Enhanced uptake of multiple sclerosis-derived myelin by THP-1 macrophages and primary human microglia

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Hendrickx, Debbie A E ^a   Schuurman, Karianne G ^a   van Draanen, Michael ^a   Hamann, Jörg ^b   Huitinga, Inge ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Demyelination; Microglia; Multiple sclerosis; Phagocytosis

Indexed keywords

MYELIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; INCUBATION TIME; LYSOSOME; MACROPHAGE; MALE; MICROGLIA; MULTIPLE SCLEROSIS; PHAGOCYTOSIS; RANK SUM TEST; VERY ELDERLY; WHITE MATTER; AGE; BRAIN; METABOLISM; MIDDLE AGED; MYELIN SHEATH; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; POSTMORTEM CHANGE; TRANSFORMED CELL LINE;

AGE FACTORS; AGED; AGED, 80 AND OVER; BRAIN; CELL LINE, TRANSFORMED; FEMALE; FLOW CYTOMETRY; HUMANS; MACROPHAGES; MALE; MICROGLIA; MIDDLE AGED; MULTIPLE SCLEROSIS; MYELIN SHEATH; PHAGOCYTOSIS; POSTMORTEM CHANGES; STATISTICS, NONPARAMETRIC; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84898778952     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-64     Document Type: Article

References (45)

1. Compston A, Coles A. Multiple sclerosis. Lancet 2008, 372:1502-1517. 10.1016/S0140-6736(08)61620-7, 18970977.
2. Sierra A, Abiega O, Shahraz A, Neumann H. Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 2013, 7:6. 3558702, 23386811.
3. Haider L, Fischer MT, Frischer JM, Bauer J, Hoftberger R, Botond G, Esterbauer H, Binder CJ, Witztum JL, Lassmann H. Oxidative damage in multiple sclerosis lesions. Brain 2011, 134:1914-1924. 10.1093/brain/awr128, 3122372, 21653539.
4. Wallberg M, Bergquist J, Achour A, Breij E, Harris RA. Malondialdehyde modification of myelin oligodendrocyte glycoprotein leads to increased immunogenicity and encephalitogenicity. Eur J Immunol 2007, 37:1986-1995. 10.1002/eji.200636912, 17523133.
5. Wheeler D, Bandaru VV, Calabresi PA, Nath A, Haughey NJ. A defect of sphingolipid metabolism modifies the properties of normal appearing white matter in multiple sclerosis. Brain 2008, 131:3092-3102. 10.1093/brain/awn190, 2577809, 18772223.
6. Chang MK, Bergmark C, Laurila A, Horkko S, Han KH, Friedman P, Dennis EA, Witztum JL. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA 1999, 96:6353-6358. 10.1073/pnas.96.11.6353, 26885, 10339591.
7. Horkko S, Bird DA, Miller E, Itabe H, Leitinger N, Subbanagounder G, Berliner JA, Friedman P, Dennis EA, Curtiss LK, Palinski W, Witztum JL. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest 1999, 103:117-128. 10.1172/JCI4533, 407862, 9884341.
8. da Costa CC, van der Laan LJ, Dijkstra CD, Bruck W. The role of the mouse macrophage scavenger receptor in myelin phagocytosis. Eur J Neurosci 1997, 9:2650-2657. 10.1111/j.1460-9568.1997.tb01694.x, 9517470.
9. Hendrickx DA, Koning N, Schuurman KG, van Strien ME, van Eden CG, Hamann J, Huitinga I. Selective upregulation of scavenger receptors in and around demyelinating areas in multiple sclerosis. J Neuropathol Exp Neurol 2013, 72:106-118. 10.1097/NEN.0b013e31827fd9e8, 23334594.
10. Mosley K, Cuzner ML. Receptor-mediated phagocytosis of myelin by macrophages and microglia: effect of opsonization and receptor blocking agents. Neurochem Res 1996, 21:481-487. 10.1007/BF02527713, 8734442.
11. Reichert F, Slobodov U, Makranz C, Rotshenker S. Modulation (inhibition and augmentation) of complement receptor-3-mediated myelin phagocytosis. Neurobiol Dis 2001, 8:504-512. 10.1006/nbdi.2001.0383, 11442357.
12. Reichert F, Rotshenker S. Complement-receptor-3 and scavenger-receptor-AI/II mediated myelin phagocytosis in microglia and macrophages. Neurobiol Dis 2003, 12:65-72. 10.1016/S0969-9961(02)00008-6, 12609490.
13. Fukumoto N, Shimaoka T, Fujimura H, Sakoda S, Tanaka M, Kita T, Yonehara S. Critical roles of CXC chemokine ligand 16/scavenger receptor that binds phosphatidylserine and oxidized lipoprotein in the pathogenesis of both acute and adoptive transfer experimental autoimmune encephalomyelitis. J Immunol 2004, 173:1620-1627.
14. Levy-Barazany H, Frenkel D. Expression of Scavenger receptor A on antigen presenting cells is important for CD4. J Neuroinflammation 2012, 9:120. 10.1186/1742-2094-9-120, 3466445, 22676725.
15. Podbielska M, Hogan EL. Molecular and immunogenic features of myelin lipids: incitants or modulators of multiple sclerosis?. Mult Scler 2009, 15:1011-1029. 10.1177/1352458509106708, 19692432.
16. Kim JK, Mastronardi FG, Wood DD, Lubman DM, Zand R, Moscarello MA. Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol Cell Proteom 2003, 2:453-462.
17. Moscarello MA, Lei H, Mastronardi FG, Winer S, Tsui H, Li Z, Ackerley C, Zhang L, Raijmakers R, Wood DD. Inhibition of peptidyl-arginine deiminases reverses protein-hypercitrullination and disease in mouse models of multiple sclerosis. Dis Model Mech 2013, 6:467-478. 10.1242/dmm.010520, 3597028, 23118341.
18. Bodil RE, Theander E, Londos E, Sandberg-Wollheim M, Larsson A, Sjoberg K, Stenberg P. Pathogenesis of autoimmune diseases: antibodies against transglutaminase, peptidylarginine deiminase and protein-bound citrulline in primary Sjogren's syndrome, multiple sclerosis and Alzheimer's disease. Scand J Immunol 2008, 67:626-631. 10.1111/j.1365-3083.2008.02115.x, 18476880.
19. Schwab C, McGeer PL. Complement activated C4d immunoreactive oligodendrocytes delineate small cortical plaques in multiple sclerosis. Exp Neurol 2002, 174:81-88. 10.1006/exnr.2001.7851, 11869036.
20. Ramaglia V, Hughes TR, Donev RM, Ruseva MM, Wu X, Huitinga I, Baas F, Neal JW, Morgan BP. C3-dependent mechanism of microglial priming relevant to multiple sclerosis. Proc Natl Acad Sci USA 2012, 109:965-970. 10.1073/pnas.1111924109, 3271873, 22219359.
21. van der Laan LJ, Ruuls SR, Weber KS, Lodder IJ, Dopp EA, Dijkstra CD. Macrophage phagocytosis of myelin in vitro determined by flow cytometry: phagocytosis is mediated by CR3 and induces production of tumor necrosis factor-alpha and nitric oxide. J Neuroimmunol 1996, 70:145-152. 10.1016/S0165-5728(96)00110-5, 8898723.
22. van der Goes A, Kortekaas M, Hoekstra K, Dijkstra CD, Amor S. The role of anti-myelin (auto)-antibodies in the phagocytosis of myelin by macrophages. J Neuroimmunol 1999, 101:61-67. 10.1016/S0165-5728(99)00133-2, 10580814.
23. Cwiklinska H, Mycko MP, Luvsannorov O, Walkowiak B, Brosnan CF, Raine CS, Selmaj KW. Heat shock protein 70 associations with myelin basic protein and proteolipid protein in multiple sclerosis brains. Int Immunol 2003, 15:241-249. 10.1093/intimm/dxg022, 12578854.
24. Kovalchin JT, Wang R, Wagh MS, Azoulay J, Sanders M, Chandawarkar RY. In vivo delivery of heat shock protein 70 accelerates wound healing by up-regulating macrophage-mediated phagocytosis. Wound Repair Regen 2006, 14:129-137. 10.1111/j.1743-6109.2006.00102.x, 16630101.
25. van Noort JM, van Sechel AC, Bajramovic JJ, El OM, Polman CH, Lassmann H, Ravid R. The small heat-shock protein alpha B-crystallin as candidate autoantigen in multiple sclerosis. Nature 1995, 375:798-801. 10.1038/375798a0, 7596414.
26. van Noort JM, Bsibsi M, Gerritsen WH, Van DV, Bajramovic JJ, Steinman L, Amor S. Alphab-crystallin is a target for adaptive immune responses and a trigger of innate responses in preactive multiple sclerosis lesions. J Neuropathol Exp Neurol 2010, 69:694-703. 10.1097/NEN.0b013e3181e4939c, 20535035.
27. Miksa M, Komura H, Wu R, Shah KG, Wang P. A novel method to determine the engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester. J Immunol Methods 2009, 342:71-77. 10.1016/j.jim.2008.11.019, 2675277, 19135446.
28. Bo L, Geurts JJ, Ravid R, Barkhof F. Magnetic resonance imaging as a tool to examine the neuropathology of multiple sclerosis. Neuropathol Appl Neurobiol 2004, 30:106-117. 10.1111/j.1365-2990.2003.00521.x, 15043708.
29. Melief J, Koning N, Schuurman KG, Van De Garde MD, Smolders J, Hoek RM, Van EM, Hamann J, Huitinga I. Phenotyping primary human microglia: tight regulation of LPS responsiveness. Glia 2012, 60(10):1506-1517. 10.1002/glia.22370, 22740309.
30. Melief J, Schuurman KG, Van De Garde MD, Smolders J, Van EM, Hamann J, Huitinga I. Microglia in normal appearing white matter of multiple sclerosis are alerted but immunosuppressed. Glia 2013, 61:1848-1861.
31. Norton WT, Poduslo SE. Myelination in rat brain: method of myelin isolation. J Neurochem 1973, 21:749-757. 10.1111/j.1471-4159.1973.tb07519.x, 4271082.
32. Raivich G, Banati R. Brain microglia and blood-derived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev 2004, 46:261-281. 10.1016/j.brainresrev.2004.06.006, 15571769.
33. Huitinga I, Van Rooijen N, De Groot CJ, Uitdehaag BM, Dijkstra CD. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med 1990, 172:1025-1033. 10.1084/jem.172.4.1025, 2188611, 2145387.
34. Huitinga I, Ruuls SR, Jung S, Van RN, Hartung HP, Dijkstra CD. Macrophages in T cell line-mediated, demyelinating, and chronic relapsing experimental autoimmune encephalomyelitis in Lewis rats. Clin Exp Immunol 1995, 100:344-351. 1534326, 7743675.
35. Durafourt BA, Moore CS, Zammit DA, Johnson TA, Zaguia F, Guiot MC, Bar-Or A, Antel JP. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 2012, 60:717-727. 10.1002/glia.22298, 22290798.
36. Sloane JA, Hinman JD, Lubonia M, Hollander W, Abraham CR. Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J Neurochem 2003, 84:157-168.
37. Streit WJ, Sammons NW, Kuhns AJ, Sparks DL. Dystrophic microglia in the aging human brain. Glia 2004, 45:208-212. 10.1002/glia.10319, 14730714.
38. Floden AM, Combs CK. Microglia demonstrate age-dependent interaction with amyloid-beta fibrils. J Alzheimers Dis 2011, 25:279-293. 3295838, 21403390.
39. Harry GJ. Microglia during development and aging. Pharmacol Ther 2013, 139(3):313-326. 10.1016/j.pharmthera.2013.04.013, 23644076.
40. Eggen BJ, Raj D, Hanisch UK, Boddeke HW. Microglial phenotype and adaptation. J Neuroimmune Pharmacol 2013, 8:807-823. 10.1007/s11481-013-9490-4, 23881706.
41. Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El KJ. The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 2013, 16:1896-1905. 10.1038/nn.3554, 24162652.
42. Confavreux C, Vukusic S. Age at disability milestones in multiple sclerosis. Brain 2006, 129:595-605. 10.1093/brain/awh714, 16415309.
43. Renoux C, Vukusic S, Confavreux C. The natural history of multiple sclerosis with childhood onset. Clin Neurol Neurosurg 2008, 110:897-904. 10.1016/j.clineuro.2008.04.009, 18534742.
44. Barnett MH, Prineas JW. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 2004, 55:458-468. 10.1002/ana.20016, 15048884.
45. van der Valk P, De Groot CJ. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol Appl Neurobiol 2000, 26:2-10. 10.1046/j.1365-2990.2000.00217.x, 10736062.