HIV disorders of the brain; pathology and pathogenesis

Frontiers in Bioscience

Volumn 11, Issue 1 P.447-888, 2006, Pages 718-732

  Del Valle, Luis ^a   Piña Oviedo, Sergio ^a  

^a TEMPLE UNIVERSITY   (United States)

Author keywords

Cryptococcosis; HIV Encephalopathy; Primary CNS Lymphomas; Progressive Multifocal Leukoencephalopathy; Review; Toxoplasmosis

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; JC POLYOMAVIRUS;

EID: 32944467987     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1830     Document Type: Review

References (160)

1. Albright AV, Soldan SS, & Gonzalez-Scarano F: Pathogenesis of human immunodeficiency virus-induced neurological disease. J Neurovirol 9: 222-227 (2003)
2. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W, & Montagnier L: Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220: 868-871 (1983)
3. Cullen BR: Regulation of gene expression in the human immunodeficiency virus type 1. Adv Virus Res 40: 1-17 (1991)
4. Malim MH, & Cullen BR: HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 65: 241-248 (1991)
5. Cohen EA, Terwilliger EF, Sodroski JG, & Haseltine WA. Identification of a protein encoded by the vpu gene of HIV-1. Nature 334: 532-534 (1988)
6. Cullen BR: Trans-activation of human immunodeficiency virus occurs via a bimodal mechanism. Cell 46: 973-982 (1986)
7. Ogawa K, Shibata R, Kiyomasu T, Higuchi I, Kishida Y, Ishimoto A, & Adachi A: Mutational analysis of the human immunodeficiency virus vpr open reading frame. J Virol 63: 4110-4114 (1989)
8. Ahmad N, & Venkatesan S: Nef protein of HIV-1 is a transcriptional repressor of HIV-1 LTR. Science 241: 1481-1485 (1988)
9. Brew BJ, Rosenblum M, & Price RW. AIDS dementia complex and primary HIV brain infection. J Neuroimmunol 20: 133-140 (1988)
10. Price RW, & Brew BJ: The AIDS dementia complex. J Infect Dis 158: 1079-1083 (1988)
11. Kato T, Hirano A, Llena JF, & Dembitzer HM: Neuropathology of acquired immune deficiency syndrome (AIDS) in 53 autopsy cases with particular emphasis on microglial nodules and multinucleated giant cells. Acta Neuropathol (Berl) 73: 287-294 (1987)
12. Everall IP, Luthert PJ, & Lantos PL: Neuronal loss in the frontal cortex in HIV infection. Lancet 337: 1119-11121 (1991)
13. Johnson RT, Glass JD, McArthur JC, & Chesebro BW: Quantitation of human immunodeficiency virus in brains of demented and nondemented patients with acquired immunodeficiency syndrome. Ann Neurol 39: 392-395 (1996)
14. Cooper DA, Gold J, Maclean P, Donovan B, Finlayson R, Barnes TG, Michelmore HM, Brooke P, & Penny R: Acute AIDS retrovirus infection. Definition of a clinical illness associated with seroconversion. Lancet 1: 537-540 (1985)
15. McArthur JC, Selnes OA, Glass JD, Hoover DR, & Bacellar H: HIV dementia. Incidence and risk factors. Res Publ Assoc Res Nerv Ment Dis 72: 251-272 (1994)
16. Navia BA: Clinical and biologic features of the AIDS dementia complex. Neuroimaging Clin N Am (1997); 7: 581-592
17. Price RW: Neurological complications of HIV infection. Lancet 348: 445-452 (1996)
18. Gabuzda DH, Ho DD, de la Monte SM, Hirsch MS, Rota TR, & Sobel RA: Immunohistochemical identification of HTLV-III antigen in brains of patients with AIDS. Ann Neurol 20: 289-295 (1986)
19. Nottet HS, Persidsky Y, Sasseville VG, Nukuna AN, Bock P, Zhai QH, Sharer LR, McComb RD, Swindells S, Soderland C, & Gendelman HE: Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J Immunol 156: 1284-1295 (1996)
20. Haase AT: Pathogenesis of lentivirus infections. Nature 322: 130-136 (1986)
21. Peluso R, Haase A, Stowring L, Edwards M, & Ventura P: A Trojan Horse mechanism for the spread of visna virus in monocytes. Virology 147: 231-236 (1985)
22. Wiley CA, Schrier RD, Nelson JA, Lampert PW, & Oldstone MB: Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci USA 83: 7089-7093 (1986)
23. Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, & Glass JD: Localization of HIV-1 in human brain using polymerase chain reaction / in situ hybridization and immunocytochemistry. Ann Neurol 39: 705-711 (1996)
24. Cosenza MA, Zhao ML, Si Q, & Lee SC: Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12: 442-455 (2002)
25. Fischer-Smith T, Croul S, Adeniyi A, Rybicka K, Morgello S, Khalili K, & Rappaport J: Macrophage / microglial accumulation and proliferating cell nuclear antigen expression in the central nervous system in human immunodeficiency virus encephalopathy. Am J Pathol 164: 2089-2099 (2004)
26. Sharer LR, Cho ES, & Epstein LG: Multinucleated giant cells and HTLV-III in AIDS encephalopathy. Hum Pathol 16: 760 (1985)
27. Brack-Werner R: Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13: 1-22 (1999)
28. Sabri F, Tresoldi E, Di Stefano M, Polo S, Monaco MC, Verani A, Fiore JR, Lusso P, Major E, Chiodi F, & Scarlatti G: Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: independence from CD4 and major chemokine receptors. Virology 264: 370-384 (1999)
29. Kanmogne GD, Kennedy RC, & Grammas P. HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: possible pathway for HIV entry into the brain and HIV-associated dementia. J Neuropathol Exp Neurol 61: 992-1000 (2002)
30. Perez A, Probert AW, Wang KK, & Sharmeen L: Evaluation of HIV-1 Tat induced neurotoxicity in rat cortical cell culture. J Neurovirol 7: 1-10 (2001)
31. Piller SC, Jans P, Gage PW, & Jans DA: Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology. Proc Natl Acad Sci USA 95: 4595-4600 (1998)
32. Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E, Lipton & SA: Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 22: 4015-4024 (2002)
33. Bukrinsky MI, Nottet HS, Schmidtmayerova H, Dubrovsky L, Flanagan CR, Mullins ME, Lipton SA, & Gendelman HE: Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease. J Exp Med 181: 735-745 (1995)
34. Dawson VL, Dawson TM, London ED, Bredt DS, & Snyder SH: Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88: 6368-6371 (1991)
35. Tyor WR, Glass JD, Griffin JW, Becker PS, McArthur JC, Bezman L, & Griffin DE: Cytokine expression in the brain during the acquired immunodeficiency syndrome. Ann Neurol 31: 349-360 (1992)
36. Vitkovic L, da Cunha A, & Tyor WR: Cytokine expression and pathogenesis in AIDS brain. Res Publ Assoc Res Nerv Ment Dis 72: 203-22 (1994)
37. Glass JD, Wesselingh SL, Selnes OA, & McArthur JC: Clinical-neuropathologic correlation in HIV-associated dementia. Neurology 43: 2230-2237 (1993)
38. Navia BA, Cho ES, Petito CK, & Price RW: The AIDS dementia complex: II. Neuropathology. Ann Neurol 19: 525-535 (1986)
39. Berger JR, & Concha M: Progressive Multifocal Leukoencephalopathy: The evolution of a disease once considered rare. J Neurovirol 1: 5-18 (1995)
40. Holman RC, Torok TJ, Belay ED, Janssen RS, & Schonberger LB: Progressive multifocal leukoencephalopathy in the United States, 1979-1994: increased mortality associated with HIV infection. Neuroepidemiology 17: 303-309 (1998)
41. Åström KE, Mancall EL, & Richardson EP Jr: Progressive multifocal leukoencephalopathy; a hitherto unrecognized complication of chronic lymphocytic leukemia and lymphoma. Brain 81: 93-111 (1958)
42. Richardson EP Jr: Progressive multifocal leukoencephalopathy. New Engl J Med 265: 815-823 (1961)
43. Schwerdt PR, Schwerdt CE, Silverman L, & Rubinstein LJ: Virions associated with progressive multifocal leukoencephalopathy. Virology 29: 511-514 (1966)
44. Silverman L, & Rubinstein LJ: Electron Microscopic Observations on a Case of Progressive Multifocal Leukoencephalopathy. Acta Neuropathologica 5: 215-224 (1965)
45. ZuRhein GM, & Chow SM: Particles resembling papovavirions in human cerebral demyelinating disease. Science 148: 1,477-1,479 (1965)
46. ZuRhein GM: Polyoma-like virions in a human demyelinating disease. Acta Neuropathol (1967); 8: 57-68
47. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, & Dessel BH: Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1: 1257-1260 (1971)
48. London WT, Houff SA, Madden DL, Fuccillo DA, Gravell M, Wallen WC, Palmer AE, Sever JL, Padgett BL, Walker DL, ZuRhein GM, & Ohashi T: Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus). Science 201: 1246-1249 (1978)
49. Ohsumi S, Motoi M, & Ogawa K: Induction of undifferentiated tumors by JC virus in the cerebrum of rats. Acta Pathol Jpn 36: 815-825 (1986)
50. Varakis J, ZuRhein GM, Padgett BL, & Walker DL: Induction of peripheral neuroblastomas in Syrian hamsters after injection as neonates with JC virus, a human polyoma virus. Cancer Res 38: 1718-1722 (1978)
51. Walker DL, Padgett BL, Zu-Rhein GM, Albert AE, & Marsh RF: Human papovavirus (JC): Induction of brain tumors in hamsters. Science 181: 674-676 (1973)
52. Zu Rhein GM, & Varakis JN: Perinatal induction of medulloblastomas in Syrian golden hamsters by a human polyomavirus (JC). Natl Cancer Inst Monogr 51: 205-208 (1979)
53. Taguchi F, Kajioka J, & Miyamura T: Prevalence rate and age acquisition of antibodies against JC virus and BK virus in human sera. Microbiol Immunol 26: 1057-1064 (1982)
54. Walker DL, & Padgett BL: The epidemiology of human polyomaviruses. In: Sever JL, and Madden D (eds.) Polyomaviruses and Human Neurological Disease. Alan R Liss Inc. New York. pp 99-106
55. Padgett BL, & Walker DL: Prevalence of antibodies in human sera against JC virus, an isolate from a case of Progressive Multifocal Leukoencephalopathy. J Infect Dis 127: 467-470 (1973)
56. Coleman DV, Gardner SD, & Field AM: Human polyomavirus infection in renal allograft recipients. Br Med J 3: 371-375 (1973)
57. Coleman DV, Wolfendale MR, Daniel RA, Dhanjal NK, Gardner SD, Gibson PE, & Field AM: A prospective study on human polyomavirus infection in pregnancy. J Infect Dis 142: 1-8 (1980)
58. Houff SA, Major EO, Kats D, Kufta CV, Sever JL, Pittaluga S, Roberts JR, Gitt J, Saini N, & Lux W: Involvement of JC virus infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy. New Engl J Med 318: 301-305 (1988)
59. Tornatore C, Berger JR, Houff SA, Curfman B, Meyers K, Winfield D, & Major EO: Detection of JC virus DNA in peripheral lymphocytes from patients with and without progressive multifocal leukoencephalopathy. Ann Neurol 31: 456-462 (1992)
60. Monaco MC, Atwood WJ, Gravell M, Tornatore CS, & Major EO: JC Virus infection of hematopoietic progenitor cells, primary B-lymphocytes, and tonsillar stromal cells: implications for viral latency. J Virol 70: 7004-7012 (1996)
61. Frisque RJ, & White FA III: The molecular biology of JCV, causative agent of progressive multifocal leukoencephalopathy. In: RP Roos (ed). Molecular Neurovirology, (1992); Humana Press, Totowa, NJ, pp 25-158
62. Salunke DM, Caspar DL, & Garcea RL: Self-assembly of purified polyomavirus capsid protein VP1. Cell 46: 895-904 (1986)
63. Adams JH, & Short IA: Progressive multifocal leukoencephalopathy. Scot Med J 10: 195-202 (1965)
64. Del Valle L, Croul S, Morgello S, Amini S, Rappaport J, & Khalili K: Detection of HIV-1 Tat and JCV Capsid Protein, VP1, in AIDS Brain with Progressive Multifocal Leukoencephalopathy. J Neurovirol 6: 221-228 (2000)
65. Major EO, Amemiya K, Tornatore CS, Houff SA, & Berger JR: Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC Virus induced demyelinating disease of the human brain. Clin Micro Rev 5: 49-73 (1992)
66. Aksamit AJ: Progressive Multifocal Leukoencephalopathy: A Review of the Pathology and Pathogenesis. Microsc Res Tech 32: 302-311 (1995)
67. Albrecht H, Hoffmann C, Degen O, Stoehr A, Plettenberg A, Mertenskotter T, Eggers C, & Stellbrink HJ: Highly active antiretroviral therapy significantly improves the prognosis of patients with HIV-associated progressive multifocal leukoencephalopathy. AIDS 12: 1149-1154 (1998)
68. Liu CK, Wei G, & Atwood WJ: Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha (2-6)-linked sialic acids. J Virol 72: 4643-4649 (1998)
69. Eash S, Tavares R, Stopa EG, Robbins SH, Brossay L, & Atwood WJ: Differential distribution of the JC virus receptor-type sialic acid in normal human tissues. Am J Pathol 164: 419-428 (2004)
70. Elphick GF, Querbes W, Jordan JA, Gee GV, Eash S, Manley K, Dugan A, Stanifer M, Bhatnagar A, Kroeze WK, Roth BL, & Atwood WJ: The human polyomavirus, JCV, uses serotonin receptors to infect cells. Science 306: 1380-1383 (2004)
71. Pho MT, Ashok A, & Atwood WJ: JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J Virol 74: 2288-2292 (2000)
72. Rhodes RH, Ward JM, Walker JL, & Russ AA: Progressive Multifocal Leukoencephalopathy and retroviral encephalitis in acquired immunodeficiency syndrome. Arc Pathol Lab Med 112: 1,207-1,213 (1988)
73. Liu Y, Sune C, & Garcia-Blanco MA: Human immunodeficiency virus type 1 Tat-dependent activation of an arrested RNA polymerase II elongation complex. Virology 255: 337-346 (1999)
74. Cullen BR: The HIV-1 Tat protein: an RNA sequence-specific processivity factor? Cell 63: 655-657 (1990)
75. Frankel AD: Activation of HIV transcription by Tat. Curr Opin Genet Dev 2: 293-298 (1992)
76. Frankel AD, & Pabo CO: Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55: 1,189-1,193 (1988)
77. Chowdhury M, Taylor JP, Tada H, Rappaport J, Wong-Staal F, Amini S, & Khalili K: Regulation of the human neurotropic virus promoter by JCV T-antigen and HIV-1 Tat protein. Oncogene 5: 1737-1742 (1990)
78. Tada H, Rappaport J, Lashgari M, Amini S, Wong-Saal F, & Khalili K: Transactivation of the JC Virus late promoter by the Tat protein of type 1 human immunodeficiency virus in glial cells. Proc Natl Acad Sci USA 87: 3,479-3,483 (1990)
79. Bicanic T, & Harrison TS: Cryptococcal meningitis. Br Med Bull 72: 99-118 (2005)
80. Wright D, Schneider A, & Berger J: Central nervous system opportunistic infections. Neuroimag Clin North Am 7: 513-525 (1997)
81. Mamidi A, DeSimone JA, & Pomerantz RJ: Central nervous system infections in individuals with HIV-1 infection. J Neurovirol 8: 158-167 (2002)
82. Kumarasamy N, Vallabhaneni S, Flanigan TP, Mayer KH, & Solomon S: Clinical profile of HIV in India. Indian J Med Res 121: 377-394 (2005)
83. Chariyalertsak S, Sirisanthana T, Saengwonloey O, & Nelson K: Clinical presentation and risk behaviors of patients with acquired immunodeficiency syndrome in Thailand, 1994-1998: Regional variation and temporal trends. Clin Infect Dis 32: 955-962 (2001)
84. Holmes CB, Losina E, Walensky RP, Yazdanpanah Y, & Freedberg K: Review of human immunodeficiency virus type 1-related opportunistic infections in Sub-Saharan Africa. Clin Infect Dis 36: 652-662 (2003)
85. Sanfelice F: Contributo alla morfologia e biologia dei blastomiceti che si sviluppano nei succhi di alcuni frutti. Ann Igien 4: 463-495 (1894)
86. Busse O: Über parasitäre zelleinschlüsse und ihre züchtung. Zentralbl Bakteriol 16: 175-180 (1894)
87. Mitchell TG, & Perfect JR: Cryptococcosis in the Era of AIDS-100 Years after the Discovery of Cryptococcus neoformans. Clin Microbiol Rev 8: 515-548 (1995)
88. Kwon-Chung KJ, Polacheck I, & Popkin TJ: Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J Bacteriol 150: 1414-1421 (1982)
89. Rhodes JC, Polacheck I, & Kwon-Chung KJ: Phenoloxidase activity and virulence in isogenic strains of Cryptococcus neoformans. Infect Immun 36: 1175-1184 (1982)
90. Bhattacharjee AK, Bennett JE, & Glaudemans CPJ: Capsular polysaccharides of Cryptococcus neoformans. Rev Infect Dis 6: 619-624 (1984)
91. Coenjaerts FEJ, Walenkamp AME, Mwinzi PN, Scharringa J, Dekker HAT, Van Strijp JAG, Cherniak R, & Hoepelman AIM: Potent inhibition of Neutrophil Migration by Cryptococcal Mannoprotein-4-Induced Desensitization. J Immunol 167: 3988-3995 (2001)
92. Dykstra MA, Friedman L, & Murphy JW: Capsule size of Cryptococcus neoformans: control and relationship to virulence. Infect Immun 16: 129-135 (1977)
93. Charlier C, Chretien F, Baudrimont M, Mordelet E, Lortholary O, & Dromer F: Capsule structure changes associated with Cryptococcus neoformans crossing the blood-brain barrier. Am J Pathol 166(2): 421-432 (2005)
94. Ikeda R, Shinoda T, Morita T, & Jacobson ES: Characterization of a phenol oxidase from Cryptococcus neoformans var. neoformans. Microbiol Immunol 37: 759-764 (1993)
95. Polacheck I, & Kwon-Chung KJ: Melanogenesis in Cryptococcus neoformans. J Gen Microbiol (1988); 134: 1037-1041
96. Jacobson ES, & Emery HS: Catecholamine uptake, melanization, and oxygen toxicity in Cryptococcus neoformans. J Bacteriol 173: 401-403 (1991)
97. Jacobson ES, & Tinnell SB: Antioxidant function of fungal melanin. J Bacteriol 175: 7102-7104 (1993)
98. Polak A: Melanin as a virulence factor in pathogenic fungi. Mycoses 33: 215-224 (1990)
99. Wehn SM, Heinz ER, Burger PC, & Boyko OB: Dilated Virchow-Robin spaces in cryptococcal meningitis associated with AIDS: CT and MR findings. J Comput Assist Tomogr 13: 756-762 (1989)
100. Everett BA, Kusske JA, Rush JL, & Pribram HW: Cryptococcal infection of the central nervous system. Surg Neurol 9: 157-163 (1978)
101. Tien RD, Chu PK, Hesselink JR, Duberg A, & Wiley C: Intracranial cryptococcosis in immunocompromised patients: CT and MR findings in 29 cases. AJNR Am J Neuroradiol 12: 283-289 (1991)
102. Caldemeyer KS, Matthews VP, Edwards-Brown MK, & Smith RR: Central Nervous System Cryptococcosis: Parenchymal Calcification and Large Gelatinous Pseudocysts. AJNR 18: 107-109 (1997)
103. Selby RC, & Lopes NM: Torulomas (cryptococcal granulomata) of the central nervous system. J Neurosurg 38: 40-46 (1973)
104. Graybill JR, Sobel J, Saag M, van Der Horst C, Powderly W, Cloud G, Riser L, Hamill R, & Dismukes W: Diagnosis and management of increased intracranial pressure in patients with AIDS and cryptococcal meningitis. Clin Infect Dis 30: 47-54 (2000)
105. Levitz SM: The ecology of Cryptococcus neoformans and the epidemiology of cryptococcosis. Rev Infect Dis 13: 1163-1169 (1991)
106. Neilson JB, Fromtling RA, & Bulmer GS: Cryptococcus neoformans: size range of infectious particles from aerosolized soil. Infect Immun 17: 634-638 (1977)
107. Chang YC, Stins MF, McCaffery MJ, Miller GF, Pare DR, Dam T, Paul-Satyasee M, Kim KS & Kwon-Chung KJ: Cyptococcal Yeast Cells Invade the Central Nervous System via Transcellular Penetration of the Blood-Brain Barrier. Infect Immun 72: 4985-4995 (2004)
108. Chen SHM, Stins MF, Huang SH, Chen YH, Kwon-Chung KJ, Chang Y, Kim KS, Suzuki K & Jong AY: Cryptococcus neoformans induces alterations in the cytoskeleton of human brain microvascular endothelial cells. J Med Microbiol 52: 961-970 (2003)
109. Levitz SM, Nong S, Seetoo K, Harrison TS, Speizer R, & Simons E: Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67: 885-890 (1999)
110. Casadevall A, Steenbergen JN, & Nosanchuk JD: 'Ready made' virulence and 'dual use' virulence factors in pathogenic environmental fungi - the Cryptococcus neoformans paradigm. Curr Opin Microbiol 6: 332-337 (2003)
111. Zangerle R, Allerberger F, Pohl P, Fritsch P, & Dierich MP: High risk of developing toxoplasmic encephalitis in AIDS patients seropositive to Toxoplasma gondii. Med Microbiol Immunol (Berl) 180: 59-66 (1991)
112. Gray F, Gherardi R, & Scaravilli F: The neuropathology of the acquired immune deficiency syndrome (AIDS). A review. Brain 111: 245-266 (1988)
113. Porter SB, & Sande MA: Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. N Engl J Med 327: 1643-1648 (1992)
114. Luft BJ, & Remington JS: Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15: 211-222 (1992)
115. Renold C, Sugar A, Chave JP, Perrin L, Delavelle J, Pizzolato G, Burkhard P, Gabriel V, & Hirschel B: Toxoplasma encephalitis in patients with the acquired immunodeficiency syndrome. Medicine (Baltimore) 71: 224-239 (1992)
116. Nicolle C, & Manceaux L: Sur une infection a corps de Leishman (ou organisme voisins) du gondi. C R Hebd Seances Acad Sci 147: 763-766 (1908)
117. Janku J: Pathogenesa a pathologicka anatomie tak nazvaneho vrozeneho kolobomu zlute skvrny v oku normaline velikem a mikrophthalmickem snalezem parazitu v sitnici. Cas Lek Cesk 62: 1021-1027 (1923)
118. de Melo EJT, & de Souza W: A cytochemistry study of the inner membrane complex of the pellicle of tachyzoites of Toxoplasma gondii. Parasitol Res 83: 252-256 (1997)
119. de Souza W, & Souto-Padrón T: Ultrastructural localization of basic proteins on the conoid, rhoptries and micronemes of Toxoplasma gondii. Z Parasitenkd 56: 123-129 (1978)
120. Sheffield HG, & Melton ML: The fine structure and reproduction of Toxoplasma gondii. J Parasitol 54: 209-226 (1968)
121. Sulzer AJ, Strobel PL, Springer EL, Roth IL, & Callaway CS: A comparative electron microscopic study of the morphology of Toxoplasma gondii by freeze-etch replication and thin sectioning technique. J Protozool 21: 710-714 (1974)
122. Morrissette NS, Murray JM, & Roos DS: Subpellicular microtubules associate with an intramembranous particle lattice in the protozoan parasite Toxoplasma gondii. J Cell Sci 110: 35-42 (1997)
123. Nichols BA, Chiappino ML, & O'Connor GR: Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J Ultrastruct Res 83: 85-98 (1983)
124. Saffer LD, Mercareau-Puijalon O, Dubrematz JF, & Schwartzman JD. Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool 39: 526-530 (1992)
125. Dubey JP, Lindsay DS, & Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 11: 267-299 (1998)
126. Handler M, Ho V, Whelan M, & Budzilovich G: Intracerebral toxoplasmosis in patients with acquired immune deficiency syndrome. J Neurosurg 59: 994-1001 (1983)
127. Rose I: Morphology and diagnostics of human toxoplasmosis. Gen Diagn Pathol 142: 257-270 (1997)
128. Strittmatter C, Lang W, Wiestler OD, & Kleihues P: The changing pattern of human immunodeficiency virus-associated cerebral toxoplasmosis: a study of 46 postmortem cases. Acta Neuropathol (Berl) 83: 475-481 (1992)
129. Gray F, Gherardi R, Wingate E, Wingate J, Fenelon G, Gaston A, Sobel A, & Poirier J: Diffuse encephalitic cerebral toxoplasmosis in AIDS. Report of four cases. J Neurol 236: 273-277 (1989)
130. Benenson MW, Takafuji ET, Lemon SM, Greenup RL, & Sulzer AJ: Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. N Engl J Med 307: 666-669 (1982)
131. Bowie WR, King AS, Werker DH, Isaac-Renton JL, Bell A, Eng SB, & Marion SA: Outbreak of toxoplasmosis associated with municipal drinking water. Lancet 350: 173-177 (1997)
132. Teutsch SM, Juranek DD, Sulzer A, Dubey JP, & Sikes RK. Epidemic toxoplasmosis associated with infected cats. N Engl J Med 300: 695-699 (1979)
133. Krick JA, & Remington JS: Toxoplasmosis in the adult - an overview. N Engl J Med 298: 550-553 (1978)
134. Beral V: The epidemiology of cancer in AIDS patients. AIDS 5 Suppl 2: S99-103 (1991)
135. Levine AM: Acquired immunodeficiency syndrome-related lymphoma. Blood 80: 8-20 (1992)
136. Biggar RJ, & Rabkin CS: The epidemiology of AIDS-related neoplasms. Hematol Oncol Clin North Am 10: 997-1010 (1996)
137. Rabkin CS: Epidemiology of AIDS-related malignancies. Curr Opin Oncol 6: 492-496 (1994)
138. Camilleri-Broët S, Davi F, Feuillard J, Seilhean D, Michiels JF, Brousset P, Epardeau B, Navratil E, Mokhtari K, Bourgeois C, Marelle L, Raphael M, & Hauw JJ: AIDS-related primary brain lymphomas: histopathologic and immunohistochemical study of 51 cases. Hum Pathol 28: 367-374 (1997)
139. Schlegel U, Schmidt-Wolf IGH, & Deckert M: Primary CNS lymphoma: clinical presentation, pathological classification, molecular pathogenesis and treatment. J Neurol Sci 181: 1-12 (2000)
140. Gill PS, Levine AM, Meyer PR, Boswell WD, Burkes RL, Parker JW, Hofman FM, Dworsky RL, & Lukes RJ: Primary central nervous system lymphoma in homosexual men. Clinical, immunologic, and pathologic features. Am J Med 78: 742-748 (1985)
141. So YT, Beckstead JH, & Davis RL: Primary central nervous system lymphoma in acquired immune deficiency syndrome: a clinical and pathological study. Ann Neurol 20: 566-572 (1986)
142. Carbone A, Dolcetti R, Gloghini A, Maestro R, Vaccher E, di Luca D, Tirelli U, & Boiocchi M. Immunophenotypic and molecular analyses of acquired immune deficiency syndrome-related and Epstein-Barr virus-associated lymphomas: a comparative study. Hum Pathol 27: 133-146 (1996)
143. Bindal AK, Blisard KS, Melin-Aldama H, & Warnick RE. Primary T-cell lymphoma of the brain in acquired immunodeficiency syndrome: case report. J Neurooncol 31: 267-271 (1997)
144. Remick SC, Diamond C, Migliozzi JA, Solis O, Wagner H Jr, Haase RF, & Ruckdeschel JC: Primary central nervous system lymphoma in patients with and without the acquired immune deficiency syndrome. A retrospective analysis and review of the literature. Medicine 69: 345-60 (1990)
145. Hochberg FH, & Miller DC. Primary central nervous system lymphoma. J Neurosurg 68: 835-853 (1988)
146. Shibata S: Sites of origin of primary intracerebral malignant lymphoma. Neurosurgery 25: 14-19 (1989)
147. Bignon YJ, Clavelou P, Ramos F, Jouvet A, Tommasi M, Tournilhac M, Dastugue B, & Plagne R: Detection of Epstein-Barr virus sequences in primary brain lymphoma without immunodeficiency. Neurology 41: 1152-1153 (1991)
148. List AF, Greer JP, Cousar JP, Johnson DH, Greco FA, Volsky DJ, & Purtilo DT: Primary brain lymphoma in the immunocompetent host: relation to Epstein-Barr virus. Mod Pathol 3: 609-612 (1990)
149. MacMahon EM, Glass JD, Hayward SD, Mann RB, Becker PS, Charache P, McArthur JC, & Ambinder RF: Epstein-Barr virus in AIDS-related primary central nervous system lymphoma. Lancet 338: 969-973 (1991)
150. Cesarman E: Epstein-Barr virus (EBV) and lymphomagenesis. Front Biosci 7: e58-65 (2002)
151. Kenney JL, Guinness ME, Curiel T, & Lacy J: Antisense to the epstein-barr virus (EBV)-encoded latent membrane protein 1 (LMP1) suppresses LMP1 and bcl-2 expression and promotes apoptosis in EBV-immortalized B cells. Blood 92: 1721-1727 (1998)
152. Eliopoulos AG, Stack M, Dawson CW, Kaye KM, Hodgkin L, Sihota S, Rowe M, and Young LS: Epstein-Barr virus-encoded LMP1 and CK40 mediate IL-6 production in epithelial cells via an NF-kappaB pathway involving TNF receptor-associated factors. Oncogene 14: 2899-2916 (1997)
153. Del Valle L, Enam S, Lara C, Miklossy J, Khalili K, & Gordon J: Primary central nervous system lymphoma expressing the human neurotropic polyomavirus, JC virus, genome. J Virol 78: 3462-3469 (2004)
154. Gallia GL, Houff SA, Major EO, & Khalili K: JC virus infection of lymphocytes-revisited. J. Infect. Dis 176: 1603-1609 (1997)
155. Tornatore C, Berger JR, Houff SA, Curfman B, Meyers K, Winfield D, & Major EO: Detection of JC virus DNA in peripheral lymphocytes from patients with and without progressive multifocal leukoencephalopathy. Ann. Neurol 31: 454-462 (1992)
156. Neel JV, Major EO, Awa AA, Glover T, Burgess A, Traub R, Curfman B, & Satoh C: Hypothesis: "Rogue cell"-type chromosomal damage in lymphocytes is associated with infection with the JC human polyoma virus and has implications for oncogenesis. Proc Natl Acad Sci USA 93: 2690-2695 (1996)
157. Allday MJ, Sinclair A, Parker G, Crawford DH, & Farrell PJ: Epstein-Barr virus efficiently immortalizes human B cells without neutralizing the function of p53. EMBO J 14: 1382-1391 (1995)
158. Bollag B, Prins C, Snyder EL, & Frisque RJ: Purified JC virus T and T' proteins differentially interact with the retinoblastoma family of tumor suppressor proteins. Virology 274: 165-178 (2000)
159. Cannell EJ, Farrell PJ, & Sinclair AJ: Epstein-Barr virus exploits the normal cell pathway to regulate Rb activity during the immortalisation of primary B-cells. Oncogene 13: 1413-1421 (1996)
160. Krynska B, Del Valle L, Gordon J, Otte J, Croul S, & Khalili K: Identification of a novel p53 mutation in JCV-induced mouse medulloblastoma. Virology 274: 65-74 (2000)