CXCR7 antagonism prevents axonal injury during experimental autoimmune encephalomyelitis as revealed by in vivo axial diffusivity

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Cruz Orengo, Lillian ^a   Chen, Ying Jr ^a   Kim, Joong H ^a   Dorsey, Denise ^a   Song, Sheng Kwei ^a   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axon; Chemokine; DTI; EAE; Multiple sclerosis; T cell

Indexed keywords

CCX 771; CHEMOKINE RECEPTOR ANTAGONIST; GLUTATHIONE TRANSFERASE P1; MYELIN; MYELIN BASIC PROTEIN; NEUROFILAMENT H PROTEIN; NEUROFILAMENT PROTEIN; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR CXCR; CMKOR1 PROTEIN, MOUSE; NEUROPROTECTIVE AGENT;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; HISTOPATHOLOGY; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; INFLAMMATORY INFILTRATE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROGLIA; PARENCHYMA; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SPINAL CORD; TH1 CELL; TREATMENT DURATION; WHITE MATTER; ANIMAL; C57BL MOUSE; CONVALESCENCE; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NERVE FIBER; NEUTROPHIL CHEMOTAXIS; PATHOLOGY;

ANIMALS; AXONS; CHEMOTAXIS, LEUKOCYTE; DIFFUSION TENSOR IMAGING; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; RECEPTORS, CXCR; RECOVERY OF FUNCTION; SPINAL CORD;

EID: 82655186582     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-170     Document Type: Article

References (67)

1. Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci 2008, 31:247-69. 10.1146/annurev.neuro.30.051606.094313, 18558855.
2. Andrews H, White K, Thomson C, Edgar J, Bates D, Griffiths I, Turnbull D, Nichols P. Increased axonal mitochondrial activity as an adaptation to myelin deficiency in the Shiverer mouse. J Neurosci Res 2006, 83(8):1533-9. 10.1002/jnr.20842, 16555298.
3. Ciccarelli O, Toosy AT, De Stefano N, Wheeler-Kingshott CA, Miller DH, Thompson AJ. Assessing neuronal metabolism in vivo by modeling imaging measures. J Neurosci 2010, 30(45):15030-3. 10.1523/JNEUROSCI.3330-10.2010, 3044872, 21068308.
4. Das Sarma J, Kenyon LC, Hingley ST, Shindler KS. Mechanisms of primary axonal damage in a viral model of multiple sclerosis. J Neurosci 2009, 29(33):10272-80. 10.1523/JNEUROSCI.1975-09.2009, 2747667, 19692601.
5. Forte M, Gold BG, Marracci G, Chaudhary P, Basso E, Johnsen D, Yu X, Fowlkes J, Rahder M, Stem K, Bernardi P, Bourdette D. Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Proc Natl Acad Sci USA 2007, 104(18):7558-63. 10.1073/pnas.0702228104, 1857227, 17463082.
6. Pohl HB, Porcheri C, Mueggler T, Bachmann LC, Martino G, Riethmacher D, Franklin RJ, Rudin M, Suter U. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J Neurosci 2011, 31(3):1069-80. 10.1523/JNEUROSCI.5035-10.2011, 21248132.
7. Su KG, Banker G, Bourdette D, Forte M. Axonal degeneration in multiple sclerosis: the mitochondrial hypothesis. Curr Neurol Neurosci Rep 2009, 9(5):411-7. 10.1007/s11910-009-0060-3, 2839873, 19664372.
8. Nikic I, Merkler D, Sorbara C, Brinkoetter M, Kreutzfeldt M, Bareyre FM, Bruck W, Bishop D, Misgeld T, Kerschensteiner M. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 2011, 17(4):495-9. 10.1038/nm.2324, 21441916.
9. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, Wilson D, Xu Q, Raz E. Control of Chemokine-Guided Cell Migration by Ligand Sequestration. Cell 2008, 132(3):463-473. 10.1016/j.cell.2007.12.034, 18267076.
10. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z, Penfold MET, Sunshine MJ, Littman DR, Kuo CJ, Wei K, McMaster BE, Wright K, Howard MC, Schall TJ. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. The Journal of Experimental Medicine 2006, 203(9):2201-2213. 10.1084/jem.20052144, 2118398, 16940167.
11. Naumann U, Cameroni E, Pruenster M, Mahabaleshwar H, Raz E, Zerwes H-G, Rot A, Thelen M. CXCR7 Functions as a Scavenger for CXCL12 and CXCL11. PLoS ONE 2010, 5(2):e9175. 10.1371/journal.pone.0009175, 2820091, 20161793.
12. Cruz-Orengo L, Holman DW, Dorsey D, Zhou L, Zhang P, Wright M, McCandless EE, Patel JR, Luker GD, Littman DR, Russell JH, Klein RS. CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J Exp Med 2011, 208(2):327-39. 10.1084/jem.20102010, 3039853, 21300915.
13. McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS. CXCL12 Limits Inflammation by Localizing Mononuclear Infiltrates to the Perivascular Space during Experimental Autoimmune Encephalomyelitis. J Immunol 2006, 177(11):8053-8064.
14. McCandless EE, Zhang B, Diamond MS, Klein RS. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proceedings of the National Academy of Sciences 2008, 105(32):11270-11275.
15. McCandless EE, Piccio L, Woerner BM, Schmidt RE, Rubin JB, Cross AH, Klein RS. Pathological Expression of CXCL12 at the Blood-Brain Barrier Correlates with Severity of Multiple Sclerosis. Am J Pathol 2008, 172(3):799-808. 10.2353/ajpath.2008.070918, 2258272, 18276777.
16. Budde MD, Kim JH, Liang H-F, Russell JH, Cross AH, Song S-K. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR in Biomedicine 2008, 21(6):589-597. 10.1002/nbm.1229, 2602834, 18041806.
17. Budde MD, Xie M, Cross AH, Song SK. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J Neurosci 2009, 29(9):2805-13. 10.1523/JNEUROSCI.4605-08.2009, 2673458, 19261876.
18. Fox RJ. Picturing Multiple Sclerosis: Conventional and Diffusion Tensor Imaging. Semin Neurol 2008, 28(04):453. 466, 10.1055/s-0028-1083689, 18843574.
19. Ge Y, Law M, Grossman RI. Applications of Diffusion Tensor MR Imaging in Multiple Sclerosis. Annals of the New York Academy of Sciences 2005, 1064(1):202-219. 10.1196/annals.1340.039, 16394158.
20. Kim JH, Budde MD, Liang H-F, Klein RS, Russell JH, Cross AH, Song S-K. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiology of Disease 2006, 21(3):626-632. 10.1016/j.nbd.2005.09.009, 16298135.
21. Kolappan M, Henderson A, Jenkins T, Wheeler-Kingshott C, Plant G, Thompson A, Miller D. Assessing structure and function of the afferent visual pathway in multiple sclerosis and associated optic neuritis. Journal of Neurology 2009, 256(3):305-319. 10.1007/s00415-009-0123-z, 19296047.
22. Sun S-W, Liang H-F, Schmidt RE, Cross AH, Song S-K. Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging. Neurobiology of Disease 2007, 28(1):30-38. 10.1016/j.nbd.2007.06.011, 2905808, 17683944.
23. Le Bihan D, Mangin J-F, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H. Diffusion tensor imaging: Concepts and applications. Journal of Magnetic Resonance Imaging 2001, 13(4):534-546. 10.1002/jmri.1076, 11276097.
24. Neil J, Miller J, Mukherjee P, Hüppi PS. Diffusion tensor imaging of normal and injured developing human brain - a technical review. NMR in Biomedicine 2002, 15(7-8):543-552. 10.1002/nbm.784, 12489100.
25. Song T, An J, Chen Q, Lee V, Laine A. Assessment of Adipose Tissue from Whole Body 3T MRI Scans. Conf Proc IEEE Eng Med Biol Soc 2005, 7:7012-5.
26. Stejskal EO, Tanner JE. Spin Diffusion Measurements: Spin Echoes in the Presence of a Time-Dependent Field Gradient. The Journal of Chemical Physics 1965, 42(1):288-292.
27. Koay CG, Chang L-C, Carew JD, Pierpaoli C, Basser PJ. A unifying theoretical and algorithmic framework for least squares methods of estimation in diffusion tensor imaging. Journal of Magnetic Resonance 2006, 182(1):115-125. 10.1016/j.jmr.2006.06.020, 16828568.
28. Abràmoff MD, Magalhães PJ, Ram SJ. Image Processing with ImageJ. Biophotonics International 2004, 11(7):36-42.
29. Rasband WS. ImageJ U.S. National Institutes of Health, Bethesda, Maryland, USA 1997, , http://imagej.nih.gov/ij
30. Ferreira T, Rasband W. The mageJ User Guide -- IJ 1.45 2010, , http://imagej.nih.gov/ij/docs/guide/
31. Herz J, Zipp F, Siffrin V. Neurodegeneration in autoimmune CNS inflammation. Exp Neurol 2010, 225(1):9-17. 10.1016/j.expneurol.2009.11.019, 19961850.
32. Siffrin V, Vogt J, Radbruch H, Nitsch R, Zipp F. Multiple sclerosis - candidate mechanisms underlying CNS atrophy. Trends Neurosci 2010, 33(4):202-10. 10.1016/j.tins.2010.01.002, 20153532.
33. Deumens R, Koopmans GC, Joosten EA. Regeneration of descending axon tracts after spinal cord injury. Prog Neurobiol 2005, 77(1-2):57-89. 10.1016/j.pneurobio.2005.10.004, 16271433.
34. Geddes JF, Hackshaw AK, Vowles GH, Nickols CD, Whitwell HL. Neuropathology of inflicted head injury in children. I. Patterns of brain damage. Brain 2001, 124(Pt 7):1290-8.
35. Geddes JF, Vowles GH, Hackshaw AK, Nickols CD, Scott IS, Whitwell HL. Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 2001, 124(Pt 7):1299-306.
36. Geddes JF, Whitwell HL. Head injury in routine and forensic pathological practice. Curr Top Pathol 2001, 95:101-24. 10.1007/978-3-642-59554-7_3, 11545051.
37. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331(6019):928-31. 10.1126/science.1201148, 21273450.
38. Kozlowski KF, Leddy JJ, Tomita M, Bergen A, Willer BS. Use of the ICECI and ICD-10 E-Coding structures to evaluate causes of head injury and concussion from sport and recreation participation in a school population. NeuroRehabilitation 2007, 22(3):191-8.
39. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996, 76(2):319-70.
40. Jackson SJ, Giovannoni G, Baker D. Fingolimod modulates microglial activation to augment markers of remyelination. Journal of neuroinflammation 2011, 8(1):76. 10.1186/1742-2094-8-76, 3152910, 21729281.
41. Mi S, Lee X, Hu Y, Ji B, Shao Z, Yang W, Huang G, Walus L, Rhodes K, Gong BJ, Miller RH, Pepinsky RB. Death receptor 6 negatively regulates oligodendrocyte survival, maturation and myelination. Nature medicine 2011, 17(7):816-21. 10.1038/nm.2373, 21725297.
42. Ludwin SK, Sternberger NH. An immunohistochemical study of myelin proteins during remyelination in the central nervous system. Acta neuropathologica 1984, 63(3):240-8. 10.1007/BF00685250, 6205535.
43. Sternberger NH, McFarlin DE, Traugott U, Raine CS. Myelin basic protein and myelin-associated glycoprotein in chronic, relapsing experimental allergic encephalomyelitis. Journal of Neuroimmunology 1984, 6(4):217-29. 10.1016/0165-5728(84)90010-9, 6203931.
44. Kumar S, Biancotti JC, Yamaguchi M, de Vellis J. Combination of growth factors enhances remyelination in a cuprizone-induced demyelination mouse model. Neurochemical research 2007, 32(4-5):783-97. 10.1007/s11064-006-9208-6, 17186374.
45. Bando Y, Ito S, Nagai Y, Terayama R, Kishibe M, Jiang YP, Mitrovic B, Takahashi T, Yoshida S. Implications of protease M/neurosin in myelination during experimental demyelination and remyelination. Neuroscience Letters 2006, 405(3):175-80. 10.1016/j.neulet.2006.06.030, 16890353.
46. Plant SR, Arnett HA, Ting JP. Astroglial-derived lymphotoxin-alpha exacerbates inflammation and demyelination, but not remyelination. Glia 2005, 49(1):1-14. 10.1002/glia.20089, 15382206.
47. Mason JL, Suzuki K, Chaplin DD, Matsushima GK. Interleukin-1beta promotes repair of the CNS. The Journal of neuroscience: the official journal of the Society for Neuroscience 2001, 21(18):7046-52.
48. Tanaka K, Nogawa S, Suzuki S, Dembo T, Kosakai A. Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in peri-infarct area in the rat brain. Brain research 2003, 989(2):172-9. 10.1016/S0006-8993(03)03317-1, 14556938.
49. Girolamo F, Ferrara G, Strippoli M, Rizzi M, Errede M, Trojano M, Perris R, Roncali L, Svelto M, Mennini T, Virgintino D. Cerebral cortex demyelination and oligodendrocyte precursor response to experimental autoimmune encephalomyelitis. Neurobiology of Disease 2011, 43(3):678-89. 10.1016/j.nbd.2011.05.021, 21679768.
50. Dandekar AA, Wu GF, Pewe L, Perlman S. Axonal Damage Is T Cell Mediated and Occurs Concomitantly with Demyelination in Mice Infected with a Neurotropic Coronavirus. J Virol 2001, 75(13):6115-6120. 10.1128/JVI.75.13.6115-6120.2001, 114327, 11390613.
51. Lee V, Carden M, Schlaepfer W, Trojanowski J. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. The Journal of Neuroscience 1987, 7(11):3474-3488.
52. Haines JD, Inglese M, Casaccia P. Axonal damage in multiple sclerosis. Mt Sinai J Med 2011, 78(2):231-43. 10.1002/msj.20246, 21425267.
53. O'Malley HA, Shreiner AB, Chen GH, Huffnagle GB, Isom LL. Loss of Na+ channel beta2 subunits is neuroprotective in a mouse model of multiple sclerosis. Mol Cell Neurosci 2009, 40(2):143-55. 10.1016/j.mcn.2008.10.001, 2670461, 19013247.
54. Jackson SJ, Lee J, Nikodemova M, Fabry Z, Duncan ID. Quantification of myelin and axon pathology during relapsing progressive experimental autoimmune encephalomyelitis in the Biozzi ABH mouse. J Neuropathol Exp Neurol 2009, 68(6):616-25. 10.1097/NEN.0b013e3181a41d23, 19458548.
55. Sobottka B, Harrer MD, Ziegler U, Fischer K, Wiendl H, Hunig T, Becher B, Goebels N. Collateral bystander damage by myelin-directed CD8+ T cells causes axonal loss. The American Journal of Pathology 2009, 175(3):1160-6. 10.2353/ajpath.2009.090340, 2731134, 19700745.
56. Shriver LP, Dittel BN. T-cell-mediated disruption of the neuronal microtubule network: correlation with early reversible axonal dysfunction in acute experimental autoimmune encephalomyelitis. Am J Pathol 2006, 169(3):999-1011. 10.2353/ajpath.2006.050791, 1698821, 16936273.
57. Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 2000, 123(Pt 6):1174-83.
58. Luo Y, Xue H, Pardo AC, Mattson MP, Rao MS, Maragakis NJ. Impaired SDF1/CXCR4 signaling in glial progenitors derived from SOD1(G93A) mice. J Neurosci Res 2007, 85(11):2422-32. 10.1002/jnr.21398, 17567884.
59. Patel JR, McCandless EE, Dorsey D, Klein RS. CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proceedings of the National Academy of Sciences 2010, 107(24):11062-11067.
60. Carbajal KS, Schaumburg C, Strieter R, Kane J, Lane TE. Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis. Proceedings of the National Academy of Sciences 2010, 107(24):11068-11073.
61. Gottle P, Kremer D, Jander S, Odemis V, Engele J, Hartung HP, Kury P. Activation of CXCR7 receptor promotes oligodendroglial cell maturation. Ann Neurol 2010, 68(6):915-24. 10.1002/ana.22214, 21154415.
62. Maysami S, Nguyen D, Zobel F, Pitz C, Heine S, Hopfner M, Stangel M. Modulation of rat oligodendrocyte precursor cells by the chemokine CXCL12. Neuroreport 2006, 17(11):1187-90. 10.1097/01.wnr.0000227985.92551.9a, 16837851.
63. Bockhorst KH, Narayana PA, Dulin J, Liu R, Rea HC, Hahn K, Wosik J, Perez-Polo JR. Normobaric hyperoximia increases hypoxia-induced cerebral injury: DTI study in rats. Journal of Neuroscience Research 2010, 88(5):1146-1156.
64. Chen Z, Ni P, Lin Y, Xiao H, Chen J, Qian G, Ye Y, Xu S, Wang J, Yang X. Visual pathway lesion and its development during hyperbaric oxygen treatment: A bold- fMRI and DTI study. Journal of Magnetic Resonance Imaging 2010, 31(5):1054-1060. 10.1002/jmri.22142, 20432338.
65. Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, Wong WM, Wang L, Su H, Chu T-H, Guo J, Zhang W, So K-F, Pepinsky B, Shao Z, Graff C, Garber E, Jung V, Wu EX, Wu W. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007, 13(10):1228-1233. 10.1038/nm1664, 17906634.
66. Duning T, Schiffbauer H, Warnecke T, Mohammadi S, Floel A, Kolpatzik K, Kugel H, Schneider A, Knecht S, Deppe M, Schäbitz WR. G-CSF Prevents the Progression of Structural Disintegration of White Matter Tracts in Amyotrophic Lateral Sclerosis: A Pilot Trial. PLoS ONE 2011, 6(3):e17770. 10.1371/journal.pone.0017770, 3056779, 21423758.
67. Yadav A, Chaudhary C, Keshavan AH, Agarwal A, Verma S, Prasad KN, Rathore RKS, Trivedi R, Gupta RK. Correlation of CSF Proinflammatory Cytokines with MRI in Tuberculous Meningitis. Academic Radiology 2010, 17(2):194-200. 10.1016/j.acra.2009.09.017, 20004599.