Microglia and motor neurons during disease progression in the SOD1G93A mouse model of amyotrophic lateral sclerosis: Changes in arginase1 and inducible nitric oxide synthase

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Lewis, Katherine E ^a   Rasmussen, Anna L ^a   Bennett, William ^a   King, Anna ^a   West, Adrian K ^a   Chung, Roger S ^a,b   Chuah, Meng I ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

Amyotrophic lateral sclerosis; Arginase1; Cervical spinal cord; Inducible nitric oxide synthase; Lumbar spinal cord; Microglia; Motor neurons; Neuroinflammation

Indexed keywords

ARGINASE 1; ARGININE; INDUCIBLE NITRIC OXIDE SYNTHASE; SUPEROXIDE DISMUTASE; UBIQUITIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; BODY WEIGHT; CERVICAL SPINAL CORD; CONTROLLED STUDY; DISEASE COURSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LUMBAR SPINAL CORD; MICROGLIA; MOTONEURON; MOUSE; NEUROPROTECTION; NONHUMAN; PHENOTYPE; TRANSGENIC MOUSE; WILD TYPE;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ARGINASE; BODY WEIGHT; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MOTOR NEURONS; MUSCLE STRENGTH; NITRIC OXIDE SYNTHASE TYPE II; PSYCHOMOTOR PERFORMANCE; SPINAL CORD; SUPEROXIDE DISMUTASE; UBIQUITIN;

EID: 84899150521     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-55     Document Type: Article

References (51)

1. Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med 1994, 330:585-591. 10.1056/NEJM199403033300901, 8302340.
2. 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 W-Y, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62. 10.1038/362059a0, 8446170.
3. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, Brown RH, Price DL, Sisodia SS, Cleveland DW. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci U S A 1994, 91:8292-8296. 10.1073/pnas.91.17.8292, 44592, 8058797.
4. 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. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775. 10.1126/science.8209258, 8209258.
5. Ferraiuolo L, Kirby J, Grierson AJ, Sendtner M, Shaw PJ. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat Rev Neurol 2011, 7:616-630. 10.1038/nrneurol.2011.152, 22051914.
6. Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 2009, 65(Suppl 1):S3-S9.
7. Van Damme P, Robberecht W. Recent advances in motor neuron disease. Curr Opin Neurol 2009, 22:486-492. 10.1097/WCO.0b013e32832ffbe3, 19593125.
8. Simpson EP, Yen AA, Appel SH. Oxidative stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Curr Opin Rheumatol 2003, 15:730-736. 10.1097/00002281-200311000-00008, 14569202.
9. Strong MJ. The basic aspects of therapeutics in amyotrophic lateral sclerosis. Pharmacol Ther 2003, 98:379-414. 10.1016/S0163-7258(03)00040-8, 12782245.
10. Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001, 57:1282-1289. 10.1212/WNL.57.7.1282, 11591849.
11. Hall ED, Oostveen JA, Gurney ME. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998, 23:249-256. 10.1002/(SICI)1098-1136(199807)23:3<249::AID-GLIA7>3.0.CO;2-#, 9633809.
12. 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, 3096756, 21176785.
13. Liao B, Zhao W, Beers DR, Henkel JS, Appel SH. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp Neurol 2012, 237:147-152. 10.1016/j.expneurol.2012.06.011, 22735487.
14. Zhao W, Xie W, Le W, Beers DR, He Y, Henkel JS, Simpson EP, Yen AA, Xiao Q, Appel SH. Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. J Neuropathol Exp Neurol 2004, 63:964-977.
15. Ferrante RJ, Shinobu LA, Schulz JB, Matthews RT, Thomas CE, Kowall NW, Gurney ME, Beal MF. Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann Neurol 1997, 42:326-334. 10.1002/ana.410420309, 9307254.
16. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci U S A 2005, 102:9936-9941. 10.1073/pnas.0502552102, 1174990, 15998743.
17. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001, 2:907-916. 10.1038/ni1001-907, 11577346.
18. Almer G, Vukosavic S, Romero N, Przedborski S. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 1999, 72:2415-2425.
19. Lee J, Ryu H, Kowall NW. Motor neuronal protection by L-arginine prolongs survival of mutant SOD1 (G93A) ALS mice. Biochem Biophys Res Commun 2009, 384:524-529. 10.1016/j.bbrc.2009.05.015, 2744197, 19427829.
20. Colton CA. Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 2009, 4:399-418. 10.1007/s11481-009-9164-4, 2773116, 19655259.
21. Leitner M, Menzies S, Lutz C. Working with ALS Mice: Guidelines for Preclinical Testing & Colony Management 2009, Bar Harbor, ME: Prize4Life and The Jackson Laboratory.
22. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. 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 1996, 224:855-862. 10.1006/bbrc.1996.1112, 8713135.
23. Herbert RP, Harris J, Chong KP, Chapman J, West AK, Chuah MI. Cytokines and olfactory bulb microglia in response to bacterial challenge in the compromised primary olfactory pathway. J Neuroinflammation 2012, 9:109. 10.1186/1742-2094-9-109, 3411416, 22642871.
24. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 1999, 19:3248-3257.
25. Ct K, Kinoshita Y, Beal MF, Donehower LA, Morrison RS. Absence of p53: no effect in a transgenic mouse model of familial amyotrophic lateral sclerosis. Exp Neurol 2000, 165:184-190. 10.1006/exnr.2000.7464, 10964497.
26. Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, Brown RH, Carroll MC. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci U S A 2008, 105:17913-17918. 10.1073/pnas.0804610105, 2581614, 18997009.
27. Gowing G, Philips T, Van Wijmeersch B, Audet JN, Dewil M, Van Den Bosch L, Billiau AD, Robberecht W, Julien JP. Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci 2008, 28:10234-10244. 10.1523/JNEUROSCI.3494-08.2008, 18842883.
28. Yang WW, Sidman RL, Taksir TV, Treleaven CM, Fidler JA, Cheng SH, Dodge JC, Shihabuddin LS. Relationship between neuropathology and disease progression in the SOD1(G93A) ALS mouse. Exp Neurol 2011, 227:287-295. 10.1016/j.expneurol.2010.11.019, 21145892.
29. Graber DJ, Hickey WF, Harris BT. Progressive changes in microglia and macrophages in spinal cord and peripheral nerve in the transgenic rat model of amyotrophic lateral sclerosis. J Neuroinflammation 2010, 7:8. 10.1186/1742-2094-7-8, 2825214, 20109233.
30. Sanagi T, Yuasa S, Nakamura Y, Suzuki E, Aoki M, Warita H, Itoyama Y, Uchino S, Kohsaka S, Ohsawa K. Appearance of phagocytic microglia adjacent to motoneurons in spinal cord tissue from a presymptomatic transgenic rat model of amyotrophic lateral sclerosis. J Neurosci Res 2010, 88:2736-2746.
31. Pan L, Yoshii Y, Otomo A, Ogawa H, Iwasaki Y, Shang HF, Hadano S. Different human copper-zinc superoxide dismutase mutants, SOD1G93A and SOD1H46R, exert distinct harmful effects on gross phenotype in mice. PLoS One 2012, 7:e33409. 10.1371/journal.pone.0033409, 3306410, 22438926.
32. Beers DR, Henkel JS, Zhao W, Wang J, Huang A, Wen S, Liao B, Appel SH. Endogenous regulatory T lymphocytes ameliorate amyotrophic lateral sclerosis in mice and correlate with disease progression in patients with amyotrophic lateral sclerosis. Brain 2011, 134:1293-1314. 10.1093/brain/awr074, 3097891, 21596768.
33. Audet JN, Gowing G, Paradis R, Soucy G, Julien JP. Ablation of proliferating cells in the CNS exacerbates motor neuron disease caused by mutant superoxide dismutase. PLoS One 2012, 7:e34932. 10.1371/journal.pone.0034932, 3327706, 22523565.
34. Henkel JS, Beers DR, Zhao W, Appel SH. Microglia in ALS: the good, the bad, and the resting. J Neuroimmune Pharmacol 2009, 4:389-398. 10.1007/s11481-009-9171-5, 19731042.
35. Gowing G, Lalancette-Hebert M, Audet JN, Dequen F, Julien JP. Macrophage colony stimulating factor (M-CSF) exacerbates ALS disease in a mouse model through altered responses of microglia expressing mutant superoxide dismutase. Exp Neurol 2009, 220:267-275. 10.1016/j.expneurol.2009.08.021, 19733170.
36. Yoshihara T, Ishigaki S, Yamamoto M, Liang Y, Niwa J, Takeuchi H, Doyu M, Sobue G. Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 2002, 80:158-167. 10.1046/j.0022-3042.2001.00683.x, 11796754.
37. Tada S, Okuno T, Yasui T, Nakatsuji Y, Sugimoto T, Kikutani H, Sakoda S. Deleterious effects of lymphocytes at the early stage of neurodegeneration in an animal model of amyotrophic lateral sclerosis. J Neuroinflammation 2011, 8:19. 10.1186/1742-2094-8-19, 3048550, 21345177.
38. Munder M, Eichmann K, Modolell M. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J Immunol 1998, 160:5347-5354.
39. Chen K, Northington FJ, Martin LJ. Inducible nitric oxide synthase is present in motor neuron mitochondria and Schwann cells and contributes to disease mechanisms in ALS mice. Brain Struct Funct 2010, 214:219-234. 10.1007/s00429-009-0226-4, 3010349, 19888600.
40. Baek KJ, Thiel BA, Lucas S, Stuehr DJ. Macrophage nitric oxide synthase subunits. Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J Biol Chem 1993, 268:21120-21129.
41. Chang CI, Liao JC, Kuo L. Arginase modulates nitric oxide production in activated macrophages. Am J Physiol 1998, 274:H342-H348.
42. Gobert AP, Daulouede S, Lepoivre M, Boucher JL, Bouteille B, Buguet A, Cespuglio R, Veyret B, Vincendeau P. L-Arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect Immun 2000, 68:4653-4657. 10.1128/IAI.68.8.4653-4657.2000, 98402, 10899869.
43. Imagama T, Ogino K, Takemoto K, Kato Y, Kataoka H, Suzuki H, Ran Z, Setiawan H, Fujikura Y, Taguchi T. Regulation of nitric oxide generation by up-regulated arginase I in rat spinal cord injury. J Clin Biochem Nutr 2012, 51:68-75. 10.3164/jcbn.D-11-00011, 3391866, 22798716.
44. Miki K, Kumar A, Yang R, Killeen ME, Delude RL. Extracellular activation of arginase-1 decreases enterocyte inducible nitric oxide synthase activity during systemic inflammation. Am J Physiol Gastrointest Liver Physiol 2009, 297:G840-G848. 10.1152/ajpgi.90716.2008, 2763806, 19713467.
45. Estevez AG, Sahawneh MA, Lange PS, Bae N, Egea M, Ratan RR. Arginase 1 regulation of nitric oxide production is key to survival of trophic factor-deprived motor neurons. J Neurosci 2006, 26:8512-8516. 10.1523/JNEUROSCI.0728-06.2006, 2570095, 16914676.
46. Ferri A, Nencini M, Casciati A, Cozzolino M, Angelini DF, Longone P, Spalloni A, Rotilio G, Carri MT. Cell death in amyotrophic lateral sclerosis: interplay between neuronal and glial cells. FASEB J 2004, 18:1261-1263.
47. Mir M, Asensio VJ, Tolosa L, Gou-Fabregas M, Soler RM, Llado J, Olmos G. Tumor necrosis factor alpha and interferon gamma cooperatively induce oxidative stress and motoneuron death in rat spinal cord embryonic explants. Neuroscience 2009, 162:959-971. 10.1016/j.neuroscience.2009.05.049, 19477238.
48. Clarkson AN, Liu H, Pearson L, Kapoor M, Harrison JC, Sammut IA, Jackson DM, Appleton I. Neuroprotective effects of spermine following hypoxic-ischemic-induced brain damage: a mechanistic study. FASEB J 2004, 18:1114-1116.
49. Dal Canto MC, Gurney ME. Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 1994, 145:1271-1279. 1887498, 7992831.
50. Feeney SJ, McKelvie PA, Austin L, Jean-Francois MJ, Kapsa R, Tombs SM, Byrne E. Presymptomatic motor neuron loss and reactive astrocytosis in the SOD1 mouse model of amyotrophic lateral sclerosis. Muscle Nerve 2001, 24:1510-1519. 10.1002/mus.1176, 11745954.
51. Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 2000, 20:2534-2542.