Astrocytes mediate HIV-1 Tat-induced neuronal damage via ligand-gated ion channel P2X7R

Journal of Neurochemistry

Volumn 132, Issue 4, 2015, Pages 464-476

  Tewari, Manju ^a   Monika, ^a   Varghese, Rebu K ^b   Menon, Malini ^b   Seth, Pankaj ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

HIV 1 neuropathogenesis; MCP 1 CCL2; neuroAIDS; neuron glia; purinergic receptor

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PURINERGIC P2X7 RECEPTOR; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; LIGAND;

APOPTOSIS; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CELL DAMAGE; EXTRACELLULAR CALCIUM; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NERVE CELL; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROTOXICITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; BIOSYNTHESIS; CELL CULTURE; CHANNEL GATING; FEMALE; PHYSIOLOGY; PREGNANCY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ASTROCYTES; CELLS, CULTURED; FEMALE; HIV-1; HUMANS; ION CHANNEL GATING; LIGANDS; NEURONS; PREGNANCY; RECEPTORS, PURINERGIC P2X7; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84922629718     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12953     Document Type: Article

References (51)

1. Abbracchio M. P., and, Burnstock G., (1994) Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol. Ther. 64, 445-475.
2. Adle-Biassette H., Wingertsmann L., Authier F. J., Kondo H., Poron F., Hery C., Bell J., Tardieu M., Gherardi R., and, Gray F., (1997) Neuronal apoptosis in the central and peripheral nervous system in HIV infection. Arch. Anat. Cytol. Pathol. 45, 86-93.
3. Buch S., Sui Y., Potula R., et al,. (2004) Role of interleukin-4 and monocyte chemoattractant protein-1 in the neuropathogenesis of X4 simian human immunodeficiency virus infection in macaques. J. Neurovirol. 10 (Suppl 1), 118-124.
4. Chang L., Ernst T., St Hillaire C., and, Conant K., (2004) Antiretroviral treatment alters relationship between MCP-1 and neurometabolites in HIV patients. Antivir. Ther. 9, 431-440.
5. Chauhan A., Turchan J., Pocernich C., Bruce-Keller A., Roth S., Butterfield D. A., Major E. O., and, Nath A., (2003) Intracellular human immunodeficiency virus Tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J. Biol. Chem. 278, 13512-13519.
6. Churchill M., and, Nath A., (2013) Where does HIV hide? A focus on the central nervous system. Curr. Opin. HIV AIDS 8, 165-169.
7. Churchill M. J., Wesselingh S. L., Cowley D., Pardo C. A., McArthur J. C., Brew B. J., and, Gorry P. R., (2009) Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann. Neurol. 66, 253-258.
8. Collo G., Neidhart S., Kawashima E., Kosco-Vilbois M., North R. A., and, Buell G., (1997) Tissue distribution of the P2X7 receptor. Neuropharmacology 36, 1277-1283.
9. Conant K., Garzino-Demo A., Nath A., McArthur J. C., Halliday W., Power C., Gallo R. C., and, Major E. O., (1998) Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc. Natl Acad. Sci. USA 95, 3117-3121.
10. Diaz-Hernandez M., Diez-Zaera M., Sanchez-Nogueiro J., Gomez-Villafuertes R., Canals J. M., Alberch J., Miras-Portugal M. T., and, Lucas J. J., (2009) Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEB J. 23, 1893-1906.
11. Duan S., and, Neary J. T., (2006) P2X(7) receptors: properties and relevance to CNS function. Glia 54, 738-746.
12. El-Hage N., Wu G., Wang J., Ambati J., Knapp P. E., Reed J. L., Bruce-Keller A. J., and, Hauser K. F., (2006) HIV-1 Tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53, 132-146.
13. Eugenin E. A., and, Berman J. W., (2013) Cytochrome C dysregulation induced by HIV infection of astrocytes results in bystander apoptosis of uninfected astrocytes by an IP3 and calcium-dependent mechanism. J. Neurochem. 127, 644-651.
14. Eugenin E. A., D'Aversa T. G., Lopez L., Calderon T. M., and, Berman J. W., (2003) MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J. Neurochem. 85, 1299-1311.
15. Eugenin E. A., Dyer G., Calderon T. M., and, Berman J. W., (2005) HIV-1 tat protein induces a migratory phenotype in human fetal microglia by a CCL2 (MCP-1)-dependent mechanism: possible role in NeuroAIDS. Glia 49, 501-510.
16. Gandelman M., Levy M., Cassina P., Barbeito L., and, Beckman J. S., (2013) P2X7 receptor-induced death of motor neurons by a peroxynitrite/FAS-dependent pathway. J. Neurochem. 126, 382-388.
17. Garden G. A., (2002) Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 40, 240-251.
18. Gulbransen B. D., Bashashati M., Hirota S. A., et al,. (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 18, 600-604.
19. Haughey N. J., Holden C. P., Nath A., and, Geiger J. D., (1999) Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. J. Neurochem. 73, 1363-1374.
20. Hazleton J. E., Berman J. W., and, Eugenin E. A., (2012) Purinergic receptors are required for HIV-1 infection of primary human macrophages. J. Immunol. 188, 4488-4495.
21. Hudson L., Liu J., Nath A., Jones M., Raghavan R., Narayan O., Male D., and, Everall I., (2000) Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J. Neurovirol. 6, 145-155.
22. Johnson T. P., Patel K., Johnson K. R., Maric D., Calabresi P. A., Hasbun R., and, Nath A., (2013) Induction of IL-17 and nonclassical T-cell activation by HIV-Tat protein. Proc. Natl Acad. Sci. USA 110, 13588-13593.
23. Kamat A., Lyons J. L., Misra V., Uno H., Morgello S., Singer E. J., and, Gabuzda D., (2012) Monocyte activation markers in cerebrospinal fluid associated with impaired neurocognitive testing in advanced HIV infection. J. Acquir. Immune Defic. Syndr. 60, 234-243.
24. Kruman I. I., Nath A., and, Mattson M. P., (1998) HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp. Neurol. 154, 276-288.
25. Lee E. O., Kim S. E., Park H. K., Kang J. L., and, Chong Y. H., (2011) Extracellular HIV-1 Tat upregulates TNF-alpha dependent MCP-1/CCL2 production via activation of ERK1/2 pathway in rat hippocampal slice cultures: inhibition by resveratrol, a phytostilbene. Exp. Neurol. 229, 399-408.
26. Messam C. A., and, Major E. O., (2000) Stages of restricted HIV-1 infection in astrocyte cultures derived from human fetal brain tissue. J. Neurovirol. 6 (Suppl 1), S90-S94.
27. Miller T. I., Borkowsky W., DiMeglio L. A., et al,. (2012) Metabolic abnormalities and viral replication are associated with biomarkers of vascular dysfunction in HIV-infected children. HIV Med. 13, 264-275.
28. Mishra M., Vetrivel S., Siddappa N. B., Ranga U., and, Seth P., (2008) Clade-specific differences in neurotoxicity of human immunodeficiency virus-1 B and C Tat of human neurons: significance of dicysteine C30C31 motif. Ann. Neurol. 63, 366-376.
29. Mocchetti I., Bachis A., and, Avdoshina V., (2012) Neurotoxicity of human immunodeficiency virus-1: viral proteins and axonal transport. Neurotox. Res. 21, 79-89.
30. Muratori C., Mangino G., Affabris E., and, Federico M., (2010) Astrocytes contacting HIV-1-infected macrophages increase the release of CCL2 in response to the HIV-1-dependent enhancement of membrane-associated TNFalpha in macrophages. Glia 58, 1893-1904.
31. Nath A., (2002) Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J. Infect. Dis. 186 (Suppl 2), S193-S198.
32. Neary J. T., Kang Y., Willoughby K. A., and, Ellis E. F., (2003) Activation of extracellular signal-regulated kinase by stretch-induced injury in astrocytes involves extracellular ATP and P2 purinergic receptors. J. Neurosci. 23, 2348-2356.
33. Nishida K., Nakatani T., Ohishi A., Okuda H., Higashi Y., Matsuo T., Fujimoto S., and, Nagasawa K., (2012) Mitochondrial dysfunction is involved in P2X7 receptor-mediated neuronal cell death. J. Neurochem. 122, 1118-1128.
34. Panenka W., Jijon H., Herx L. M., Armstrong J. N., Feighan D., Wei T., Yong V. W., Ransohoff R. M., and, MacVicar B. A., (2001) P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J. Neurosci. 21, 7135-7142.
35. Parvathenani L. K., Tertyshnikova S., Greco C. R., Roberts S. B., Robertson B., and, Posmantur R., (2003) P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J. Biol. Chem. 278, 13309-13317.
36. Peng W., Cotrina M. L., Han X., Yu H., Bekar L., Blum L., Takano T., Tian G. F., Goldman S. A., and, Nedergaard M., (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc. Natl Acad. Sci. USA 106, 12489-12493.
37. Sanz J. M., Chiozzi P., Ferrari D., Colaianna M., Idzko M., Falzoni S., Fellin R., Trabace L., and, Di Virgilio F., (2009) Activation of microglia by amyloid beta requires P2X7 receptor expression. J. Immunol. 182, 4378-4385.
38. Seror C., Melki M. T., Subra F., et al,. (2011) Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J. Exp. Med. 208, 1823-1834.
39. Shi B., De Girolami U., He J., Wang S., Lorenzo A., Busciglio J., and, Gabuzda D., (1996) Apoptosis induced by HIV-1 infection of the central nervous system. J. Clin. Invest. 98, 1979-1990.
40. Shieh C. H., Heinrich A., Serchov T., van Calker D., and, Biber K., (2014) P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-alpha in cultured mouse microglia. Glia 62, 592-607.
41. Shiramizu B., Lau E., Tamamoto A., Uniatowski J., and, Troelstrup D., (2006) Feasibility assessment of cerebrospinal fluid from HIV-1-infected children for HIV proviral DNA and monocyte chemoattractant protein 1 alleles. J. Investig. Med. 54, 468-472.
42. Siddappa N. B., Venkatramanan M., Venkatesh P., Janki M. V., Jayasuryan N., Desai A., Ravi V., and, Ranga U., (2006) Transactivation and signaling functions of Tat are not correlated: biological and immunological characterization of HIV-1 subtype-C Tat protein. Retrovirology 3, 53.
43. Singh I. N., Goody R. J., Dean C., Ahmad N. M., Lutz S. E., Knapp P. E., Nath A., and, Hauser K. F., (2004) Apoptotic death of striatal neurons induced by human immunodeficiency virus-1 Tat and gp120: Differential involvement of caspase-3 and endonuclease G. J. Neurovirol. 10, 141-151.
44. Skaper S. D., Debetto P., and, Giusti P., (2010) The P2X7 purinergic receptor: from physiology to neurological disorders. FASEB J. 24, 337-345.
45. Sorrell M. E., and, Hauser K. F., (2014) Ligand-gated purinergic receptors regulate HIV-1 Tat and morphine related neurotoxicity in primary mouse striatal neuron-glia co-cultures. J. Neuroimmune Pharmacol. 9, 233-244.
46. Suadicani S. O., Brosnan C. F., and, Scemes E., (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2 + signaling. J. Neurosci. 26, 1378-1385.
47. Thompson K. A., McArthur J. C., and, Wesselingh S. L., (2001) Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia. Ann. Neurol. 49, 745-752.
48. Tovar Y. R. L. B., Kolson D. L., Bandaru V. V., Drewes J. L., Graham D. R., and, Haughey N. J., (2013) Adenosine triphosphate released from HIV-infected macrophages regulates glutamatergic tone and dendritic spine density on neurons. J. Neuroimmune Pharmacol. 8, 998-1009.
49. Volonte C., Apolloni S., Skaper S. D., and, Burnstock G., (2012) P2X7 receptors: channels, pores and more. CNS Neurol. Disord. Drug. Targets 11, 705-721.
50. Weiss J. M., Nath A., Major E. O., and, Berman J. W., (1999) HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J. Immunol. 163, 2953-2959.
51. Zhou B. Y., Liu Y., Kim B., Xiao Y., and, He J. J., (2004) Astrocyte activation and dysfunction and neuron death by HIV-1 Tat expression in astrocytes. Mol. Cell. Neurosci. 27, 296-305.