1110689108
60. Gurney ME: Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 1994, 331: 1721-1722. 10.1056/NEJM199412223312516
61. Sapan CV, Lundblad RL, Price NC: Colorimetric protein assay techniques. Biotechnol Appl Biochem 1999, 29: 99-108.
62. Kawaguchi M, Shibata N, Horiuchi S, Kobayashi M: Glyoxal inactivates glutamate transporter-1 in cultured rat astrocytes. Neuropathology 2005, 25: 27-36. 10.1111/j.1440-1789.2004.00579.x