Involvement of activated microglia in increased vulnerability of motoneurons after facial nerve avulsion in presymptomatic amyotrophic lateral sclerosis model rats

GLIA

Volumn 60, Issue 5, 2012, Pages 782-793

  Sanagi, Tomomi ^a   Nakamura, Yasuko ^a   Suzuki, Eri ^a   Uchino, Shigeo ^a   Aoki, Masashi ^b   Warita, Hitoshi ^b   Itoyama, Yasuto ^b,c   Kohsaka, Shinichi ^a   Ohsawa, Keiko ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

Author keywords

Chemotaxis; Facial nuclei; Phagocytosis; Proliferation

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; MESSENGER RNA; PURINERGIC P2Y12 RECEPTOR;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; FACIAL NERVE; FACIAL NERVE INJURY; LASER MICRODISSECTION; MICROGLIA; MOTONEURON; NERVE CELL NECROSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FACIAL NERVE INJURIES; HUMANS; MICROGLIA; MOTOR NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; SUPEROXIDE DISMUTASE;

EID: 84858079462     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22308     Document Type: Article

References (44)

1. Alexianu ME, Kozovska M, Appel SH. 2001. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57: 1282-1289.
2. Aoki M, Kato S, Nagai M, Itoyama Y. 2005. Development of a rat model of amyotrophic lateral sclerosis expressing a human SOD1 transgene. Neuropathology 25: 365-370.
3. Aoki M, Ogasawara M, Matsubara Y, Narisawa K, Nakamura S, Itoyama Y, Abe K. 1993. Mild ALS in Japan associated with novel SOD mutation. Nat Genet 5: 323-324.
4. 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.
5. Boillee S, Vande Velde C, Cleveland DW. 2006a. ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron 52: 39-59.
6. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. 2006b. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312: 1389-1392.
7. Bruijn LI, Miller TM, Cleveland DW. 2004. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 27: 723-749.
8. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
9. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302: 113-117.
10. Deng YY, Lu J, Ling EA, Kaur C. 2009. Monocyte chemoattractant protein-1 (MCP-1) produced via NF-kappaB signaling pathway mediates migration of amoeboid microglia in the periventricular white matter in hypoxic neonatal rats. Glia 57: 604-621.
11. Hai T, Hartman MG. 2001. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: Activating transcription factor proteins and homeostasis. Gene 273: 1-11.
12. Hall ED, Oostveen JA, Gurney ME. 1998. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23: 249-256.
13. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9: 1512-1519.
14. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21: 1975-1982.
15. Ikeda K, Aoki M, Kawazoe Y, Sakamoto T, Hayashi Y, Ishigaki A, Nagai M, Kamii R, Kato S, Itoyama Y, Watabe K. 2005. Motoneuron degeneration after facial nerve avulsion is exacerbated in presymptomatic transgenic rats expressing human mutant Cu/Zn superoxide dismutase. J Neurosci Res 82: 63-70.
16. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. 1996. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224: 855-862.
17. Inoue K, Koizumi S, Tsuda M. 2007. The role of nucleotides in the neuron-glia communication responsible for the brain functions. J Neurochem 102: 1447-1458.
18. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446: 1091-1095.
19. Linda H, Skold MK, Ochsmann T. 2011. Activating transcription factor 3, a useful marker for regenerative response after nerve root injury. Front Neurol 2: 30.
20. 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.
21. Lopez-Redondo F, Nakajima K, Hondo S, Kohsaka S. 2000. Glutamate transporter GLT-1 is highly expressed in activated microglia following facial nerve axotomy. Brain Res Mol Brain Res 76: 429-435.
22. Maeda M, Tsuda M, Tozaki-Saitoh H, Inoue K, Kiyama H. 2010. Nerve injury-activated microglia engulf myelinated axons in a P2Y12 signaling-dependent manner in the dorsal horn. Glia 58: 1838-1846.
23. Malaspina A, Ngoh SF, Ward RE, Hall JC, Tai FW, Yip PK, Jones C, Jokic N, Averill SA, Michael-Titus AT, Priestley JV. 2010. Activation transcription factor-3 activation and the development of spinal cord degeneration in a rat model of amyotrophic lateral sclerosis. Neuroscience 169: 812-827.
24. Martin LJ, Kaiser A, Price AC. 1999. Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J Neurobiol 40: 185-201.
25. Nagai M, Aoki M, Miyoshi I, Kato M, Pasinelli P, Kasai N, Brown RH Jr., Itoyama Y. 2001. Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: Associated mutations develop motor neuron disease. J Neurosci 21: 9246-9254.
26. Nakajima K, Graeber MB, Sonoda M, Tohyama Y, Kohsaka S, Kurihara T. 2006. In vitro proliferation of axotomized rat facial nucleus-derived activated microglia in an autocrine fashion. J Neurosci Res 84: 348-359.
27. Nakajima K, Kohsaka S. 2001. Microglia: Activation and their significance in the central nervous system. J Biochem 130: 169-175.
28. Nakajima K, Kohsaka S. 2004. Microglia: Neuroprotective and neurotrophic cells in the central nervous system. Curr Drug Targets Cardiovasc Haematol Disord 4: 65-84.
29. Nakajima K, Shimojo M, Hamanoue M, Ishiura S, Sugita H, Kohsaka S. 1992. Identification of elastase as a secretory protease from cultured rat microglia. J Neurochem 58: 1401-1408.
30. Neumann H, Kotter MR, Franklin RJ. 2009. Debris clearance by microglia: An essential link between degeneration and regeneration. Brain 132(Pt 2): 288-295.
31. Ohsawa K, Irino Y, Sanagi T, Nakamura Y, Suzuki E, Inoue K, Kohsaka S. 2010. P2Y12 receptor-mediated integrin-beta1 activation regulates microglial process extension induced by ATP. Glia 58: 790-801.
32. 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.
33. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW. 1999. Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30: 77-105.
34. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O Regan JP, Deng HX, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung WY, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vanca MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, Brown RH Jr. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
35. Rosen DR, Sapp P, O'Regan J, McKenna-Yasek D, Schlumpf KS, Haines JL, Gusella JF, Horvitz HR, Brown RHJr. 1994. Genetic linkage analysis of familial amyotrophic lateral sclerosis using human chromosome 21 microsatellite DNA markers. Am J Med Genet 51: 61-69.
36. Ruan RS, Leong SK, Yeoh KH. 1995. The role of nitric oxide in facial motoneuronal death. Brain Res 698: 163-168.
37. Sanagi T, Yuasa S, Nakamura Y, Suzuki E, Aoki M, Warita H, Itoyama Y, Uchino S, Kohsaka S, Ohsawa K. 2010. Appearance of phagocytic microglia adjacent to motoneurons in spinal cord tissue from a presymptomatic transgenic rat model of amyotrophic lateral sclerosis. J Neurosci Res 88: 2736-2746.
38. Saxena S, Cabuy E, Caroni P. 2009. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 12: 627-636.
39. Song DY, Yang YC, Shin DH, Sugama S, Kim YS, Lee BH, Joh TH, Cho BP. 2008. Axotomy-induced dopaminergic neurodegeneration is accompanied with c-Jun phosphorylation and activation transcription factor 3 expression. Exp Neurol 209: 268-278.
40. Stolzing A, Grune T. 2004. Neuronal apoptotic bodies: Phagocytosis and degradation by primary microglial cells. FASEB J 18: 743-745.
41. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, Yonenobu K, Ochi T, Noguchi K. 2000. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol Cell Neurosci 15: 170-182.
42. Vlug AS, Teuling E, Haasdijk ED, French P, Hoogenraad CC, Jaarsma D. 2005. ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur J Neurosci 22: 1881-1894.
43. Yin T, Sandhu G, Wolfgang CD, Burrier A, Webb RL, Rigel DF, Hai T, Whelan J. 1997. Tissue-specific pattern of stress kinase activation in ischemic/reperfused heart and kidney. J Biol Chem 272: 19943-19950.
44. Zhou Y, Ling EA, Dheen ST. 2007. Dexamethasone suppresses monocyte chemoattractant protein-1 production via mitogen activated protein kinase phosphatase-1 dependent inhibition of Jun N-terminal kinase and p38 mitogen-activated protein kinase in activated rat microglia. J Neurochem 102: 667-678.