LPS and IL-1 differentially activate mouse and human astrocytes: Role of CD14

GLIA

Volumn 62, Issue 6, 2014, Pages 999-1013

  Tarassishin, Leonid ^a   Suh, Hyeon Sook ^a   Lee, Sunhee C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Brain; Cytokines; Evolution; Inflammation; Innate immunity; Poly IC; Species; TLR

Indexed keywords

BETA INTERFERON; CD14 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN MD 2; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CELL ACTIVATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INNATE IMMUNITY; MICROGLIAL CELL CULTURE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SPECIES DIFFERENCE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; DRUG EFFECTS; FETUS; PHYSIOLOGY; TOXICITY;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD14; ASTROCYTES; CELLS, CULTURED; FETUS; HUMANS; INTERLEUKIN-1; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; SPECIES SPECIFICITY;

EID: 84898051513     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22657     Document Type: Article

References (73)

1. Akira S, Takeda K, Kaisho T. 2001. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol 2:675-680.
2. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
3. Beschorner R, Nguyen TD, Gozalan F, Pedal I, Mattern R, Schluesener HJ, Meyermann R, Schwab JM. 2002a. CD14 expression by activated parenchymal microglia/macrophages and infiltrating monocytes following human traumatic brain injury. Acta Neuropathol 103:541-549.
4. Beschorner R, Schluesener HJ, Gozalan F, Meyermann R, Schwab JM. 2002b. Infiltrating CD14+ monocytes and expression of CD14 by activated parenchymal microglia/macrophages contribute to the pool of CD14+ cells in ischemic brain lesions. J Neuroimmunol 126:107-115.
5. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. 1990. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 27:229-237.
6. Brahmachari S, Fung YK, Pahan K. 2006. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 26:4930-4939.
7. Chung IY, Norris JG, Benveniste EN. 1991. Differential tumor necrosis factor alpha expression by astrocytes from experimental allergic encephalomyelitis-susceptible and -resistant rat strains. J Exp Med 173:801-811.
8. Cosenza MA, Zhao ML, Si Q, Lee SC. 2002. Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12:442-455.
9. Cosenza-Nashat MA, Bauman A, Zhao ML, Morgello S, Suh HS, Lee SC. 2011. Cannabinoid receptor expression in HIV encephalitis and HIV-associated neuropathologic comorbidities. Neuropathol Appl Neurobiol 37:464-483.
10. Cosenza-Nashat MA, Kim MO, Zhao ML, Suh HS, Lee SC. 2006. CD45 isoform expression in microglia and inflammatory cells in HIV-1 encephalitis. Brain Pathol 16:256-265.
11. Dinarello CA. 1998. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int Rev Immunol 16:457-499.
12. Dinarello CA. 2010. IL-1: Discoveries, controversies and future directions. Eur J Immunol 40:599-606.
13. Downer EJ, Clifford E, Gran B, Nel HJ, Fallon PG, Moynagh PN. 2011. Identification of the synthetic cannabinoid R(+)WIN55, 212-2 as a novel regulator of IFN regulatory factor 3 (IRF3) activation and IFNβ expression: Relevance to therapeutic effects in models of multiple sclerosis. J Biol Chem 286:10316-10328.
14. Du F, Qian ZM, Zhu L, Wu XM, Qian C, Chan R, Ke Y. 2010. Purity, cell viability, expression of GFAP and bystin in astrocytes cultured by different procedures. J Cell Biochem 109:30-37.
15. Fearns C, Kravchenko VV, Ulevitch RJ, Loskutoff DJ. 1995. Murine CD14 gene expression in vivo: Extramyeloid synthesis and regulation by lipopolysaccharide. J Exp Med 181:857-866.
16. Fearns C, Loskutoff DJ. 1997. Role of tumor necrosis factor alpha in induction of murine CD14 gene expression by lipopolysaccharide. Infect Immun 65:4822-4831.
17. Galea E, Reis DJ, Fox ES, Xu H, Feinstein DL. 1996. CD14 mediate endotoxin induction of nitric oxide synthase in cultured brain glial cells. J Neuroimmunol 64:19-28.
18. Giulian D, Baker TJ, Shih LC, Lachman LB. 1986. Interleukin 1 of the central nervous system is produced by ameboid microglia. J Exp Med 164:594-604.
19. Godowski PJ. 2005. A smooth operator for LPS responses. Nat Immunol 6:544-546.
20. Godoy B, Murgas P, Tichauer J, Von BR. 2012. Scavenger receptor class A ligands induce secretion of IL1beta and exert a modulatory effect on the inflammatory activation of astrocytes in culture. J Neuroimmunol 251:6-13.
21. Gorina R, Font-Nieves M, Marquez-Kisinousky L, Santalucia T, Planas AM. 2011. Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59:242-255.
22. Gottschall PE, Tatsuno I, Arimura A. 1994. Regulation of interleukin-6 (IL-6) secretion in primary cultured rat astrocytes: Synergism of interleukin-1 (IL-1) and pituitary adenylate cyclase activating polypeptide (PACAP). Brain Res 637:197-203.
23. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, Barber GN, Lin R, Hiscott J. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: Direct involvement in the regulation of interferon-stimulated genes. J Virol 76:5532-5539.
24. Griffin WS, Sheng JG, Roberts GW, Mrak RE. 1995. Interleukin-1 expression in different plaque types in Alzheimer's disease: Significance in plaque evolution. J Neuropathol Exp Neurol 54:276-281.
25. 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.
26. Hamby ME, Coppola G, Ao Y, Geschwind DH, Khakh BS, Sofroniew MV. 2012. Inflammatory mediators alter the astrocyte transcriptome and calcium signaling elicited by multiple G-protein-coupled receptors. J Neurosci 32:14489-14510.
27. Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M. 2013. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12:342-353.
28. Henn A, Lund S, Hedtjarn M, Schrattenholz A, Porzgen P, Leist M. 2009. The suitability of BV2 cells as alternative model system for primary microglia cultures or for animal experiments examining brain inflammation. ALTEX 26:83-94.
29. Hiscott J, Lin R, Nakhaei P, Paz S. 2006. MasterCARD: A priceless link to innate immunity. Trends Mol Med 12:53-56.
30. 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.
31. Hua LL, Kim MO, Brosnan CF, Lee SC. 2002. Modulation of astrocyte inducible nitric oxide synthase and cytokine expression by interferon beta is associated with induction and inhibition of interferon gamma-activated sequence binding activity. J Neurochem 83:1120-1128.
32. Huber M, Kalis C, Keck S, Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Beutler B, Galanos C, Freudenberg MA. 2006. R-form LPS, the master key to the activation ofTLR4/MD-2-positive cells. Eur J Immunol 36:701-711.
33. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Huber M, Kalis C, Keck S, Galanos C, Freudenberg M, Beutler B. 2005. CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6:565-570.
34. John GR, Lee SC, Brosnan CF. 2003. Cytokines: Powerful regulators of glial cell activation. Neuroscientist 9:10-22.
35. Kawai T, Takeuchi O, Fujita T, Inoue J, Muhlradt PF, Sato S, Hoshino K, Akira S. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167:5887-5894.
36. 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.
37. Krause D, Suh HS, Tarassishin L, Cui QL, Durafourt BA, Choi N, Bauman A, Cosenza-Nashat M, Antel JP, Zhao ML, Lee SC. 2011. The tryptophan metabolite 3-hydroxyanthranilic acid plays anti-inflammatory and neuroprotective roles during inflammation role of hemeoxygenase-1. Am J Pathol 179:1360-1372.
38. Kumamaru H, Saiwai H, Kobayakawa K, Kubota K, Rooijen NV, Inoue K, Iwamoto Y, Okada S. 2012. Liposomal clodronate selectively eliminates microglia from primary astrocyte cultures. J Neuroinflammation 9:116.
39. Lange SC, Bak LK, Waagepetersen HS, Schousboe A, Norenberg MD. 2012. Primary cultures of astrocytes: Their value in understanding astrocytes in health and disease. Neurochem Res 37:2569-2588.
40. Lee SC, Dickson DW, Liu W, Brosnan CF. 1993a. Induction of nitric oxide synthase activity in human astrocytes by IL-1β and IFNγ. J Neuroimmunol 46:19-24.
41. Lee SC, Liu W, Brosnan CF, Dickson DW. 1992. Characterization of human fetal dissociated CNS cultures with an emphasis on microglia. Lab Invest 67:465-475.
42. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW. 1993b. Cytokine production by human fetal microglia and astrocytes: Differential induction by LPS and IL-1β. J Immunol 150:2659-2667.
43. Lee SC, Liu W, Roth P, Dickson DW, Berman JW, Brosnan CF. 1993c. Macrophage colony-stimulating factor in human fetal astrocytes and microglia. Differential regulation by cytokines and lipopolysaccharide, and modulation of class II MHC on microglia. J Immunol 150:594-604.
44. 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 USA 86:6348-6352.
45. Liu J, Zhao M-L, Brosnan CF, Lee SC. 1996. Expression of type II nitric oxide synthase in primary human astrocytes and microglia: Role of IL-1β and IL-1 receptor antagonist. J Immunol 157:3569-3576.
46. Liu JS, Amaral TD, Brosnan CF, Lee SC. 1998. IFNs are critical regulators of IL-1 receptor antagonist and IL-1 expression in human microglia. J Immunol 161:1989-1996.
47. Liu JS, Zhao ML, Brosnan CF, Lee SC. 2001. Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am J Pathol 158:2057-2066.
48. Ma D, Jin S, Li E, Doi Y, Parajuli B, Noda M, Sonobe Y, Mizuno T, Suzumura A. 2013. The neurotoxic effect of astrocytes activated with toll-like receptor ligands. J Neuroimmunol 254:10-18.
49. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, Leung PY, Harrington CA, Stenzel-Poore MP. 2009. Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: A critical role for IRF3. J Neurosci 29:9839-9849.
50. Minguet S, Dopfer EP, Pollmer C, Freudenberg MA, Galanos C, Reth M, Huber M, Schamel WW. 2008. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk. Eur J Immunol 38:2475-2487.
51. Molle C, Goldman M, Goriely S. 2010. Critical role of the IFN-stimulated gene factor 3 complex in TLR-mediated IL-27p28 gene expression revealing a two-step activation process. J Immunol 184:1784-1792.
52. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104:1604-1609.
53. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M. 2009. Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276-3287.
54. Pang Y, Cai Z, Rhodes PG. 2001. Analysis of genes differentially expressed in astrocytes stimulated with lipopolysaccharide using cDNA arrays. Brain Res 914:15-22.
55. Pugin J, Ulevitch RJ, Tobias PS. 1993. A critical role for monocytes and CD14 in endotoxin-induced endothelial cell activation. J Exp Med 178:2193-2200.
56. Regen T, van RD, Scheffel J, Kastriti ME, Revelo NH, Prinz M, Bruck W, Hanisch UK. 2011. CD14 and TRIF govern distinct responsiveness and responses in mouse microglial TLR4 challenges by structural variants of LPS. Brain Behav Immun 25:957-970.
57. Saura J. 2007. Microglial cells in astroglial cultures: A cautionary note. J Neuroinflammation 4:26.
58. Steinman L. 2008a. A rush to judgment on Th17. J Exp Med 205:1517-1522.
59. Steinman L. 2008b. Nuanced roles of cytokines in three major human brain disorders. J Clin Invest 118:3557-3563.
60. Suh HS, Cosenza-Nashat M, Choi N, Zhao ML, Li JF, Pollard JW, Jirtle RL, Goldstein H, Lee SC. 2010. Insulin-like growth factor 2 receptor is an IFNγ-inducible microglial protein that facilitates intracellular HIV replication: Implications for HIV-induced neurocognitive disorders. Am J Pathol 177:2446-2458.
61. Summers L, Kangwantas K, Nguyen L, Kielty C, Pinteaux E. 2010. Adhesion to the extracellular matrix is required for interleukin-1 beta actions leading to reactive phenotype in rat astrocytes. Mol Cell Neurosci 44:272-281.
62. Sun J, Zheng JH, Zhao M, Lee S, Goldstein H. 2008. 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 82:5562-5572.
63. Tarassishin L, Bauman A, Suh HS, Lee SC. 2013. Anti-viral and anti-inflammatory mechanisms of the innate immune transcription factor interferon regulatory factor 3: Relevance to human CNS diseases. J Neuroimmune Pharmacol 8:132-144.
64. Tarassishin L, Lee SC. 2013. Interferon regulatory factor 3 alters glioma inflammatory and invasive properties. J Neurooncol 113:185-194.
65. Tarassishin L, Loudig O, Bauman A, Shafit-Zagardo B, Suh HS, Lee SC. 2011a. Interferon regulatory factor 3 inhibits astrocyte inflammatory gene expression through suppression of the proinflammatory miR-155 and miR-155*. Glia 59:1911-1922.
66. Tarassishin L, Suh HS, Lee SC. 2011b. Interferon regulatory factor 3 plays an anti-inflammatory role in microglia by activating the PI3K/Akt pathway. J Neuroinflammation 8:187.
67. Uliasz TF, Hamby ME, Jackman NA, Hewett JA, Hewett SJ 2012. Generation of primary astrocyte cultures devoid of contaminating microglia. Methods Mol Biol 814:61-79.
68. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431-1433.
69. Xia Y, Yamagata K, Krukoff TL. 2006. Differential expression of the CD14/TLR4 complex and inflammatory signaling molecules following i.c.v. administration of LPS. Brain Res 1095:85-95.
70. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA. 2012. Genomic analysis of reactive astrogliosis. J Neurosci 32:6391-6410.
71. Zhao ML, Kim MO, Morgello S, Lee SC. 2001. Expression of inducible nitric oxide synthase, interleukin-1 and caspase-1 in HIV-1 encephalitis. J Neuroimmunol 115:182-191.
72. Zhao ML, Liu JS, He D, Dickson DW, Lee SC. 1998. Inducible nitric oxide synthase expression is selectively induced in astrocytes isolated from adult human brain. Brain Res 813:402-405.
73. Ziegler-Heitbrock HW, Ulevitch RJ. 1993. CD14: Cell surface receptor and differentiation marker. Immunol Today 14:121-125.