Human immunodeficiency virus-1/surface glycoprotein 120 induces apoptosis through RNA-activated protein kinase signaling in neurons

Journal of Neuroscience

Volumn 27, Issue 41, 2007, Pages 11047-11055

  Alirezaei, Mehrdad ^a   Watry, Debbie D ^a   Flynn, Claudia F ^a   Kiosses, William B ^a   Masliah, Eliezer ^b   Williams, Bryan R G ^c   Kaul, Marcus ^d   Lipton, Stuart A ^b,d   Fox, Howard S ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MONASH UNIVERSITY   (Australia)

^d BURNHAM INSTITUTE   (United States)

Author keywords

Apoptosis; Caspase 3; gp120; Neurodegeneration; PACT; PKR

Indexed keywords

CASPASE 3; DIZOCILPINE; DOUBLE STRANDED RNA; GLYCOPROTEIN GP 120; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN TISSUE; CELL CULTURE; CELL NUCLEUS; CONTROLLED STUDY; DEMENTIA; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN TISSUE; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ADULT; AIDS DEMENTIA COMPLEX; ANIMALS; APOPTOSIS; CELLS, CULTURED; EIF-2 KINASE; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 35348892709     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2733-07.2007     Document Type: Article

References (50)

1. Bagetta G, Corasaniti MT, Aloe L, Berliocchi L, Costa N, Finazzi-Agro A, Nistico G (1996) Intracerebral injection of human immunodeficiency virus type 1 coat protein gp120 differentially affects the expression of nerve growth factor and nitric oxide synthase in the hippocampus of rat. Proc Natl Acad Sci USA 93:928-933.
2. Balachandran S, Kim CN, Yeh WC, Mak TW, Bhalla K, Barber GN (1998) Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J 17:6888-6902.
3. Bando Y, Onuki R, Katayama T, Manabe T, Kudo T, Taira K, Tohyama M (2005) Double-strand RNA dependent protein kinase (PKR) is involved in the extrastriatal degeneration in Parkinson's disease and Huntington's disease. Neurochem Int 46:11-18.
4. Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF (2000) PKR stimulates NF-kappaB irrespective of its kinase function by interacting with the IkappaB kinase complex. Mol Cell Biol 20:4532-4542.
5. Bonnet MC, Daurat C, Ottone C, Meurs EF (2006) The N-terminus of PKR is responsible for the activation of the NF-kappaB signaling pathway by interacting with the IKK complex. Cell Signal 18:1865-1875.
6. Brenneman DE, Westbrook GL, Fitzgerald SP, Ennist DL, Elkins KL, Ruff MR, Pert CB (1988) Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature 335:639-642.
7. Chang RC, Wong AK, Ng HK, Hugon J (2002a) Phosphorylation of eukaryotic initiation factor-2alpha (eIF2alpha) is associated with neuronal degeneration in Alzheimer's disease. NeuroReport 13:2429-2432.
8. Chang RC, Suen KC, Ma CH, Elyaman W, Ng HK, Hugon J (2002b) Involvement of double-stranded RNA-dependent protein kinase and phosphorylation of eukaryotic initiation factor-2alpha in neuronal degeneration. J Neurochem 83:1215-1225.
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. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70:1032-1060.
11. 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.
12. Garden GA, Guo W, Jayadev S, Tun C, Balcaitis S, Choi J, Montine TJ, Moller T, Morrison RS (2004) HIV associated neurodegeneration requires p53 in neurons and microglia. FASEB J 18:1141-1143.
13. Gilbert SJ, Duance VC, Mason DJ (2002) Tumour necrosis factor alpha upregulates protein kinase R (PKR)-activating protein (PACT) and increases phosphorylation of PKR and eukaryotic initiation factor 2-alpha in articular chondrocytes. Biochem Soc Trans 30:886-889.
14. Haughey NJ, Mattson MP (2002) Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 31 [Suppl 2]:S55-S61.
15. Hu JH, Zhang H, Wagey R, Krieger C, Pelech SL (2003) Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord. J Neurochem 85:432-442.
16. Huang S, Qu LK, Cuddihy AR, Ragheb R, Taya Y, Koromilas AE (2003) Protein kinase inhibitor 2-aminopurine overrides multiple genotoxic stress-induced cellular pathways to promote cell survival. Oncogene 22:3721-3733.
17. Iwamura T, Yoneyama M, Koizumi N, Okabe Y, Namiki H, Samuel CE, Fujita T (2001) PACT, a double-stranded RNA binding protein acts as a positive regulator for type I interferon gene induced by Newcastle disease virus. Biochem Biophys Res Commun 282:515-523.
18. Jagus R, Joshi B, Barber GN (1999) PKR, apoptosis and cancer. Int J Biochem Cell Biol 31:123-138.
19. Jammi NV, Whitby LR, Beal PA (2003) Small molecule inhibitors of the RNA-dependent protein kinase. Biochem Biophys Res Commun 308:50-57.
20. Kaul M, Lipton SA (1999) Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci USA 96:8212-8216.
21. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988-994.
22. 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.
23. Khan MZ, Brandimarti R, Musser BJ, Resue DM, Fatatis A, Meucci O (2003) The chemokine receptor CXCR4 regulates cell-cycle proteins in neurons. J Neurovirol 9:300-314.
24. 2+]i homeostasis and induce neurotoxicity in human embryonic neurons. Eur J Neurosci 7:2285-2293.
25. 2+ prevents neurotoxicity. Brain Res 598:196-202.
26. Lipton SA, Gendelman HE (1995) Seminars in medicine of the Beth Israel Hospital, Boston. Dementia associated with the acquired immunodeficiency syndrome. N Engl J Med 332:934-940.
27. Lipton SA, Sucher NJ, Kaiser PK, Dreyer EB (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111-118.
28. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12 [Suppl 1]:893-904.
29. McArthur JC, Brew BJ, Nath A (2005) Neurological complications of HIV infection. Lancet Neurol 4:543-555.
30. 2+]i and the toxic actions of the HIV coat protein gp120. Eur J Neurosci 11:1167-1178.
31. 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.
32. Onuki R, Bando Y, Suyama E, Katayama T, Kawasaki H, Baba T, Tohyama M, Taira K (2004) An RNA-dependent protein kinase is involved in tunicamycin-induced apoptosis and Alzheimer's disease. EMBO J 23:959-968.
33. Patel RC, Sen GC (1998) PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J 17:4379-4390.
34. Peel AL (2004) PKR activation in neurodegenerative disease. J Neuropathol Exp Neurol 63:97-105.
35. Peel AL, Bredesen DE (2003) Activation of the cell stress kinase PKR in Alzheimer's disease and human amyloid precursor protein transgenic mice. Neurobiol Dis 14:52-62.
36. Peel AL, Rao RV, Cottrell BA, Hayden MR, Ellerby LM, Bredesen DE (2001) Double-stranded RNA-dependent protein kinase, PKR, binds preferentially to Huntington's disease (HD) transcripts and is activated in HD tissue. Hum Mol Genet 10:1531-1538.
37. Peters GA, Hartmann R, Qin J, Sen GC (2001) Modular structure of PACT: distinct domains for binding and activating PKR. Mol Cell Biol 21:1908-1920.
38. Prostko CR, Dholakia JN, Brostrom MA, Brostrom CO (1995) Activation of the double-stranded RNA-regulated protein kinase by depletion of endoplasmic reticular calcium stores. J Biol Chem 270:6211-6215.
39. Scheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3:211-216.
40. Scheuner D, Patel R, Wang F, Lee K, Kumar K, Wu J, Nilsson A, Karin M, Kaufman RJ (2006) Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 281:21458-21468.
41. Shimazawa M, Hara H (2006) Inhibitor of double stranded RNA-dependent protein kinase protects against cell damage induced by ER stress. Neurosci Lett 409:192-195.
42. Srivastava SP, Kumar KU, Kaufman RJ (1998) Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J Biol Chem 273:2416-2423.
43. Suen KC, Yu MS, So KF, Chang RC, Hugon J (2003) Upstream signaling pathways leading to the activation of double-stranded RNA-dependent serine/threonine protein kinase in beta-amyloid peptide neurotoxicity. J Biol Chem 278:49819-49827.
44. Takada Y, Ichikawa H, Pataer A, Swisher S, Aggarwal BB (2007) Genetic deletion of PKR abrogates TNF-induced activation of IkappaBalpha kinase, JNK, Akt and cell proliferation but potentiates p44/p42 MAPK and p38 MAPK activation. Oncogene 26:1201-1212.
45. Takizawa T, Tatematsu C, Watanabe M, Yoshida M, Nakajima K (2000) Three leucine-rich sequences and the N-terminal region of double-stranded RNA-activated protein kinase (PKR) are responsible for its cytoplasmic localization. J Biochem (Tokyo) 128:471-476.
46. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188-193.
47. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, Lipton SA (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:513-517.
48. Williams BR (1999) PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120.
49. Yang YL, Reis LF, Pavlovic J, Aguzzi A, Schafer R, Kumar A, Williams BR, Aguet M, Weissmann C (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J 14:6095-6106.
50. Yeung MC, Liu J, Lau AS (1996) An essential role for the interferon-inducible, double-stranded RNA-activated protein kinase PKR in the tumor necrosis factor-induced apoptosis in U937 cells. Proc Natl Acad Sci USA 93:12451-12455.