Macrophage-mediated inflammation and glial response in the skeletal muscle of a rat model of familial amyotrophic lateral sclerosis (ALS)

Experimental Neurology

Volumn 277, Issue , 2016, Pages 275-282

  Van Dyke, Jonathan M ^a   Smit Oistad, Ivy M ^a   Macrander, Corey ^a   Krakora, Dan ^a   Meyer, Michael G ^a   Suzuki, Masatoshi ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Amyotrophic lateral sclerosis (ALS); Glial activation; Inflammation; Skeletal muscle; SOD1G93A rats

Indexed keywords

CHOLINERGIC RECEPTOR; GFRA1 PROTEIN, RAT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; INTERLEUKIN 1BETA; LEUKOCYTE ANTIGEN; NERVE PROTEIN; PROTEIN S100B; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENETICS; GLIA; INFLAMMATION; MACROPHAGE; METABOLISM; NEUROMUSCULAR JUNCTION; PATHOLOGY; PHYSIOLOGY; RAT; SCHWANN CELL; SKELETAL MUSCLE; TRANSGENIC RAT;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIGENS, CD; DISEASE MODELS, ANIMAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; NEUROGLIA; NEUROMUSCULAR JUNCTION; RATS; RATS, TRANSGENIC; RECEPTORS, CHOLINERGIC; S100 CALCIUM BINDING PROTEIN BETA SUBUNIT; SCHWANN CELLS; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84955454731     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.01.008     Document Type: Article

References (54)

1. Ajroud-Driss S., Siddique T. Sporadic and hereditary amyotrophic lateral sclerosis (ALS). Biochim. Biophys. Acta 2015, 1852:679-684.
2. Astrow S.H., Son Y.J., Thompson W.J. Differential neural regulation of a neuromuscular junction-associated antigen in muscle fibers and Schwann cells. J. Neurobiol. 1994, 25:937-952.
3. Azzouz M., Ralph G.S., Storkebaum E., Walmsley L.E., Mitrophanous K.A., Kingsman S.M., Carmeliet P., Mazarakis N.D. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 2004, 429:413-417.
4. Barber S.C., Shaw P.J. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 2010, 48:629-641.
5. Beers D.R., Zhao W., Liao B., Kano O., Wang J., Huang A., Appel S.H., Henkel J.S. Neuroinflammation modulates distinct regional and temporal clinical responses in ALS mice. Brain Behav. Immun. 2011, 25:1025-1035.
6. Blokhuis A.M., Groen E.J., Koppers M., van den Berg L.H., Pasterkamp R.J. Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 2013, 125:777-794.
7. Bogaert E., d'Ydewalle C., Van Den Bosch L. Amyotrophic lateral sclerosis and excitotoxicity: from pathological mechanism to therapeutic target. CNS Neurol. Disord. Drug Targets 2010, 9:297-304.
8. Boillee S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
9. Borel J.F., Feurer C., Gubler H.U., Stahelin H. Biological effects of cyclosporin A: a new antilymphocytic agent. 1976. Agents Actions 1994, 43:179-186.
10. Cheng C., Zochodne D.W. In vivo proliferation, migration and phenotypic changes of Schwann cells in the presence of myelinated fibers. Neuroscience 2002, 115:321-329.
11. Chiu I.M., Phatnani H., Kuligowski M., Tapia J.C., Carrasco M.A., Zhang M., Maniatis T., Carroll M.C. Activation of innate and humoral immunity in the peripheral nervous system of ALS transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20960-20965.
12. De Miguel M.P., Fuentes-Julian S., Blazquez-Martinez A., Pascual C.Y., Aller M.A., Arias J., Arnalich-Montiel F. Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr. Mol. Med. 2012, 12:574-591.
13. Dibaj P., Steffens H., Zschuntzsch J., Nadrigny F., Schomburg E.D., Kirchhoff F., Neusch C. In vivo imaging reveals distinct inflammatory activity of CNS microglia versus PNS macrophages in a mouse model for ALS. PLoS One 2011, 6.
14. Duffy L.M., Chapman A.L., Shaw P.J., Grierson A.J. Review: the role of mitochondria in the pathogenesis of amyotrophic lateral sclerosis. Neuropathol. Appl. Neurobiol. 2011, 37:336-352.
15. Dupuis L., Loeffler J.P. Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models. Curr. Opin. Pharmacol. 2009, 9:341-346.
16. Evans M.C., Couch Y., Sibson N., Turner M.R. Inflammation and neurovascular changes in amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 2013, 53:34-41.
17. Feng Z., Ko C.P. The role of glial cells in the formation and maintenance of the neuromuscular junction. Ann. N. Y. Acad. Sci. 2008, 1132:19-28.
18. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glass J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 2004, 185:232-240.
19. Graber D.J., Hickey W.F., Harris B.T. 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.
20. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
21. Hall E.D., Oostveen J.A., Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 1998, 23:249-256.
22. Hayes-Punzo A., Mulcrone P., Meyer M., McHugh J., Svendsen C.N., Suzuki M. Gonadectomy and dehydroepiandrosterone (DHEA) do not modulate disease progression in the G93A mutant SOD1 rat model of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2012, 13:311-314.
23. Hegedus J., Putman C.T., Tyreman N., Gordon T. Preferential motor unit loss in the SOD1 G93A transgenic mouse model of amyotrophic lateral sclerosis. J. Physiol. 2008, 586:3337-3351.
24. Henderson C.E., Phillips H.S., Pollock R.A., Davies A.M., Lemeulle C., Armanini M., Simmons L., Moffet B., Vandlen R.A., Simpson L.C. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 1994, 266:1062-1064.
25. Holness C.L., Simmons D.L. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 1993, 81:1607-1613.
26. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1604-1609.
27. Kang H., Tian L., Son Y.J., Zuo Y., Procaccino D., Love F., Hayworth C., Trachtenberg J., Mikesh M., Sutton L., Ponomareva O., Mignone J., Enikolopov G., Rimer M., Thompson W. Regulation of the intermediate filament protein nestin at rodent neuromuscular junctions by innervation and activity. J. Neurosci. 2007, 27:5948-5957.
28. Kang H., Tian L., Mikesh M., Lichtman J.W., Thompson W.J. Terminal Schwann cells participate in neuromuscular synapse remodeling during reinnervation following nerve injury. J. Neurosci. 2014, 34:6323-6333.
29. Kaspar B.K., Llado J., Sherkat N., Rothstein J.D., Gage F.H. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 2003, 301:839-842.
30. Keller A.F., Gravel M., Kriz J. Live imaging of amyotrophic lateral sclerosis pathogenesis: disease onset is characterized by marked induction of GFAP in Schwann cells. Glia 2009, 57:1130-1142.
31. Krakora D., Macrander C., Suzuki M. Neuromuscular junction protection for the potential treatment of amyotrophic lateral sclerosis. Neurol. Res. Int. 2012, 2012:379657.
32. Krakora D., Mulcrone P., Meyer M., Lewis C., Bernau K., Gowing G., Zimprich C., Aebischer P., Svendsen C.N., Suzuki M. Synergistic effects of GDNF and VEGF on lifespan and disease progression in a familial ALS rat model. Mol. Ther. 2013, 21:1602-1610.
33. Liu J.X., Brannstrom T., Andersen P.M., Pedrosa-Domellof F. Distinct changes in synaptic protein composition at neuromuscular junctions of extraocular muscles versus limb muscles of ALS donors. PLoS One 2013, 8.
34. Meissner F., Molawi K., Zychlinsky A. Mutant superoxide dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:13046-13050.
35. Mitchell R.M., Freeman W.M., Randazzo W.T., Stephens H.E., Beard J.L., Simmons Z., Connor J.R. A CSF biomarker panel for identification of patients with amyotrophic lateral sclerosis. Neurology 2009, 72:14-19.
36. Mohajeri M.H., Figlewicz D.A., Bohn M.C. Intramuscular grafts of myoblasts genetically modified to secrete glial cell line-derived neurotrophic factor prevent motoneuron loss and disease progression in a mouse model of familial amyotrophic lateral sclerosis. Hum. Gene Ther. 1999, 10:1853-1866.
37. Moloney E.B., de Winter F., Verhaagen J. ALS as a distal axonopathy: molecular mechanisms affecting neuromuscular junction stability in the presymptomatic stages of the disease. Front. Neurosci. 2014, 8:252.
38. Nagai M., Aoki M., Miyoshi I., Kato M., Pasinelli P., Kasai N., Brown R.H., Itoyama Y. Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci. 2001, 21:9246-9254.
39. Nikodemova M., Small A.L., Smith S.M., Mitchell G.S., Watters J.J. Spinal but not cortical microglia acquire an atypical phenotype with high VEGF, galectin-3 and osteopontin, and blunted inflammatory responses in ALS rats. Neurobiol. Dis. 2014, 69:43-53.
40. Notturno F., Capasso M., DeLauretis A., Carpo M., Uncini A. Glial fibrillary acidic protein as a marker of axonal damage in chronic neuropathies. Muscle Nerve 2009, 40:50-54.
41. Olmos G., Llado J. Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity. Mediators Inflamm. 2014, 2014:861231.
42. Peters O.M., Ghasemi M., Brown R.H. Emerging mechanisms of molecular pathology in ALS. J. Clin. Invest. 2015, 125:1767-1779.
43. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011, 10:253-263.
44. Philips T., Rothstein J.D. Rodent Models of Amyotrophic Lateral Sclerosis. Curr. Protoc. Pharmacol. 2015, 69:5.67.1-5.67.21.
45. Pun S., Santos A.F., Saxena S., Xu L., Caroni P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat. Neurosci. 2006, 9:408-419.
46. Radford R.A., Morsch M., Rayner S.L., Cole N.J., Pountney D.L., Chung R.S. The established and emerging roles of astrocytes and microglia in amyotrophic lateral sclerosis and frontotemporal dementia. Front. Cell. Neurosci. 2015, 9:414.
47. Robinson A.P., White T.M., Mason D.W. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 1986, 57:239-247.
48. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
49. Suzuki M., McHugh J., Tork C., Shelley B., Klein S.M., Aebischer P., Svendsen C.N. GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS One 2007, 2:e689.
50. Suzuki M., Tork C., Shelley B., McHugh J., Wallace K., Klein S.M., Lindstrom M.J., Svendsen C.N. Sexual dimorphism in disease onset and progression of a rat model of ALS. Amyotroph. Lateral Scler. 2007, 8:20-25.
51. Suzuki M., McHugh J., Tork C., Shelley B., Hayes A., Bellantuono I., Aebischer P., Svendsen C.N. Direct muscle delivery of GDNF with human mesenchymal stem cells improves motor neuron survival and function in a rat model of familial ALS. Mol. Ther. 2008, 16:2002-2010.
52. Tovar Y.R.L.B., Ramirez-Jarquin U.N., Lazo-Gomez R., Tapia R. Trophic factors as modulators of motor neuron physiology and survival: implications for ALS therapy. Front. Cell. Neurosci. 2014, 8:61.
53. Vercelli A., Mereuta O.M., Garbossa D., Muraca G., Mareschi K., Rustichelli D., Ferrero I., Mazzini L., Madon E., Fagioli F. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 2008, 31:395-405.
54. Yang Z., Wang K.K. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci. 2015.