Microglial regulation of immunological and neuroprotective functions of astroglia

GLIA

Volumn 63, Issue 1, 2015, Pages 118-131

  Chen, Shih Heng ^a   Oyarzabal, Esteban A ^a   Sung, Yueh Feng ^a,b   Chu, Chun Hsien ^a   Wang, Qingshan ^a   Chen, Shiou Lan ^c   Lu, Ru Band ^d,e   Hong, Jau Shyong ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Astroglia; Glial cell line derived neurotrophic factor; Glial interaction; Microglia; Neuroinflammation; Neuroprotection

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; NITRITE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTOMA CELL LINE; BRAIN NERVE CELL; CELL INTERACTION; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOMODULATION; MACROGLIA; MICROGLIA; NEUROPROTECTION; NONHUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RAT; REGULATORY MECHANISM; RNA ANALYSIS; ANIMAL; ASTROCYTE; CELL CULTURE; FISCHER 344 RAT; GLIOSIS; IMMUNOLOGY; METABOLISM; NERVE CELL;

ANIMALS; ASTROCYTES; CELLS, CULTURED; FEMALE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIOSIS; LIPOPOLYSACCHARIDES; MICROGLIA; NEURONS; RATS, INBRED F344; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84911991140     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22738     Document Type: Article

References (77)

1. Alcendor DJ, Charest AM, Zhu WQ, Vigil HE, Knobel SM. 2012. Infection and upregulation of proinflammatory cytokines in human brain vascular pericytes by human cytomegalovirus. J Neuroinflammation 9:95.
2. Banks WA, Robinson SM. 2010. Minimal penetration of lipopolysaccharide across the murine blood-brain barrier. Brain Behav Immun 24:102-109.
3. Bell MD, Lopez-Gonzalez R, Lawson L, Hughes D, Fraser I, Gordon S, Perry VH. 1994. Upregulation of the macrophage scavenger receptor in response to different forms of injury in the CNS. J Neurocytol 23:605-613.
4. Beutner C, Linnartz-Gerlach B, Schmidt SV, Beyer M, Mallmann MR, Staratschek-Jox A, Schultze JL, Neumann H. 2013. Unique transcriptome signature of mouse microglia. Glia 61:1429-1442.
5. Biber K, Owens T, Boddeke E. 2014. What is microglia neurotoxicity (Not)? Glia 62:841-854.
6. Bowman CC, Rasley A, Tranguch SL, Marriott I. 2003. Cultured astrocytes express toll-like receptors for bacterial products. Glia 43:281-291.
7. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL. 2014. Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17:131-143.
8. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, Miller SD. 2005. Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49:360-374.
9. Cassina P, Peluffo H, Pehar M, Martinez-Palma L, Ressia A, Beckman JS, Estevez AG, Barbeito L. 2002. Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J Neurosci Res 67:21-29.
10. Chakravarty S, Herkenham M. 2005. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 25:1788-1796.
11. Chen SH, Oyarzabal EA, Hong JS. 2013. Preparation of rodent primary cultures for neuron-glia, mixed glia, enriched microglia, and reconstituted cultures with microglia. Methods Mol Biol 1041:231-240.
12. Chen SH, Wu HM, Ossola B, Schendzielorz N, Wilson BC, Chu CH, Chen SL, Wang Q, Zhang D, Qian L, Li X, Hong JS, Lu RB. 2012. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, protects dopaminergic neurons from neurotoxin-induced damage. Br J Pharmacol 165:494-505.
13. Chittajallu R, Aguirre A, Gallo V. 2004. NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol 561:109-122.
14. Chorna NE, Santiago-Perez LI, Erb L, Seye CI, Neary JT, Sun GY, Weisman GA, Gonzalez FA. 2004. P2Y receptors activate neuroprotective mechanisms in astrocytic cells. J Neurochem 91:119-132.
15. Chung IY, Benveniste EN. 1990. Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta. J Immunol 144:2999-3007.
16. Crocker SJ, Frausto RF, Whitton JL, Milner R. 2008. A novel method to establish microglia-free astrocyte cultures: Comparison of matrix metalloproteinase expression profiles in pure cultures of astrocytes and microglia. Glia 56:1187-1198.
17. Dong Y, Benveniste EN. 2001. Immune function of astrocytes. Glia 36:180-190.
18. Dringen R. 2000. Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649-671.
19. Esen N, Tanga FY, DeLeo JA, Kielian T. 2004. Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus. J Neurochem 88:746-758.
20. Falsig J, Porzgen P, Lotharius J, Leist M. 2004. Specific modulation of astrocyte inflammation by inhibition of mixed lineage kinases with CEP-1347. J Immunol 173:2762-2770.
21. Falsig J, Porzgen P, Lund S, Schrattenholz A, Leist M. 2006. The inflammatory transcriptome of reactive murine astrocytes and implications for their innate immune function. J Neurochem 96:893-907.
22. Farina C, Aloisi F, Meinl E. 2007. Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138-145.
23. Farina C, Krumbholz M, Giese T, Hartmann G, Aloisi F, Meinl E. 2005. Preferential expression and function of Toll-like receptor 3 in human astrocytes. J Neuroimmunol 159:12-19.
24. Fiedorowicz A, Figiel I, Zaremba M, Dzwonek K, Schliebs R, Oderfeld-Nowak B. 2008. Trimethyltin-evoked apoptosis of murine hippocampal granule neurons is accompanied by the expression of interleukin-1beta and interleukin-1 receptor antagonist in cells of ameboid phenotype, the majority of which are NG2-positive. Brain Res Bull 77:19-26.
25. Figiel I. 2008. Pro-inflammatory cytokine TNF-alpha as a neuroprotective agent in the brain. Acta neurobiologiae experimentalis 68:526-534.
26. Foo LC, Allen NJ, Bushong EA, Ventura PB, Chung WS, Zhou L, Cahoy JD, Daneman R, Zong H, Ellisman MH, Barres BA. 2011. Development of a method for the purification and culture of rodent astrocytes. Neuron 71:799-811.
27. Galea E, Reis DJ, Feinstein DL. 1994. Cloning and expression of inducible nitric oxide synthase from rat astrocytes. J Neurosci Res 37:406-414.
28. Gao Q, Lu J, Huo Y, Baby N, Ling EA, Dheen ST. 2010. NG2, a member of chondroitin sulfate proteoglycans family mediates the inflammatory response of activated microglia. Neuroscience 165:386-394.
29. Gasque P, Chan P, Mauger C, Schouft MT, Singhrao S, Dierich MP, Morgan BP, Fontaine M. 1996. Identification and characterization of complement C3 receptors on human astrocytes. J Immunol 156:2247-2255.
30. Gegg ME, Beltran B, Salas-Pino S, Bolanos JP, Clark JB, Moncada S, Heales SJ. 2003. Differential effect of nitric oxide on glutathione metabolism and mitochondrial function in astrocytes and neurones: Implications for neuroprotection/neurodegeneration? J Neurochem 86:228-237.
31. Giulian D, Baker TJ. 1986. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163-2178.
32. Giulian D, Li J, Li X, George J, Rutecki PA. 1994. The impact of microglia-derived cytokines upon gliosis in the CNS. Dev Neurosci 16:128-136.
33. Goss JR, O'Malley ME, Zou L, Styren SD, Kochanek PM, DeKosky ST. 1998. Astrocytes are the major source of nerve growth factor upregulation following traumatic brain injury in the rat. Exp Neurol 149:301-309.
34. Hamby ME, Uliasz TF, Hewett SJ, Hewett JA. 2006. Characterization of an improved procedure for the removal of microglia from confluent monolayers of primary astrocytes. J Neurosci Methods 150:128-137.
35. Hansson E, Muyderman H, Leonova J, Allansson L, Sinclair J, Blomstrand F, Thorlin T, Nilsson M, Ronnback L. 2000. Astroglia and glutamate in physiology and pathology: Aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication. Neurochem Int 37:317-329.
36. Hetier E, Ayala J, Bousseau A, Denefle P, Prochiantz A. 1990. Amoeboid microglial cells and not astrocytes synthesize TNF-alpha in Swiss Mouse brain cell cultures. Eur J Neurosci 2:762-768.
37. Holm TH, Draeby D, Owens T. 2012. Microglia are required for astroglial Toll-like receptor 4 response and for optimal TLR2 and TLR3 response. Glia 60:630-638.
38. Kajihara H, Tsutsumi E, Kinoshita A, Nakano J, Takagi K, Takeo S. 2001. Activated astrocytes with glycogen accumulation in ischemic penumbra during the early stage of brain infarction: Immunohistochemical and electron microscopic studies. Brain Res 909:92-101.
39. Kanai T, Uraushihara K, Totsuka T, Nemoto Y, Fujii R, Kawamura T, Makita S, Sawada D, Yagita H, Okumura K, Watanabe M. 2006. Ameliorating effect of saporin-conjugated anti-CD11b monoclonal antibody in a murine T-cell-mediated chronic colitis. J Gastroenterol Hepatol 21:1136-1142.
40. Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, Steinhauser C, Nave KA, Trotter J. 2008. NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46:743-757.
41. Kitada M, Rowitch DH. 2006. Transcription factor co-expression patterns indicate heterogeneity of oligodendroglial subpopulations in adult spinal cord. Glia 54:35-46.
42. Krasowska-Zoladek A, Banaszewska M, Kraszpulski M, Konat GW. 2007. Kinetics of inflammatory response of astrocytes induced by TLR 3 and TLR4 ligation. J Neurosci Res 85:205-212.
43. Kuno R, Yoshida Y, Nitta A, Nabeshima T, Wang J, Sonobe Y, Kawanokuchi J, Takeuchi H, Mizuno T, Suzumura A. 2006. The role of TNF-alpha and its receptors in the production of NGF and GDNF by astrocytes. Brain Res 1116:12-18.
44. Kutsch O, Oh J, Nath A, Benveniste EN. 2000. Induction of the chemokines interleukin-8 and IP-10 by human immunodeficiency virus type 1 tat in astrocytes. J Virol 74:9214-9221.
45. Laflamme N, Rivest S. 2001. Toll-like receptor 4: The missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J 15:155-163.
46. Lafortune L, Nalbantoglu J, Antel JP. 1996. Expression of tumor necrosis factor alpha (TNF alpha) and interleukin 6 (IL-6) mRNA in adult human astrocytes: comparison with adult microglia and fetal astrocytes. J Neuropathol Exp Neurol 55:515-521.
47. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T. 2002. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22:2478-2486.
48. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. 2003. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100:8514-8519.
49. Levine JM, Enquist LW, Card JP. 1998. Reactions of oligodendrocyte precursor cells to alpha herpesvirus infection of the central nervous system. Glia 23:316-328.
50. Levine JM, Reynolds R, Fawcett JW. 2001. The oligodendrocyte precursor cell in health and disease. Trends in neurosciences 24:39-47.
51. Lieberman AP, Pitha PM, Shin HS, Shin ML. 1989. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci U S A 86:6348-6352.
52. Lin LF, Doherty DH, Lile JD, Bektesh S, Collins F. 1993. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130-1132.
53. Liu B, Du L, Hong J-S. 2000. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther 293:607-617.
54. Liu Y, Qin L, Wilson BC, An L, Hong JS, Liu B. 2002. Inhibition by naloxone stereoisomers of beta-amyloid peptide (1-42)-induced superoxide production in microglia and degeneration of cortical and mesencephalic neurons. J Pharmacol Exp Ther 302:1212-1219.
55. Losciuto S, Dorban G, Gabel S, Gustin A, Hoenen C, Grandbarbe L, Heuschling P, Heurtaux T. 2012. An efficient method to limit microglia-dependent effects in astroglial cultures. J Neurosci Methods 207:59-71.
56. Mallon BS, Shick HE, Kidd GJ, Macklin WB. 2002. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22:876-885.
57. McCarthy KD, de Vellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
58. Melief J, Koning N, Schuurman KG, Van De Garde MD, Smolders J, Hoek RM, Van Eijk M, Hamann J, Huitinga I. 2012. Phenotyping primary human microglia: Tight regulation of LPS responsiveness. Glia 60:1506-1517.
59. Nakase T, Sohl G, Theis M, Willecke K, Naus CC. 2004. Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes. Am J Pathol 164:2067-2075.
60. O'Callaghan JP, Sriram K. 2005. Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Exp Opin Drug Saf 4:433-442.
61. Okun E, Griffioen KJ, Lathia JD, Tang SC, Mattson MP, Arumugam TV. 2009. Toll-like receptors in neurodegeneration. Brain Res Rev 59:278-292.
62. Park C, Lee S, Cho IH, Lee HK, Kim D, Choi SY, Oh SB, Park K, Kim JS, Lee SJ. 2006. TLR3-mediated signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 53:248-256.
63. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. 2012. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 109:E197-E205.
64. Remy S, Naveilhan P, Paille V, Brachet P, Neveu I. 2003. Lipopolysaccharide and TNFalpha regulate the expression of GDNF, neurturin and their receptors. Neuroreport 14:1529-1534.
65. Rocha SM, Cristovao AC, Campos FL, Fonseca CP, Baltazar G. 2012. Astrocyte-derived GDNF is a potent inhibitor of microglial activation. Neurobiol Dis 47:407-415.
66. Salimi K, Moser KV, Marksteiner J, Reindl M, Humpel C. 2003. GDNF and TGF-beta1 promote cell survival in serum-free cultures of primary rat microglia. Cell Tissue Res 312:135-139.
67. Saura J. 2007. Microglial cells in astroglial cultures: A cautionary note. J Neuroinflammation 4:26.
68. Schmid CD, Melchior B, Masek K, Puntambekar SS, Danielson PE, Lo DD, Sutcliffe JG, Carson MJ. 2009. Differential gene expression in LPS/IFNgamma activated microglia and macrophages: In vitro versus in vivo. J Neurochem 109 (Suppl 1):117-125.
69. Sola C, Casal C, Tusell JM, Serratosa J. 2002. Astrocytes enhance lipopolysaccharide-induced nitric oxide production by microglial cells. Eur J Neurosci 16:1275-1283.
70. Tabernero A, Orfao A, Medina JM. 1996. Astrocyte differentiation in primary culture followed by flow cytometry. Neurosci Res 24:131-138.
71. Tacconi MT. 1998. Neuronal death: Is there a role for astrocytes? Neurochem Res 23:759-765.
72. Vincent VA, Tilders FJ, Van Dam AM. 1997. Inhibition of endotoxin-induced nitric oxide synthase production in microglial cells by the presence of astroglial cells: a role for transforming growth factor beta. Glia 19:190-198.
73. von Bernhardi R, Eugenin J. 2004. Microglial reactivity to beta-amyloid is modulated by astrocytes and proinflammatory factors. Brain Res 1025:186-193.
74. Welser-Alves JV, Milner R. 2013. Microglia are the major source of TNF-alpha and TGF-beta1 in postnatal glial cultures; regulation by cytokines, lipopolysaccharide, and vitronectin. Neurochem Int 63:47-53.
75. Xing B, Xin T, Zhao L, Hunter RL, Chen Y, Bing G. 2010. Glial cell line-derived neurotrophic factor protects midbrain dopaminergic neurons against lipopolysaccharide neurotoxicity. J Neuroimmunol 225:43-51.
76. Zhang D, Hu X, Qian L, O'Callaghan JP, Hong JS. 2010. Astrogliosis in CNS pathologies: Is there a role for microglia? Mol Neurobiol 41:232-241.
77. Zhu L, Xiang P, Guo K, Wang A, Lu J, Tay SS, Jiang H, He BP. 2012. Microglia/monocytes with NG2 expression have no phagocytic function in the cortex after LPS focal injection into the rat brain. Glia 60:1417-1426.