High sensitivity detection of JC-virus DNA in postmortem brain tissue by in situ PCR

Journal of NeuroVirology

Volumn 6, Issue 1, 2000, Pages 61-74

  Samorei, Ingrid W ^a   Schmid, Michael ^b   Pawlita, Michael ^c   Vinters, Harry V ^d   Diebold, Klaus ^a   Mundt, Christoph ^a   Von Einsiedel, Regina W ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Institute of Virology   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UCLA MEDICAL CENTER   (United States)

Author keywords

Human immunodeficiency virus (HIV); In situ hybridization (ISH); In situ PCR; JC virus (JCV); Progressive multifocal leukoencephalopathy (PML)

Indexed keywords

HYDROGEN PEROXIDE; MYELIN; REAGENT; VIRUS DNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; ASTROCYTE; AUTOPSY; BRAIN TISSUE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DEVICE; DNA DETERMINATION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; INTERMETHOD COMPARISON; JC VIRUS; MICROSCOPY; NEUROPATHOLOGY; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY;

HUMAN IMMUNODEFICIENCY VIRUS; JC VIRUS;

EID: 0034025264     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.3109/13550280009006383     Document Type: Article

References (80)

1. Agostini HT, Ryschkewitsch CF, Mory R, Singer EJ, Stoner GL (1997a). JC virus (JCV) genotypes in brain tissue from patients with progressive multifocal leukoencephalopathy (PML) and in urine from controls without PML: increased frequency of JCV type 2 in PML. J Infect Dis 176: 1-8.
2. Agostini HT, Ryschkewitsch CF, Singer EJ, Stoner GL (1997b). JC virus regulatory region rearrangements and genotypes in progressive multifocal leukoencephalopathy: two independent aspects of virus variation. J Gen Virol 78: 659-664.
3. Aksamit AJ, Mourrain P, Sever JL, Major EO (1985). Progressive multifocal leukoencephalopathy: investigation of three cases using in situ hybridization with JC virus biotinylated DNA probe. Ann Neurol 18: 490-496.
4. Aksamit AJ, Sever JL, Major EO (1986). Progressive multifocal leukoencephalopathy: JC virus detection by in situ hybridization compared with immunohistochemistry. Neurology 36: 499-504.
5. Aksamit AJ, Major EO, Ghatak NR, Sidhu GS, Parisi JE, Guccion JG (1987). Diagnosis of progressive multifocal leukoencephalopathy by brain biopsy with biotin labeled DNA : DNA in situ hybridization. J Neuropathol Exp Neurol 46: 556-566.
6. Aksamit AJ, Gendelman HE, Orenstein JM, Pezeshkpour GH (1990). AIDS-associated progressive multifocal leukoencephalopathy (PML): comparison to non-AIDS PML with in situ hybridization and immunohisto-chemistry. Neurology 40: 1073-1078.
7. Anders KH, Guerra WF, Tomiyasu U, Verity MA, Vinters HV (1986). The neuropathology of AIDS. UCLA Experience and Review. Am J Pathol 124: 537-558.
8. Antinori A, Ammassari A, De Luca A, Cingolani A, Murri R, Scoppettuolo G, Fortini M, Tartaglione T, Larocca LM, Zannoni G, Cattani P, Grillo R, Roselli R, Iacoangeli M, Scerrati M, Ortona L (1997). Diagnosis of AIDS-related focal brain lesions: a decision-making analysis based on clinical and neuroradiologic characteristics combined with polymerase chain reaction assays in CSF. Neurology 48: 687-694.
9. Arthur RR, Dagostin S, Shah KV (1989). Detection of BK virus and JC virus in urine and brain tissue by the polymerase chain reaction. J Clin Microbiol 27: 1174-1179.
10. Aström KE, Mancall EL, Richardson EP (1958). Progressive multifocal leukoencephalopathy. Brain 81: 93-111.
11. Ault GS (1997). Activity of JC virus archetype and PML-type regulatory regions. J Gen Virol 78: 163-169.
12. Azzi A, De Santis R, Ciappi S, Leoncini F, Sterrantino G, Marino N, Mazzotta F, Laszlo D, Fanci R, Bosi A (1996). Human polyomaviruses DNA detection in peripheral blood leukocytes from immunocompetent and immunocompromised individuals. J Neurovirol 2: 411-416.
13. Bagasra O, Hauptman SP, Lischner HW, Sachs M, Pomerantz RJ (1992). Detection of human immunodeficiency virus type 1 provirus in mononuclear cells by in situ polymerase chain reaction. N Engl J Med 326: 1385-1391.
14. Bagasra O, Seshamma T, Pomerantz RJ (1993). Polymerase chain reaction in situ: intracellular amplification and detection of HIV-1 proviral DNA and other specific genes. J Immunol Methods 158: 131-145.
15. Bagasra O, Lavi E, Bobroski L, Khalili K, Pestaner JP, Tawadros R, Pomerantz RJ (1996). Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: identification by the combination of in situ polymerase chain reaction and imminohisto-chemistry. AIDS 10: 573-585.
16. Bagasra O, Bobroski L, Sarker A, Bagasra A, Saikumari P, Pomerantz RJ (1997). Absence of the inducible form of nitric oxide synthase in the brains of patients with the acquired immunodeficiency syndrome. J Neurovirol 3: 153-167.
17. Boldorini R, Cristina S, Vago L, Tosoni A, Guzzetti S, Costanzi G (1993). Ultrastrucrtural studies in the lytic phase of progressive multifocal leukoencephalopathy in AIDS patients. Ultrastruct Pathol 17: 599-609.
18. Boshoff C, Schulz TF, Kennedy MM, Graham AK, Fisher C, Thomas A, McGee JO, Weiss RA, O'Leary JJ (1995). Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat Med 1: 1274-1278.
19. Brooks BR, Walker DL (1984). Progressive multifocal leukoencephalopathy. Neurol Clin 2: 299-313.
20. Chen RH, Fuggle SV (1993). In situ cDNA polymerase chain reaction. A novel technique for detecting mRNA expression. Am J Pathol 143: 1527-1534.
21. Cheng JD, Nuovo GJ (1994). Utility of reverse transcriptase (RT) in situ polymerase chain reaction (PCR) in the diagnosis of viral infections. J Histotechnol 17: 247-251.
22. Chesters PM, Heritage J, McCance DJ (1983). Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J Infect Dis 147: 676-684.
23. Chiu KP, Cohen SH, Morris DW, Jordan GW (1992). Intracellular amplification of proviral DNA in tissue sections using the polymerase chain reaction. J Histochem Cytochem 40: 333-341.
24. Dörries K (1984). Progressive multifocal leukoencephalopathy: analysis of JC virus DNA from brain and kidney tissue. Virus Res 1: 25-38.
25. Dörries K, Loeber G, Meixensberger J (1987). Association of polyomaviruses JC, SV40, and BK with human brain tumors. Virology 160: 268-270.
26. Dörries K, Arendt G, Eggers C, Roggendorf W, Dörries R (1998). Nucleic acid detection as a diagnostic tool in polyomavirus JC induced progressive multifocal leukoencephalopathy. J Med Virol 54: 196-203.
27. Dubois V, Dutronc H, Lafon ME, Poinsot V, Pellegrin JL, Ragnaud JM, Ferrer AM, Fleury HJ (1997). Latency and reactivation of JC virus in peripheral blood of human immunodeficiency virus type 1-infected patients. J Clin Microbiol 35: 2288-2292.
28. Einsiedel von RW, Fife TD, Aksamit AJ, Cornford ME, Secor DL, Tomiyasu U, Itabashi HH, Vinters HV (1993). Progressive multifocal leukoencephalopathy in AIDS: a clinicopathologic study and review of the literature. J Neurol 240: 391-406.
29. Elsner C, Dörries K (1992). Evidence of human polyomavirus BK and JC infection in normal brain tissue. Virology 191: 72-80.
30. Embretson J, Zupancic M, Beneke J, Till M, Wolinsky S, Ribas JL, Burke A, Haase AT (1993). Analysis of human immunodeficiency virus-infected tissues by amplification and in situ hybridization reveals latent and permissive infections at single-cell resolution. Proc Natl Acad Sci USA 90: 357-361.
31. Ferrante P, Caldarelli-Stefano R, Omodeo-Zorini E, Vago L, Boldorini R, Costanzi G (1995). PCR detection of JC virus DNA in brain tissue from patients with and without progressive multifocal leukoencephalopathy. J Med Virol 47: 219-225.
32. Gallia GL, Houff SA, Major EO, Khalili K (1997). Review: JC virus infection of lymphocytes-revisited. J Infect Dis 176: 1603-1609.
33. Grinnell BW, Martin JD, Padgett BL, Walker DL (1983). Naturally occurring and passage-induced variation in the genome of JC virus. Prog Clin Biol Res 105: 61-77.
34. Hamann K, Menke M, Peters J, Carstens A, Weisner D, Krams M, Pawaresch MR (1996). Detection of interleukin 6 mRNA in human lymph node tissue on the GeneAmp in situ PCR system 1000. Research News, Perkin Elmer Applied Biosystems.
35. Houff SA, Major E, Katz DA, Kufta CV, Sever JL, Pittaluga S, Roberts JR, Gitt J, Saini N, Lux W (1988). Involvement of JC virus-infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy. N Engl J Med 318: 301-305.
36. Isaacson SH, Asher DM, Gajdusek DC, Gibbs Jr CJ (1994). Detection of RNA viruses in archival brain tissue by in situ RT-PCR amplification and labeled-probe hybridization. Cell Vis 1: 25-29.
37. Itoyama Y, Webster HD, Sternberger NH, Richardson EJ, Walker DL, Querles RH, Padgett BL (1982). Distribution of papovavirus, myelin-associated glycoprotein, and myelin basic protein in progressive multifocal leukoencephalopathy lesions. Ann Neurol 11: 396-407.
38. Jochum W, Weber T, Frye S, Hunsmann G, Luke W, Aguzzi A (1997). Detection of JC virus by anti-VP1 immunohistochemistry in brains with progressive multifocal leukoencephalopathy. Acta Neuropathol 94: 226-231.
39. Kepes J, Chou S, Price LJ (1975). Progressive leukoencephalopathy with 10 year survival in a patient with nontropical sprue: report of a case with unusual light and electron microscopic features. Neurology 25: 1006-1012.
40. Kitamura T, Sugimoto C, Kato A, Ebihara H, Suzuki M, Taguchi F, Kawabe K, Yogo Y (1997). Persistent JC virus (JCV) infection is demonstrated by continuous shedding of the same JCV strains. J Clin Microbiol 35: 1255-1257.
41. Komminoth P, Long AA, Ray R, Wolfe HJ (1992). In situ polymerase chain reaction detection of viral DNA, single-copy genes, and gene rearrangements in cell suspensions and cytospins. Diagn Mol Pathol 1: 85-97.
42. Komminoth P, Heitz PhU, Long AA (1994a). In situ polymerase chain reaction: general methodology and recent advances. Verh Dtsch Ges Path 78: 146-152.
43. Komminoth P, Adams V, Long AA, Roth J, Saremaslani P, Flury R, Schmid M, Heitz PhU (1994b). Evaluation of methods for hepatitis C virus detection in archival liver biopsies: Comparison of histology, immunohistochemistry, in-situ hybridization, reverse transcriptase polymerase chain reaction (RT-PCR) and in situ RT-PCR. Path Res Pract 190: 1017-1025.
44. Kuchelmeister K, Bergmann M, Gullotta F (1993). Cellular changes in the cerebellar granular layer in AIDS-associated PML. Neuropathol Appl Neurobiol 19: 398-401.
45. Lafon ME, Dutronc H, Dubois V, Pellegrin I, Barbeau P, Ragnaud JM, Pellegrin JL, Fleury HJ (1998). JC virus remains latent in peripheral blood B lymphocytes but replicates actively in urine from AIDS patients. J Infect Dis 177: 1502-1505.
46. Levin MC, Fox RJ, Lehky T, Walter M, Fox CH, Flerlage N, Bamford R, Jacobson S (1996). PCR-in situ hybridization detection of human T-cell lymphotropic virus type 1 (HTLV-1) tax proviral DNA in peripheral blood lymphocytes of patients with HTLV-1-associated neurologic disease. J Virol 70: 924-933.
47. Lewis F (1996). An approach to in situ PCR. In situ PCR manual. Perkin Elmer Applied Biosystems: Foster City, CA, USA.
48. Long AA, Komminoth P, Wolfe HJ (1993). Comparison of indirect and direct in situ polymerase chain reaction in cell preparations and tissue sections. Histochemistry 99: 151-162.
49. Martinez A, Miller M, Quinn K, Unsworth EJ, Ebina M, Cuttitta F (1995). Non-radioactive localization of nucleic acids by direct in situ PCR and in situ RT-PCR in paraffin-embedded sections. J Histochem Cytochem 43: 739-747.
50. Mazlo M, Tariska I (1980). Morphological demonstration of the first phase of polyomavirus replication in oligodendroglia cells of human brain in progressive multifocal leucoencephalopathy (PML). Acta Neuropathol 49: 133-143.
51. Mazlo M, Tariska I (1982) Are astrocytes infected in progressive multifocal leukoencephalopathy (PML)? Acta Neuropathol 56: 45-51.
52. Monaco MC, Atwood WJ, Gravell M, Tornatore CS, Major EO (1996). JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency. J Virol 70: 7004-7012.
53. Mori M, Kurata H, Tajima M, Shimada H (1991) JC virus detection by in situ hybridization in brain tissue from elderly patients. Ann Neurol 29: 428-432.
54. Muciaccia B, Uccini S, Filippini A, Ziparo E, Paraire F, Baroni CD, Stefanini M (1998). Presence and cellular distribution of HIV in the testes of seropositive subjects: an evaluation by in situ PCR hybridization. FASEB J 12: 151-163.
55. Myers C, Frisque RJ, Arthur RR (1989). Direct isolation and characterization of JC virus from urine samples of renal and bone marrow transplant patients. J Virol 63: 4445-4449.
56. Naif H and Cunningham A (1996). In situ PCR for detection of HIV using digoxygenin-labeled oligonucleotides. PCR-Bibliographie Sonderheft. pp 88-89, Boehringer Mannheim: Mannheim, Germany.
57. Nuovo GJ, Gallery F, MacConnell P, Becker J, Bloch W (1991a). An improved technique for the in situ detection of DNA after polymerase chain reaction amplification. Am J Pathol 139: 1239-1244.
58. Nuovo GJ, MacConnell P, Forde A, Delvenne P (1991b). Detection of human papillomavirus DNA in formalin-fixed tissues by in situ hybridization after amplification by polymerase chain reaction. Am J Pathol 139: 847-854.
59. Nuovo GJ, Gorgone GA, MacConnell P, Margiotta M, Gorevic PD (1992). In situ localization of PCR-amplified human and viral cDNAs. PCR Methods Appl 2: 117-123.
60. Nuovo GJ, Lidonnici K, MacConnell P, Lane B (1993). Intracellular localization of polymerase chain reaction (PCR)-amplified hepatitis C cDNA. Am J Surg Pathol 17: 683-690.
61. Nuovo GJ and Forde A (1995). An improved system for reverse transcriptase in situ PCR. J Histotechnol 18: 295-299.
62. O'Leary JJ, Browne G, Landers RJ, Crowley M, Healy I, Street JT, Pollock AM, Murphy J, Johnsons MI, Lewis FA, Mohamdee O, Cullinane C, Doyle CT (1994). The importance of fixation procedures on DNA template and its suitability for solution-phase polymerase chain reaction and PCR in situ hybridization. Histochem J 26: 337-346.
63. Ohshima K, Kikuchi M, Kobari S, Masuda Y, Yoneda S, Takeshita M (1995). Demonstration of Epstein-Barr virus genomes, using polymerase chain reaction in situ hybridization in paraffin-embedded lymphoid tissues. Pathol Res Pract 191: 139-147.
64. Peters J, Krams M, Wacker HH, Carstens A, Weisner D, Hamann K, Menke M, Harms D, Parwaresch R (1997). Detection of rare RNA sequences by single-enzyme in situ reverse transcription-polymerase chain reaction. High-resolution analyses of interleukin-6 mRNA in paraffin sections of lymph nodes. Am J Pathol 150: 469-476.
65. Pietzuch A, Bodemer M, Frye S, Cinque P, Trebst C, Lüke W, Weber T (1996). Expression of JCV-specific cDNA in peripheral blood lymphocytes of palients with PML, HIV infection, multiple sclerosis and in healthy controls. J Neurovirol 2: 46.
66. Richardson EP (1961). Progressive multifocal leukoencephalopathy. N Engl J Med 265: 815-823.
67. Sällström JF, Zehbe I, Alemi M, Wilander E (1993). Pitfalls of in situ polymerase chain reaction (PCR) using direct incorporation of labeled nucleotides. Anticancer Res 13: 1153-1154.
68. Simon S, Reipert B, Eibl MM, Steinkasserer A (1997). Detection of phosphatidylinositol glycan class A gene transcripts by RT in situ PCR hybridization: a comparative study using fluorescein, texas red, and digoxygenin-11 dUTP for color detection. J Histochem Cytochem 45: 1659-1664.
69. Strayer DS, Duan I, Ozaki J, Milano LE, Bobraski LE, Bagasra O (1997), Titering replication-defective virus for use in gene transfer. Biotechniques 22: 447-450.
70. Tani K, Kurokawa K, Nasu M (1998). Development of a direct in situ PCR method for detection of specific bacteria in natural environments. Appl Environ Microbiol 64: 1536-1540.
71. Telenti A, Aksamit AJJ, Proper J, Smith TF (1990). Detection of JC virus DNA by polymerase chain reaction in patients with progressive multifocal leukoencephalopathy. J Infect Dis 162: 858-861.
72. Tolker-Nielsen T, Holmstrom K, Molin S (1997). Visualization of specific gene expression in individual Salmonella typhimurium cells by in situ PCR. Appl Environ Microbiol 63: 4196-4203.
73. Walker F, Bedel C, Dauge-Geffroy MC, Lehy T, Madelenat P, Potet F (1996). Improved detection of human papillomavirus infection in genital intraepithelial neoplasia in human immunodeficiency virus positive (HIV +) women by polymerase chain reaction-in situ hybridization. Diagn Mol Pathol 5: 136-146.
74. Weber T, Klapper PE, Cleator GM, Bodemer M, Luke W, Knowles W, Cinque P, Van Loon AM, Grandien M, Hammarin AL, Ciardi M, Bogdanovic G (1997). Polymerase chain reaction for detection of JC virus DNA in cerebrospinal fluid: a quality control study. European Union Concerted Action on Viral Meningitis and Encephalitis. J Virol Methods 69: 231-237.
75. Weber T, Major EO (1997), Progressive multifocal leukoencephalopathy: molecular biology, pathogenesis and clinical impact. Intervirology 40: 98-111.
76. White FA, Ishaq M, Stoner GL, Frisque RJ (1992). JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. J Virol 66: 5726-5734.
77. Xie B, Oyamada T, Yoshikawa H, Oyamada T, Yoshikawa T (1997). Detection of proviral DNA of bovine leukaemia virus in cattle by a combination of in-situ hybridization and the polymerase chain reaction. J Comp Pathol 116: 87-96.
78. Yin J, Kaplitt MG, Kwong AD, Pfaff DW (1998). In situ PCR for in vivo detection of foreign genes transferred into rat brain. Brain Res 783: 347-354.
79. Zehbe I, Hacker GW, Sällström JF, Muss W, Hauser-Kronberger C, Rylander E, Wilander E (1994). PCR in situ hybridization (PISH) and in situ self-sustained sequence replication-based amplification (in situ 3SR). Cell Vis 1: 46-47.
80. ZuRhein GM, Chou SM (1965). Particles resembling papova viruses in human cerebral demyelinating disease. Science 148: 1477-1479.