Spinal but not cortical microglia acquire an atypical phenotype with high VEGF, galectin-3 and osteopontin, and blunted inflammatory responses in ALS rats

Neurobiology of Disease

Volumn 69, Issue , 2014, Pages 43-53

  Nikodemova, Maria ^a   Small, Alissa L ^a   Smith, Stephanie M C ^a   Mitchell, Gordon S ^a   Watters, Jyoti J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

ALS; Gene expression; Lipopolysaccharide (LPS); M1 M2 phenotype; Microglia

Indexed keywords

ARGINASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; GALECTIN 3; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; OSTEOPONTIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ARGINASE; ARGINASE I, RAT; COPPER ZINC SUPEROXIDE DISMUTASE; SPP1 PROTEIN, RAT; SUPEROXIDE DISMUTASE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL COUNT; CONTROLLED STUDY; DRUG DESIGN; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; INFLAMMATION; INFLAMMATORY INFILTRATE; MACROPHAGE; MALE; MICROGLIA; MOTONEURON; MOUSE STRAIN; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; SPINAL CORD VENTRAL HORN; ANIMAL; DISEASE COURSE; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ARGINASE; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GALECTIN 3; HUMANS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MICROGLIA; OSTEOPONTIN; PHENOTYPE; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; SPINAL CORD; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84897401941     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.11.009     Document Type: Article

References (52)

1. Ahtoniemi T., Jaronen M., Keksa-Goldsteine V., Goldsteins G., Kiostinaho J. Mutant SOD1 from spinal cord of G93A rats is destabilized and binds to inner mitochondrial membrane. Neurobiol. Dis. 2008, 32:479-485.
2. Ajami B., Bennett J.L., Krieger C., Tetzlaff W., Rossi F.M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 2007, 10(12):1538-1543.
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(6990):413-417.
4. Beers D.R., Henkel J.S., Xiao Q., Zhao W., Wang J., Yen A.A., Siklos L., McKercher S.R., Appel S.H. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(43):16021-16026.
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(5):1025-1035.
6. Benatar M. Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol. Dis. 2007, 26(1):1-13.
7. Boillee S., Vande Velde C., Cleveland D.W. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52(1):39-59.
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(5778):1389-1392.
9. Chen H.Y., Liu F.T., Yang R.Y. Roles of galectin-3 in immune responses. Archivum immunologiae et therapiae experimentalis 2005, 53(6):497-504.
10. Cudkowicz M.E., Shefner J.M., Schoenfeld D.A., Zhang H., Andreasson K.I., Rothstein J.D., Drachman D.B. Trial of celecoxib in amyotrophic lateral sclerosis. Ann. Neurol. 2006, 60(1):22-31.
11. Dibaj P., Steffens H., Zschuntzsch J., Kirchhoff F., Schomburg E.D., Neusch C. In vivo imaging reveals rapid morphological reactions of astrocytes towards focal lesions in an ALS mouse model. Neurosci. Lett. 2011, 497(2):148-151.
12. Fendrick S.E., Xue Q.S., Streit W.J. Formation of multinucleated giant cells and microglial degeneration in rats expressing a mutant Cu/Zn superoxide dismutase gene. J. Neuroinflammation 2007, 4:9.
13. Gordon P.H., Moore D.H., Miller R.G., Florence J.M., Verheijde J.L., Doorish C., Hilton J.F., Spitalny G.M., MacArthur R.B., Mitsumoto H., Neville H.E., Boylan K., Mozaffar T., Belsh J.M., Ravits J., Bedlack R.S., Graves M.C., McCluskey L.F., Barohn R.J., Tandan R. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol. 2007, 6(12):1045-1053.
14. 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.
15. Gupta P.K., Prabhakar S., Sharma S., Anand A. Vascular endothelial growth factor-A (VEGF-A) and chemokine ligand-2 (CCL2) in amyotrophic lateral sclerosis (ALS) patients. J. Neuroinflammation 2011, 8:47.
16. Hashimoto M., Sun D., Rittling S.R., Denhardt D.T., Young W. Osteopontin-deficient mice exhibit less inflammation, greater tissue damage, and impaired locomotor recovery from spinal cord injury compared with wild-type controls. J. Neurosci. 2007, 27(13):3603-3611.
17. Hensley K., Fedynyshyn J., Ferrell S., Floyd R.A., Gordon B., Grammas P., Hamdheydari L., Mhatre M., Mou S., Pye Q.N., Stewart C., West M., West S., Williamson K.S. Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol. Dis. 2003, 14(1):74-80.
18. Ilieva H., Polymenidou M., Cleveland D.W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. The Journal of cell biology 2009, 187(6):761-772.
19. Kawamura M.F., Yamasaki R., Kawamura N., Tateishi T., Nagara Y., Matsushita T., Ohyagi Y., Kira J. Impaired recruitment of neuroprotective microglia and T cells during acute neuronal injury coincides with increased neuronal vulnerability in an amyotrophic lateral sclerosis model. Exp. Neurol. 2012, 234(2):437-445.
20. Keller A.F., Gravel M., Kriz J. Treatment with minocycline after disease onset alters astrocyte reactivity and increases microgliosis in SOD1 mutant mice. Exp. Neurol. 2011, 228(1):69-79.
21. Kriz J., Nguyen M.D., Julien J.P. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 2002, 10(3):268-278.
22. Lalancette-Hebert M., Swarup V., Beaulieu J.M., Bohacek I., Abdelhamid E., Weng Y.C., Sato S., Kriz J. Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J. Neurosci. 2012, 32(30):10383-10395.
23. Lee J.C., Seong J., Kim S.H., Lee S.J., Cho Y.J., An J., Nam D.H., Joo K.M., Cha C.I. Replacement of microglial cells using clodronate liposome and bone marrow transplantation in the central nervous system of SOD1(G93A) transgenic mice as an in vivo model of amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 2012, 418(2):359-365.
24. Lerman B.J., Hoffman E.P., Sutherland M.L., Bouri K., Hsu D.K., Liu F.T., Rothstein J.D., Knoblach S.M. Deletion of galectin-3 exacerbates microglial activation and accelerates disease progression and demise in a SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Brain and behavior 2012, 2(5):563-575.
25. Li B., Xu W., Luo C., Gozal D., Liu R. VEGF-induced activation of the PI3-K/Akt pathway reduces mutant SOD1-mediated motor neuron cell death. Brain Res. Mol. Brain Res. 2003, 111(1-2):155-164.
26. Liao B., Zhao W., Beers D.R., Henkel J.S., Appel S.H. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp. Neurol. 2012, 237(1):147-152.
27. Lund S.A., Giachelli C.M., Scatena M. The role of osteopontin in inflammatory processes. Journal of cell communication and signaling 2009, 3(3-4):311-322.
28. MacKinnon A.C., Farnworth S.L., Hodkinson P.S., Henderson N.C., Atkinson K.M., Leffler H., Nilsson U.J., Haslett C., Forbes S.J., Sethi T. Regulation of alternative macrophage activation by galectin-3. J. Immunol. 2008, 180(4):2650-2658.
29. Maetzler W., Berg D., Funke C., Sandmann F., Stunitz H., Maetzler C., Nitsch C. Progressive secondary neurodegeneration and microcalcification co-occur in osteopontin-deficient mice. Am. J. Pathol. 2010, 177(2):829-839.
30. Maetzler W., Berg D., Schalamberidze N., Melms A., Schott K., Mueller J.C., Liaw L., Gasser T., Nitsch C. Osteopontin is elevated in Parkinson's disease and its absence leads to reduced neurodegeneration in the MPTP model. Neurobiol. Dis. 2007, 25(3):473-482.
31. Matsumoto T., Imagama S., Hirano K., Ohgomori T., Natori T., Kobayashi K., Muramoto A., Ishiguro N., Kadomatsu K. CD44 expression in astrocytes and microglia is associated with ALS progression in a mouse model. Neurosci. Lett. 2012, 520(1):115-120.
32. Nichols N.L., Gowing G., Satriotomo I., Nashold L.J., Dale EA Suzuki M., Avalos P., Mulcrone P.L., McHugh J., Svendsen C.N., Mitchell G.S. Intermittent hypoxia and stem cell implants preserve breathing capacity in a rodent model of ALS. Am. J. Respir. Crit. Care Med. 2012, 187(5):535-542.
33. Nikodemova M., Watters J.J. Outbred ICR/CD1 mice display more severe neuroinflammation mediated by microglial TLR4/CD14 activation than inbred C57Bl/6 mice. Neuroscience 2011, 190:67-74.
34. Nikodemova M., Watters J.J. Efficient isolation of live microglia with preserved phenotypes from adult mouse brain. J. Neuroinflammation 2012, 9:147.
35. Pan L., Yoshii Y., Otomo A., Ogawa H., Iwasaki Y., Shang H.F., 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(3):e33409.
36. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011, 10(3):253-263.
37. 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., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362(6415):59-62.
38. 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(12):2736-2746.
39. Sano H., Hsu D.K., Apgar J.R., Yu L., Sharma B.B., Kuwabara I., Izui S., Liu F.T. Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Invest. 2003, 112(3):389-397.
40. Sargsyan S.A., Blackburn D.J., Barber S.C., Grosskreutz J., De Vos K.J., Monk P.N., Shaw P.J. A comparison of in vitro properties of resting SOD1 transgenic microglia reveals evidence of reduced neuroprotective function. BMC neuroscience 2011, 12:91.
41. Sargsyan S.A., Monk P.N., Shaw P.J. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia 2005, 51(4):241-253.
42. Solomon J.N., Lewis C.A., Ajami B., Corbel S.Y., Rossi F.M., Krieger C. Origin and distribution of bone marrow-derived cells in the central nervous system in a mouse model of amyotrophic lateral sclerosis. Glia 2006, 53(7):744-753.
43. 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(1):20-25.
44. Thomsen G.M., Gowing G., Avalos P., Latter J., Staggenborg K., ZedellaV Lin A., Svendsen C. A study of corticospinal motor neurons in rat model of amyotrophic lateralsclerosis. Neuroscience Meeting Planner 2012, (Program No.346.08.), Society for Neuroscience, New Orleans, LA, (Online).
45. Walther M., Kuklinski S., Pesheva P., Guntinas-Lichius O., Angelov D.N., Neiss W.F., Asou H., Probstmeier R. Galectin-3 is upregulated in microglial cells in response to ischemic brain lesions, but not to facial nerve axotomy. J. Neurosci. Res. 2000, 61(4):430-435.
46. Werdelin L., Boysen G., Jensen T.S., Mogensen P. Immunosuppressive treatment of patients with amyotrophic lateral sclerosis. Acta neurologica Scandinavica 1990, 82(2):132-134.
47. Weydt P., Yuen E.C., Ransom B.R., Moller T. Increased cytotoxic potential of microglia from ALS-transgenic mice. Glia 2004, 48(2):179-182.
48. Xie Y., Weydt P., Howland D.S., Kliot M., Moller T. Inflammatory mediators and growth factors in the spinal cord of G93A SOD1 rats. Neuroreport 2004, 15(16):2513-2516.
49. Zheng C., Nennesmo I., Fadeel B., Henter J.I. Vascular endothelial growth factor prolongs survival in a transgenic mouse model of ALS. Ann. Neurol. 2004, 56(4):564-567.
50. Zheng C., Skold M.K., Li J., Nennesmo I., Fadeel B., Henter J.I. VEGF reduces astrogliosis and preserves neuromuscular junctions in ALS transgenic mice. Biochem. Biophys. Res. Commun. 2007, 363(4):989-993.
51. Zhou J.Y., Afjehi-Sadat L., Asress S., Duong D.M., Cudkowicz M., Glass J.D., Peng J. Galectin-3 is a candidate biomarker for amyotrophic lateral sclerosis: discovery by a proteomics approach. Journal of proteome research 2010, 9(10):5133-5141.
52. Zhu S., Stavrovskaya I.G., Drozda M., Kim B.Y., Ona V., Li M., Sarang S., Liu A.S., Hartley D.M., Wu du C., Gullans S., Ferrante R.J., Przedborski S., Kristal B.S., Friedlander R.M. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002, 417(6884):74-78.