Proton magnetic resonance spectroscopy reveals neuroprotection by oral minocycline in a nonhuman primate model of accelerated NeuroAIDS

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Ratai, Eva Maria ^a,b   Bombardier, Jeffrey P ^a,e   Joo, Chan Gyu ^a,b   Annamalai, Lakshmanan ^b,f   Burdo, Tricia H ^c   Campbell, Jennifer ^c   Fell, Robert ^a   Hakimelahi, Reza ^a,b   He, Julian ^a,b   Autissier, Patrick ^c   Lentz, Margaret R ^a,b   Halpern, Elkan F ^a   Masliah, Eliezer ^d   Williams, Kenneth C ^c   Westmoreland, Susan V ^b   González, R Gilberto ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON COLLEGE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BRANDEIS UNIVERSITY   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLIAL FIBRILLARY ACIDIC PROTEIN; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; MICROTUBULE ASSOCIATED PROTEIN 1; MINOCYCLINE; N ACETYLASPARTIC ACID; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; GLIA CELL; HIV ASSOCIATED DEMENTIA; IMMUNOHISTOCHEMISTRY; MICROGLIA; NERVE CELL; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; VIRUS LOAD;

ADMINISTRATION, ORAL; AIDS-ASSOCIATED NEPHROPATHY; ANIMALS; BIOLOGICAL MARKERS; CD8-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; HUMANS; LYMPHOCYTE DEPLETION; MACACA MULATTA; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICROGLIA; MINOCYCLINE; NEURONS; NEUROPROTECTIVE AGENTS; PROTONS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRAL LOAD;

AIDS VIRUS; ANIMALIA; MACACA MULATTA; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 77956416346     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010523     Document Type: Article

References (83)

1. Navia BA, Cho ES, Petito CK, Price RW (1986) The AIDS dementia complex: II. Neuropathology. Ann Neurol 19: 525-535.
2. Navia BA, Jordan BD, Price RW (1986) The AIDS dementia complex: I. Clinical features. Ann Neurol 19: 517-524.
3. Nath A, Schiess N, Venkatesan A, Rumbaugh J, Sacktor N, et al. (2008) Evolution of HIV dementia with HIV infection. Int Rev Psychiatry 20: 25-31.
4. McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157: 3-10.
5. Sacktor N (2002) The epidemiology of human immunodeficiency virusassociated neurological disease in the era of highly active antiretroviral therapy. J Neurovirol 8 Suppl 2: 115-121.
6. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988-994.
7. Gartner S (2000) HIV infection and dementia. Science 287: 602-604.
8. Meucci O, Fatatis A, Simen AA, Bushell TJ, Gray PW, et al. (1998) Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc Natl Acad Sci USA 95: 14500-14505.
9. Nath A, Psooy K, Martin C, Knudsen B, Magnuson DS, et al. (1996) Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J Virol 70: 1475-1480.
10. Letendre S, Marquie-Beck J, Capparelli E, Best B, Clifford D, et al. (2008) Validation of the CNS Penetration-Effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch Neurol 65: 65-70.
11. Zemke D, Majid A (2004) The potential of minocycline for neuroprotection in human neurologic disease. Clin Neuropharmacol 27: 293-298.
12. Stirling DP, Koochesfahani KM, Steeves JD, Tetzlaff W (2005) Minocycline as a neuroprotective agent. Neuroscientist 11: 308-322.
13. Blum D, Chtarto A, Tenenbaum L, Brotchi J, Levivier M (2004) Clinical potential of minocycline for neurodegenerative disorders. Neurobiol Dis 17: 359-366.
14. Baptiste DC, Fehlings MG (2006) Pharmacological approaches to repair the injured spinal cord. J Neurotrauma 23: 318-334.
15. Si Q, Cosenza M, Kim MO, Zhao ML, Brownlee M, et al. (2004) A novel action of minocycline: inhibition of human immunodeficiency virus type 1 infection in microglia. J Neurovirol 10: 284-292.
16. Zink MC, Uhrlaub J, DeWitt J, Voelker T, Bullock B, et al. (2005) Neuroprotective and anti-human immunodeficiency virus activity of minocycline. Jama 293: 2003-2011.
17. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, et al. (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283: 857-860.
18. Schmitz JE, Simon MA, Kuroda MJ, Lifton MA, Ollert MW, et al. (1999) A nonhuman primate model for the selective elimination of CD8+ lymphocytes using a mouse-human chimeric monoclonal antibody. Am J Pathol 154: 1923-1932.
19. Williams K, Westmoreland S, Greco J, Ratai E, Lentz M, et al. (2005) Magnetic resonance spectroscopy reveals that activated monocytes contribute to neuronal injury in SIV neuroAIDS. J Clin Invest 115: 2534-2545.
20. Ratai EM, Pilkenton SJ, PBJ, GJC, Turk KW, et al. (2009) 7 Tesla MR Spectroscopy reveals that CD8 T lymphocyte depletion has no effect on brain metabolite concentration confirming the accelerated rhesus macaque model of neuroAIDS. International Society for Magnetic Resonance in Medicine, 17th Scientific Meeting and Exhibition, Honolulu, HI, USA.
21. Urenjak J, Williams SR, Gadian DG, Noble M (1992) Specific expression of Nacetylaspartate in neurons, oligodendrocyte-type-2 astrocyte progenitors, and immature oligodendrocytes in vitro. J Neurochem 59: 55-61.
22. Moffett JR, Namboodiri MA, Cangro CB, Neale JH (1991) Immunohistochemical localization of N-acetylaspartate in rat brain. Neuroreport 2: 131-134.
23. Ratai E-M, Bombardier JP, Joo CG, Lentz MR, He J, et al. (2009) Brain creatine elevation and NAA reduction detected by 3T 1H MR spectroscopy indicates neuronal dysfunction in the setting of enhanced glial high energy metabolism in a macaque model of NeuroAIDS. 9th International Symposium on NeuroVirology, Miami Beach, FL, USA.
24. Ratai EM, Bombardier JP, Joo CG, He J, Annamalai L, et al. (2009) Increases in Creatine detected by MRS utilizing a macaque model of neuroAIDS suggests glial activation and inflammation. International Society for Magnetic Resonance in Medicine, 17th Scientific Meeting and Exhibition, Honolulu, HI, USA.
25. Brand A, Richter-Landsberg C, Leibfritz D (1993) Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 15: 289-298.
26. Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, et al. (2006) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. Aids 20: 879-887.
27. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, et al. (1998) Microgliaspecific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57: 1-9.
28. Persidsky Y, Zheng J, Miller D, Gendelman HE (2000) Mononuclear phagocytes mediate blood-brain barrier compromise and neuronal injury during HIV-1- associated dementia. J Leukoc Biol 68: 413-422.
29. Persidsky Y, Gendelman HE (2003) Mononuclear phagocyte immunity and the neuropathogenesis of HIV-1 infection. J Leukoc Biol 74: 691-701.
30. Kaul M, Zheng J, Okamoto S, Gendelman HE, Lipton SA (2005) HIV-1 infection and AIDS: consequences for the central nervous system. Cell Death Differ 12 Suppl 1: 878-892.
31. Nath A (2002) Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 186 Suppl 2: S193-198.
32. Sharer LR (1992) Pathology of HIV-1 infection of the central nervous system. A review. J Neuropathol Exp Neurol 51: 3-11.
33. Dickson DW, Mattiace LA, Kure K, Hutchins K, Lyman WD, et al. (1991) Microglia in human disease, with an emphasis on acquired immune deficiency syndrome. Lab Invest 64: 135-156.
34. Burudi EME, Fox HS (2001) Simian Immunodeficiency Virus Model of HIVInduced Central Nervous System Dysfunction. Adv Virus Reaserch 56: 435-468.
35. Desrosiers RC (1990) The simian immunodeficiency viruses. Annu Rev Immunol 8: 557-578.
36. Zink MC, Amedee AM, Mankowski JL, Craig L, Didier P, et al. (1997) Pathogenesis of SIV encephalitis. Selection and replication of neurovirulent SIV. Am J Pathol 151: 793-803.
37. Murray EA, Rausch DM, Lendvay J, Sharer LR, Eiden LE (1992) Cognitive and motor impairments associated with SIV infection in rhesus monkeys. Science 255: 1246-1249.
38. Sharer LR, Baskin GB, Cho ES, Murphey-Corb M, Blumberg BM, et al. (1988) Comparison of simian immunodeficiency virus and human immunodeficiency virus encephalitides in the immature host. Ann Neurol, 23 Suppl: S108-112.
39. Westmoreland SV, Halpern E, Lackner AA (1998) Simian immunodeficiency virus encephalitis in rhesus macaques is associated with rapid disease progression. J Neurovirol 4: 260-268.
40. Zink MC, Suryanarayana K, Mankowski JL, Shen A, Piatak M, Jr., et al. (1999) High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 73: 10480-10488.
41. Zink M, Clements J (2000) A Rapid, Reproducible Model of AIDS and Encephelitis in SIV infected Macaques Demnstrates the Role of Viral Load in CNS Disease. NeuroAIDS 3: online-October.
42. Zink MC, Clements JE (2002) A novel simian immunodeficiency virus model that provides insight into mechanisms of human immunodeficiency virus central nervous system disease. J Neurovirol 8 Suppl 2: 42-48.
43. Weed MR, Hienz RD, Brady JV, Adams RJ, Mankowski JL, et al. (2003) Central nervous system correlates of behavioral deficits following simian immunodeficiency virus infection. J Neurovirol 9: 452-464.
44. Williams K, Alvarez X, Lackner AA (2001) Central nervous system perivascular cells are immunoregulatory cells that connect the CNS with the peripheral immune system. Glia 36: 156-164.
45. Williams KC, Hickey WF (2002) Central nervous system damage, monocytes and macrophages, and neurological disorders in AIDS. Annu Rev Neurosci 25: 537-562.
46. Chang L, Ernst T, Leonido-Yee M, Walot I, Singer E (1999) Cerebral metabolite abnormalities correlate with clinical severity of HIV-1 cognitive motor complex. Neurology 52: 100-108.
47. Marcus CD, Taylor-Robinson SD, Sargentoni J, Ainsworth JG, Frize G, et al. (1998) 1H MR spectroscopy of the brain in HIV-1-seropositive subjects: evidence for diffuse metabolic abnormalities. Metab Brain Dis 13: 123-136.
48. Salvan AM, Vion-Dury J, Confort-Gouny S, Nicoli F, Lamoureux S, et al. (1997) Brain proton magnetic resonance spectroscopy in HIV-related encephalopathy: identification of evolving metabolic patterns in relation to dementia and therapy. AIDS Res Hum Retroviruses 13: 1055-1066.
49. Moller HE, Vermathen P, Lentschig MG, Schuierer G, Schwarz S, et al. (1999) Metabolic characterization of AIDS dementia complex by spectroscopic imaging. J Magn Reson Imaging 9: 10-18.
50. Meyerhoff DJ, Bloomer C, Cardenas V, Norman D, Weiner MW, et al. (1999) Elevated subcortical choline metabolites in cognitively and clinically asymptomatic HIV+ patients. Neurology 52: 995-1003.
51. Cheng LL, Ma MJ, Becerra L, Ptak T, Tracey I, et al. (1997) Quantitative Neuropathology by High Resolution Magic Angle Spinning Proton Magnetic Resonance Spectroscopy. Proc Natl Acad USA 94: 6408-6413.
52. Gonzalez RG, Cheng LL, Westmoreland SV, Sakaie KE, Becerra LR, et al. (2000) Early brain injury in the SIV-macaque model of AIDS. Aids 14: 2841-2849.
53. Lentz MR, Kim JP, Westmoreland SV, Greco JB, Fuller RA, et al. (2005) Quantitative neuropathologic correlates of changes in ratio of N-acetylaspartate to creatine in macaque brain. Radiology 235: 461-468.
54. Lentz MR, Lee V, Westmoreland SV, Ratai EM, Halpern EF, et al. (2008) Factor analysis reveals differences in brain metabolism in macaques with SIV/ AIDS and those with SIV-induced encephalitis. NMR Biomed 21: 878-887.
55. Chang L, Ernst T, Witt MD, Ames N, Gaiefsky M, et al. (2002) Relationships among brain metabolites, cognitive function, and viral loads in antiretroviralnaive HIV patients. Neuroimage 17: 1638-1648.
56. Chang L, Ernst T, Witt MD, Ames N, Walot I, et al. (2003) Persistent brain abnormalities in antiretroviral-naive HIV patients 3 months after HAART. Antivir Ther 8: 17-26.
57. Ratai EM, Pilkenton SJ, Greco JB, Lentz MR, Bombardier JP, et al. (2009) In vivo proton magnetic resonance spectroscopy reveals region specific metabolic responses to SIV infection in the macaque brain. BMC Neurosci 10: 63.
58. Barker PB, Lee RR, McArthur JC (1995) AIDS dementia complex: evaluation with proton MR spectroscopic imaging. Radiology 195: 58-64.
59. Tracey I, Carr CA, Guimaraes AR, Worth JL, Navia BA, et al. (1996) Brain choline-containing compounds are elevated in HIV-positive patients before the onset of AIDS dementia complex: A proton magnetic resonance spectroscopic study. Neurology 46: 783-788.
60. Greco JB, Westmoreland SV, Ratai EM, Lentz MR, Sakaie K, et al. (2004) In vivo 1H MRS of brain injury and repair during acute SIV infection in the macaque model of neuroAIDS. Magn Reson Med 51: 1108-1114.
61. Kim JP, Lentz MR, Westmoreland SV, Greco JB, Ratai EM, et al. (2005) Relationship between astrogliosis and 1H MRS measures of brain Cho/Cr and MI/Cr in a primate model. AJNR Am J Neuroradiol 6: 752-759.
62. Chong WK, Sweeney B, Wilkinson ID, Paley M, Hall-Craggs MA, et al. (1993) Proton spectroscopy of the brain in HIV infection: correlation with clinical, immunologic, and MR imaging findings. Radiology 188: 119-124.
63. Thiel G (1993) Synapsin I, synapsin II, and synaptophysin: marker proteins of synaptic vesicles. Brain Pathol 3: 87-95.
64. Bissel SJ, Wang G, Ghosh M, Reinhart TA, Capuano S, 3rd, et al. (2002) Macrophages relate presynaptic and postsynaptic damage in simian immunodeficiency virus encephalitis. Am J Pathol 160: 927-941.
65. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, et al. (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad SciUS A 96: 13496-13500.
66. Murata Y, Rosell A, Scannevin RH, Rhodes KJ, Wang X, et al. (2008) Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke 39: 3372-3377.
67. Popovic N, Schubart A, Goetz BD, Zhang SC, Linington C, et al. (2002) Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann Neurol 51: 215-223.
68. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, et al. (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22: 1763-1771.
69. Lin S, Zhang Y, Dodel R, Farlow MR, Paul SM, et al. (2001) Minocycline blocks nitric oxide-induced neurotoxicity by inhibition p38 MAP kinase in rat cerebellar granule neurons. Neurosci Lett 315: 61-64.
70. Follstaedt SC, Barber SA, Zink MC (2008) Mechanisms of minocycline-induced suppression of simian immunodeficiency virus encephalitis: inhibition of apoptosis signal-regulating kinase 1. J Neurovirol 14: 376-388.
71. Jenwitheesuk E, Samudrala R (2007) Identification of potential HIV-1 targets of minocycline. Bioinformatics 23: 2797-2799.
72. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95: 15769-15774.
73. Sriram K, Miller DB, O'Callaghan JP (2006) Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem 96: 706-718.
74. Tsuji M, Wilson MA, Lange MS, Johnston MV (2004) Minocycline worsens hypoxic-ischemic brain injury in a neonatal mouse model. Exp Neurol 189: 58-65.
75. Smith DL, Woodman B, Mahal A, Sathasivam K, Ghazi-Noori S, et al. (2003) Minocycline and doxycycline are not beneficial in a model of Huntington's disease. Ann Neurol 54: 186-196.
76. Diguet E, Fernagut PO, Wei X, Du Y, Rouland R, et al. (2004) Deleterious effects of minocycline in animal models of Parkinson's disease and Huntington's disease. Eur J Neurosci 19: 3266-3276.
77. Diguet E, Gross CE, Tison F, Bezard E (2004) Rise and fall of minocycline in neuroprotection: need to promote publication of negative results. Exp Neurol 189: 1-4.
78. Gordon PH, Moore DH, Miller RG, Florence JM, Verheijde JL, et al. (2007) Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol 6: 1045-1053.
79. Ogg RJ, Kingsley PB, Taylor JS (1994) WET, a T1- and B1-insensitive watersuppression method for in vivo localized 1H NMR spectroscopy. J Magn Reson B 104: 1-10.
80. Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30: 672-679.
81. Lifson JD, Rossio JL, Piatak M, Jr., Parks T, Li L, et al. (2001) Role of CD8(+) lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J Virol 75: 10187-10199.
82. Masliah E, Achim CL, Ge N, DeTeresa R, Terry RD, et al. (1992) Spectrum of human immunodeficiency virus-associated neocortical damage. Ann Neurol 32: 321-329.
83. Everall IP, DeTeresa R, Terry R, Masliah E (1997) Comparison of two quantitative methods for the evaluation of neuronal number in the frontal cortex in Alzheimer disease. J Neuropathol Exp Neurol 56: 1202-1206.