Absence of CCL2 and CCL3 Ameliorates Central Nervous System Grey Matter But Not White Matter Demyelination in the Presence of an Intact Blood–Brain Barrier

Molecular Neurobiology

Volumn 53, Issue 3, 2016, Pages 1551-1564

  Janssen, Katharina ^a   Rickert, Mira ^a   Clarner, Tim ^a   Beyer, Cordian ^a   Kipp, Markus ^a,b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Chemokines; CNS; Cuprizone; Multiple sclerosis

Indexed keywords

CUPRIZONE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; CCL3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN LEVEL; CCL2 GENE; CCL3 GENE; CELL ACTIVATION; CELL COUNT; CELL LOSS; CHROMOSOME 11; CORPUS CALLOSUM; CUPRIZONE-INDUCED DEMYELINATION; DEMYELINATION; DENTATE GYRUS; DISEASE SEVERITY; DNA SEQUENCE; GENE; GENE DELETION; GENETIC VARIABILITY; GENOTYPE; GRAY MATTER; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOUSE; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PERITONEUM MACROPHAGE; PROTEIN FUNCTION; SOMATOSENSORY CORTEX; WHITE MATTER; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; DEFICIENCY; DEMYELINATING DISEASE; DISEASE MODEL; FEMALE; GENETICS; GLIOSIS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; VISCERA;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CCL3; CUPRIZONE; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; FEMALE; GLIOSIS; GRAY MATTER; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; VISCERA; WHITE MATTER;

EID: 84961174322     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9113-6     Document Type: Article

References (87)

1. van der Valk P, De Groot CJ (2000) Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol Appl Neurobiol 26:2–10
2. Lassmann H (2005) Multiple sclerosis pathology: evolution of pathogenetic concepts. Brain Pathol 15:217–222
3. Kabat EA, Wolf A, Bezer AE (1946) Rapid production of acute disseminated encephalomyelitis in rhesus monkeys by injection of brain tissue with adjuvants. Science 104:362–363. doi:10.1126/science.104.2703.362
4. Lorentzen JC et al (1995) Protracted, relapsing and demyelinating experimental autoimmune encephalomyelitis in DA rats immunized with syngeneic spinal cord and incomplete Freund's adjuvant. J Neuroimmunol 63:193–205
5. van der Star BJ, Vogel DY, Kipp M, Puentes F, Baker D, Amor S (2012) In vitro and in vivo models of multiple sclerosis. CNS Neurol Disord Drug Targets 11:570–588
6. Corthals AP (2011) Multiple sclerosis is not a disease of the immune system. Q Rev Biol 86:287–321
7. Nakahara J, Aiso S, Suzuki N (2010) Autoimmune versus oligodendrogliopathy: the pathogenesis of multiple sclerosis. Arch Immunol Ther Exp (Warsz) 58:325–333. doi:10.1007/s00005-010-0094-x
8. Nakahara J, Maeda M, Aiso S, Suzuki N (2012) Current concepts in multiple sclerosis: autoimmunity versus oligodendrogliopathy. Clin Rev Allergy Immunol 42:26–34. doi:10.1007/s12016-011-8287-6
9. Stys PK (2013) Pathoetiology of multiple sclerosis: are we barking up the wrong tree? F1000Prime Rep 5:20. doi:10.12703/P5-20
10. Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458–468. doi:10.1002/ana.20016
11. Gay FW, Drye TJ, Dick GW, Esiri MM (1997) The application of multifactorial cluster analysis in the staging of plaques in early multiple sclerosis. Identification and characterization of the primary demyelinating lesion. Brain J Neurol 120(Pt 8):1461–1483
12. Lassmann H (2003) Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci 206:187–191
13. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ (2007) Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? Brain 130:2800–2815. doi:10.1093/brain/awm236
14. Prineas JW et al (2001) Immunopathology of secondary-progressive multiple sclerosis. Ann Neurol 50:646–657
15. Sanders V, Conrad AJ, Tourtellotte WW (1993) On classification of post-mortem multiple sclerosis plaques for neuroscientists. J Neuroimmunol 46:207–216
16. van der Valk P, Amor S (2009) Preactive lesions in multiple sclerosis. Curr Opin Neurol 22:207–213. doi:10.1097/WCO.0b013e32832b4c76
17. Li H, Newcombe J, Groome NP, Cuzner ML (1993) Characterization and distribution of phagocytic macrophages in multiple sclerosis plaques. Neuropathol Appl Neurobiol 19:214–223
18. Kuhlmann T, Lucchinetti C, Zettl UK, Bitsch A, Lassmann H, Bruck W (1999) Bcl-2-expressing oligodendrocytes in multiple sclerosis lesions. Glia 28:34–39. doi:10.1002/(SICI)1098-1136(199910)28:1<34::AID-GLIA4>3.0.CO;2-8
19. Kipp M, Clarner T, Dang J, Copray S, Beyer C (2009) The cuprizone animal model: new insights into an old story. Acta Neuropathol 118:723–736. doi:10.1007/s00401-009-0591-3
20. Skripuletz T, Gudi V, Hackstette D, Stangel M (2011) De- and remyelination in the CNS white and grey matter induced by cuprizone: the old, the new, and the unexpected. Histol Histopathol 26:1585–1597
21. Buschmann JP, Berger K, Awad H, Clarner T, Beyer C, Kipp M (2012) Inflammatory response and chemokine expression in the white matter corpus callosum and gray matter cortex region during cuprizone-induced demyelination. J Mol Neurosci MN 48:66–76. doi:10.1007/s12031-012-9773-x
22. Gudi V et al (2009) Regional differences between grey and white matter in cuprizone induced demyelination. Brain Res 1283:127–138. doi:10.1016/j.brainres.2009.06.005
23. Kipp M et al (2011) The hippocampal fimbria of cuprizone-treated animals as a structure for studying neuroprotection in multiple sclerosis. Inflamm Res 60:723–726. doi:10.1007/s00011-011-0339-0
24. Baggiolini M (1998) Chemokines and leukocyte traffic. Nature 392:565–568. doi:10.1038/33340
25. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354:610–621. doi:10.1056/NEJMra052723
26. Luster AD (1998) Chemokines—chemotactic cytokines that mediate inflammation. N Engl J Med 338:436–445. doi:10.1056/NEJM199802123380706
27. Ubogu EE, Cossoy MB, Ransohoff RM (2006) The expression and function of chemokines involved in CNS inflammation. Trends Pharmacol Sci 27:48–55. doi:10.1016/j.tips.2005.11.002
28. Fernandez EJ, Lolis E (2002) Structure, function, and inhibition of chemokines. Ann Rev Pharmacol Toxicol 42:469–499. doi:10.1146/annurev.pharmtox.42.091901.11583842/1/469
29. Rossi D, Zlotnik A (2000) The biology of chemokines and their receptors. Annu Rev Immunol 18:217–242. doi:10.1146/annurev.immunol.18.1.217
30. Laing KJ, Secombes CJ (2004) Chemokines. Dev Comp Immunol 28:443–460. doi:10.1016/j.dci.2003.09.006
31. Murphy PM (2002) International Union of Pharmacology. XXX. Update on chemokine receptor nomenclature. Pharmacol Rev 54:227–229
32. Mackay CR (2001) Chemokines: immunology's high impact factors. Nat Immunol 2:95–101. doi:10.1038/84298
33. Andjelkovic AV, Song L, Dzenko KA, Cong H, Pachter JS (2002) Functional expression of CCR2 by human fetal astrocytes. J Neurosci Res 70:219–231. doi:10.1002/jnr.10372
34. Biber K, Dijkstra I, Trebst C, De Groot CJ, Ransohoff RM, Boddeke HW (2002) Functional expression of CXCR3 in cultured mouse and human astrocytes and microglia. Neuroscience 112:487–497
35. Grizenkova J, Akhtar S, Brandner S, Collinge J, Lloyd SE (2014) Microglial Cx3cr1 knockout reduces prion disease incubation time in mice. BMC Neurosci 15:44. doi:10.1186/1471-2202-15-44
36. Heesen M et al (1996) Mouse astrocytes respond to the chemokines MCP-1 and KC, but reverse transcriptase-polymerase chain reaction does not detect mRNA for the KC or new MCP-1 receptor. J Neurosci Res 45:382–391. doi:10.1002/(SICI)1097-4547(19960815)45:4<382::AID-JNR7>3.0.CO;2-5
37. McMillin M et al (2014) Neuronal CCL2 is upregulated during hepatic encephalopathy and contributes to microglia activation and neurological decline. J Neuroinflammation 11:121. doi:10.1186/1742-2094-11-121
38. Odemis V, Moepps B, Gierschik P, Engele J (2002) Interleukin-6 and cAMP induce stromal cell-derived factor-1 chemotaxis in astroglia by up-regulating CXCR4 cell surface expression. Implications for Brain Inflammation. J Biol Chem 277:39801–39808. doi:10.1074/jbc.M200472200
39. Tanabe S et al (1997) Functional expression of the CXC-chemokine receptor-4/fusin on mouse microglial cells and astrocytes. J Immunol 159:905–911
40. Glabinski AR, Ransohoff RM (1999) Chemokines and chemokine receptors in CNS pathology. J Neurovirol 5:3–12
41. McMahon EJ, Cook DN, Suzuki K, Matsushima GK (2001) Absence of macrophage-inflammatory protein-1alpha delays central nervous system demyelination in the presence of an intact blood-brain barrier. J Immunol 167:2964–2971
42. Henkel JS et al (2004) Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55:221–235. doi:10.1002/ana.10805
43. Nash KR et al (2013) Fractalkine overexpression suppresses tau pathology in a mouse model of tauopathy. Neurobiol Aging 34:1540–1548. doi:10.1016/j.neurobiolaging.2012.12.011
44. Asevedo E et al (2013) Impact of peripheral levels of chemokines, BDNF and oxidative markers on cognition in individuals with schizophrenia. J Psychiatr Res 47:1376–1382. doi:10.1016/j.jpsychires.2013.05.032
45. Krauthausen M, Saxe S, Zimmermann J, Emrich M, Heneka MT, Muller M (2014) CXCR3 modulates glial accumulation and activation in cuprizone-induced demyelination of the central nervous system. J Neuroinflammation 11:109. doi:10.1186/1742-2094-11-109
46. Patel JR, McCandless EE, Dorsey D, Klein RS (2010) CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination. Proc Natl Acad Sci U S A 107:11062–11067. doi:10.1073/pnas.1006301107
47. Patel JR et al (2012) Astrocyte TNFR2 is required for CXCL12-mediated regulation of oligodendrocyte progenitor proliferation and differentiation within the adult CNS. Acta Neuropathol 124:847–860. doi:10.1007/s00401-012-1034-0
48. Skripuletz T et al (2013) Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain J Neurol 136:147–167. doi:10.1093/brain/aws262
49. Acs P et al (2009) 17beta-estradiol and progesterone prevent cuprizone provoked demyelination of corpus callosum in male mice. Glia 57:807–814. doi:10.1002/glia.20806
50. Groebe A, Clarner T, Baumgartner W, Dang J, Beyer C, Kipp M (2009) Cuprizone treatment induces distinct demyelination, astrocytosis, and microglia cell invasion or proliferation in the mouse cerebellum. Cerebellum 8:163–174. doi:10.1007/s12311-009-0099-3
51. Kipp M et al (2008) Brain-region-specific astroglial responses in vitro after LPS exposure. J Mol Neurosci MN 35:235–243. doi:10.1007/s12031-008-9057-7
52. Clarner T, Parabucki A, Beyer C, Kipp M (2011) Corticosteroids impair remyelination in the corpus callosum of cuprizone-treated mice. J Neuroendocrinol 23:601–611. doi:10.1111/j.1365-2826.2011.02140.x
53. Kipp M et al (2011) Brain lipid binding protein (FABP7) as modulator of astrocyte function. Physiol Res 60(Suppl 1):S49–S60
54. Slowik A, Schmidt T, Beyer C, Amor S, Clarner T, Kipp M (2015) The sphingosine 1-phosphate receptor agonist FTY720 is neuroprotective after cuprizone-induced CNS demyelination. Br J Pharmacol 172:80–92. doi:10.1111/bph.12938
55. Braun A, Dang J, Johann S, Beyer C, Kipp M (2009) Selective regulation of growth factor expression in cultured cortical astrocytes by neuro-pathological toxins. Neurochem Int 55:610–618. doi:10.1016/j.neuint.2009.06.004
56. Kipp M et al (2011) BLBP-expression in astrocytes during experimental demyelination and in human multiple sclerosis lesions. Brain Behav Immun 25:1554–1568. doi:10.1016/j.bbi.2011.05.003
57. Cook DN et al (1995) Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science 269:1583–1585
58. Lu B et al (1998) Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med 187:601–608
59. Clarner T et al (2012) Myelin debris regulates inflammatory responses in an experimental demyelination animal model and multiple sclerosis lesions. Glia 60:1468–1480. doi:10.1002/glia.22367
60. Skripuletz T et al (2008) Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent. Am J Pathol 172:1053–1061. doi:10.2353/ajpath.2008.070850
61. Liu L et al (2010) CXCR2-positive neutrophils are essential for cuprizone-induced demyelination: relevance to multiple sclerosis. Nat Neurosci 13:319–326. doi:10.1038/nn.2491
62. Lassmann H, Bruck W, Lucchinetti CF (2007) The immunopathology of multiple sclerosis: an overview. Brain Pathol 17:210–218. doi:10.1111/j.1750-3639.2007.00064.x
63. Ludwin SK, Johnson ES (1981) Evidence for a "dying-back" gliopathy in demyelinating disease. Ann Neurol 9:301–305. doi:10.1002/ana.410090316
64. Krauspe BM et al (2014) Short-Term Cuprizone Feeding Verifies N-Acetylaspartate Quantification as a Marker of Neurodegeneration. J Mol Neurosci MN. doi:10.1007/s12031-014-0412-6
65. Hesse A et al (2010) In toxic demyelination oligodendroglial cell death occurs early and is FAS independent. Neurobiol Dis 37:362–369. doi:10.1016/j.nbd.2009.10.016
66. Remington LT, Babcock AA, Zehntner SP, Owens T (2007) Microglial recruitment, activation, and proliferation in response to primary demyelination. Am J Pathol 170:1713–1724. doi:10.2353/ajpath.2007.060783
67. Biancotti JC, Kumar S, de Vellis J (2008) Activation of inflammatory response by a combination of growth factors in cuprizone-induced demyelinated brain leads to myelin repair. Neurochem Res 33:2615–2628. doi:10.1007/s11064-008-9792-8
68. Yao Y, Tsirka SE (2014) Monocyte chemoattractant protein-1 and the blood-brain barrier. Cell Mol Life Sci CMLS 71:683–697. doi:10.1007/s00018-013-1459-1
69. Szczucinski A, Losy J (2007) Chemokines and chemokine receptors in multiple sclerosis. Potential targets for new therapies. Acta Neurol Scand 115:137–146. doi:10.1111/j.1600-0404.2006.00749.x
70. Charo IF (1999) CCR2: from cloning to the creation of knockout mice. Chem Immunol 72:30–41
71. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713–726
72. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ (2000) CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 192:899–905
73. −/−) mice: susceptibility in multiple strains. Am J Pathol 162:139–150. doi:10.1016/s0002-9440(10)63805-9
74. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD (2000) Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 192:1075–1080
75. Collins PD, Marleau S, Griffiths-Johnson DA, Jose PJ, Williams TJ (1995) Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med 182:1169–1174
76. Tran EH, Kuziel WA, Owens T (2000) Induction of experimental autoimmune encephalomyelitis in C57BL/6 mice deficient in either the chemokine macrophage inflammatory protein-1alpha or its CCR5 receptor. Eur J Immunol 30:1410–1415. doi:10.1002/(sici)1521-4141(200005)30:5<1410::aid-immu1410>3.0.co;2-l
77. Karpus WJ, Kennedy KJ (1997) MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J Leukoc Biol 62:681–687
78. Manczak M, Jiang S, Orzechowska B, Adamus G (2002) Crucial role of CCL3/MIP-1alpha in the recurrence of autoimmune anterior uveitis induced with myelin basic protein in Lewis rats. J Autoimmun 18:259–270
79. Cross AK, Woodroofe MN (1999) Chemokines induce migration and changes in actin polymerization in adult rat brain microglia and a human fetal microglial cell line in vitro. J Neurosci Res 55:17–23
80. Cudaback E, Yang Y, Montine TJ, Keene CD (2014) APOE genotype-dependent modulation of astrocyte chemokine CCL3 production. Glia. doi:10.1002/glia.22732
81. El-Hage N et al (2006) HIV-1 Tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53:132–146. doi:10.1002/glia.20262
82. Hinojosa AE, Garcia-Bueno B, Leza JC, Madrigal JL (2011) CCL2/MCP-1 modulation of microglial activation and proliferation. J Neuroinflammation 8:77. doi:10.1186/1742-2094-8-77
83. Wang HK et al (2008) Free radical production in CA1 neurons induces MIP-1alpha expression, microglia recruitment, and delayed neuronal death after transient forebrain ischemia. J Neurosci Off J Soc Neurosci 28:1721–1727. doi:10.1523/jneurosci.4973-07.2008
84. Yang G et al (2011) Neuronal MCP-1 mediates microglia recruitment and neurodegeneration induced by the mild impairment of oxidative metabolism. Brain Pathol 21:279–297. doi:10.1111/j.1750-3639.2010.00445.x
85. Han Y, Wang J, Zhou Z, Ransohoff RM (2000) TGFbeta1 selectively up-regulates CCR1 expression in primary murine astrocytes. Glia 30:1–10
86. Quinones MP et al (2008) Role of astrocytes and chemokine systems in acute TNFalpha induced demyelinating syndrome: CCR2-dependent signals promote astrocyte activation and survival via NF-kappaB and Akt. Mol Cell Neurosci 37:96–109. doi:10.1016/j.mcn.2007.08.017
87. Lee YK et al (2009) CCR5 deficiency induces astrocyte activation, Abeta deposit and impaired memory function. Neurobiol Learn Mem 92:356–363. doi:10.1016/j.nlm.2009.04.003