Innate immune activation in the pathogenesis of a murine model of globoid cell leukodystrophy

American Journal of Pathology

Volumn 184, Issue 2, 2014, Pages 382-396

  Snook, Eric R ^a   Fisher Perkins, Jeanne M ^a   Sansing, Hope A ^a   Lee, Kim M ^a   Alvarez, Xavier ^a   MacLean, Andrew G ^a   Peterson, Karin E ^b   Lackner, Andrew A ^a   Bunnell, Bruce A ^a,c  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b National Institute of Allergy and Infectious Diseases   (United States)

^c TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL DEATH; CONTROLLED STUDY; CORRELATION ANALYSIS; DEMYELINATION; DISEASE COURSE; EMBRYO; GLOBOID CELL LEUKODYSTROPHY; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VITRO STUDY; INNATE IMMUNITY; MACROPHAGE; MICROGLIA; MOUSE; NEUROPIL; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; TWITCHER MOUSE; UPREGULATION;

AGING; ANIMALS; ASTROCYTES; CALCIUM-BINDING PROTEINS; CELL AGGREGATION; CELL LINE; CELL SHAPE; CHEMOKINES; DISEASE MODELS, ANIMAL; FLUORESCENCE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNITY, INNATE; LEUKODYSTROPHY, GLOBOID CELL; MACROPHAGES; MICE; MICROFILAMENT PROTEINS; MICROGLIA; MYELIN SHEATH; OLIGODENDROGLIA; PSYCHOSINE; RHOMBENCEPHALON; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2; UP-REGULATION;

EID: 84892143840     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.10.011     Document Type: Article

References (67)

1. K. Suzuki, and Y. Suzuki Globoid cell leucodystrophy (Krabbe's disease): deficiency of galactocerebroside β-galactosidase Proc Natl Acad Sci U S A 66 1970 302 309
2. T. Kanazawa, S. Nakamura, M. Momoi, T. Yamaji, H. Takematsu, H. Yano, H. Sabe, A. Yamamoto, T. Kawasaki, and Y. Kozutsumi Inhibition of cytokinesis by a lipid metabolite, psychosine J Cell Biol 149 2000 943 950
3. D.-S. Im, C.E. Heise, T. Nguyen, B.F. O'Dowd, and K.R. Lynch Identification of a molecular target of psychosine and its role in globoid cell formation J Cell Biol 153 2001 429 434
4. A.S. Reddy, J.H. Kim, J.A. Hawkins-Salsbury, S.L. Macauley, E.T. Tracy, C.A. Vogler, X. Han, S.-K. Song, D.F. Wozniak, S.C. Fowler, R.S. Klein, and M.S. Sands Bone marrow transplantation augments the effect of brain- and spinal cord-directed adeno-associated virus 2/5 gene therapy by altering inflammation in the murine model of globoid-cell leukodystrophy J Neurosci 31 2011 9945 9957
5. S. Giri, M. Jatana, R. Rattan, J.S. Won, I. Singh, and A.K. Singh Galactosylsphingosine (psychosine)-induced expression of cytokine-mediated inducible nitric oxide synthases via AP-1 and C/EBP: implications for Krabbe disease FASEB J 16 2002 661 672
6. S. Giri, M. Khan, N. Nath, I. Singh, and A. Singh The role of AMPK in psychosine mediated effects on oligodendrocytes and astrocytes: implication for Krabbe disease J Neurochem 105 2008 1820 1833
7. J.T. Borda, X. Alvarez, M. Mohan, M.S. Ratterree, K. Phillippi- Falkenstein, A.A. Lackner, and B.A. Bunnell Clinical and immunopathologic alterations in rhesus macaques affected with globoid cell leukodystrophy Am J Pathol 172 2008 98 111
8. A. Bashir, and E. Haq Effect of psychosine on inducible nitric-oxide synthase expression under different culture conditions: implications for Krabbe disease Eur Rev Med Pharmacol Sci 15 2011 1282 1287
9. K. Suzuki Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status Neurochem Res 23 1998 251 259
10. M. Taniike, I. Mohri, N. Eguchi, D. Irikura, Y. Urade, S. Okada, and K. Suzuki An apoptotic depletion of oligodendrocytes in the twitcher, a murine model of globoid cell leukodystrophy J Neuropathol Exp Neurol 58 1999 644 653
11. M. Zaka, and D.A. Wenger Psychosine-induced apoptosis in a mouse oligodendrocyte progenitor cell line is mediated by caspase activation Neurosci Lett 358 2004 205 209
12. P. Formichi, E. Radi, C. Battisti, A. Pasqui, G. Pompella, P.E. Lazzerini, F. Laghi-Pasini, A. Leonini, A.D. Stefano, and A. Federico Psychosine-induced apoptosis and cytokine activation in immune peripheral cells of Krabbe patients J Cell Physiol 212 2007 737 743
13. E. Haq, S. Giri, I. Singh, and A.K. Singh Molecular mechanism of psychosine-induced cell death in human oligodendrocyte cell line J Neurochem 86 2003 1428 1440
14. M. Jatana, S. Giri, and A.K. Singh Apoptotic positive cells in Krabbe brain and induction of apoptosis in rat C6 glial cells by psychosine Neurosci Lett 330 2002 183 187
15. T. Yagi, E.J. McMahon, S. Takikita, I. Mohri, G.K. Matsushima, and K. Suzuki Fate of donor hematopoietic cells in demyelinating mutant mouse, twitcher, following transplantation of GFP+ bone marrow cells Neurobiol Dis 16 2004 98 109
16. Y.P. Wu, J. Matsuda, A. Kubota, and K. Suzuki Infiltration of hematogenous lineage cells into the demyelinating central nervous system of twitcher mice J Neuropathol Exp Neurol 59 2000 628 639
17. S.M. LeVine, and D.C. Brown IL-6 and TNF-α expression in brains of twitcher, quaking and normal mice J Neuroimmunol 73 1997 47 56
18. C.B. Ripoll, M. Flaat, J. Klopf-Eiermann, J.M. Fisher-Perkins, C.B. Trygg, B.A. Scruggs, M.L. McCants, H.P. Leonard, A.F. Lin, S. Zhang, M.E. Eagle, X. Alvarez, Y.T. Li, S.C. Li, J.M. Gimble, and B.A. Bunnell Mesenchymal lineage stem cells have pronounced anti-inflammatory effects in the twitcher mouse model of Krabbe's disease Stem Cells 29 2011 67 77
19. Y. Alvarez, I. Valera, C. Municio, E. Hugo, F. Padrón, L. Blanco, M. Rodriguez, N. Fernández, and M.S. Crespo Eicosanoids in the innate immune response: TLR and non-TLR routes Mediators Inflamm 2010 2010 doi: pii:201929
20. J.J. Bajramovic Regulation of innate immune responses in the central nervous system CNS Neurol Disord Drug Targets 10 2011 4 24
21. R. Bhat, and L. Steinman Innate and adaptive autoimmunity directed to the central nervous system Neuron 64 2009 123 132
22. B. Finsen, and T. Owens Innate immune responses in central nervous system inflammation FEBS Lett 585 2011 3806 3812
23. S. Akira, and K. Takeda Toll-like receptor signalling Nat Rev Immunol 4 2004 499 511
24. M.F. Farez, F.J. Quintana, R. Gandhi, G. Izquierdo, M. Lucas, and H.L. Weiner Toll-like receptor 2 and poly(ADP-ribose) polymerase 1 promote central nervous system neuroinflammation in progressive EAE Nat Immunol 10 2009 958 964
25. J.A. Sloane, C. Batt, Y. Ma, Z.M. Harris, B. Trapp, and T. Vartanian Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through TLR2 Proc Natl Acad Sci U S A 107 2010 11555 11560
26. M. Casula, A.M. Iyer, W.G.M. Spliet, J.J. Anink, K. Steentjes, M. Sta, D. Troost, and E. Aronica Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue Neuroscience 179 2011 233 243
27. K. Chen, P. Iribarren, J. Hu, J. Chen, W. Gong, E.H. Cho, S. Lockett, N.M. Dunlop, and J.M. Wang Activation of toll-like receptor 2 on microglia promotes cell uptake of Alzheimer disease-associated amyloid beta peptide J Biol Chem 281 2006 3651 3659
28. M. Jana, C.A. Palencia, and K. Pahan Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer's disease J Immunol 181 2008 7254 7262
29. S.M. LeVine, D.L. Wetzel, and A.J. Eilert Neuropathology of twitcher mice: examination by histochemistry, immunohistochemistry, lectin histochemistry and Fourier transform infrared microspectroscopy Int J Dev Neurosci 12 1994 275 288
30. K.A. Terrell, T.A. Rasmussen, C. Trygg, B.A. Bunnell, and W.R. Buck Molecular beacon genotyping for globoid cell leukodystrophy from hair roots in the twitcher mouse and rhesus macaque J Neurosci Methods 163 2007 60 66
31. B. Yang, C. Tian, Z.G. Zhang, F.C. Han, R. Azem, H. Yu, Y. Zheng, G. Jin, J.E. Arnold, and Q.Y. Zheng Sh3pxd2b mice are a model for craniofacial dysmorphology and otitis media PLoS One 6 2011 e22622
32. L.B. Davidson, R. Nessar, P. Kempaiah, D.J. Perkins, and T.F. Byrd Mycobacterium abscessus glycopeptidolipid prevents respiratory epithelial TLR2 signaling as measured by HβD2 gene expression and IL-8 release PLoS One 6 2011 e29148
33. J.T. Borda, X. Alvarez, M. Mohan, A. Hasegawa, A. Bernardino, S. Jean, P. Aye, and A.A. Lackner CD163, a marker of perivascular macrophages, is up-regulated by microglia in simian immunodeficiency virus encephalitis after haptoglobin-hemoglobin complex stimulation and is suggestive of breakdown of the blood-brain barrier Am J Pathol 172 2008 725 737
34. D.L. Farkas, C. Du, G.W. Fisher, C. Lau, W. Niu, E.S. Wachman, and R.M. Levenson Non-invasive image acquisition and advanced processing in optical bioimaging Comput Med Imaging Graph 22 1998 89 102
35. M. Meldgaard, C. Fenger, K.L. Lambertsen, M.D. Pedersen, R. Ladeby, and B. Finsen Validation of two reference genes for mRNA level studies of murine disease models in neurobiology J Neurosci Methods 156 2006 101 110
36. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method Methods 25 2001 402 408
37. S.D. Lewis, N.B. Butchi, M. Khaleduzzaman, T.W. Morgan, M. Du, S. Pourciau, D.G. Baker, S. Akira, and K.E. Peterson Toll-like receptor 7 is not necessary for retroviral neuropathogenesis but does contribute to virus-induced neuroinflammation J Neurovirol 14 2008 492 502
38. J. Sun, J.H. Zheng, M. Zhao, S. Lee, and H. Goldstein Increased in vivo activation of microglia and astrocytes in the brains of mice transgenic for an infectious R5 human immunodeficiency virus type 1 provirus and for CD4-specific expression of human cyclin T1 in response to stimulation by lipopolysaccharides J Virol 82 2008 5562 5572
39. I. Jou, J.H. Lee, S.Y. Park, H.J. Yoon, E.-H. Joe, and E.J. Park Gangliosides trigger inflammatory responses via TLR4 in brain glia Am J Pathol 168 2006 1619 1630
40. H.J. Yoon, S.B. Jeon, K. Suk, D.K. Choi, Y.J. Hong, and E.J. Park Contribution of TLR2 to the initiation of ganglioside-triggered inflammatory signaling Mol Cells 25 2008 99 104
41. L.-C. Hung, C.-C. Lin, S.-K. Hung, B.-C. Wu, M.-D. Jan, S.-H. Liou, and S.-L. Fu A synthetic analog of α-galactosylceramide induces macrophage activation via the TLR4-signaling pathways Biochem Pharmacol 73 2007 1957 1970
42. I. Tennant, J. Pound, L. Marr, J. Willems, S. Petrova, C. Ford, M. Paterson, A. Devitt, and C. Gregory Innate recognition of apoptotic cells: novel apoptotic cell-associated molecular patterns revealed by crossreactivity of anti-LPS antibodies Cell Death Differ 20 2013 698 708
43. D. Foell, H. Wittkowski, T. Vogl, and J. Roth S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules J Leukoc Biol 81 2007 28 37
44. G.M. Barton, and R. Medzhitov Toll-like receptors and their ligands Curr Top Microbiol Immunol 270 2002 81 92
45. M. Carty, and A.G. Bowie Evaluating the role of Toll-like receptors in diseases of the central nervous system Biochem Pharmacol 81 2011 825 837
46. C.S. Jack, N. Arbour, J. Manusow, V. Montgrain, M. Blain, E. McCrea, A. Shapiro, and J.P. Antel TLR signaling tailors innate immune responses in human microglia and astrocytes J Immunol 175 2005 4320 4330
47. S. Janssens, and R. Beyaert Role of toll-like receptors in pathogen recognition Clin Microbiol Rev 16 2003 637 646
48. T. Kaisho, and S. Akira Toll-like receptors and their signaling mechanism in innate immunity Acta Odontol Scand 59 2001 124 130
49. X. Du, B. Fleiss, H. Li, B. D'Angelo, Y. Sun, C. Zhu, H. Hagberg, O. Levy, C. Mallard, and X. Wang Systemic stimulation of TLR2 impairs neonatal mouse brain development PLoS One 6 2011 e19583
50. E. Okun, K.J. Griffioen, T.G. Son, J.H. Lee, N.J. Roberts, M.R. Mughal, E. Hutchison, A. Cheng, T.V. Arumugam, J.D. Lathia, H. van Praag, and M.P. Mattson TLR2 activation inhibits embryonic neural progenitor cell proliferation J Neurochem 114 2010 462 474
51. M. Bsibsi, A. Nomden, J.M. van Noort, and W. Baron Toll-like receptors 2 and 3 agonists differentially affect oligodendrocyte survival, differentiation, and myelin membrane formation J Neurosci Res 90 2012 388 398
52. R.N. Aravalli, S. Hu, T.N. Rowen, J.M. Palmquist, and J.R. Lokensgard Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus J Immunol 175 2005 4189 4193
53. Y.-C. Chiu, C.-Y. Lin, C.-P. Chen, K.-C. Huang, K.-M. Tong, C.-Y. Tzeng, T.-S. Lee, H.-C. Hsu, and C.-H. Tang Peptidoglycan enhances IL-6 production in human synovial fibroblasts via TLR2 receptor, focal adhesion kinase, Akt, and AP-1-dependent pathway J Immunol 183 2009 2785 2792
54. S. Miranda-Hernandez, N. Gerlach, J.M. Fletcher, E. Biros, M. Mack, H. Korner, and A.G. Baxter Role for MyD88, TLR2 and TLR9 but not TLR1, TLR4 or TLR6 in experimental autoimmune encephalomyelitis J Immunol 187 2011 791 804
55. M. Roy, J.F. Richard, A. Dumas, and L. Vallières CXCL1 can be regulated by IL-6 and promotes granulocyte adhesion to brain capillaries during bacterial toxin exposure and encephalomyelitis J Neuroinflammation 9 2012 18
56. A. Spooren, K. Kolmus, G. Laureys, R. Clinckers, J. De Keyser, G. Haegeman, and S. Gerlo Interleukin-6, a mental cytokine Brain Res Rev 67 2011 157 183
57. K.K. Bowen, R.J. Dempsey, and R. Vemuganti Adult interleukin-6 knockout mice show compromised neurogenesis Neuroreport 22 2011 126 130
58. T.V. Pedchenko, and S.M. LeVine IL-6 deficiency causes enhanced pathology in twitcher (globoid cell leukodystrophy) mice Exp Neurol 158 1999 459 468
59. I. Jakovcevski, R. Filipovic, Z. Mo, S. Rakic, and N. Zecevic Oligodendrocyte development and the onset of myelination in the human fetal brain Front Neuroanat 3 2009 5
60. K.M. Omari, G. John, R. Lango, and C.S. Raine Role for CXCR2 and CXCL1 on glia in multiple sclerosis Glia 53 2006 24 31
61. H.H. Tsai, E. Frost, V. To, S. Robinson, C. Ffrench-Constant, R. Geertman, R.M. Ransohoff, and R.H. Miller The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration Cell 110 2002 373 383
62. K.M. Omari, S.E. Lutz, L. Santambrogio, S.A. Lira, and C.S. Raine Neuroprotection and remyelination after autoimmune demyelination in mice that inducibly overexpress CXCL1 Am J Pathol 174 2009 164 176
63. L. Liu, M.K. Callahan, D. Huang, and R.M. Ransohoff Chemokine receptor CXCR3: an unexpected enigma P.S. Gerald, Current Topics in Developmental Biology 2005 Academic Press Salt Lake City, UT 149 181
64. K.M. Omari, G.R. John, S.C. Sealfon, and C.S. Raine CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis Brain 128 2005 1003 1015
65. T.L. Sørensen, C. Trebst, P. Kivisäkk, K.L. Klaege, A. Majmudar, R. Ravid, H. Lassmann, D.B. Olsen, R.M. Strieter, R.M. Ransohoff, and F. Sellebjerg Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system J Neuroimmunol 127 2002 59 68
66. G. Conductier, N. Blondeau, A. Guyon, J.-L. Nahon, and C. RovËre The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases J Neuroimmunol 224 2010 93 100
67. T.V. Pedchenko, I.G. Bronshteyn, and S.M. LeVine TNF-receptor 1 deficiency fails to alter the clinical and pathological course in mice with globoid cell leukodystrophy (twitcher mice) but affords protection following LPS challenge J Neuroimmunol 110 2000 186 194