JCV agnoprotein-induced reduction in CXCL5/LIX secretion by oligodendrocytes is associated with activation of apoptotic signaling in neurons

Journal of Cellular Physiology

Volumn 227, Issue 8, 2012, Pages 3119-3127

  Merabova, Nana ^a   Kaminski, Rafal ^a   Krynska, Barbara ^a,b   Amini, Shohreh ^a,c   Khalili, Kamel ^a   Darbinyan, Armine ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

^c Temple University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGNOPROTEIN; CELL PROTEIN; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GLYCOGEN SYNTHASE KINASE; GRANULOCYTE CHEMOTACTIC PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN LIX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; AXONAL INJURY; BRAIN CELL; BRAIN NERVE CELL; CELL INTERACTION; CELL LEVEL; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; NERVE INJURY; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; POLYOMA VIRUS; POLYOMAVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT;

ANIMALS; APOPTOSIS; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINE CXCL5; CULTURE MEDIA, CONDITIONED; GLYCOGEN SYNTHASE KINASE 3; HUMANS; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEURONS; OLIGODENDROGLIA; RATS; SIGNAL TRANSDUCTION; VIRAL REGULATORY AND ACCESSORY PROTEINS;

JC POLYOMAVIRUS; RATTUS;

EID: 84860484358     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.23065     Document Type: Article

References (83)

1. Atta UR, Harvey K, Siddiqui RA. 1999. Interleukin-8: An autocrine inflammatory mediator. Curr Pharm Des 5: 241-253.
2. Bajetto A, Bonavia R, Barbero S, Schettini G. 2002. Characterization of chemokines and their receptors in the central nervous system: Physiopathological implications. J Neurochem 82: 1311-1329.
3. Berger JR. 2007. Progressive multifocal leukoencephalopathy. Curr Neurol Neurosci Rep 7: 461-469.
4. Berger JR. 2011. The basis for modeling progressive multifocal leukoencephalopathy pathogenesis. Curr Opin Neurol 24: 262-267.
5. Berger JR, Houff S. 2006. Progressive multifocal leukoencephalopathy: Lessons from AIDS and natalizumab. Neurol Res 28: 299-305.
6. Berger JR, Kaszovitz B, Post MJ, Dickinson G. 1987. Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. A review of the literature with a report of sixteen cases. Ann Intern Med 107: 78-87.
7. Brooks BR, Walker DL. 1984. Progressive multifocal leukoencephalopathy. Neurol Clin 2: 299-313.
8. Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, Hultgren B, Wood WI, Moore MW. 1995. Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265: 682-684.
9. Caldarelli-Stefano R, Vago L, Omodeo-Zorini E, Mediati M, Losciale L, Nebuloni M, Costanzi G, Ferrante P. 1999. Detection and typing of JC virus in autopsy brains and extraneural organs of AIDS patients and nonimmunocompromised individuals. J Neurovirol 5: 125-133.
10. Carson KR, Evens AM, Richey EA, Habermann TM, Focosi D, Seymour JF, Laubach J, Bawn SD, Gordon LI, Winter JN, Furman RR, Vose JM, Zelenetz AD, Mamtani R, Raisch DW, Dorshimer GW, Gottardi-Littell NR, Talley RL, Sartor O, Green D, Major EO, Bennett CL. 2009. Progressive multifocal leukoencephalopathy following rituximab therapy in HIV negative patients: A report of 57 cases from the Research on Adverse Drug Event and Reports (RADAR) project. Blood 113: 4834-4840.
11. Cartier L, Hartley O, Dubois-Dauphin M, Krause KH. 2005. Chemokine receptors in the central nervous system: Role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 48: 16-42.
12. Chan JR, Watkins TA, Cosgaya JM, Zhang C, Chen L, Reichardt LF, Shooter EM, Barres BA. 2004. NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes. Neuron 43: 183-191.
13. Chang L, Miller BL, McBride D, et al. 1995. Brain lesions in patients with AIDS: H-1 MR spectroscopy. Radiology 197: 525-531.
14. Chang L, Ernst T, Tornatore C, Aronow H, Melchor R, Walot I, Singer E, Cornford M. 1997. Metabolite abnormalities in progressive multifocal leukoencephalopathy by proton magnetic resonance spectroscopy. Neurology 48: 836-845.
15. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, et al. 2000. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403: 434-439.
16. Clark-Lewis I, Dewald B, Geiser T, Moser B, Baggiolini M. 1993. Platelet factor 4 binds to interleukin 8 receptors and activates neutrophils when its N terminus is modified with Glu-Leu-Arg. Proc Natl Acad Sci USA 90: 3574-3577.
17. Clifford DB, De Luca A, Simpson DM, Arendt G, Giovannoni G, Nath A. 2010. Natalizumab-associated progressive multifocal leukoencephalopathy in patients with multiple sclerosis: Lessons from 28 cases. Lancet Neurol 9: 438-446. Review.
18. Darbinyan A, Darbinian N, Safak M, Radhakrishnan S, Giordano A, Khalili K. 2002. Evidence for dysregulation of cell cycle by human polyomavirus, JCV, late auxiliary protein. Oncogene 21: 5574-5581.
19. Darbinyan A, Siddiqui KM, Slonina D, Darbinian N, Amini S, White MK, Khalili K. 2004. Role of JC virus agnoprotein in DNA repair. J Virol 78: 8593-8600.
20. Darbinyan A, White MK, Akan S, Radhakrishnan S, Del Valle L, Amini S, Khalili K. 2007. Alterations of DNA damage repair pathways resulting from JCV infection. Virology 364: 73-86.
21. De Paola M, Buanne P, Biordi L, Bertini R, Ghezzi P, Mennini T. 2007. Chemokine MIP-2/CXCL2, acting on CXCR2, induces motor neuron death in primary cultures. Neuroimmunomodulation 14: 310-316.
22. Del Valle L, Khalili K. 2010. Detection of human polyomavirus proteins, T-antigen and agnoprotein, in human tumor tissue arrays. J Med Virol 82: 806-811.
23. Dupree JL, Mason JL, Marcus JR, Stull M, Levinson R, Matsushima GK, Popko B. 2004. Oligodendrocytes assist in the maintenance of sodium channel clusters independent of the myelin sheath. Neuron Glia Biol 1: 179-192.
24. Elsner C, Dorries K. 1992. Evidence of human polyomavirus BK and JC infection in normal brain tissue. Virology 191: 72-80.
25. Frisque RJ. 2001. Structure and function of JC virus T' proteins. J Neurovirol 7: 293-297. Review.
26. Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R. 1999. Wnt3a-/--like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev 13: 709-717.
27. Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, Newman W, Groopman JE. 1998. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem 273: 23169-23175.
28. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65: 391-426.
29. Harper SJ, LoGrasso P. 2001. Signalling for survival and death in neurones: The role of stress-activated kinases, JNK and p38. Cell Signal 13: 299-310.
30. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. 1998. Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512.
31. Horuk R, Martin AW, Wang Z, Schweitzer L, Gerassimides A, Guo H, Lu Z, Hesselgesser J, Perez HD, Kim J, Parker J, Hadley TJ, Peiper SC. 1997. Expression of chemokine receptors by subsets of neurons in the central nervous system, J Immunol 158: 2882-2890.
32. Hosking MP, Liu L, Ransohoff RM, Lane TE. 2009. A protective role for ELR+ chemokines during acute viral encephalomyelitis. PLoS Pathog 5: e1000648.
33. Hosking MP, Tirotta E, Ransohoff RM, Lane TE. 2010. CXCR2 signaling protects oligodendrocytes and restricts demyelination in a mouse model of viral-induced demyelination. PLoS ONE 5: e11340.
34. Hou J, Major EO. 2000. Progressive multifocal leukoencephalopathy: JC virus induced demyelination in the immune compromised host. J Neurovirol 6: S98-S100.
35. Iranzo A, Moreno A, Pujol J, Marti-Fabregas J, Domingo P, Molet J, Ris J, Cadafalch J. 1999. Proton magnetic resonance spectroscopy pattern of progressive multifocal leukoencephalopathy in AIDS. J Neurol Neurosurg Psychiatry 66: 520-523.
36. Johnson EM. 2010. Structural evaluation of new human polyomaviruses provides clues to pathobiology. Trends Microbiol 18: 215-223.
37. Jones SA, Moser B, Thelen M. 1995. A comparison of post-receptor signal transduction events in Jurkat cells transfected with either IL-8R1 or IL-8R2. Chemokine mediated activation of p42/p44 MAP-kinase (ERK-2), FEBS Lett 364: 211-214.
38. Khalili K, White MK, Sawa H, Nagashima K, Safak M. 2005. The agnoprotein of polyomaviruses: A multifunctional auxiliary protein. J Cell Physiol 204: 1-7. Review.
39. Khalili K, White MK, Lublin F, Ferrante P, Berger JR. 2007. Reactivation of JC virus and development of PML in patients with multiple sclerosis. Neurology 68: 985-990.
40. Khan MZ, Brandimarti R, Shimizu S, Nicolai J, Crowe E, Meucci O. 2008. The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ 15: 1663-1672.
41. Kitamura T, Aso Y, Kuniyoshi N, Hara K, Yogo Y. 1990. High incidence of urinary JC virus excretion in nonimmunosuppressed older patients. J Infect Dis 161: 1128-1133.
42. Limatola C, Ciotti MT, Mercanti D, Vacca F, Ragozzino D, Giovannelli A, Santoni A, Eusebi F, Miledi R. 2000. The chemokine growth-related gene product beta protects rat cerebellar granule cells from apoptotic cell death through alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors. Proc Natl Acad Sci USA 97: 6197-6201.
43. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
44. Louis JC, Magal E, Muir D, Manthorpe M, Varon S. 1992. CG4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J Neurosci Res 31: 193-204.
45. Merabova N, Kaniowska D, Kaminski R, Deshmane SL, White MK, Amini S, Darbinyan A, Khalili K. 2008. JC virus agnoprotein inhibits in vitro differentiation of oligodendrocytes and promotes apoptosis. J Virol 82: 1558-1569.
46. Miller RJ, Rostene W, Apartis E, Banisadr G, Biber K, Milligan ED, White FA, Zhang J. 2008. Chemokine action in the nervous system. J Neurosci 28: 11792-11795.
47. Milner RJ, Lai C, Nave KA, Lenoir D, Ogata J, Sutcliffe JG. 1985. Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 42: 931-939.
48. Miloso M, Scuteri A, Foudah D, Tredici G. 2008. MAPKs as mediators of cell fate determination: An approach to neurodegenerative diseases. Curr Med Chem 15: 538-548.
49. Moll NM, Rietsch AM, Ransohoff AJ, et al. 2008. Cortical demyelination in PML and MS: similarities and differences. Neurology 70: 336-343.
50. Monaco MC, Jensen PN, Hou J, Durham LC, Major EO. 1998. Detection of JC virus DNA in human tonsil tissue: Evidence for site of initial viral infection. J Virol 72: 9918-9923.
51. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT. 1994. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13: 757.
52. Nair VD, Olanow CW. 2008. Differential modulation of Akt/glycogen synthase kinase-3beta pathway regulates apoptotic and cytoprotective signaling responses. J Biol Chem 283: 15469-15478.
53. Nave KA. 2010. Myelination and the trophic support of long axons. Nat Rev Neurosci 11: 275-283.
54. Nave KA, Trapp BD. 2008. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31: 535-561.
55. Nguyen D, Stangel M. 2001. Expression of the chemokine receptors CXCR1 and CXCR2 in rat oligodendroglial cells. Brain Res Dev Brain Res 128: 77-81.
56. Omari KM, John GR, Sealfon SC, Raine CS. 2005. CXC chemokine receptors on human oligodendrocytes: Implications for multiple sclerosis. Brain 128: 1003-1015.
57. Padgett BL, Walker DL. 1973. Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. J Infect Dis 127: 467-470.
58. Piaton G, Gould RM, Lubetzki C. 2010. Axon-oligodendrocyte interactions during developmental myelination, demyelination and repair. J Neurochem 114: 1243-1260.
59. Randhawa P, Shapiro R, Vats A. 2005. Quantitation of DNA of polyomaviruses BK and JC in human kidneys. J Infect Dis 192: 504-509.
60. Rasband MN, Tayler J, Kaga Y, Yang Y, Lappe-Siefke C, Nave KA, Bansal R. 2005. CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50: 86-90.
61. Rovai LE, Herschman HR, Smith JB. 1998. The murine neutrophil-chemoattractant chemokines LIX, KC, and MIP-2 have distinct induction kinetics, tissue distributions, and tissue-specific sensitivities to glucocorticoid regulation in endotoxemia. J Leukoc Biol 64: 494-502.
62. Ryves WJ, Harwood AJ. 2001. Lithium inhibits glycogen synthase kinase-3 by competition for magnesium. Biochem Biophys Res Commun 280: 720-725.
63. Semple BD, Kossmann T, Morganti-Kossmann MC. 2010. Role of chemokines in CNS health and pathology: A focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J Cereb Blood Flow Metab 30: 459-473.
64. Simmons ML, Frondoza CG, Coyle JT. 1991. Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience 45: 37-45.
65. 1H-MR spectroscopy for metabolic characterisation of diffuse and focal brain lesions in patients infected with HIV. J Neurol Neurosurg Psychiatry 64: 516-523.
66. Smith JB, Rovai LE, Herschman HR. 1997. Sequence similarities of a subgroup of CXC chemokines related to murine LIX: Implications for the interpretation of evolutionary relationships among chemokines. J Leukoc Biol 62: 598-603.
67. Stambolic V, Ruel L, Woodgett JR. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr Biol 6: 1664-1668.
68. Strieter RM, Polverini PJ, Arenberg DA, Walz A, Opdenakker G, Van Damme J, Kunkel SL. 1995. Role of C-X-C chemokines as regulators of angiogenesis in lung cancer. J Biol Chem 270: 27348-27357.
69. Tan CS, Koralnik IJ. 2010. Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: Clinical features and pathogenesis. Lancet Neurol 9: 425-437.
70. Tan CS, Dezube BJ, Bhargava P, Autissier P, Wuthrich C, Miller J, Koralnik IJ. 2009. Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: Implications for viral latency and neurotropic transformation. J Infect Dis 199: 881-888.
71. Tan CS, Ellis LC, Wüthrich C, Ngo L, Broge TA Jr, Saint-Aubyn J, Miller JS, Koralnik IJ. 2010. JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J Virol 84: 9200-9209.
72. Tsai HH, Frost E, To V, Robinson S, Ffrench-Constant C, Geertman R, Ransohoff RM, Miller RH. 2002. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 110: 373-383.
73. Vago L, Nebuloni M, Sala E, Cinque P, Bonetto S, Isella A, Ottoni L, Crociati A, Costanzi G. 1996. JCV-DNA and BKV-DNA in the CNS tissue and CSF of AIDS patients and normal subjects. Study of 41 cases and review of the literature. J Acquir Immune Defic Syndr Hum Retrovirol 12: 139-146.
74. Vallès A, Grijpink-Ongering L, de Bree FM, Tuinstra T, Ronken E. 2006. Differential regulation of the CXCR2 chemokine network in rat brain trauma: Implications for neuroimmune interactions and neuronal survival. Neurobiol Dis 22: 312-322.
75. Watson K, Fan GH. 2005. Macrophage inflammatory protein 2 inhibits beta-amyloid peptide (1-42)-mediated hippocampal neuronal apoptosis through activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling pathways. Mol Pharmacol 67: 757-765.
76. White MK, Khalili K. 2011. Pathogenesis of progressive multifocal leukoencephalopathy-Revisited. J Infect Dis 203: 578-586.
77. White FA, Ishaq M, Stoner GL, Frisque RJ. 1992. JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. J Virol 66: 5726-5734.
78. Wu D, LaRosa GJ, Melvin SI. 1993. G protein-coupled signal transduction pathways for interleukin-8. Science 261: 101-103.
79. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331.
80. Xia M, Qin S, McNamara M, Mackay C, Hyman BT. 1997. Interleukin-8 receptor B immunoreactivity in brain and neuritic plaques of Alzheimer's disease. Am J Pathol 150: 1267-1274.
81. Yogo Y, Kitamura T, Sugimoto C, et al. 1990. Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. J Virol 64: 3139-3143.
82. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10: 1443-1454.
83. Yu X, Malenka RC. 2003. Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6: 1169-1177.