HIV and SIV induce alterations in CNS CaMKII expression and activation: A potential mechanism for cognitive impairment

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2776-2784

  Gupta, Ravi G ^a   Kelly, Kathleen M ^a   Helke, Kris L ^a,d   Queen, Suzanne E ^a   Karper, Jami M ^a   Dorsey, Jamie L ^a   Brice, Angela K ^a   Adams, Robert J ^a   Tarwater, Patrick M ^b   Kolson, Dennis L ^c   Mankowski, Joseph L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Paul L Foster School of Medicine   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; SYNAPTOPHYSIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BRAIN; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVATION; EXPOSURE; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MONOCYTE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS LOAD; ANIMAL; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; FRONTAL LOBE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS; METABOLISM; NERVE CELL; PATHOLOGY; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SYNAPSE; VIROLOGY;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; ENZYME ACTIVATION; FRONTAL LOBE; HIPPOCAMPUS; HIV; HIV INFECTIONS; HUMANS; MACACA MULATTA; NEURONS; RATS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SYNAPSES; SYNAPTOPHYSIN; VIRAL LOAD;

EID: 77953205890     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090809     Document Type: Article

References (47)

1. Foley J, Ettenhofer M, Wright M, Hinkin C: Emerging issues in the neuropsychology of HIV infection. Current HIV/AIDS Reports 2008, 5:204-211
2. McArthur JC: HIV dementia: an evolving disease. J Neuroimmunol 2004, 157:3-10
3. Grant I, Sacktor N, McArthur JC: HIV neurocognitive disorders. In The neurology of AIDS (ed 2). Gendelman HE, Grant I, Everall I, Lipton SA, Swindells S (Editors). New York: Oxford University Press, 2005. pp. 359-373
4. Heaton RK, Grant I, Butters N, White DA, Kirson D, Atkinson JH, McCutchan JA, Taylor MJ, Kelly MD, Ellis RJ, Wolfson T, Velin R, Marcotte TD, Hesselink JR, Jernigan TL, Chandler J, Wallace M, Abramson I: The HNRC 500 - Neuropsychology of HIV infection at different disease stages. J Int Neuropsychol Soc 1995, 1:231-251
5. Rippeth JD, Heaton RK, Carey CL, Marcotte TD, Moore DJ, Gonzalez R, Wolfson T, Grant I: Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. J Int Neuropsychol Soc 2004, 10:1-14
6. Masliah E: Mechanisms of synaptic dysfunction in Alzheimer's disease. Histol Histopathol 1995, 10:509-519
7. Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, Mallory M, Achim CL, McCutchan JA, Nelson JA, Atkinson JH, Grant I: Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HRNC Group. The HIV Neurobehavioral Research Center. Ann Neurol 1997, 42:963-972
8. Arnold SE: Contributions of neuropathology to understanding schizophrenia in late life. Harv Rev Psychiatry 2001, 9:69-76
9. Law AJ, Weickert CS, Hyde TM, Kleinman JE, Harrison PJ: Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines. Am J Psychiatry 2004, 161:1848-1855
10. Zink WE, Anderson E, Boyle J, Hock L, Rodriguez-Sierra J, Xiong H, Gendelman HE, Persidsky Y: Impaired spatial cognition and synaptic potentiation in a murine model of human immunodeficiency virus type 1 encephalitis. J Neurosci 2002, 22:2096-2105 (Pubitemid 35386510)
11. Weed MR, Gold LH, Polis I, Koob GF, Fox HS, Taffe MA: Impaired performance on a rhesus monkey neuropsychological testing battery following simian immunodeficiency virus infection. AIDS Res Hum Retroviruses 2004, 20:77-89
12. Miller P, Zhabotinsky AM, Lisman JE, Wang X-J: The Stability of a Stochastic CaMKII Switch: Dependence on the Number of Enzyme Molecules and Protein Turnover. PLoS Biol 2005, 3:e107
13. Lisman J, Schulman H, Cline H: The molecular basis of CaMKII function in synaptic and behavioral memory. Nat Rev Neurosci 2002, 3:175-190
14. Giese KP, Nikolai FB, Filipkowski RK, Silva AJ: Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 1998, 279:870-873
15. Glazewski S, Chen CM, Silva A, Fox K: Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex. Science 1996, 272:421-423 (Pubitemid 26138181)
16. Glazewski S, Giese KP, Silva A, Fox K: The role of alpha-CaMKII autophosphorylation in neocortical experience-dependent plasticity. Nat Neurosci 2000, 3:911-918
17. Frankland PW, O'Brien C, Ohno M, Kirkwood A, Silva A: Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 2001, 411:309-313
18. O'Donnell LA, Agrawal A, Jordan-Sciutto KL, Dichter MA, Lynch DR, Kolson DL: Human immunodeficiency virus (HIV)-induced neurotoxicity: roles for the NMDA receptor subtypes. J Neurosci 2006, 26:981-990
19. Wilcox KS, Buchhalter J, Dichter MA: Properties of inhibitory and excitatory synapses between hippocampal neurons in very low-density cultures. Synapse 1994, 18:128-151
20. Zink MC, Suryanarayana K, Mankowski JL, Shen A, Piatak M Jr, Spelman JP, Carter DL, Adams RJ, Lifson JD, Clements JE: High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 1999, 73:10480-10488
21. Mankowski JL, Queen SE, Kirstein LM, Spelman JP, Laterra J, Simpson IA, Adams RJ, Clements JE, Zink MC: Alterations in blood-brain barrier glucose transport in SIV-infected macaques. J Neurovirol 1999, 5:695-702 (Pubitemid 30032095)
22. Mankowski JL, Queen SE, Tarwater PJ, Adams RJ, Guilarte TR: Elevated peripheral benzodiazepine receptor expression in simian immunodeficiency virus encephalitis. J Neurovirol 2003, 9:94-100
23. Chen W, Sulcove J, Frank I, Jaffer S, Ozdener H, Kolson DL: Development of a human neuronal cell model for human immunodeficiency virus (HIV)-infected macrophage-induced neurotoxicity: apoptosis induced by HIV type 1 primary isolates and evidence for involvement of the bcl-2/bcl-xl-sensitive intrinsic apoptosis pathway. J Virol 2002, 76:9407-9419
24. Arundine M, Tymianski M: Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003, 34:325-337
25. Haughey NJ, Mattson MP: Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 2002, 31:55-61
26. Ellis R, Langford D, Masliah E: HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat Rev Neurosci 2007, 8:33-44
27. Wiley CA, Masliah E, Morey M, Lemere C, DeTeresa R, Grafe M, Hansen L, Terry R: Neocortical damage during HIV infection. Ann Neurol 1991, 29:651-657
28. Masliah E, Terry RD, Alford M, DeTeresa R: Quantitative immunohistochemistry of synaptophysin in human neocortex: an alternative method to estimate density of presynaptic terminals in paraffin sections. J Histochem Cytochem 1990, 38:837-844 (Pubitemid 20177851)
29. Saito S, Kobayashi S, Ohashi Y, Igarashi M, Komiya Y, Ando S: Decreased synaptic density in aged brains and its prevention by rearing under enriched environment as revealed by synaptophysin contents. J Neurosci Res 1994, 39:57-62 (Pubitemid 24286535)
30. Gray BC, Siskova Z, Perry VH, O'Connor V: Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology. Neurobiol Dis 2009, 35:63-74
31. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel DW Jr, Morris JC: Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001, 56:127-129 (Pubitemid 32059669)
32. Tanaka S, Saito M, Morimatsu M, Ohama E: Immunohistochemical studies of the PrP(CJD) deposition in Creutzfeldt-Jakob disease. Neuropathology 2000, 20:124-133
33. Gonzalez RG, Cheng LL, Westmoreland SV, Sakaie KE, Becerra LR, Lee PL, Masliah E, Lackner AA: Early brain injury in the SIV-macaque model of AIDS. AIDS 2000, 14:2841-2849
34. Bissel SJ, Wang G, Ghosh M, Reinhart TA, Capuano S 3rd, Stefano Cole K, Murphey-Corb M, Piatak M Jr, Lifson JD, Wiley CA: Macrophages relate presynaptic and postsynaptic damage in simian immunodeficiency virus encephalitis. Am J Pathol 2002, 160:927-941 (Pubitemid 34224582)
35. Wu HY, Hsu FC, Gleichman AJ, Baconguis I, Coulter DA, Lynch DR: FYN-mediated phosphorylation of NR2B TYR-1336 controls calpain-mediated NR2B cleavage in neuron and heterologous systems. J Biol Chem 2007, 282:20075-20087
36. Churn SB, Limbrick D, Sombati S, DeLorenzo RJ: Excitotoxic activation of the NMDA receptor results in inhibition of calcium/calmodulin kinase II activity in cultured hippocampal neurons. J Neurosci 1995, 15:3200-3214
37. Zhou Y, Takahashi E, Li W, Halt A, Wiltgen B, Ehninger D, Li GD, Hell JW, Kennedy MB, Silva AJ: Interactions between the NR2B Receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 2007, 27:13843-13853
38. Silva AJ, Paylor R, Wehner JM, Tonegawa S: Impaired spatial learning in alpha-calcium calmodulin kinase II mutant mice. Science 1992, 257:206-211
39. Silva AJ, Rosahl TW, Chapman PF, Marowitz Z, Friedman E, Frankland PW, Cestari V, Cioffi D, Sudhof TC, Bourtchuladze R: Impaired learning in mice with abnormal short-lived plasticity. Curr Biol 1996, 6:1509-1518 (Pubitemid 27012250)
40. Hayashi N, Matsubara M, Jinbo Y, Titani K, Izumi Y, Matsushima N: Nef of HIV-1 interacts directly with calcium-bound calmodulin. Protein Sci 2002, 11:529-537
41. Churn SB, Taft WC, Billingsley MS, Blair RE, DeLorenzo RJ: Temperature modulation of ischemic neuronal death and inhibition of calcium/ calmodulin-dependent protein kinase II in gerbils. Stroke 1990, 21:1715-1721
42. Shackelford DA, Yeh RY, Hsu M, Buzsaki G, Zivin JA: Effect of cerebral ischemia on calcium/calmodulin-dependent protein kinase II activity and phosphorylation. J Cereb Blood Flow Metabol 1995, 15:450-461
43. Waxham NM, Grotta CJ, Silva JA, Strong R, Aronowski J: Ischemia-induced neuronal damage: a role for calcium/calmodulin-dependent protein kinase II. J Cereb Blood Flow Metabol 1996, 16:1-6 (Pubitemid 26007946)
44. Park JK, Namgung U, Lee CJ, Park JO, Jin SH, Kwon OB, Ko SR, Kim SW, Kang EJ, Ko JH, Lee SM, Kim DH, Won MH: Calcium-independent CaMKII activity is involved in ginsenoside Rb1-mediated neuronal recovery after hypoxic damage. Life Sci 2005, 76:1013-1025
45. Novak G, Seeman P, Tallerico T: Increased expression of calcium/calmodulin-dependent protein kinase IIβ in frontal cortex in schizophrenia and depression. Synapse 2006, 59:61-68
46. Kaul M, Garden GA, Lipton SA: Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 2001, 410:988-994
47. Bellizzi MJ, Lu SM, Gelbard HA: Protecting the synapse: evidence for a rational strategy to treat HIV-1 associated neurologic disease. J Neuroimmune Pharmacol 2006, 1:20-31