Astrocytes produce interferon-alpha and CXCL10, but not IL-6 or CXCL8, in Aicardi-Goutières syndrome

GLIA

Volumn 56, Issue 5, 2008, Pages 568-578

  van Heteren, Jane T ^a,b   Rozenberg, Flore ^c   Aronica, Eleonora ^b   Troost, Dirk ^b   Lebon, Pierre ^c   Kuijpers, Taco W ^a  

^a EMMA CHILDREN S HOSPITAL   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

AGS; Chemokine; Cytokine; Virus

Indexed keywords

ALPHA INTERFERON; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GROWTH FACTOR; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; CXCL10 PROTEIN, HUMAN; IL8 PROTEIN, HUMAN;

ADOLESCENT; ADULT; AGED; AICARDI GOUTIERES SYNDROME; ANIMAL CELL; ARTICLE; ASTROCYTE; AUTOPSY; BRAIN CALCIFICATION; BRAIN TISSUE; CELL FUNCTION; CELL INFILTRATION; CELL TYPE; CENTRAL NERVOUS SYSTEM INFECTION; CHILD; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENCEPHALITIS; FEVER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFANT; INNATE IMMUNITY; LEUKOCYTE; LYMPHOCYTE ACTIVATION; MAJOR CLINICAL STUDY; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN DETERMINATION; PROTEIN FUNCTION; SEIZURE; VIRUS MENINGITIS; BLOOD; BRAIN DISEASE; CADAVER; CALCINOSIS; CEREBROSPINAL FLUID; COMPARATIVE STUDY; FEMALE; GLIOSIS; MALE; METABOLISM; MIDDLE AGED; MULTIPLE MALFORMATION SYNDROME; NEWBORN; PATHOLOGY; PRESCHOOL CHILD;

ABNORMALITIES, MULTIPLE; ADULT; AGED; ASTROCYTES; BRAIN DISEASES; CALCINOSIS; CHEMOKINE CXCL10; CHILD; CHILD, PRESCHOOL; ENCEPHALITIS; FEMALE; GLIOSIS; HUMANS; INFANT; INFANT, NEWBORN; INTERFERON-ALPHA; INTERLEUKIN-6; INTERLEUKIN-8; MALE; MENINGITIS, VIRAL; MIDDLE AGED; POSTMORTEM CHANGES;

EID: 44949218591     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20639     Document Type: Article

References (60)

1. Akwa Y, Hassett DE, Eloranta ML, Sandberg K, Masliah E, Powell H, Whittton JL, Bloom FE, Campbell IL. 1998. Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration. J Immunol 161:5016-5026.
2. Aronica E, Yankaya B, Jansen GH, Leensta S, van Veelen CW, Gorter JA, Troost D. 2001. Ionotropic and metabotropic glutamate receptor protein expression in glioneuronal tumours from patients with intractable epilepsy. Neuropath AppI Neurobiol 27:223-237.
3. Asensio VC, Kincaid C, Campbell IL. 1999. Chemokines and the inflammatory response to viral infection in the central nervous system with a focus on lymphocytic choriomeningitis virus. J Neurovirol 5:65-75.
4. Barth PG, Walter A, van Gelderen I. 1999. Aicardi-Goutieres syndrome: a genetic microangiopathy? Acta Neuropahtol 98:212-216.
5. Bhowmick S, Duseja R, Das S, Appaiahgiri MB, Vrati S, Basu A. 2007. Induction of IP-10 (CXCL10) in astrocytes following Japanese encephalitis. Neurosci Lett 414:45-50.
6. Bowman CC, Rasley A, Tranguch SL, Marriott I. 2003. Cultured astrocytes express toll-like receptors for bacterial products. Glia 43:281-291.
7. Boztug K, Carson MJ, Pham-Mitchell N, Asensio VC, DeMartino J, Campbell IL. 2002. Leukocyte infiltration, but not neurodegeneration, in the CNS of transgenic mice with astrocyte production of the CXC chemokine ligand 10. J Immunol 169:1505-1515.
8. Campbell IL, Krucker T, Steffensen S, Akwa Y, Powell HC, Lane T, Carr DJ, Gold LH, Henriksen SJ, Siggins GR. 1999. Structural and functional neuropathology in transgenic mice with CNS expression of IFN-α. Brain Res 835:46-61.
9. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, Miller SD. 2005. Differential activation of astrocytes by inane and adaptive immune stimuli. Glia 49:360-374.
10. Carpentier PA, Williams BR, Miller SD. 2007. Distinct roles of protein kinase R, toll-like receptor 3 in the activation of astrocytes by viral stimuli. Glia 55:239-252.
11. Cheeran MC, Hu S, Sheng WS, Rashid A, Peterson PK, Lokensgard JR. 2005. Differential responses of human brain cells to West Nile virus infection. J Neurovirol 11:512-524.
12. Cheeran MC, Hu S, Yager SL, Gekker G, Peterson PK, Lokensgard JR. 2001. Cytomegalovirus induces cytokine and chemokine production differentially in microglia and astrocytes: Antiviral implications. J Neurovirol 7:135-147.
13. Christensen JE, de Lemos C, Moos T, Christensen JP, Thomsen AR. 2006. CXCL10 is the key ligand for CXCR3 on CD8 effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J Immunol 176:4235-4243.
14. Cribier B, Djeridi N, Peltre B, Grosshans E. 2001. A histologic and immundhistochemical study of chilblains. J Am Acad Dermatol 45: 924-929.
15. Crow YJ, Hayward BE, Parmar R, Robins P, Leitch A, Ali M, Black DN, van Bokhoven H, Brunner HG, Hamel BC, Corry PC, Cowan FM, Frints SG, Klepper J, Livingston JH, Lynch SA, Massey RF, Meritet JF, Michaud JL, Ponsot G, Voit T, Lebon P, Bonthron DT, Jackson AP, Barnes DE, Lindahl T. 2006a. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREXI cause Aicardi-Goutières syndrome at the AGS1 locus. Nat Genet 38:917-920.
16. Crow YJ, Leitch A, Hayward BE, Garner A, Parmar R, Griffith E, Ali M, Semple C, Aicardi J, Babul-Hirji R, Baumann C, Baxter P, Bertini E, Chandler KE, Chitayat D, Cau D, Déry C, Fazzi E, Goizet C, King MD, Klepper J, Lacombe D, Lanzi G, Lyall H, Martínez-Frías ML, Mathieu M, McKeown C, Monier A, Oade Y, Quarrell OW, Rittey CD, Rogers RC, Sanchis A, Stephenson JBP, Tacke U, Till M, Tolmie JL, Tomlin P, Voit T, Weschke B, Woods CG, Lebon P, Bonthron DT, Ponting CP, Jackson AP. 2006b. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutières syndrome and mimic congenital viral brain infection. Nat Genet 38:910-916.
17. Dimova PS, Mikova OA. 2005. Case of Aicardi-Goutieres syndrome with long-lasting increase of cerebrospinal interferon-α. J Child Neurol 20:915-919.
18. dos Santos AC, Barsante MM, Arantes RM, Bernard CC, Teixeira MM, Carvalho-Tavares J. 2005. CCL2 and CCL5 mediate leukocyte adhesion in experimental autoimmune encephalomyelitis-an intravital microscopy study. J Neuroimmunol 162:122-129.
19. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD. 2002. IFN-γ-inducible protein 10 (IP-10; CXCL10)-deficienty mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168:3195-3204.
20. 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.
21. Eugenin EA, Osiecki K, Lopez L, Goldstein H, Calderon TM, Berman JW. 2006. CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: A potential mechanism of HIV-CNS invasion and NeuroAIDS. J Neurosci 26:1098-1106.
22. Farina C, Krumholz 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.
23. Fife BT, Kennedy KJ, Paniagua MC, Lukacs NW, Kunkel SL, Luster AD, Karpus WJ. 2001. CXCL10 (IFN-γ-inducible protein-10) control of encephalitogenic CD4+ T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. J Immunol 166:7617-7624.
24. Giunti D, Borsellino G, Benelli R, Marchese M, Capello E, Valle MT, Pedemonte E, Noonan D, Albini A, Bernardi G, Mancardi GL, Battistini L, Uccelli A. 2003. Phenotypic and functional analysis of T cells homing to the CSF of subjects with inflammatory diseases of the CNS. J Leukoc Biol 73:584-590.
25. Goutières F. 2005. Aicardi-Goutieres syndrome. Brain Dev 27:201-206.
26. Goutieres F, Aicardi J, Barth PG, Lebon P. 1998. Aicardi-Goutieres syndrome: An update and results of interferon-α studies. Ann Neurol 44:900-907.
27. Ho HH, Ivashkiv LB. 2006. Role of STAT3 in type I interferon responses. Negative regulation of STAT1-dependent inflammatory gene activation. J Biol Chem 281:14111-14118.
28. Huang D, Wujek J, Kidd G, He TT, Cardona A, Sasse ME, Stein EJ, Kish J, Tani M, Charo IF, Proudfoot AE, Rollins BJ, Handel T, Ransohoff RM. 2005. Chronic expression of monocyte chemoattractant protein-1 in the central nervous system causes delayed encephalopathy and impaired microglial function in mice. FASEB J 19:761-772.
29. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, Shapiro A, Antel JP. 2005. TLR signaling tailors inane immune responses in human microglia and astrocytes. J Immunol 175:4320-4330.
30. Karpus WJ, Kennedy KJ, Fife BT, Bennett JL, Dal Canto MC, Kunkel SL, Lukaes NW. 2006. Anti-CCL2 treatment inhibits Theiler's murine encephalomyelitis virus-induced demyelinating disease. J Neurovirol 12:251-261.
31. Klein RS. 2004. Regulation of neuroinflammation: The role of CXCL10 in lymphocyte infiltration during autoimmune encephalomyelitis. J Cell Biochem 92:213-222.
32. Kolb SA, Sporer B, Lahrtz F, Koedel U, Pfister HW, Fontana A. 1999. Identification of a T cell chemotactic factor in the cerebrospinal fluid of HIV-1-infected individuals as interferon-γ inducible protein 10. J Neuroimmunol 93:172-181.
33. Kothare SV, Pungavkar SA, Patkar DP, Sainam NI, Naik MH, Gadani S. 2006. Regression of white matter hypodensities with age in Aicardi-Goutieres syndrome: A case report. Childs Nerv Syst 22: 1503-1506.
34. Krasowska-Zoladek A, Banaszewska M, Kraszpulski M, Konat GW. 2007. Kinetics of inflammatory response of astrocytes induced by TLR3 and TLR4 ligation. J Neurosci Res 85:205-212.
35. Lanzi G, Fazzi E, D'Arrigo S. 2002. Aicardi-Goutieres syndrome: A description of 21 new cases and a comparison with the literature. Eur J Paediatr Neurol 6 (Suppl):A9-A22.
36. Lanzi G, Fazzi E, D'Arrigo S, Orcesi S, Maraucci I, Uggetti C, Bertini E, Lebon P. 2005. The natural history of Aicardi-Goutieres syndrome: Follow-up of 11 Italian patients. Neurology 64:1621-1624.
37. Lebon P, Meritet JF, Krivine A, Rozenberg F. 2002. Interferon and Aicardi-Goutieres syndrome. Eur J Paediatr Neurol 6:A43-A53.
38. Lebon P, Badoual J, Ponsot G, Goutibres F, Hemeury-Cukier F, Aicardi J. 1988, Intrathecal synthesis of interferon-α in infants with progressive familial encephalopathy. J Neurol Sci 84:201-208.
39. Lebre MC, van der Aar AM, van Baarsen L, van Capel TM, Schuitenmaker JH, Kapsenberg ML, de Jong EC. 2007. Human keratinocytes express functional toll-like receptor 3, 4, 5 and 9. J Invest Dermatol 127:331-341.
40. Lellouch-Tubiana A, Fohlen M, Robain O, Rozenberg F. 2000. Immunocytochemical characterization of long-term persistent immune activation in human brain after herpes simplex encephalitis. Neuropath Appl Neurobiol 26:285-294.
41. 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.
42. Liu L, Huang D, Matsui M, He TT, Hu T, DeMartino J, Lu B, Gerard C, Ransohoff RM. 2006. Severe disease, unaltered leukocyte migration, and reduced IFN-γ production in CXCR3-/- mice with experimental autoimmune encephalomyelitis. J Immunol 76:4399-4409.
43. Liu MT, Chen BP, Oertel P, Buchmeier MJ, Hamilton TA, Armstrong DA, Lane TE. 2001. The chemokines IP-10 and Mig are essential in host defense following infection with a neurotropic coronavirus. Adv Exp, Med Biol 494:323-327.
44. Loetscher M, Loetscher P, Brass N, Meese E, Moser B. 1998. Lymphocyte-specific chemokine receptor CXCR3: Regulation, chemokine binding and gene location. Eur J Immunol 28:3696-3705.
45. Mahad D, Callahan MK, Williams KA, Ubogu EE, Kivisakk P, Tucky B, Kidd G, Kingsbury GA, Chang A, Fox RJ, Mack M, Sniderman MB, Ravid R, Staugaitis SM, Stins MF, Ransohoff RM. 2006. Modulating CCR2 and CCL2 at the blood-brain barrier: Relevance for multiple sclerosis pathogenesis. Brain 129:212-223.
46. Malm G, Engman ML. 2007. Congenital cytomegalovirus infections. Semin in Fetal Neonatal Med 12:154-159.
47. Monteiro de Almeida S, Letendre S, Zimmerman J, Kolakowski S, Lazzaretto D, McCutchan JA, Ellis R. 2006. Relationship of CSF leukocytosis to compartmentalized changes in MCP-1/CCL2 in the CSF of HIV-infected patients undergoing interruption of antiretroviral therapy. J Neuroimmunol 179:180-185.
48. Palma JP, Kim BS. 2004. The scope and activation mechanisms of chemokine gene expression in primary astrocytes following infection with Theiler's virus. J Neuroimmunol 149:121-129.
49. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, Estes ML, Thomas DM, Tuohy VK 1993. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 7:592-600.
50. Rasmussen M, Skullerud K, Bakke SJ, Lebon P, Jahnsen FL. 2005. Cerebral thrombotic microangiopathy and antiphospholipid antibodies in Aicardi-Goutieres syndrome-report of two sisters. Neuropediatrics 36:399-402.
51. Rho MB, Wesselingh S, Glass JD, McArthur JC, Choi S, Griffin J, Tyor WR. 1995. A potential role for interferon-α in the pathogenesis of HIV-associated dementia. Brain Behav Immun 9:366-377.
52. Rice G, Newman WG, Dean J, Patrick T, Parmar R, Flintoff K, Robins P, Harvey S, Hollis T, O'Hara A, Herrick AL, Bowden AP, Perrino FW, Lindahl T, Barnes DE, Crow YJ. 2007a. Heterozygous mutations in TREX1 cause familial chilblain lupus and dominant Aicardi-Goutières syndrome. Am J Hum Genet 80:811-815.
53. Rice G, Patrick T, Parmar R, Taylor CF, Aeby A, Aicardi J, Artuch R, Attard Montalto S, Bacino CA, Barroso B, Baxter P, Benko WS, Bergmann C, Bertini E, Biancheri R, Blair EM, Blau N, Bonthron DT, Briggs T, Brueton LA, Brunner HG, Burke CJ, Carr IM, Carvalho DR, Chandler KE, Christen HJ, Corry PC, Cowan FM, Cox H, D'Arrigo S, Dean J, De Laet C, De Praeter C, Déry C, Ferrie CD, Flintoff K, Frints SGM, Garcia-Cazorla A, Gener B, Goizet C, Goutières F, Green AJ, Guët A, Hamel BCJ, Hayward BE, Heiberg A, Hennekam RC, Husson M, Jackson AP, Jayatunga R, Jiang YH, Kant SG, Kao A, Kotzot D, Kratzer W, Lacombe D, Lagae L, Landrieu PG, Lanzi G, Leitch A, Lim MJ, Livingston JH, Lourenco CM, Lyall EGH, Lynch SA, Lyons MJ, Marom D, McClure JP, MeWilliam R, Melancon SB, Mewasingh LD, Moutard ML, Nischal KK, Øtergaard JR, Prendiville J, Rasmussen M, Rogers RC, Roland D, Rosser EM, Rostasy K, Roubertie A, Sanchis A, Schiffmann R, Scholl-Bürgi S, Seal S, Shalev SA, Sierra Corcoles C, Sinha GP, Soler D, Spiegel R, Stephenson JBP, Tacke U, Tan TY, Till M, Tolmie JL, Tomlin P, Vagnarelli F, Valente EM, van Coster RNA, van der As N, Vanderver A, Vles JSH, Voit T, Wassmer E, Weschke B, Whiteford ML, Willemsen MAA, Zankl A, Zuberi SM, Orcesi S, Fazzi E, Lebon P, Crow YJ. 2007b. Clinical and molecular phenotype of Aicardi- Goutières syndrome. Am J Hum Genet 81:713-725.
54. Sanchis A, Cervero L, Bataller A, Tortajada JL, Huguet J, Crow YJ, Ali M, Higuet LJ, Martinez-Frias ML. 2005. Genetic syndromes mimic congenital infections. J Pediatr 146:701-705.
55. Shacklett BL, Cox CA, Wilkens DT, Karlsson RK, Nilsson A, Nixon DF, Price RW. 2004. Increased adhesion molecule and chemokine receptor expression on CD8+ T cells trafficking to cerebrospinal fluid in HIV-1 infection. J Infect Dis 189:2202-2212.
56. Sorensen TL, Trebst C, Kivisakk P, Klaege KL, Majmudar A, Ravid R, Lassmann H, Olsen DB, Strieter RM, Ransohoff RM, Sellebjerg F. 2002. Multiple sclerosis: A study of CXCL10 and CXCR2 co-localization in the inflamed central nervous system. J Neuroimmunol 127:59-68.
57. Takeshita S, Takeshita F, Haddad DE, Janabi N, Klinman DM. 2001. Activation of microglia and astrocytes by CpG oligodeoxynucleotides. Neuroreport 12:3029-3032.
58. Trifilo MJ, Lane TE. 2003. Adenovirus-mediated expression of CXCL10 in the central nervous system results in T-cell recruitment and limited neuropathology. J Neruovirol 9:315-324.
59. Tsunoda I, Lane TE, Blacked J, Fujinami RS. 2004. Distinct roles for IP-10/CXCL10 in three animal models, Theiler's virus infection EAE, MHV infection, for multiple sclerosis: Implication of differing roles for IP-10 Mult Scler 10:26-34.
60. van den Pol AN, Robek MD, Ghosh PK, Ozduman Y, Bandi P, Whim MD, Wollmann G. 2007. Cytomegalovirus induces interferon-stimulated gene expression and is attenuated by interferon in the developing brain. J Virol 81:332-348.