JC virus reactivation during prolonged natalizumab monotherapy for multiple sclerosis

Annals of Neurology

Volumn 75, Issue 6, 2014, Pages 925-934

  Chalkias, Spyridon ^a   Dang, Xin ^a,b   Bord, Evelyn ^a,b   Stein, Marion C ^b   Kinkel, R Philip ^b   Sloane, Jacob A ^b   Donnelly, Maureen ^b   Ionete, Carolina ^c   Houtchens, Maria K ^d   Buckle, Guy J ^d   Batson, Stephanie ^a,b   Koralnik, Igor J ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; BETA1A INTERFERON; CD34 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CYCLOPHOSPHAMIDE; MITOXANTRONE; NATALIZUMAB; VIRUS DNA;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; BLOOD ANALYSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SELECTION; CELLULAR IMMUNITY; CEREBROSPINAL FLUID; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; FEMALE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; JC VIRUS; LONG TERM CARE; MALE; MONOCYTE; MONONUCLEAR CELL; MONOTHERAPY; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMORPHONUCLEAR CELL; PREVALENCE; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TREATMENT DURATION; URINALYSIS; VIRUS LOAD; VIRUS REACTIVATION;

ADULT; AGED; ANTIBODIES, MONOCLONAL, HUMANIZED; DNA, VIRAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOLOGIC FACTORS; INTERFERON-BETA; INTERFERON-GAMMA; JC VIRUS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; POLYOMAVIRUS INFECTIONS; RETROSPECTIVE STUDIES; STATISTICS AS TOPIC; T-LYMPHOCYTES; TIME FACTORS;

EID: 84903700329     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24148     Document Type: Article

References (49)

1. Tan CS, Koralnik IJ,. Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: clinical features and pathogenesis. Lancet Neurol 2010; 9: 425-437.
2. Major EO,. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu Rev Med 2010; 61: 35-47.
3. Bloomgren G, Richman S, Hotermans C, et al. Risk of natalizumab- associated progressive multifocal leukoencephalopathy. N Engl J Med 2012; 366: 1870-1880.
4. Sorensen PS, Bertolotto A, Edan G, et al. Risk stratification for progressive multifocal leukoencephalopathy in patients treated with natalizumab. Mult Scler 2012; 18: 143-152.
5. Alvarez-Lafuente R, Garcia-Montojo M, De Las Heras V, et al. Interferon-beta treatment and active replication of the JC virus in relapsing-remitting multiple sclerosis patients. Eur J Neurol 2007; 14: 233-236.
6. Chen Y, Bord E, Tompkins T, et al. Asymptomatic reactivation of JC virus in patients treated with natalizumab. N Engl J Med 2009; 361: 1067-1074.
7. Dominguez-Mozo MI, Garcia-Montojo M, De Las Heras V, et al. Anti-JCV antibodies detection and JCV DNA levels in PBMC, serum and urine in a cohort of Spanish multiple sclerosis patients treated with natalizumab. J Neuroimmune Pharmacol 2013; 8: 1277-1286.
8. Fragoso YD, Mendes MF, Arruda WO, et al. Nearly one-half of Brazilian patients with multiple sclerosis using natalizumab are DNA-JC virus positive. Arq Neuropsiquiatr 2013; 71: 780-782.
9. Hendel-Chavez H, de Goer de Herve MG, Giannesini C, et al. Immunological hallmarks of JC virus replication in multiple sclerosis patients on long-term natalizumab therapy. J Virol 2013; 87: 6055-6059.
10. Jilek S, Jaquiery E, Hirsch HH, et al. Immune responses to JC virus in patients with multiple sclerosis treated with natalizumab: a cross-sectional and longitudinal study. Lancet Neurol 2010; 9: 264-272.
11. Lin J, Bettin P, Lee JK, et al. Cerebrospinal fluid and serum JC virus antibody detection in multiple sclerosis patients treated with natalizumab. J Neuroimmunol 2013; 261: 123-128.
12. Perkins MR, Ryschkewitsch C, Liebner JC, et al. Changes in JC virus-specific T cell responses during natalizumab treatment and in natalizumab-associated progressive multifocal leukoencephalopathy. PLoS Pathog 2012; 8: e1003014.
13. Sadiq SA, Puccio LM, Brydon EW,. JCV detection in multiple sclerosis patients treated with natalizumab. J Neurol 2010; 257: 954-958.
14. Schwab N, Hohn KG, Schneider-Hohendorf T, et al. Immunological and clinical consequences of treating a patient with natalizumab. Mult Scler 2012; 18: 335-344.
15. Lee P, Plavina T, Castro A, et al. A second-generation ELISA (STRATIFY JCV DxSelect) for detection of JC virus antibodies in human serum and plasma to support progressive multifocal leukoencephalopathy risk stratification. J Clin Virol 2013; 57: 141-146.
16. Ryschkewitsch C, Jensen P, Hou J, et al. Comparison of PCR-Southern hybridization and quantitative real-time PCR for the detection of JC and BK viral nucleotide sequences in urine and cerebrospinal fluid. J Virol Methods 2004; 121: 217-221.
17. Gheuens S, Bord E, Kesari S, et al. Role of CD4+ and CD8+ T-cell responses against JC virus in the outcome of patients with progressive multifocal leukoencephalopathy (PML) and PML with immune reconstitution inflammatory syndrome. J Virol 2011; 85: 7256-7263.
18. Berger JR, Aksamit AJ, Clifford DB, et al. PML diagnostic criteria: consensus statement from the AAN Neuroinfectious Disease Section. Neurology 2013; 80: 1430-1438.
19. Koralnik IJ, Wuthrich C, Dang X, et al. JC virus granule cell neuronopathy: a novel clinical syndrome distinct from progressive multifocal leukoencephalopathy. Ann Neurol 2005; 57: 576-580.
20. Iacobaeus E, Ryschkewitsch C, Gravell M, et al. Analysis of cerebrospinal fluid and cerebrospinal fluid cells from patients with multiple sclerosis for detection of JC virus DNA. Mult Scler 2009; 15: 28-35.
21. Alvarez-Lafuente R, Garcia-Montojo M, De Las Heras V, et al. JC virus in cerebrospinal fluid samples of multiple sclerosis patients at the first demyelinating event. Mult Scler 2007; 13: 590-595.
22. Koralnik IJ, Boden D, Mai VX, et al. JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology 1999; 52: 253-260.
23. Yousry TA, Pelletier D, Cadavid D, et al. Magnetic resonance imaging pattern in natalizumab-associated progressive multifocal leukoencephalopathy. Ann Neurol 2012; 72: 779-787.
24. Wattjes MP, Richert ND, Killestein J, et al. The chameleon of neuroinflammation: magnetic resonance imaging characteristics of natalizumab-associated progressive multifocal leukoencephalopathy. Mult Scler 2013; 19: 1826-1840.
25. Wattjes MP, Verhoeff L, Zentjens W, et al. Punctate lesion pattern suggestive of perivascular inflammation in acute natalizumab-associated progressive multifocal leukoencephalopathy: productive JC virus infection or preclinical PML-IRIS manifestation? J Neurol Neurosurg Psychiatry 2013; 84: 1176-1177.
26. Phan-Ba R, Lommers E, Tshibanda L, et al. MRI preclinical detection and asymptomatic course of a progressive multifocal leucoencephalopathy (PML) under natalizumab therapy. J Neurol Neurosurg Psychiatry 2012; 83: 224-226.
27. Wuthrich C, Popescu BF, Gheuens S, et al. Natalizumab-associated progressive multifocal leukoencephalopathy in a patient with multiple sclerosis: a postmortem study. J Neuropathol Exp Neurol 2013; 72: 1043-1051.
28. Mancuso R, Saresella M, Hernis A, et al. JC virus detection and JC virus-specific immunity in natalizumab-treated multiple sclerosis patients. J Transl Med 2012; 10: 248.
29. Major EO, Frohman E, Douek D,. JC viremia in natalizumab-treated patients with multiple sclerosis. N Engl J Med 2013; 368: 2240-2241.
30. Rudick RA, O'Connor PW, Polman CH, et al. Assessment of JC virus DNA in blood and urine from natalizumab-treated patients. Ann Neurol 2010; 68: 304-310.
31. Major EO, Frohman E, Douek D,. More on JC viremia in natalizumab-treated patients with multiple sclerosis. N Engl J Med 2013; 369: 1280.
32. Dorries K, Sbiera S, Drews K, et al. Association of human polyomavirus JC with peripheral blood of immunoimpaired and healthy individuals. J Neurovirol 2003; 9 (suppl 1): 81-87.
33. Monaco MC, Atwood WJ, Gravell M, et al. JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency. J Virol 1996; 70: 7004-7012.
34. Monaco MC, Sabath BF, Durham LC, Major EO,. JC virus multiplication in human hematopoietic progenitor cells requires the NF-1 class D transcription factor. J Virol 2001; 75: 9687-9695.
35. Monaco MC, Shin J, Major EO,. JC virus infection in cells from lymphoid tissue. Dev Biol Stand 1998; 94: 115-122.
36. Tan CS, Dezube BJ, Bhargava P, et al. 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. J Infect Dis 2009; 199: 881-888.
37. Saure C, Warnke C, Zohren F, et al. Natalizumab and impedance of the homing of CD34+ hematopoietic progenitors. Arch Neurol 2011; 68: 1428-1431.
38. Warnke C, Smolianov V, Dehmel T, et al. CD34+ progenitor cells mobilized by natalizumab are not a relevant reservoir for JC virus. Mult Scler 2011; 17: 151-156.
39. Chapagain ML, Nerurkar VR,. Human polyomavirus JC (JCV) infection of human B lymphocytes: a possible mechanism for JCV transmigration across the blood-brain barrier. J Infect Dis 2010; 202: 184-191.
40. Lafon ME, Dutronc H, Dubois V, et al. JC virus remains latent in peripheral blood B lymphocytes but replicates actively in urine from AIDS patients. J Infect Dis 1998; 177: 1502-1505.
41. Dubois V, Dutronc H, Lafon ME, et al. Latency and reactivation of JC virus in peripheral blood of human immunodeficiency virus type 1-infected patients. J Clin Microbiol 1997; 35: 2288-2292.
42. Niino M, Bodner C, Simard ML, et al. Natalizumab effects on immune cell responses in multiple sclerosis. Ann Neurol 2006; 59: 748-754.
43. White FA III, Ishaq M, Stoner GL, Frisque RJ,. JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy. J Virol 1992; 66: 5726-5734.
44. Tan CS, Ellis LC, Wuthrich C, et al. JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J Virol 2010; 84: 9200-9209.
45. Perez-Liz G, Del Valle L, Gentilella A, et al. Detection of JC virus DNA fragments but not proteins in normal brain tissue. Ann Neurol 2008; 64: 379-387.
46. Caldarelli-Stefano R, Vago L, Omodeo-Zorini E, et al. Detection and typing of JC virus in autopsy brains and extraneural organs of AIDS patients and non-immunocompromised individuals. J Neurovirol 1999; 5: 125-133.
47. Delbue S, Branchetti E, Boldorini R, et al. Presence and expression of JCV early gene large T antigen in the brains of immunocompromised and immunocompetent individuals. J Med Virol 2008; 80: 2147-2152.
48. Stuve O, Marra CM, Jerome KR, et al. Immune surveillance in multiple sclerosis patients treated with natalizumab. Ann Neurol 2006; 59: 743-747.
49. Aly L, Yousef S, Schippling S, et al. Central role of JC virus-specific CD4+ lymphocytes in progressive multi-focal leucoencephalopathy-immune reconstitution inflammatory syndrome. Brain 2011; 134 (pt 9): 2687-2702.