NG2 expressed by macrophages and oligodendrocyte precursor cells is dispensable in experimental autoimmune encephalomyelitis

Brain

Volumn 134, Issue 5, 2011, Pages 1315-1330

  Moransard, Martijn ^a   Dann, Angela ^b   Staszewski, Ori ^b   Fontana, Adriano ^a   Prinz, Marco ^b   Suter, Tobias ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

glial scar; macrophage; multiple sclerosis; oligodendrocyte progenitor; TGF

Indexed keywords

NG2 PROTEIN; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL SUBPOPULATION; CENTRAL NERVOUS SYSTEM; CHIMERA; CONTROLLED STUDY; DISEASE COURSE; FEMALE; KNOCKOUT MOUSE; LEUKOCYTE; MACROPHAGE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RECURRENT DISEASE; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS; ANTIGENS, CD; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; OLIGODENDROGLIA; PROTEOGLYCANS; RNA, MESSENGER; SPINAL CORD; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 79957511882     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr070     Document Type: Article

References (48)

1. Alonso G. NG2 proteoglycan-expressing cells of the adult rat brain: Possible involvement in the formation of glial scar astrocytes following stab wound. Glia 2005; 49: 318-38. (Pubitemid 40222911)
2. Asher RA, Morgenstern DA, Properzi F, Nishiyama A, Levine JM, Fawcett JW. Two separate metalloproteinase activities are responsible for the shedding and processing of the NG2 proteoglycan in vitro. Mol Cell Neurosci 2005; 29: 82-96. (Pubitemid 40603883)
3. Bocchini V, Mazzolla R, Barluzzi R, Blasi E, Sick P, Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J Neurosci Res 1992; 31: 616-21.
4. Bu J, Akhtar N, Nishiyama A. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 2001; 34: 296-310. (Pubitemid 32579452)
5. Chen ZJ, Ughrin Y, Levine JM. Inhibition of axon growth by oligodendrocyte precursor cells. Mol Cell Neurosci 2002; 20: 125-39. (Pubitemid 34634332)
6. Dawson MR, Levine JM, Reynolds R. NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors? J Neurosci Res 2000; 61: 471-9.
7. de Castro R Jr, Tajrishi R, Claros J, Stallcup WB. Differential responses of spinal axons to transection: Influence of the NG2 proteoglycan. Exp Neurol 2005; 192: 299-309. (Pubitemid 40341676)
8. Di Bello IC, Dawson MR, Levine JM, Reynolds R. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J Neurocytol 1999; 28: 365-81. (Pubitemid 30321016)
9. Dou CL, Levine JM. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 1994; 14: 7616-28. (Pubitemid 24379769)
10. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999; 49: 377-91. (Pubitemid 29385505)
11. Fiedorowicz A, Figiel I, Zaremba M, Dzwonek K, Oderfeld-Nowak B. The ameboid phenotype of NG2 ( + ) cells in the region of apoptotic dentate granule neurons in trimethyltin intoxicated mice shares antigen properties with microglia/macrophages. Glia 2008; 56: 209-22. (Pubitemid 350292313)
12. Foote AK, Blakemore WF. Inflammation stimulates remyelination in areas of chronic demyelination. Brain 2005; 128 (Pt 3): 528-39. (Pubitemid 40380188)
13. Gao Q, Lu J, Huo Y, Baby N, Ling EA, Dheen ST. NG2, a member of chondroitin sulfate proteoglycans family mediates the inflammatory response of activated microglia. Neuroscience 2010; 165: 386-94.
14. Grako KA, Ochiya T, Barritt D, Nishiyama A, Stallcup WB. PDGF (alpha)- receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J Cell Sci 1999; 112(Pt 6): 905-15. (Pubitemid 29179323)
15. Hampton DW, Rhodes KE, Zhao C, Franklin RJ, Fawcett JW. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 2004; 127: 813-20. (Pubitemid 39099547)
16. Hesske L, Vincenzetti C, Heikenwalder M, Prinz M, Reith W, Fontana A, et al. Induction of inhibitory CNS-derived and stimulatory blood-derived DCs suggests a dual role for GM-CSF in CNS inflammation. Brain 2010; 133: 1637-54.
17. Hossain-Ibrahim MK, Rezajooi K, Stallcup WB, Lieberman AR, Anderson PN. Analysis of axonal regeneration in the central and peripheral nervous systems of the NG2-deficient mouse. BMC Neurosci 2007; 8: 80.
18. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 2002; 22: 2792-803. (Pubitemid 37465828)
19. Kucharova K, Stallcup WB. The NG2 proteoglycan promotes oligodendrocyte progenitor proliferation and developmental myelination. Neuroscience 2010; 166: 185-94.
20. Laabs TL, Wang H, Katagiri Y, McCann T, Fawcett JW, Geller HM. Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J Neurosci 2007; 27: 14494-501.
21. Larsen PH, Wells JE, Stallcup WB, Opdenakker G, Yong VW. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J Neurosci 2003; 23: 11127-35. (Pubitemid 37548948)
22. Levine JM. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 1994; 14: 4716-30.
23. Matsumoto H, Kumon Y, Watanabe H, Ohnishi T, Shudou M, Chuai M, et al. Accumulation of macrophage-like cells expressing NG2 proteoglycan and Iba1 in ischemic core of rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 2008; 28: 149-63.
24. McKinnon RD, Piras G, Ida JA Jr, Dubois-Dalcq M. A role for TGF-beta in oligodendrocyte differentiation. J Cell Biol 1993; 121: 1397-407.
25. Mildner A, Mack M, Schmidt H, Bruck W, Djukic M, Zabel MD, et al. CCR2 + Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 2009; 132 (Pt 9): 2487-500.
26. Moon LD, Fawcett JW. Reduction in CNS scar formation without concomitant increase in axon regeneration following treatment of adult rat brain with a combination of antibodies to TGFbeta1 and beta2. Eur J Neurosci 2001; 14: 1667-77. (Pubitemid 35478035)
27. Moransard M, Sawitzky M, Fontana A, Suter T. Expression of the HGF receptor c-met by macrophages in experimental autoimmune encephalomyelitis. Glia 2010; 58: 559-71.
28. Morgenstern DA, Asher RA, Fawcett JW. Chondroitin sulphate proteoglycans in the CNS injury response. Prog Brain Res 2002; 137: 313-32. (Pubitemid 35460952)
29. Nishiyama A, Lin XH, Stallcup WB. Generation of truncated forms of the NG2 proteoglycan by cell surface proteolysis. Mol Biol Cell 1995; 6: 1819-32.
30. Nishiyama A, Yu M, Drazba JA, Tuohy VK. Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. J Neurosci Res 1997; 48: 299-312. (Pubitemid 27232704)
31. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nat Rev Neurosci 2009; 10: 9-22.
32. Paglinawan R, Malipiero U, Schlapbach R, Frei K, Reith W, Fontana A. TGFbeta directs gene expression of activated microglia to an anti-inflammatory phenotype strongly focusing on chemokine genes and cell migratory genes. Glia 2003; 44: 219-31. (Pubitemid 37484473)
33. Prinz M, Garbe F, Schmidt H, Mildner A, Gutcher I, Wolter K, et al. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest 2006; 116: 456-64. (Pubitemid 43228363)
34. Raasch J, Zeller N, van Loo G, Merkler D, Mildner A, Erny D, et al. IkB kinase 2 determines oligodendrocyte loss by non-cell-autonomous activation of NF-kB in the central nervous system. Brain 2011; 134: 1184-98.
35. Reynolds R, Dawson M, Papadopoulos D, Polito A, Di Bello IC, Pham- Dinh D, et al. The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and multiple sclerosis. J Neurocytol 2002; 31: 523-36. (Pubitemid 37378263)
36. Rezajooi K, Pavlides M, Winterbottom J, Stallcup WB, Hamlyn PJ, Lieberman AR, et al. NG2 proteoglycan expression in the peripheral nervous system: Upregulation following injury and comparison with CNS lesions. Mol Cell Neurosci 2004; 25: 572-84. (Pubitemid 38481468)
37. Rhodes KE, Raivich G, Fawcett JW. The injury response of oligodendrocyte precursor cells is induced by platelets, macrophages and inflammation-associated cytokines. Neuroscience 2006; 140: 87-100. (Pubitemid 43668445)
38. Smirkin A, Matsumoto H, Takahashi H, Inoue A, Tagawa M, Ohue S, et al. Iba1( + )/NG2( + ) macrophage-like cells expressing a variety of neuroprotective factors ameliorate ischemic damage of the brain. J Cereb Blood Flow Metab 2009; 30: 603-15.
39. Stallcup WB. The NG2 proteoglycan: Past insights and future prospects. J Neurocytol 2002; 31: 423-35. (Pubitemid 37378256)
40. Tan AM, Zhang W, Levine JM. NG2: A component of the glial scar that inhibits axon growth. J Anat 2005; 207: 717-25. (Pubitemid 43019731)
41. Tan AM, Colletti M, Rorai AT, Skene JH, Levine JM. Antibodies against the NG2 proteoglycan promote the regeneration of sensory axons within the dorsal columns of the spinal cord. J Neurosci 2006; 26: 4729-39. (Pubitemid 44315312)
42. Tang X, Davies JE, Davies SJ. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 2003; 71: 427-44. (Pubitemid 36159501)
43. Tigges U, Hyer EG, Scharf J, Stallcup WB. FGF2-dependent neovascularization of subcutaneous matrigel plugs is initiated by bone marrow-derived pericytes and macrophages. Development 2008; 135: 523-32.
44. Trotter J, Karram K, Nishiyama A. NG2 cells: Properties, progeny and origin. Brain Res Rev 2010; 63: 72-82.
45. Ughrin YM, Chen ZJ, Levine JM. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 2003; 23: 175-86. (Pubitemid 36050417)
46. Wu J, Yoo S, Wilcock D, Lytle JM, Leung PY, Colton CA, et al. Interaction of NG2( + ) glial progenitors and microglia/macrophages from the injured spinal cord. Glia 2010; 58: 410-22.
47. Yokoyama A, Sakamoto A, Kameda K, Imai Y, Tanaka J. NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia 2006; 53: 754-68.
48. Zhu L, Lu J, Tay SS, Jiang H, He BP. Induced NG2 expressing microglia in the facial motor nucleus after facial nerve axotomy. Neuroscience 2010; 166: 842-51.