Involvement of miR-196a in HIV-associated neurocognitive disorders

Apoptosis

Volumn 19, Issue 8, 2014, Pages 1202-1214

  Bagashev, Asen ^a   Mukerjee, Ruma ^a   Santerre, Maryline ^a   Del Carpio Cano, Fabiola E ^a   Shrestha, Jenny ^a   Wang, Ying ^a   He, Johnny J ^b   Sawaya, Bassel E ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

c Abl; HIV 1 Tat; miR 196a; Neuronal degeneration; p73

Indexed keywords

MICRORNA; MICRORNA 196A; PROTEIN P53; PROTEIN P73; RETINOBLASTOMA PROTEIN; TRANSACTIVATOR PROTEIN; TYROSINE; UNCLASSIFIED DRUG; ABELSON KINASE; DNA BINDING PROTEIN; MIRN196 MICRORNA, HUMAN; NUCLEAR PROTEIN; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73;

ABELSON MURINE LEUKEMIA ONCOVIRUS; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN DYSFUNCTION; CELL DEATH; CELL VIABILITY ASSAY; DEREGULATION; HIV ASSOCIATED DEMENTIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; C57BL MOUSE; CELL SURVIVAL; COGNITION DISORDERS; COMPLICATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; NERVE CELL; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE;

ANIMALS; APOPTOSIS; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; COGNITION DISORDERS; DNA-BINDING PROTEINS; HIV INFECTIONS; HIV-1; HUMANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; NEURONS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-ABL; RETINOBLASTOMA PROTEIN; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84904256518     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1003-2     Document Type: Article

References (63)

1. Zucchini S, Pittaluga A, Brocca-Cofano E, Summa M, Fabris M, De Michele R et al (2013) Increased excitability in tat-transgenic mice: role of tat in HIV-related neurological disorders. Neurobiol Dis 55:110-119
2. Fitting S, Ignatowska-Jankowska BM, Bull C, Skoff RP, Lichtman AH, Wise LE et al (2013) Synaptic dysfunction in the hippocampus accompanies learning and memory deficits in human immunodeficiency virus type-1 Tat transgenic mice. Biol Psychiatry 73:443-453
3. Hahn YK, Vo P, Fitting S, Block ML, Hauser KF, Knapp PE (2010) beta-Chemokine production by neural and glial progenitor cells is enhanced by HIV-1 Tat: effects on microglial migration. J Neurochem 114:97-109
4. Chang JR, Mukerjee R, Bagashev A, Del Valle L, Chabrashvili T, Hawkins BJ et al (2011) HIV-1 Tat protein promotes neuronal dysfunction through disruption of microRNAs. J Biol Chem 286:41125-41134
5. Arese M, Ferrandi C, Primo L, Camussi G, Bussolino F (2001) HIV-1 Tat protein stimulates in vivo vascular permeability and lymphomononuclear cell recruitment. J Immunol 166:1380-1388 (Pubitemid 32060301)
6. Rayne F, Debaisieux S, Yezid H, Lin YL, Mettling C, Konate K et al (2010) Phosphatidylinositol-(4,5)-bisphosphate enables efficient secretion of HIV-1 Tat by infected T-cells. EMBO J 29:1348-1362
7. Debaisieux S, Rayne F, Yezid H, Beaumelle B (2012) The ins and outs of HIV-1 Tat. Traffic 13:355-363
8. Tryoen-Tóth P, Chasserot-Golaz S, Tu A, Gherib P, Bader MF, Beaumelle B et al (2013) HIV-1 Tat protein inhibits neurosecretion by binding to phosphatidylinositol 4,5-bisphosphate. J Cell Sci 126:454-463
9. Norman JP, Perry SW, Kasischke KA, Volsky DJ, Gelbard HA (2007) HIV-1 trans activator of transcription protein elicits mitochondrial hyperpolarization and respiratory deficit, with dysregulation of complex IV and nicotinamide adenine dinucleotide homeostasis in cortical neurons. J Immunol 178:869-876 (Pubitemid 46095159)
10. Hui L, Chen X, Haughey NJ, Geiger JD (2012) Role of endolysosomes in HIV-1 Tat-induced neurotoxicity. ASN Neuro 4:243-252
11. Garden GA, Guo W, Jayadev S, Tun C, Balcaitis S, Choi J et al (2004) HIV associated neurodegeneration requires p53 in neurons and microglia. FASEB J 18:1141-1143 (Pubitemid 39561550)
12. Mukerjee R, Deshmane SL, Fan S, Del Valle L, White MK, Khalili K et al (2008) Involvement of the p53 and p73 transcription factors in neuroAIDS. Cell Cycle 7:2682-2690
13. Mukerjee R, Claudio PP, Chang JR, Del Valle L, Sawaya BE (2010) Transcriptional regulation of HIV-1 gene expression by p53. Cell Cycle 9:4569-4578
14. Sabatier JM, Vives E, Mabrouk K, Benjouad A, Rochat H, Duval A et al (1991) Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J Virol 65:961-967
15. Carey AN, Liu X, Mintzopoulos D, Paris JJ, Muschamp JW, McLaughlin JP, Kaufman MJ (2013) Conditional Tat protein expression in the GT-tg bigenic mouse brain induces gray matter density reductions. Prog Neuropsychopharmacol Biol Psychiatry 43:49-54
16. Li ST, Matsushita M, Moriwaki A, Saheki Y, Lu YF, Tomizawa K, Wu HY, Terada H, Matsui H (2004) HIV-1 Tat inhibits longterm potentiation and attenuates spatial learning (vol 54, pp 362, 2004). Ann Neurol 55:758 (Pubitemid 38544343)
17. Joerger AC, Rajagopalan S, Natan E, Veprintsev DB, Robinson CV, Fersht AR (2009) Structural evolution of p53, p63, and p73: implication for heterotetramer formation. Proc Nat Acad Sci USA 106:17705-17710
18. Melino G, Lu X, Gasco M, Crook T, Knight RA (2003) Functional regulation of p73 and p63: development and cancer. Trends Biochem Sci 28:663-670 (Pubitemid 37500901)
19. Flores ER, Tsai KY, Crowley D, Sengupta S, Yang A, McKeon F, Jacks T (2002) p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416:560-564 (Pubitemid 34288861)
20. Rossi M, De Laurenzi V, Munarriz E, Green DR, Liu YC, Vousden KH, Cesareni G, Melino G (2005) The ubiquitin-protein ligase Itch regulates p73 stability. EMBO J 24:836-848 (Pubitemid 40396112)
21. Grob TJ, Novak U, Maisse C, Barcaroli D, Lüthi AU, Pirnia F et al (2001) Human Delta Np73 regulates a dominant negative feedback loop for TAp73 and p53. Cell Death Differ 8:1213-1223 (Pubitemid 34048476)
22. Moll UM, Slade N (2004) p63 and p73: roles in development and tumor formation. Mol Cancer Res 2:371-386 (Pubitemid 39031071)
23. Murray-Zmijewski F, Lane DP, Bourdon JC (2006) p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress. Cell Death Differ 13:962-972
24. Ensoli B, Buonaguro L, Barillari G, Fiorelli V, Gendelman R, Morgan RA, Wingfield P, Gallo RC (1993) Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 67:277-287 (Pubitemid 23002988)
25. Kashanchi F, Piras G, Radonovich MF, Duvall JF, Chiang C-M, Roeder RG, Brady JN (1994) Interaction of human TFIID with the HIV-1 transactivator Tat. Nature 367:295-299
26. Kim BO, Liu Y, Ruan Y, Xu ZC, Schantz L, He JJ (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162:1693-1707 (Pubitemid 36512853)
27. Sawaya BE, Khalili K, Mercer WE, Denisova L, Amini S (1998) Cooperative actions of HIV-1 Vpr and p53 modulate viral gene transcription. J Biol Chem 273:20052-20057 (Pubitemid 28377557)
28. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20 (Pubitemid 40094598)
29. Amini S, Mameli G, Del Valle L, Skowronska A, Reiss K, Gelman BB, White MK, Khalili K, Sawaya BE (2005) p73 interacts with human immunodeficiency virus type 1 Tat in astrocytic cells and prevents its acetylation on lysine 28. Mol Cell Biol 25:8126-8138 (Pubitemid 41263005)
30. Liu J, Uematsu H, Tsuchida N, Ikeda M-A (2011) Essential role of caspase-8 in p53/p73-dependent apoptosis induced by etoposide in head and neck carcinoma cells. Mol Cancer 10:95
31. Tsai KKC, Yuan ZM (2003) c-Abl stabilizes p73 by a phosphorylation- augmented interaction. Cancer Res 63:3418-3424 (Pubitemid 36735903)
32. Codelia VA, Cisterna M, Alvarez AR, Moreno RD (2010) p73 participates in male germ cells apoptosis induced by etoposide. Mol Hum Reprod 16:734-742
33. Costanzo A, Merlo P, Pediconi N, Fulco M, Sartorelli V, Cole PA et al (2002) DNA damage-dependent acetylation of p73 dictates the selective activation of apoptotic target genes. Mol Cell 9:175-186 (Pubitemid 34127781)
34. Zhao B, Li L, Lei Q, Guan KL (2010) The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 24:862-874
35. Nagano K, Itagaki C, Izumi T, Nunomura K, Soda Y, Tani K, Takahashi N, Takenawa T, Isobe T (2006) Rb plays a role in survival of Abl-dependent human tumor cells as a downstream effector of Abl tyrosine kinase. Oncogene 25:493-502 (Pubitemid 43164460)
36. Logotheti S, Michalopoulos I, Sideridou M, Daskalos A, Kossida S, Spandidos DA et al (2010) Sp1 binds to the external promoter of the p73 gene and induces the expression of TAp73 gamma in lung cancer. FEBS J 277:3014-3027
37. Sudhakar C, Jain N, Swarup G (2008) Sp1-like sequences mediate human caspase-3 promoter activation by p73 and cisplatin. FEBS J 275:2200-2213 (Pubitemid 351569559)
38. Corn PG, Kuerbitz SJ, van Noesel MM, Esteller M, Compitello N, Baylin SB, Herman JG (1999) Transcriptional silencing of the p73 gene in acute lymphoblastic leukemia and Burkitt's lymphoma is associated with 5′ CpG island methylation. Cancer Res 59:3352-3356 (Pubitemid 29334490)
39. Liu K, Zhan M, Zheng P (2008) Loss of p73 expression in six non-small cell lung cancer cell lines is associated with 5′ CPG island methylation. Exp Mol Pathol 84:59-63 (Pubitemid 351163262)
40. Chouliaras L, Mastroeni D, Delvaux E, Grover A, Kenis G, Hof PR et al (2013) Consistent decrease in global DNA methylation and hydroxymethylation in the hippocampus of Alzheimer's disease patients. Neurobiol Aging 34:2091-2099
41. Kriaucionis S, Heintz N (2009) The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324:929-930
42. Guo JU, Su Y, Zhong C, Ming G-I, Song H (2011) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145:423-434
43. Jin S-G, Wu X, Li AX, Pfeifer GP (2011) Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res 39:5015-5024
44. Valinluck V, Sowers LC (2007) Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res 67:946-950
45. Wu H, Zhang Y (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25:2436-2452
46. Bagashev A, Fan S, Mukerjee R, Claudio PP, Chabrashvili T, Leng RP, Benchimol S, Sawaya BE (2013) Cdk9 phosphorylates Pirh2 protein and prevents degradation of p53 protein. Cell Cycle 12:1569-1577
47. Saunders M, Eldeen MB, Del Valle L, Reiss K, Peruzzi F, Mameli G et al (2005) p73 modulates HIV-1 Tat transcriptional and apoptotic activities in human astrocytes. Apoptosis 10:1419-1431 (Pubitemid 43117686)
48. Alvarez AR, Sandoval PC, Leal NR, Castro PU, Kosik KS (2004) Activation of the neuronal c-Abl tyrosine kinase by amyloid-betapeptide and reactive oxygen species. Neurobiol Dis 17:326-336 (Pubitemid 39345788)
49. Yuan ZM, Shioya H, Ishiko T, Sun X, Gu J, Huang YY et al (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage (vol 399, p 814, 1999). Nature 400:792 (Pubitemid 29399544)
50. Duan M, Yao H, Hu G, Chen X, Lund AK, Buch S (2013) HIV Tat induces expression of ICAM-1 in HUVECs: implications for miR-221/-222 in HIV-associated cardiomyopathy. PLoS One 8:e60170
51. Mishra R, Singh SK (2013) HIV-1 Tat C modulates expression of miRNA-101 to suppress VE-cadherin in human brain microvascular endothelial cells. J Neurosci 33:5992-6000
52. Zhang H-S, Chen X-Y, Wu T-C, Sang W-W, Ruan Z (2012) MiR-34a is involved in Tat-induced HIV-1 long terminal repeat (LTR) transactivation through the SIRT1/NF kappa B pathway. FEBS Lett 586:4203-4207
53. Zhang H-S, Wu T-C, Sang W-W, Ruan Z (2012) MiR-217 is involved in Tat-induced HIV-1 long terminal repeat (LTR) transactivation by down-regulation of SIRT1. Biochem Biophys Acta 1823:1017-1023
54. Chen X-Y, Zhang H-S, Wu T-C, Sang W-W, Ruan Z (2013) Down-regulation of NAMPT expression by miR-182 is involved in Tat-induced HIV-1 long terminal repeat (LTR) transactivation. Int J Biochem Cell Biol 45:292-298
55. Eletto D, Russo G, Passiatore G, Del Valle L, Giordano A, Khalili K, Gualco E, Peruzzi F (2008) Inhibition of SNAP25 expression by HIV-1 Tat involves the activity of mir-128a. J Cell Physiol 216:764-770
56. Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H et al (2012) Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis 3:381
57. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457-467 (Pubitemid 32729974)
58. Song L, Nath A, Geiger JD, Moore A, Hochman S (2003) Human immunodeficiency virus type 1 Tat protein directly activates neuronal N-methyl-D-aspartate receptors at an allosteric zinc-sensitive site. J Neurovirol 9:399-403 (Pubitemid 36874714)
59. Eugenin EA, King JE, Nath A, Calderon TM, Zukin RS, Bennett MV, Berman JW (2007) HIV-tat induces formation of an LRP-PSD-95-NMDAR-nNOS complex that promotes apoptosis in neurons and astrocytes. Proc Natl Acad Sci USA 104:3438-3443 (Pubitemid 46364177)
60. Aksenov MY, Aksenova MV, Mactutus CF, Booze RM (2012) D1/NMDA receptors and concurrent methamphetamine+HIV-1 Tat neurotoxicity. J Neuroimmune Pharmacol 7:599-608
61. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N et al (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26:731-743 (Pubitemid 46856247)
62. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH et al (2007) Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26:745-752 (Pubitemid 46856245)
63. Agostini M, Tucci P, Killick R, Candi E, Sayan BS, di Val Cervo PR et al (2011) Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proc Natl Acad Sci USA 108:21093-21098