PTEN gene silencing prevents HIV-1 gp120IIIB-induced degeneration of striatal neurons

Journal of NeuroVirology

Volumn 17, Issue 1, 2011, Pages 41-49

  Zou, Shiping ^a   El Hage, Nazira ^a   Podhaizer, Elizabeth M ^a   Knapp, Pamela E ^a   Hauser, Kurt F ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Akt protein kinase B; Apoptosis; Neuro acquired immunodeficiency syndrome (neuroAIDS); Regulated cell death; SiRNA

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; FOCAL ADHESION KINASE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 120 IIIB; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RECOMBINANT GLYCOPROTEIN GP 120; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMOSOME 10; CONTROLLED STUDY; CORPUS STRIATUM; EMBRYO; ENZYME ACTIVITY; GENE CASSETTE; GENE SILENCING; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; NONVIRAL GENE THERAPY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RNA INTERFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CELLS, CULTURED; GENE SILENCING; HIV ENVELOPE PROTEIN GP120; HIV-1; MICE; MICE, INBRED ICR; NEOSTRIATUM; NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTORS, CCR5; RECEPTORS, CXCR4; RNA, SMALL INTERFERING;

HUMAN IMMUNODEFICIENCY VIRUS 1; RODENTIA;

EID: 79952982191     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-010-0016-z     Document Type: Article

References (68)

1. Bachis A, Major EO, Mocchetti I (2003) Brain-derived neurotrophic factor inhibits human immunodeficiency virus-1/gp120-mediated cerebellar granule cell death by preventing gp120 internalization. J Neurosci 23:5715-5722 (Pubitemid 36807850)
2. Bachis A, Biggio F, Major EO, Mocchetti I (2009) M-and T-tropic HIVs promote apoptosis in rat neurons. J Neuroimmune Pharmacol 4:150-160
3. Bakalkin G, Watanabe H, Jezierska J, Depoorter C, Verschuuren-Bemelmans C, Bazov I, Artemenko KA, Yakovleva T, Dooijes D, Van de Warrenburg BPC, Zubarev RA, Kremer B, Knapp PE, Hauser KF, Wijmenga C, Nyberg F, Sinke RJ, Verbeek DS (2010) Prodynorphin mutations cause the neurodegenerative disorder spinocerebellar ataxia type 23. Am J Hum Genet 87:593-603
4. Barry FA, Gibbins JM (2002) Protein kinase B is regulated in platelets by the collagen receptor glycoprotein VI. J Biol Chem 277:12874-12878 (Pubitemid 34952653)
5. Benos DJ, Hahn BH, Bubien JK, Ghosh SK, Mashburn NA, Chaikin MA, Shaw GM, Benveniste EN (1994) Envelope glycoprotein gp120 of human immunodeficiency virus type 1 alters ion transport in astrocytes: implications for AIDS dementia complex. Proc Natl Acad Sci USA 91:494-498 (Pubitemid 24041428)
6. Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17(657-700):657-700 (Pubitemid 29241137)
7. Bhattacharya J, Peters PJ, Clapham PR (2003) CD4-independent infection of HIV and SIV: implications for envelope conformation and cell tropism in vivo. AIDS 17(Suppl 4): S35-S43
8. Degtyarev M, De MA, Orr C, Lin J, Lee BB, Tien JY, Prior WW, van Dijk S, Wu H, Gray DC, Davis DP, Stern HM, Murray LJ, Hoeflich KP, Klumperman J, Friedman LS, Lin K (2008) Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 183:101-116
9. Dreyer EB, Kaiser PK, Offermann JT, Lipton SA (1990) HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364-367
10. Endo H, Nito C, Kamada H, Nishi T, Chan PH (2006) Activation of the Akt/GSK3beta signaling pathway mediates survival of vulnerable hippocampal neurons after transient global cerebral ischemia in rats. J Cereb Blood Flow Metab 26:1479-1489 (Pubitemid 44809077)
11. Everall IP, Bell C, Mallory M, Langford D, Adame A, Rockestein E, Masliah E (2002) Lithium ameliorates HIV-gp120-mediated neurotoxicity. Mol Cell Neurosci 21:493-501 (Pubitemid 36062734)
12. Francois F, Klotman ME (2003) Phosphatidylinositol 3-kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4+ T lymphocytes and macrophages. J Virol 77:2539-2549 (Pubitemid 36222778)
13. Freeman DJ, Li AG, Wei G, Li HH, Kertesz N, Lesche R, Whale AD, Martinez-Diaz H, Rozengurt N, Cardiff RD, Liu X, Wu H (2003) PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and-independent mechanisms. Cancer Cell 3:117-130 (Pubitemid 37443385)
14. Gabuzda D, Wang J (2000) Chemokine receptors and mechanisms of cell death in HIV neuropathogenesis. J Neurovirol 6(Suppl 1): S24-S32 (Pubitemid 30342774)
15. Gao T, Furnari F, Newton AC (2005) PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Mol Cell 18:13-24 (Pubitemid 40444644)
16. Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E, Lipton SA (2002) Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 22:4015-4024 (Pubitemid 37465710)
17. Garden GA, Guo W, Jayadev S, Tun C, Balcaitis S, Choi J, Montine TJ, Moller T, Morrison RS (2004) HIV associated neurodegen-eration requires p53 in neurons and microglia. FASEB J 18:1141-1143 (Pubitemid 39561550)
18. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69-81 (Pubitemid 40070332)
19. Hesselgesser J, Halks-Miller M, DelVecchio V, Peiper SC, Hoxie J, Kolson DL, Taub D, Horuk R (1997) CD4-independent association between HIV-1 gp120 and CXCR4: functional chemokine receptors are expressed in human neurons. Curr Biol 7:112-121 (Pubitemid 27155620)
20. Hesselgesser J, Taub D, Baskar P, Greenberg M, Hoxie J, Kolson DL, Horuk R (1998) Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 8:595-598 (Pubitemid 28222895)
21. Holden CP, Nath A, Haughey NJ, Geiger JD (1999) Involvement of Na+/H+ exchangers, Ca2+ channels, and excitatory amino acid receptors in intracellular Ca2+ responses to HIV-1 gp120 in cultured human fetal brain cells. Neuroscience 91:1369-1378
22. Hu S, Sheng WS, Lokensgard JR, Peterson PK (2005) Morphine potentiates HIV-1 gp120-induced neuronal apoptosis. J Infect Dis 191:886-889 (Pubitemid 40349803)
23. Huang MB, Bond VC (2000) Involvement of protein kinase C in HIV-1 gp120-induced apoptosis in primary endothelium. J Acquir Immune Defic Syndr 25:375-389 (Pubitemid 32055568)
24. Huang MB, Hunter M, Bond VC (1999) Effect of extracellular human immunodeficiency virus type 1 glycoprotein 120 on primary human vascular endothelial cell cultures. AIDS Res Hum Retroviruses 15:1265-1277 (Pubitemid 29449405)
25. Jordan CA, Watkins BA, Kufta C, Dubois-Dalcq M (1991) Infection of brain microglial cells by human immunodeficiency virus type 1 is CD4 dependent. J Virol 65:736-742
26. Kapasi AA, Fan S, Singhal PC (2001) Role of 14-3-3epsilon, c-Myc/Max, and Akt phosphorylation in HIV-1 gp 120-induced mesangial cell proliferation. Am J Physiol Renal Physiol 280: F333-F342
27. Kaul M, Lipton SA (1999) Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci USA 96:8212-8216 (Pubitemid 29328434)
28. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988-994 (Pubitemid 32335850)
29. Kaul M, Ma Q, Medders KE, Desai MK, Lipton SA (2007) HIV-1 coreceptors CCR5 and CXCR4 both mediate neuronal cell death but CCR5 paradoxically can also contribute to protection. Cell Death Differ 14:296-305 (Pubitemid 46092232)
30. Khan MZ, Brandimarti R, Patel JP, Huynh N, Wang J, Huang Z, Fatatis A, Meucci O (2004) Apoptotic and antiapoptotic effects of CXCR4: is it a matter of intrinsic efficacy? Implications for HIV neuropathogenesis. AIDS Res Hum Retrovir 20:1063-1071 (Pubitemid 39392011)
31. Kolson DL (2002) Neuropathogenesis of central nervous system HIV-1 infection. Clin Lab Med 22:703-717 (Pubitemid 35014996)
32. Kurose K, Zhou XP, Araki T, Cannistra SA, Maher ER, Eng C (2001) Frequent loss of PTEN expression is linked to elevated phosphorylated Akt levels, but not associated with p27 and cyclin D1 expression, in primary epithelial ovarian carcinomas. Am J Pathol 158:2097-2106 (Pubitemid 32545195)
33. Kurose K, Gilley K, Matsumoto S, Watson PH, Zhou XP, Eng C (2002) Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet 32:355-357 (Pubitemid 35266108)
34. Langford D, Hurford R, Hashimoto M, Digicaylioglu M, Masliah E (2005) Signalling crosstalk in FGF2-mediated protection of endothelial cells from HIV-gp120. BMC Neurosci 6(8):8
35. Lannuzel A, Lledo PM, Lamghitnia HO, Vincent JD, Tardieu M (1995) HIV-1 envelope proteins gp120 and gp160 potentiate NMDA-induced [Ca2+]i increase, alter [Ca2+]i homeostasis and induce neurotoxicity in human embryonic neurons. Eur J Neurosci 7:2285-2293
36. Lannuzel A, Barnier JV, Hery C, Huynh VT, Guibert B, Gray F, Vincent JD, Tardieu M (1997) Human immunodeficiency virus type 1 and its coat protein gp120 induce apoptosis and activate JNK and ERK mitogen-activated protein kinases in human neurons. Ann Neurol 42:847-856 (Pubitemid 28008414)
37. Lipton SA (1992) Memantine prevents HIV coat protein-induced neuronal injury in vitro. Neurology 42:1403-1405
38. Lipton SA (1994) HIV-related neuronal injury. Potential therapeutic intervention with calcium channel antagonists and NMDA antagonists. Mol Neurobiol 8:181-196
39. Lipton SA (1996) Similarity of neuronal cell injury and death in AIDS dementia and focal cerebral ischemia: potential treatment with NMDA open-channel blockers and nitric oxide-related species. Brain Pathol 6:507-517 (Pubitemid 26388720)
40. Lipton SA, Sucher NJ, Kaiser PK, Dreyer EB (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111-118
41. Madani N, Kozak SL, Kavanaugh MP, Kabat D (1998) gp120 envelope glycoproteins of human immunodeficiency viruses competitively antagonize signaling by coreceptors CXCR4 and CCR5. Proc Natl Acad Sci USA 95:8005-8010 (Pubitemid 28326056)
42. Medders KE, Sejbuk NE, Maung R, Desai MK, Kaul M (2010) Activation of p38 MAPK is required in monocytic and neuronal cells for HIV glycoprotein 120-induced neurotoxicity. J Immunol 185:4883-4895
43. Meucci O, Miller RJ (1996) gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-beta1. J Neurosci 16:4080-4088 (Pubitemid 26192404)
44. Meucci O, Fatatis A, Simen AA, Bushell TJ, Gray PW, Miller RJ (1998) Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc Natl Acad Sci USA 95:14500-14505 (Pubitemid 28549396)
45. Meucci O, Fatatis A, Simen AA, Miller RJ (2000) Expression of CX3CR1 chemokine receptors on neurons and their role in neuronal survival. Proc Natl Acad Sci USA 97:8075-8080 (Pubitemid 30460775)
46. Miyawaki T, Ofengeim D, Noh KM, Latuszek-Barrantes A, Hemmings BA, Follenzi A, Zukin RS (2009) The endogenous inhibitor of Akt, CTMP, is critical to ischemia-induced neuronal death. Nat Neurosci 12:618-626
47. Ning K, Pei L, Liao M, Liu B, Zhang Y, Jiang W, Mielke JG, Li L, Chen Y, El-Hayek YH, Fehlings MG, Zhang X, Liu F, Eubanks J, Wan Q (2004) Dual neuroprotective signaling mediated by downregulating two distinct phosphatase activities of PTEN. J Neurosci 24:4052-4060 (Pubitemid 38544231)
48. Ohagen A, Ghosh S, He J, Huang K, Chen Y, Yuan M, Osathanondh R, Gartner S, Shi B, Shaw G, Gabuzda D (1999) Apoptosis induced by infection of primary brain cultures with diverse human immunodeficiency virus type 1 isolates: evidence for a role of the envelope. J Virol 73:897-906 (Pubitemid 29036740)
49. Peng F, Dhillon N, Callen S, Yao H, Bokhari S, Zhu X, Baydoun HH, Buch S (2008a) Platelet-derived growth factor protects neurons against gp120-mediated toxicity. J Neurovirol 14:62-72 (Pubitemid 351314974)
50. Peng F, Dhillon NK, Yao H, Zhu X, Williams R, Buch S (2008b) Mechanisms of platelet-derived growth factor-mediated neuroprotection - implications in HIV dementia. Eur J Neurosci 28:1255-1264
51. Pulliam L, West D, Haigwood N, Swanson RA (1993) HIV-1 envelope gp120 alters astrocytes in human brain cultures. AIDS Res Hum Retroviruses 9:439-444 (Pubitemid 23186058)
52. Robinson B, Li Z, Nath A (2007) Nucleoside reverse transcriptase inhibitors and human immunodeficiency virus proteins cause axonal injury in human dorsal root ganglia cultures. J Neurovirol 13:160-167 (Pubitemid 46780091)
53. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM (2005) Phosphorylation and regulation ofAkt/PKB by the rictor-mTOR complex. Science 307:1098-1101 (Pubitemid 40262113)
54. Sato S, Fujita N, Tsuruo T (2002) Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J Biol Chem 277:39360-39367 (Pubitemid 35190909)
55. Singh IN, Goody RJ, Dean C, Ahmad NM, Lutz SE, Knapp PE, Nath A, Hauser KF (2004) Apoptotic death of striatal neurons induced by HIV-1 Tat and gp120: differential involvement of caspase-3 and endonuclease G. J Neurovirol 10:141-151 (Pubitemid 38868152)
56. Singh IN, El-Hage N, Campbell ME, Lutz SE, Knapp PE, Nath A, Hauser KF (2005) Differential involvement of p38 and JNK MAP kinases in HIV-1 Tat and gp120-induced apoptosis and neurite degeneration in striatal neurons. Neuroscience 135:781-790 (Pubitemid 41407741)
57. Stambolic V, MacPherson D, Sas D, Lin Y, Snow B, Jang Y, Benchimol S, Mak TW (2001) Regulation of PTEN transcription by p53. Mol Cell 8:317-325 (Pubitemid 32831549)
58. Tamura M, Gu J, Danen EH, Takino T, Miyamoto S, Yamada KM (1999) PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 274:20693-20703
59. Trushin SA, Algeciras-Schimnich A, Vlahakis SR, Bren GD, Warren S, Schnepple DJ, Badley AD (2007) Glycoprotein 120 binding to CXCR4 causes p38-dependent primary T cell death that is facilitated by, but does not require cell-associated CD4. J Immunol 178:4846-4853 (Pubitemid 46595266)
60. Wan Q, Douglas SD, Wang X, Kolson DL, O'Donnell LA, Ho WZ (2006) Morphine upregulates functional expression of neurokinin-1 receptor in neurons. J Neurosci Res 84:1588-1596 (Pubitemid 44683152)
61. Wang SI, Puc J, Li J, Bruce JN, Cairns P, Sidransky D, Parsons R (1997) Somatic mutations of PTEN in glioblastoma multiforme. Cancer Res 57:4183-4186 (Pubitemid 27413419)
62. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, Ghorpade A, Rothstein JD, Volsky DJ (2003) Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312:60-73 (Pubitemid 36918460)
63. Yi Y, Lee C, Liu QH, Freedman BD, Collman RG (2004) Chemokine receptor utilization and macrophage signaling by human immunodeficiency virus type 1 gp120: implications for neuropathogenesis. J Neurovirol 10:91-96, Suppl 1 (Pubitemid 38325099)
64. Yoo LI, Liu DW, Le VS, Bronson RT, Wu H, Yuan J (2006) Pten deficiency activates distinct downstream signaling pathways in a tissue-specific manner. Cancer Res 66:1929-1939
65. Zhang K, Rana F, Silva C, Ethier J, Wehrly K, Chesebro B, Power C (2003) Human immunodeficiency virus type 1 envelopemediated neuronal death: uncoupling of viral replication and neurotoxicity. J Virol 77:6899-6912 (Pubitemid 36666883)
66. Zhao TY, Zou SP, Alimova YV, Wang G, Hauser KF, Ghandour MS, Knapp PE (2006) Short interfering RNA-induced gene silencing is transmitted between cells from the mammalian central nervous system. J Neurochem 98:1541-1550 (Pubitemid 44200444)
67. Zhao T, Adams MH, Zou SP, El-Hage N, Hauser KF, Knapp PE (2007) Silencing the PTEN gene is protective against neuronal death induced by humanimmunodeficiency virus type1 Tat. JNeurovirol13:97-106 (Pubitemid 46780085)
68. Zheng J, Thylin MR, Ghorpade A, Xiong H, Persidsky Y, Cotter R, Niemann D, Che M, Zeng YC, Gelbard HA, Shepard RB, Swartz JM, Gendelman HE (1999) Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. J Neuroimmunol 98:185-200 (Pubitemid 29317545)