Polyomavirus JC in the context of immunosuppression: A series of adaptive, DNA replication-driven recombination events in the development of progressive multifocal leukoencephalopathy

Clinical and Developmental Immunology

Volumn 2013, Issue , 2013, Pages

  Johnson, Edward M ^a   Wortman, Margaret J ^a   Dagdanova, Ayuna V ^a   Lundberg, Patric S ^a   Daniel, Dianne C ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NONCODING CONTROL REGION; UNCLASSIFIED DRUG; VIRUS PROTEIN; UNTRANSLATED RNA;

AMINO ACID SEQUENCE; CELL TYPE; DNA REPLICATION; DNA STRUCTURE; IMMUNE DEFICIENCY; JC VIRUS; NONHUMAN; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PROTEIN SECONDARY STRUCTURE; REVIEW; VIRUS RECOMBINATION; VIRUS VIRULENCE; BRAIN; CONFORMATION; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; GLIA; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE; MUTATION; OLIGODENDROGLIA; PATHOLOGY; VIROLOGY; VIRUS REPLICATION;

BRAIN; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, VIRAL; HUMANS; IMMUNE TOLERANCE; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; LYMPHOCYTES; MUTATION; NEUROGLIA; NUCLEIC ACID CONFORMATION; OLIGODENDROGLIA; RNA, UNTRANSLATED; VIRUS REPLICATION;

EID: 84877269847     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2013/197807     Document Type: Review

References (82)

1. Grinnell B. W., Padgett B. L., Walker D. L., Distribution of nonintegrated DNA from JC papovavirus in organs of patients with progressive multifocal leukoencephalopathy. Journal of Infectious Diseases 1983 147 4 669 675 2-s2.0-0020580072 (Pubitemid 13088240)
2. Kean J. M., Rao S., Wang M., Garcea R. L., Seroepidemiology of human polyomaviruses. PLoS Pathogens 2009 5 3 e1000363 2-s2.0-63449123993 10.1371/journal.ppat.1000363
3. Knowles W. A., Discovery and epidemiology of the human polyomaviruses BK virus (BKV) and JC virus (JCV). Advances in Experimental Medicine and Biology 2006 577 19 45 2-s2.0-33745630722 10.1007/0-387-32957-9-2
4. Reid C. E., Li H., Sur G., Carmillo P., Bushnell S., Tizard R., McAuliffe M., Tonkin C., Simon K., Goelz S., Cinque P., Gorelik L., Carulli J. P., Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. Journal of Infectious Diseases 2011 204 2 237 244 2-s2.0-79958755750 10.1093/infdis/jir256
5. Berger J. R., Kaszovitz B., Post M. J. D., Dickinson G., Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection: a review of the literature with a report of sixteen cases. Annals of Internal Medicine 1987 107 1 78 87 2-s2.0-0023229323 (Pubitemid 17098643)
6. Cinque P., Koralnik I. J., Gerevini S., Miro J. M., Price R. W., Progressive multifocal leukoencephalopathy in HIV-1 infection. The Lancet Infectious Diseases 2009 9 10 625 636 2-s2.0-70349188237 10.1016/S1473-3099(09) 70226-9
7. Clifford D. B., Opportunistic viral infections in the setting of human immunodeficiency virus. Seminars in Neurology 1999 19 2 185 192 2-s2.0-0032858262 (Pubitemid 29477591)
8. Ferenczy M. W., Marshall L. J., Nelson C. D., Atwood W. J., Nath A., Khalili K., Major E. O., Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clinical Microbiology Reviews 2012 25 3 471 506
9. Johnson E. M., Structural evaluation of new human polyomaviruses provides clues to pathobiology. Trends in Microbiology 2010 18 5 215 223 2-s2.0-77952553011 10.1016/j.tim.2010.01.001
10. Major E. O., Amemiya K., Tornatore C. S., Houff S. A., Berger J. R., Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clinical Microbiology Reviews 1992 5 1 49 73 2-s2.0-0026500952
11. Padgett B. L., Rogers C. M., Walker D. L., JC virus, a human polyomavirus associated with progressive multifocal leukoencephalopathy: additional biological characteristics and antigenic relationships. Infection and Immunity 1977 15 2 656 662 2-s2.0-0017343810 (Pubitemid 8045504)
12. Berger J. R., Houff S., Progressive multifocal leukoencephalopathy: lessons from AIDS and natalizumab. Neurological Research 2006 28 3 299 305 2-s2.0-33646788719 10.1179/016164106X98198 (Pubitemid 43765116)
13. Clifford D. B., DeLuca A., Simpson D. M., Arendt G., Giovannoni G., Nath A., Natalizumab-associated progressive multifocal leukoencephalopathy in patients with multiple sclerosis: lessons from 28 cases. The Lancet Neurology 2010 9 4 438 446 2-s2.0-77949279537 10.1016/S1474-4422(10)70028-4
14. Gorelik L., Lerner M., Bixler S., Crossman M., Schlain B., Simon K., Pace A., Cheung A., Chen L. L., Berman M., Zein F., Wilson E., Yednock T., Sandrock A., Goelz S. E., Subramanyam M., Anti-JC virus antibodies: implications for PML risk stratification. Annals of Neurology 2010 68 3 295 303 2-s2.0-77956387401 10.1002/ana.22128
15. Tan C. S., Koralnik I. J., Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: clinical features and pathogenesis. The Lancet Neurology 2010 9 4 425 437 2-s2.0-77949297173 10.1016/S1474-4422(10) 70040-5
16. Chang C. F., Tada H., Khalili K., The role of a pentanucleotide repeat sequence, AGGGAAGGGA, in the regulation of JC virus DNA replication. Gene 1994 148 2 309 314 2-s2.0-0028126580 10.1016/0378-1119(94)90704-8 (Pubitemid 24333691)
17. Frisque R. J., White F. A., Roos R., The molecular biology of JC virus cative agent of progressive multifocal leukencephalopathy. Molecular Neurovirology 1992 Totowa, NJ, USA Humana Press
18. Gosert R., Kardas P., Major E. O., Hirsch H. H., Rearranged JC virus noncoding control regions found in progressive multifocal leukoencephalopathy patient samples increase virus early gene expression and replication rate. Journal of Virology 2010 84 20 10448 10456 2-s2.0-77957195722 10.1128/JVI.00614-10
19. Ault G. S., Stoner G. L., Two major types of JC virus defined in progressive multifocal leukoencephalopathy brain by early and late coding region DNA sequences. Journal of General Virology 1992 73 10 2669 2678 2-s2.0-0026722851
20. Gorelik L., Reid C., Testa M., Brickelmaier M., Bossolasco S., Pazzi A., Bestetti A., Carmillo P., Wilson E., McAuliffe M., Tonkin C., Carulli J. P., Lugovskoy A., Lazzarin A., Sunyaev S., Simon K., Cinque P., Progressive multifocal leukoencephalopathy (PML) development is associated with mutations in JC virus capsid protein VP1 that change its receptor specificity. The Journal of Infectious Diseases 2011 204 1 103 114
21. Stoner G. L., Ryschkewitsch C. F., Capsid protein VP1 deletions in JC virus from two AIDS patients with progressive multifocal leukoencephalopathy. Journal of Neurovirology 1995 1 2 189 194 2-s2.0-0029311751
22. Sunyaev S. R., Lugovskoy A., Simon K., Gorelik L., Adaptive mutations in the JC virus protein capsid are associated with progressive multifocal leukoencephalopathy (PML). PLoS Genetics 2009 5 2 2-s2.0-61449209921 10.1371/journal.pgen.1000368 e1000368
23. Li J. J., Kelly T. J., Simian virus 40 DNA replication in vitro. Proceedings of the National Academy of Sciences of the United States of America 1984 81 22 6973 6977 2-s2.0-0007914702 (Pubitemid 15216680)
24. Nathans D., Danna K. J., Specific origin in SV40 DNA replication. Nature 1972 236 68 200 202 2-s2.0-0015515837
25. Vassilev L., Johnson E. M., Mapping initiation sites of DNA replication in vivo using polymerase chain reaction amplification of nascent strand segments. Nucleic Acids Research 1989 17 19 7693 7705 2-s2.0-0024458475 (Pubitemid 19251941)
26. Stillman B., Chromatin assembly during SV40 DNA replication in vitro. Cell 1986 45 4 555 565 2-s2.0-0022519177 (Pubitemid 16014976)
27. Weinberg D. H., Collins K. L., Simancek P., Russo A., Wold M. S., Virshup D. M., Kelly T. J., Reconstitution of simian virus 40 DNA replication with purified proteins. Proceedings of the National Academy of Sciences of the United States of America 1990 87 22 8692 8696 2-s2.0-0025204504 10.1073/pnas.87.22. 8692 (Pubitemid 120007574)
28. Frisque R. J., Bream G. L., Cannella M. T., Human polyomavirus JC virus genome. Journal of Virology 1984 51 2 458 469 2-s2.0-0021242613 (Pubitemid 14091437)
29. Padgett B. L., Walker D. L., ZuRhein G. M., Eckroade R. J., Dessel B. H., Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. The Lancet 1971 1 7712 1257 1260 2-s2.0-0015232447
30. Padgett B. L., Walker D. L., ZuRhein G. M., Varakis J. N., Differential neurooncogenicity of strains of JC virus, a human polyoma virus, in newborn Syrian hamsters. Cancer Research 1977 37 3 718 720 2-s2.0-0017334193 (Pubitemid 8051633)
31. Yogo Y., Kitamura T., Sugimoto C., Ueki T., Aso Y., Hara K., Taguchi F., Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. Journal of Virology 1990 64 6 3139 3143 2-s2.0-0025302980 (Pubitemid 20171319)
32. Martin J. D., King D. M., Slauch J. M., Frisque R. J., Differences in regulatory sequences of naturally occurring JC virus variants. Journal of Virology 1985 53 1 306 311 2-s2.0-0021995514 (Pubitemid 15194972)
33. Chen N. N., Chang C. F., Gallia G. L., Kerr D. A., Johnson E. M., Krachmarov C. P., Barr S. M., Frisque R. J., Bollag B., Khalili K., Cooperative action of cellular proteins YB-1 and Pur α with the tumor antigen of the human JC polyomavirus determines their interaction with the viral lytic control element. Proceedings of the National Academy of Sciences of the United States of America 1995 92 4 1087 1091 2-s2.0-0028799664 10.1073/pnas.92.4.1087
34. Johnson E. M., The Pur protein family: clues to function from recent studies on cancer and AIDS. Anticancer Research A 2003 23 3 2093 2100 2-s2.0-0041304714 (Pubitemid 36897169)
35. Johnson E. M., Daniel D. C., Gordon J., The Pur protein family: genetic and structural features in development and disease. Journal of Cellular Physiology 2013 228 5 930 937 10.1002/jcp.24237
36. Khalili K., Del Valle L., Muralidharan V., Gault W. J., Darbinian N., Otte J., Meier E., Johnson E. M., Daniel D. C., Kinoshita Y., Amini S., Gordon J., Pur α is essential for postnatal brain development and developmentally coupled cellular proliferation as revealed by genetic inactivation in the mouse. Molecular and Cellular Biology 2003 23 19 6857 6875 2-s2.0-0141557777 10.1128/MCB.23.19.6857-6875.2003 (Pubitemid 37214656)
37. Krachmarov C. P., Chepenik L. G., Barr-Vagell S., Khalili K., Johnson E. M., Activation of the JC virus Tat-responsive transcriptional control element by association of the Tat protein of human immunodeficiency virus 1 with cellular protein Pur α Proceedings of the National Academy of Sciences of the United States of America 1996 93 24 14112 14117 2-s2.0-0030474833 10.1073/pnas.93.24.14112 (Pubitemid 26424254)
38. White M. K., Johnson E. M., Khalili K., Multiple roles for Puralpha in cellular and viral regulation. Cell Cycle 2009 8 3 1 7 2-s2.0-63649099035
39. Frisque R. J., Nucleotide sequence of the region encompassing the JC virus origin of DNA replication. Journal of Virology 1983 46 1 170 176 2-s2.0-0020693742 (Pubitemid 13161256)
40. Myers C., Frisque R. J., Arthur R. R., Direct isolation and characterization of JC virus from urine samples of renal and bone marrow transplant patients. Journal of Virology 1989 63 10 4445 4449 2-s2.0-0024417378 (Pubitemid 19229448)
41. Houff S. A., Berger J. R., The bone marrow, B cells, and JC virus. Journal of NeuroVirology 2008 14 5 341 343 2-s2.0-57049142007 10.1080/13550280802348222 (Pubitemid 352762873)
42. Houff S. A., Major E. O., Katz D. A., Kufta C. V., Sever J. L., Pittaluga S., Roberts J. R., 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. The New England Journal of Medicine 1988 318 5 301 305 2-s2.0-0023860204 (Pubitemid 18034522)
43. Marzocchetti A., Wuthrich C., Tan C. S., Tompkins T., Bernal-Cano F., Bhargava P., Ropper A. H., Koralnik I. J., Rearrangement of the JC virus regulatory region sequence in the bone marrow of a patient with rheumatoid arthritis and progressive multifocal leukoencephalopathy. Journal of NeuroVirology 2008 14 5 455 458 2-s2.0-57049182365 10.1080/13550280802356837 (Pubitemid 352762885)
44. Schneider E. M., Dorries K., High frequency of polyomavirus infection in lymphoid cell preparations after allogeneic bone marrow transplantation. Transplantation Proceedings 1993 25 1, part 2 1271 1273 2-s2.0-0027478242 (Pubitemid 23078983)
45. Tan C. S., Dezube B. J., Bhargava P., Autissier P., Wüthrich C., Miller J., Koralnik I. J., Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: implications for viral latency and neurotropic transformation. Journal of Infectious Diseases 2009 199 6 881 888 2-s2.0-65649083713 10.1086/597117
46. Chapagain M. L., Nerurkar V. R., Human polyomavirus JC (JCV) infection of luman B lymphocytes: a possible mechanism for JCV transmigration across the blood-brain barrier. Journal of Infectious Diseases 2010 202 2 184 191 2-s2.0-77954594238 10.1086/653823
47. Monaco M. C. G., Atwood W. J., Gravell M., Tornatore C. S., Major E. O., JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency. Journal of Virology 1996 70 10 7004 7012 2-s2.0-0029794531 (Pubitemid 26307415)
48. Rieckmann P., Michel U., Kehrl J. H., Regulation of JC virus expression in B lymphocytes. Journal of Virology 1994 68 1 217 222 2-s2.0-0027976781
49. Dorries K., Vogel E., Gunther S., Czub S., Infection of human polyomaviruses JC and BK in peripheral blood leukocytes from immunocompetent individuals. Virology 1994 198 2 59 70 2-s2.0-0028239405
50. Ault G. S., Stoner G. L., Human polyomavirus JC promoter/enhancer rearrangement patterns from progressive multifocal leukoencephalopathy brain are unique derivatives of a single archetypal structure. Journal of General Virology 1993 74, part 8 1499 1507 2-s2.0-0027297367 (Pubitemid 23243159)
51. + cells. Immunology 2001 104 4 410 417 2-s2.0-0035679747 10.1046/j.1365-2567.2001.01336.x (Pubitemid 34037833)
52. + hematopoietic progenitor cells from maternal peripheral blood. Blood 1997 89 7 2347 2358 2-s2.0-0030893721 (Pubitemid 27143281)
53. Sirard C., Lapidot T., Vormoor J., Cashman J. D., Doedens M., Murdoch B., Jamal N., Messner H., Addey L., Minden M., Laraya P., Keating A., Eaves A., Lansdorp P. M., Eaves C. J., Dick J. E., Normal and leukemic SCID-repopulating cells (SRC) coexist in the bone marrow and peripheral blood from CML patients in chronic phase, whereas leukemic SRC are detected in blast crisis. Blood 1996 87 4 1539 1548 2-s2.0-13344262695 (Pubitemid 26056919)
54. Newman J. T., Frisque R. J., Identification of JC virus variants in multiple tissues of pediatric and adult PML patients. Journal of Medical Virology 1999 58 1 79 86 (Pubitemid 29172126)
55. White F. A. III, Ishaq M., Stoner G. L., Frisque R. J., JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. Journal of Virology 1992 66 10 5726 5734 2-s2.0-0026671618
56. Perez-Liz G., Del Valle L., Gentilella A., Croul S., Khalili K., Detection of JC virus DNA fragments but not proteins in normal brain tissue. Annals of Neurology 2008 64 4 379 387 2-s2.0-55849085378 10.1002/ana.21443
57. Chapagain M. L., Verma S., Mercier F., Yanagihara R., Nerurkar V. R., Polyomavirus JC infects human brain microvascular endothelial cells independent of serotonin receptor 2A. Virology 2007 364 1 55 63 2-s2.0-34249661722 10.1016/j.virol.2007.02.018 (Pubitemid 46829276)
58. Weaver D. T., Fields-Berry S. C., DePamphilis M. L., The termination region for SV40 DNA replication directs the mode of separation for the two sibling molecules. Cell 1985 41 2 565 575 2-s2.0-0022343627 (Pubitemid 16219426)
59. Tapper D. P., DePamphilis M. L., Preferred DNA sites are involved in the arrest and initiation of DNA synthesis during replication of SV40 DNA. Cell 1980 22 1, part 1 97 108 2-s2.0-0019135281 (Pubitemid 11226432)
60. Weaver D. T., DePamphilis M. L., The role of palindromic and non-palindromic sequences in arresting DNA synthesis in vitro and in vivo. Journal of Molecular Biology 1984 180 4 961 986 2-s2.0-0021633812 (Pubitemid 15016238)
61. Herzberg K., Bashkirov V. I., Rolfsmeier M., Haghnazari E., McDonald W. H., Anderson S., Bashkirova E. V., Yates J. R., Heyer W. D., Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Molecular and Cellular Biology 2006 26 22 8396 8409 2-s2.0-33750990221 10.1128/MCB.01317-06 (Pubitemid 44748573)
62. Hoadley K. A., Xue Y., Ling C., Takata M., Wang W., Keck J. L., Defining the molecular interface that connects the Fanconi anemia protein FANCM to the Bloom syndrome dissolvasome. Proceedings of the National Academy of Sciences of the United States of America 2012 109 12 4437 4442 10.1073/pnas.1117279109
63. Kamath-Loeb A. S., Shen J. C., Schmitt M. W., Loeb L. A., The Werner syndrome exonuclease facilitates DNA degradation and high fidelity DNA polymerization by human DNA polymerase delta. The Journal of Biological Chemistry 2012 287 15 12480 12490 10.1074/jbc.M111.332577
64. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., Takeda S., Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair 2006 5 9-10 1021 1029 2-s2.0-33747889217 10.1016/j.dnarep.2006.05.022 (Pubitemid 44291617)
65. Weitao T., Budd M., Hoopes L. L. M., Campbell J. L., Dna2 helicase/nuclease causes replicative fork stalling and double-strand breaks in the ribosomal DNA of Saccharomyces cerevisiae. Journal of Biological Chemistry 2003 278 25 22513 22522 2-s2.0-0038604455 10.1074/jbc.M301610200 (Pubitemid 36830306)
66. Weaver D. T., DePamphilis M. L., Specific sequences in native DNA that arrest synthesis by DNA polymerase alpha. Journal of Biological Chemistry 1982 257 4 2075 2086 2-s2.0-0020490330
67. Shah S. N., Opresko P. L., Meng X., Lee M. Y. W. T., Eckert K. A., DNA structure and the Werner protein modulate human DNA polymerase delta-dependent replication dynamics within the common fragile site FRA16D. Nucleic Acids Research 2009 38 4 1149 1162 2-s2.0-77950355795 10.1093/nar/gkp1131
68. Voineagu I., Narayanan V., Lobachev K. S., Mirkin S. M., Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proceedings of the National Academy of Sciences of the United States of America 2008 105 29 9936 9941 2-s2.0-48249141027 10.1073/pnas.0804510105
69. Walsh E., Wang X., Lee M. Y., Eckert K. A., Mechanism of replicative DNA polymerase delta pausing and a potential role for DNA polymerase kappa in common fragile site replication. Journal of Molecular Biology 2013 425 2 232 243
70. Karpenshif Y., Bernstein K. A., From yeast to mammals: recent advances in genetic control of homologous recombination. DNA Repair 2012 11 10 781 788 10.1016/j.dnarep.2012.07.001
71. Allen C., Ashley A. K., Hromas R., Nickoloff J. A., More forks on the road to replication stress recovery. Journal of Molecular Cell Biology 2011 3 1 4 12
72. Zuker M., Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 2003 31 13 3406 3415 2-s2.0-0042121256 10.1093/nar/gkg595 (Pubitemid 37442169)
73. Mirkin S. M., DNA structures, repeat expansions and human hereditary disorders. Current Opinion in Structural Biology 2006 16 3 351 358 2-s2.0-33744807443 10.1016/j.sbi.2006.05.004 (Pubitemid 43831649)
74. Jenab S., Johnson E. M., A dual-circular plasmid structure dependent on DNA replication generated in monkey COS7 cells and cell extracts. Biochemical and Biophysical Research Communications 1989 160 1 53 59 2-s2.0-0024573579 (Pubitemid 19116460)
75. Holliday R., The recombination, repair and modification of DNA. DNA Repair 2011 10 10 993 999 10.1016/j.dnarep.2011.04.005
76. Berger J. R., Clifford D. B., The manifold faces of PML and the challenge of diagnosis. Neurology 2011 77 23 2006 2007 10.1212/WNL.0b013e31823b9c8f
77. Chowdhury M., Taylor J. P., 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 1990 5 12 1737 1742 2-s2.0-0025650314 (Pubitemid 120034698)
78. Daniel D. C., Kinoshita Y., Khan M. A., Del Valle L., Khalili K., Rappaport J., Johnson E. M., Internalization of exogenous human immunodeficiency virus-1 protein, Tat, by KG-1 oligodendroglioma cells followed by stimulation of DNA replication initiated at the JC virus origin. DNA and Cell Biology 2004 23 12 858 867 2-s2.0-10344253813 10.1089/dna.2004.23.858 (Pubitemid 39628294)
79. Gallia G. L., Johnson E. M., Khalili K., Survey and summary: puralpha: a multifunctional single-stranded DNA- and RNA-binding protein. Nucleic Acids Research 2000 28 17 3197 3205 10.1093/nar/28.17.3197 (Pubitemid 30662283)
80. Gallia G. L., Safak M., Khalili K., Interaction of the single-stranded DNA-binding protein Pur α with the human polyomavirus JC virus early protein T-antigen. Journal of Biological Chemistry 1998 273 49 32662 32669 2-s2.0-0032484017 10.1074/jbc.273.49.32662 (Pubitemid 28557649)
81. Daniel D. C., Wortman M. J., Schiller R. J., Liu H., Gan L., Mellen J. S., Chang C. F., Gallia G. L., Rappaport J., Khalili K., Johnson E. M., Coordinate effects of human immunodeficiency virus type 1 protein Tat and cellular protein Pur α on DNA replication initiated at the JC virus origin. Journal of General Virology 2001 82, part 7 1543 1553 2-s2.0-0034959094 (Pubitemid 32611494)
82. Engsig F. N., Hansen A. B. E., Omland L. H., Kronborg G., Gerstoft J., Laursen A. L., Pedersen C., Mogensen C. B., Nielsen L., Obel N., Incidence, clinical presentation, and outcome of progressive multifocal leukoencephalopathy in HIV-infected patients during the highly active antiretroviral therapy era: a nationwide cohort study. Journal of Infectious Diseases 2009 199 1 77 83 2-s2.0-58749083385 10.1086/595299