Persistent parvovirus B19 infection in non-erythroid tissues: Possible role in the inflammatory and disease process

Virus Research

Volumn 190, Issue , 2014, Pages 8-16

  Adamson Small, Laura A ^a   Ignatovich, Igor V ^a   Laemmerhirt, Monica G ^a   Hobbs, Jacqueline A ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Erythroid; Erythrovirus; Inflammation; Parvovirus

Indexed keywords

CAPSID PROTEIN; VIRUS ANTIBODY; VIRUS DNA; VIRUS MESSENGER RNA; VIRUS RNA;

BONE MARROW; COLON; CROSS REACTION; DISEASE ASSOCIATION; DNA METHYLATION; ENZYME IMMUNOASSAY; ERYTHEMA INFECTIOSUM; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN PARVOVIRUS B19; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIVER; LYMPHOID TISSUE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SINGLE STRAND CONFORMATION POLYMORPHISM; SOUTHERN BLOTTING; SYNOVIUM; TESTIS; THYROID GLAND; VIRUS CAPSID; VIRUS DETECTION; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION; ANTIBODY SPECIFICITY; DISEASE COURSE; ERYTHROID PRECURSOR CELL; GENETICS; IMMUNOLOGY; PARVOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

DISEASE PROGRESSION; ERYTHROID PRECURSOR CELLS; HUMANS; ORGAN SPECIFICITY; PARVOVIRIDAE INFECTIONS; PARVOVIRUS B19, HUMAN; VIRUS REPLICATION;

EID: 84906097868     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.06.017     Document Type: Review

References (127)

1. Abe K., Kiuchi T., Tanaka K., Edamoto Y., Aiba N., Sata T. Characterization of erythrovirus B19 genomes isolated in liver tissues from patients with fulminant hepatitis and biliary atresia who underwent liver transplantation. Int. J. Med. Sci. 2007, 4(2):105-109.
2. Adamson L.A., Fowler L.J., Clare-Salzler M.J., Hobbs J.A. Parvovirus B19 infection in Hashimoto's thyroiditis, papillary thyroid carcinoma, and anaplastic thyroid carcinoma. Thyroid 2011, 21(4):411-417.
3. Adamson L.A., Fowler L.J., Ewald A.S., Clare-Salzler M.J., Hobbs J.A. Infection and persistence of erythrovirus B19 in benign and cancerous thyroid tissues. J. Med. Virol. 2013, (Epub ahead of print).
4. Amand J.S., Astell C.R. Identification and characterization of a family of 11-kDa proteins encoded by the human parvovirus B19. Virology 1993, 192(1):121-131.
5. Anderson L., Tsou C., Parker R., Chorba T., Wulff H., Tattersall P., Mortimer P. Detection of antibodies and antigens of human parvovirus B19 by enzyme-linked immunosorbent assay. J. Clin. Microbiol. 1986, 24(4):522-526.
6. Baskan E.B., Yilmaz E., Saricaoglu H., Alkan G., Ercan I., Mistik R., Adim S.B., Goral G., Dilek K., Tunali S. Detection of parvovirus B19 DNA in the lesional skin of patients with Behcet's disease. Clin. Exp. Dermatol. 2007, 32(2):186-190.
7. Bergallo M., Costa C., Sidoti F., Novelli M., Ponti R., Castagnoli C., Merlino C., Bernengo M.G., Cavallo R. Variants of parvovirus B19: bioinformatical evaluation of nested PCR assays. Intervirology 2008, 51(2):75-80.
8. Bock C.T., Klingel K., Kandolf R. Human parvovirus B19-associated myocarditis. N. Engl. J. Med. 2010, 362(13):1248-1249.
9. Bonvicini F., La Placa M., Manaresi E., Gallinella G., Gentilomi G.A., Zerbini M., Musiani M. Parvovirus b19 DNA is commonly harboured in human skin. Dermatology 2010, 220(2):138-142.
10. Brown K., Young N. Human parvovirus B19: pathogenesis of disease. Human parvovirus B19 1996, 105-119.
11. Brown K.E., Anderson S.M., Young N.S. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 1993, 262(5130):114-117.
12. Bunyan D.J., Bullman H.M., Lever M., Saminathan S.D., Keng W.T., Araffin R., Robinson D.O. Different denaturation rates between methylated and non-methylated genomic DNA can result in allele-specific PCR amplification. Open J. Genet. 2011, 1(2):13-14.
13. Carrière C., Boulanger P., Delsert C. Rapid and sensitive method for the detection of B19 virus DNA using the polymerase chain reaction with nested primers. J. Virol. Methods 1993, 44(2-3):221-234.
14. Chen A.Y., Zhang E.Y., Guan W., Cheng F., Kleiboeker S., Yankee T.M., Qiu J. The small 11kDa nonstructural protein of human parvovirus B19 plays a key role in inducing apoptosis during B19 virus infection of primary erythroid progenitor cells. Blood 2010, 115(5):1070-1080.
15. Corcioli F., Zakrzewska K., Rinieri A., Fanci R., Innocenti M., Civinini R., De Giorgi V., Di Lollo S., Azzi A. Tissue persistence of parvovirus B19 genotypes in asymptomatic persons. J. Med. Virol. 2008, 80(11):2005-2011.
16. Corcioli F., Zakrzewska K., Fanci R., De Giorgi V., Innocenti M., Rotellini M., Di Lollo S., Azzi A. Human parvovirus PARV4 DNA in tissues from adult individuals: a comparison with human parvovirus B19 (B19V). Virol. J. 2010, 7:272.
17. Corsini J., Tal J., Winocour E. Directed integration of minute virus of mice DNA into episomes. J. Virol. 1997, 71(12):9008-9015.
18. Cossart Y.E., Cant B., Field A.M., Widdows D. Parvovirus-like particles in human sera. Lancet 1975, 305(7898):72-73.
19. Dennert R., Velthuis S., Schalla S., Eurlings L., van Suylen R.J., van Paassen P., Tervaert J.W., Wolffs P., Goossens V.J., Bruggeman C., Waltenberger J., Crijns H.J., Heymans S. Intravenous immunoglobulin therapy for patients with idiopathic cardiomyopathy and endomyocardial biopsy-proven high PVB19 viral load. Antivir. Ther. 2010, 15(2):193-201.
20. Diss T.C., Pan L.X., Du M.Q., Peng H.Z., Kerr J.R. Parvovirus B19 is associated with benign testes as well as testicular germ cell tumours. Mol. Pathol. 1999, 52(6):349-352.
21. Doerig C., Hirt B., Antonietti J.-P., Beard P. Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. J. Virol. 1990, 64(1):387-396.
22. Durigon E.L., Erdman D.D., Gary G.W., Pallansch M.A., Torok T.J., Anderson L.J. Multiple primer pairs for polymerase chain reaction (PCR) amplification of human parvovirus B19 DNA. J. Virol. Methods 1993, 44(2-3):155-165.
23. Erdman D.D., Usher M.J., Tsou C., Caul E.O., Gary G.W., Kajigaya S., Young N.S., Anderson L.J. Human parvovirus B19 specific IgG, IgA, and IgM antibodies and DNA in serum specimens from persons with erythema infectiosum. J. Med. Virol. 1991, 35(2):110-115.
24. Ergunay K., Tezel G.G., Dogan A.I., Ozen H., Sirin G., Ozbay M., Karabulut E., Ustacelebi S. Testicular persistence of parvovirus B19: evidence for preferential infection of germ cell tumors. Pathol. Res. Pract. 2008, 204(9):649-653.
25. Escher F., Kühl U., Sabi T., Suckau L., Lassner D., Poller W., Schultheiss H.P., Noutsias M. Immunohistological detection of parvovirus B19 capsid proteins in endomyocardial biopsies from dilated cardiomyopathy patients. Med. Sci. Monit. 2008, 14(6):CR333-CR338.
26. Fan M.M., Tamburic L., Shippam-Brett C., Zagrodney D.B., Astell C.R. The small 11-kDa protein from B19 parvovirus binds growth factor receptor-binding protein 2 in vitro in a Src homology 3 domain/ligand-dependent manner. Virology 2001, 291(2):285-291.
27. Fasano C., Kanduc D. Selfness-nonselfness in designing an anti-B19 erythrovirus vaccine. Self/nonself 2011, 2(2):114-119.
28. Fauquet C.M., Mayo M., Maniloff J., Desselberger U., Ball L.A. Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. 2005, (Access Online via Elsevier).
29. Fremont M., Metzger K., Rady H., Hulstaert J., De Meirleir K. Detection of herpesviruses and parvovirus B19 in gastric and intestinal mucosa of chronic fatigue syndrome patients. In Vivo 2009, 23(2):209-213.
30. Fu Y., Ishii K.K., Munakata Y., Saitoh T., Kaku M., Sasaki T. Regulation of tumor necrosis factor alpha promoter by human Parvovirus B19 NS1 through activation of AP-1 and AP-2. J. Virol. 2002, 76(11):5395-5403.
31. Grant J.K., Yin N.C., Zaytoun A.M., Waseem H., Hobbs J.A. Persistent adeno-associated virus 2 and parvovirus B19 sequences in post-mortem human cerebellum. Cerebellum 2009, 8(4):490-498.
32. Gray A., Guillou L., Zufferey J., Rey F., Kurt A.-M., Jichlinski P., Leisinger H.-J., Benhattar J. Persistence of parvovirus B19 DNA in testis of patients with testicular germ cell tumours. J. Gen. Virol. 1998, 79(3):573-579.
33. Heegaard E.D., Brown K.E. Human parvovirus B19. Clin. Microbiol. Rev. 2002, 15(3):485-505.
34. Hemauer A., von Poblotzki A., Gigler A., Cassinotti P., Siegl G., Wolf H., Modrow S. Sequence variability among different parvovirus B19 isolates. J. Gen. Virol. 1996, 77(8):1781-1785.
35. Hemauer A., Gigler A., Searle K., Beckenlehner K., Raab U., Broliden K., Wolf H., Enders G., Modrow S. Seroprevalence of parvovirus B19 NS1-specific IgG in B19-infected and uninfected individuals and in infected pregnant women. J. Med. Virol. 2000, 60(1):48-55.
36. Hokynar K., Brunstein J., Soderlund-Venermo M., Kiviluoto O., Partio E.K., Konttinen Y., Hedman K. Integrity and full coding sequence of B19 virus DNA persisting in human synovial tissue. J. Gen. Virol. 2000, 81(Pt 4):1017-1025.
37. Hokynar K., Soderlund-Venermo M., Pesonen M., Ranki A., Kiviluoto O., Partio E.K., Hedman K. A new parvovirus genotype persistent in human skin. Virology 2002, 302(2):224-228.
38. Hsu T.C., Tzang B.S., Huang C.N., Lee Y.J., Liu G.Y., Chen M.C., Tsay G.J. Increased expression and secretion of interleukin-6 in human parvovirus B19 non-structural protein (NS1) transfected COS-7 epithelial cells. Clin. Exp. Immunol. 2006, 144(1):152-157.
39. Hübschen J.M., Mihneva Z., Mentis A.F., Schneider F., Aboudy Y., Grossman Z., Rudich H., Kasymbekova K., Sarv I., Nedeljkovic J., Tahita M.C., Tarnagda Z., Ouedraogo J.-B., Gerasimova A.G., Moskaleva T.N., Tikhonova N.T., Chitadze N., Forbi J.C., Faneye A.O., Otegbayo J.A., Charpentier E., Muller C.P. Phylogenetic analysis of human parvovirus B19 sequences from eleven different countries confirms the predominance of genotype 1 and suggests the spread of genotype 3b. J. Clin. Microbiol. 2009, 47(11):3735-3738.
40. Ignatovich I.V., Hobbs J.A. Human parvovirus B19 infection leads to downregulation of thyroid, estrogen, and retinoid hormone receptor expression. Virology 2013, 446(1-2):173-179.
41. Kapoor A., Hornig M., Asokan A., Williams B., Henriquez J.A., Lipkin W.I. Bocavirus episome in infected human tissue contains non-identical termini. PLoS ONE 2011, 6(6):e21362.
42. Karetnyi Y.V., Beck P.R., Markin R.S., Langnas A.N., Naides S.J. Human parvovirus B19 infection in acute fulminant liver failure. Arch. Virol 1999, 144(9):1713-1724.
43. Kawase M., Momoeda M., Young N.S., Kajigaya S. Most of the VP1 unique region of B19 parvovirus is on the capsid surface. Virology 1995, 211(2):359-366.
44. Kerr J.R., Curran M.D., Moore J.E., Erdman D.D., Coyle P.V., Nunoue T., Middleton D., Ferguson W.P. Genetic diversity in the non-structural gene of parvovirus B19 detected by single-stranded conformational polymorphism assay (SSCP) and partial nucleotide sequencing. J. Virol. Methods 1995, 53(2-3):213-222.
45. Kerr J., Curran M. Applications of polymerase chain reaction-single stranded conformational polymorphism to microbiology. Clin. Mol. Pathol. 1996, 49(6):M315-M320.
46. Kerr J.R., Umene K. The molecular epidemiology of parvovirus B19. Rev. Med. Microbiol. 1997, 8(1):21-32.
47. Kerr J.R., Cunniffe V.S. Antibodies to parvovirus B19 non-structural protein are associated with chronic but not acute arthritis following B19 infection. Rheumatology (Oxford) 2000, 39(8):903-908.
48. Kerr J.R., Kaushik N., Fear D., Baldwin D.A., Nuwaysir E.F., Adcock I.M. Single-nucleotide polymorphisms associated with symptomatic infection and differential human gene expression in healthy seropositive persons each implicate the cytoskeleton, integrin signaling, and oncosuppression in the pathogenesis of human parvovirus B19 infection. J. Infect. Dis. 2005, 192(2):276-286.
49. Kotin R.M., Menninger J.C., Ward D.C., Berns K.I. Mapping and direct visualization of a region-specific viral DNA integration site on chromosome 19q13-qter. Genomics 1991, 10(3):831-834.
50. Kühl U., Pauschinger M., Bock T., Klingel K., Schwimmbeck C.P., Seeberg B., Krautwurm L., Poller W., Schultheiss H.P., Kandolf R. Parvovirus B19 infection mimicking acute myocardial infarction. Circulation 2003, 108(8):945-950.
51. Kühl U., Pauschinger M., Noutsias M., Seeberg B., Bock T., Lassner D., Poller W., Kandolf R., Schultheiss H.P. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with idiopathic left ventricular dysfunction. Circulation 2005, 111(7):887-893.
52. Kühl U., Rohde M., Lassner D., Gross U.M., Escher F., Schultheiss H.P. miRNA as activity markers in Parvo B19 associated heart disease. Herz 2012, 37(6):637-643.
53. Li Y., Wang J., Zhu G., Zhang X., Zhai H., Zhang W., Wang W., Huang G. Detection of parvovirus B19 nucleic acids and expression of viral VP1//VP2 antigen in human colon carcinoma. Am. J. Gastroenterol. 2007, 102(7):1489-1498.
54. Lüsebrink J., Schildgen V., Tillmann R.L., Wittleben F., Böhmer A., Müller A., Schildgen O. Detection of head-to-tail DNA sequences of human bocavirus in clinical samples. PLoS ONE 2011, 6(5):e19457.
55. Lunardi C., Tiso M., Borgato L., Nanni L., Millo R., De Sandre G., Severi A.B., Puccetti A. Chronic parvovirus B19 infection induces the production of anti-virus antibodies with autoantigen binding properties. Eur. J. Immunol. 1998, 28(3):936-948.
56. Luo W., Astell C.R. A novel protein encoded by small RNAs of parvovirus B19. Virology 1993, 195(2):448-455.
57. Manning A., Willey S.J., Bell J.E., Simmonds P. Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J. Infect. Dis. 2007, 195(9):1345-1352.
58. Moffatt S., Tanaka N., Tada K., Nose M., Nakamura M., Muraoka O., Hirano T., Sugamura K. A cytotoxic nonstructural protein, NS1, of human parvovirus B19 induces activation of interleukin-6 gene expression. J. Virol. 1996, 70(12):8485-8491.
59. Moimas S., Zacchigna S., Merlo M., Buiatti A., Anzini M., Dreas L., Salvi A., Di Lenarda A., Giacca M., Sinagra G. Idiopathic dilated cardiomyopathy and persistent viral infection: lack of association in a controlled study using a quantitative assay. Heart Lung Circ. 2012, 21(12):787-793.
60. Munakata Y., Saito-Ito T., Kumura-Ishii K., Huang J., Kodera T., Ishii T., Hirabayashi Y., Koyanagi Y., Sasaki T. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 2005, 106(10):3449-3456.
61. Nguyen Q.T., Sifer C., Schneider V., Allaume X., Servant A., Bernaudin F., Auguste V., Garbarg-Chenon A. Novel human erythrovirus associated with transient aplastic anemia. J. Clin. Microbiol. 1999, 37(8):2483-2487.
62. Norja P., Hokynar K., Aaltonen L.-M., Chen R., Ranki A., Partio E.K., Kiviluoto O., Davidkin I., Leivo T., Eis-Hübinger A.M., Schneider B., Fischer H.-P., Tolba R., Vapalahti O., Vaheri A., Söderlund-Venermo M., Hedman K. Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc. Natl. Acad. Sci. 2006, 103(19):7450-7453.
63. Nuesch J.P., Lacroix J., Marchini A., Rommelaere J. Molecular pathways: rodent parvoviruses - mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 2012, 18(13):3516-3523.
64. Ohtsuka T., Yamazaki S. Altered prevalence of human parvovirus B19 component genes in systemic sclerosis skin tissue. Br. J. Dermatol. 2005, 152(5):1078-1080.
65. Page C., Hoffmann T.W., Benzerdjeb N., Duverlie G., Sevestre H., Desailloud R. Detection of erythrovirus B19 in thyroidectomy specimens from Graves' disease patients: a case-control study. J. Med. Virol. 2013, 85(8):1414-1419.
66. Polcz M.E., Adamson L.A., Datar R.S., Fowler L.J., Hobbs J.A. Detection of parvovirus B19 capsid proteins in testicular tissues. Urology 2012, 79(3). 744.e9-15.
67. Polcz M.E., Adamson L.A., Lu X., Chang M.N., Fowler L.J., Hobbs J.A. Increased IL-6 detection in adult and pediatric lymphoid tissue harboring parvovirus B19. J. Clin. Virol. 2013, 57(3):233-238.
68. Rohrer C., Gartner B., Sauerbrei A., Bohm S., Hottentrager B., Raab U., Thierfelder W., Wutzler P., Modrow S. Seroprevalence of parvovirus B19 in the German population. Epidemiol. Infect. 2008, 136(11):1564-1575.
69. Saikawa T., Anderson S., Momoeda M., Kajigaya S., Young N.S. Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J. Virol. 1993, 67(6):3004-3009.
70. Schildgen O., Qiu J., Söderlund-Venermo M. Genomic features of the human bocaviruses. Future Virol. 2012, 7(1):31-39.
71. Servant A., Laperche S., Lallemand F., Marinho V., De Saint Maur G., Meritet J.F., Garbarg-Chenon A. Genetic diversity within human erythroviruses: identification of three genotypes. J. Virol. 2002, 76(18):9124-9134.
72. Sidoti F., Fierro M.T., Costa C., Ponti R., Bergallo M., Comessatti A., Fumagalli M., Novelli M., Merlino C., Cavallo R., Bernengo M.G. Prevalence and significance of human parvovirus variants in skin from primary cutaneous T cell lymphomas, inflammatory dermatoses and healthy subjects. Arch. Dermatol. Res. 2009, 301(9):647-652.
73. Söderlund-Venermo M., Hokynar K., Nieminen J., Rautakorpi H., Hedman K. Persistence of human parvovirus B19 in human tissues. Pathol. Biol. (Paris) 2002, 50(5):307-316.
74. Sol N., Le Junter J., Vassias I., Freyssinier J.M., Thomas A., Prigent A.F., Rudkin B.B., Fichelson S., Morinet F. Possible interactions between the NS-1 protein and tumor necrosis factor alpha pathways in erythroid cell apoptosis induced by human parvovirus B19. J. Virol. 1999, 73(10):8762-8770.
75. Stieger K., Schroeder J., Provost N., Mendes-Madeira A., Belbellaa B., Le Meur G., Weber M., Deschamps J.Y., Lorenz B., Moullier P., Rolling F. Detection of intact rAAV particles up to 6 years after successful gene transfer in the retina of dogs and primates. Mol. Ther. 2009, 17(3):516-523.
76. Takahashi Y., Murai C., Shibata S., Munakata Y., Ishii T., Ishii K., Saitoh T., Sawai T., Sugamura K., Sasaki T. Human parvovirus B19 as a causative agent for rheumatoid arthritis. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(14):8227-8232.
77. Tolfvenstam T., Papadogiannakis N., Andersen A., Akre O. No association between human parvovirus B19 and testicular germ cell cancer. J. Gen. Virol. 2002, 83(Pt 9):2321-2324.
78. von Poblotzki A., Gigler A., Lang B., Wolf H., Modrow S. Antibodies to parvovirus B19 NS-1 protein in infected individuals. J. Gen. Virol. 1995, 76(3):519-527.
79. von Poblotzki A., Hemauer A., Gigler A., Puchhammer-Stöckl E., Heinz F.X., Pont J., Laczika K., Wolf H., Modrow S. Antibodies to the nonstructural protein of parvovirus B19 in persistently infected patients: implications for pathogenesis. J. Infect. Dis. 1995, 175(5):1356-1359.
80. Wang J., Zhang W., Liu H., Wang D., Li Y., Wang W., Wang L., He F., Wang Z., Yan Q. Detection of human parvovirus B19 in papillary thyroid carcinoma. Br. J. Cancer 2008, 98(3):611-618.
81. Wang J., Zhang W., Liu H., Wang D., Wang W., Li Y., Wang Z., Wang L., Zhang W., Huang G. Parvovirus B19 infection associated with Hashimoto's thyroiditis in adults. J. Infect. 2010, 60(5):360-370.
82. Weigel-Kelley K.A., Yoder M.C., Srivastava A. Recombinant human parvovirus B19 vectors: erythrocyte P antigen is necessary but not sufficient for successful transduction of human hematopoietic cells. J. Virol. 2001, 75(9):4110-4116.
83. Wilson G.M., Jindal H.K., Yeung D.E., Chen W., Astell C.R. Expression of minute virus of mice major nonstructural protein in insect cells: purification and identification of ATPase and helicase activities. Virology 1991, 185(1):90-98.
84. Wong S., Young N.S., Brown K.E. Prevalence of parvovirus B19 in liver tissue: no association with fulminant hepatitis or hepatitis-associated aplastic anemia. J. Infect. Dis. 2003, 187(10):1581-1586.
85. Yalcin A., Serin M.S., Emekdas G., Tiftik N., Aslan G., Eskandari G., Tezcan S. Promoter methylation of P15(INK4B) gene is possibly associated with parvovirus B19 infection in adult acute leukemias. Int. J. Lab. Hematol. 2009, 31(4):407-419.
86. Young N.S., Brown K.E. Parvovirus B19. N. Engl. J. Med. 2004, 350(6):586-597.
87. Zakrzewska K., Corcioli F., Carlsen K.M., Giuggioli D., Fanci R., Rinieri A., Ferri C., Azzi A. Human parvovirus B19 (B19V) infection in systemic sclerosis patients. Intervirology 2009, 52(5):279-282.
88. Zhang W.P., Wang J.H., Wang W.Q., Chen X.Q., Wang Z., Li Y.F., Hu P.Z., Zhang W., Wang L., Wang D., Huang G.S. An association between parvovirus B19 and Kikuchi-Fujimoto disease. Viral Immunol. 2007, 20(3):421-428.
89. Zhi N., Zadori Z., Brown K.E., Tijssen P. Construction and sequencing of an infectious clone of the human parvovirus B19. Virology 2004, 318(1):142-152.
90. Alter P., Rupp H., Maisch B. Activated nuclear transcription factor kappaB in patients with myocarditis and dilated cardiomyopathy - relation to inflammation and cardiac function. Biochem. Biophys. Res. Commun. 2006, 339(1):180-187.
91. Cassinotti P., Burtonboy G., Fopp M., Siegl G. Evidence for persistence of human parvovirus B19 DNA in bone marrow. J. Med. Virol. 1997, 53(3):229-232.
92. Cassinotti P., Siegl G., Michel B.A., Bruhlmann P. Presence and significance of human parvovirus B19 DNA in synovial membranes and bone marrow from patients with arthritis of unknown origin. J. Med. Virol. 1998, 56(3):199-204.
93. Crowson A.N., Magro C.M., Dawood M.R. A causal role for parvovirus B19 infection in adult dermatomyositis and other autoimmune syndromes. J. Cutan. Pathol. 2000, 27(10):505-515.
94. da Costa A.C., Bendit I., de Oliveira A.C., Kallas E.G., Sabino E.C., Sanabani S.S. Investigation of human parvovirus B19 occurrence and genetic variability in different leukaemia entities. Clin. Microbiol. Infect. 2013, 19(1):E31-E43.
95. Eis-Hübinger A.M., Reber U., Abdul-Nour T., Glatzel U., Lauschke H., Putz U. Evidence for persistence of parvovirus B19 DNA in livers of adults. J. Med. Virol. 2001, 65(2):395-401.
96. Hobbs J.A. Detection of adeno-associated virus 2 and parvovirus B19 in the human dorsolateral prefrontal cortex. J. Neurovirol. 2006, 12(3):190-199.
97. Justinien E., Pannier C., Page C., Segard C., Strunski V., Sevestre H., Duverlie G., Desailloud R. Parvovirus B19 infection: a possible role in autoimmune thyroid diseases. 12th European Congress of Endocrinology 2010, (Endocrine Abstract).
98. Kempf W., Kazakov D.V., Palmedo G., Fraitag S., Schaerer L., Kutzner H. Pityriasis lichenoides et varioliformis acuta with numerous CD30(+) cells: a variant mimicking lymphomatoid papulosis and other cutaneous lymphomas. A clinicopathologic, immunohistochemical, and molecular biological study of 13 cases. Am. J. Surg. Pathol. 2012, 36(7):1021-1029.
99. Kerr J.R., Cartron J.P., Curran M.D., Moore J.E., Elliott J.R., Mollan R.A. A study of the role of parvovirus B19 in rheumatoid arthritis. Br. J. Rheumatol. 1995, 34(9):809-813.
100. Kerr J.R., Ferguson W.P., Mcmillan S.A., Bruce I.N., Bell A.L. Parvovirus B19 and acute joint swelling in rheumatoid arthritis patients. Ann. Rheum. Dis. 1996, 55(9):648-649.
101. Kuethe F., Lindner J., Matschke K., Wenzel J.J., Norja P., Ploetze K., Schaal S., Kamvissi V., Bornstein S.R., Schwanebeck U., Modrow S. Prevalence of parvovirus B19 and human bocavirus DNA in the heart of patients with no evidence of dilated cardiomyopathy or myocarditis. Clin. Infect. Dis. 2009, 49(11):1660-1666.
102. Kühl U., Lassner D., Pauschinger M., Gross U.M., Seeberg B., Noutsias M., Poller W., Schultheiss H.P. Prevalence of erythrovirus genotypes in the myocardium of patients with dilated cardiomyopathy. J. Med. Virol. 2008, 80(7):1243-1251.
103. Lotze U., Egerer R., Gluck B., Zell R., Sigusch H., Erhardt C., Heim A., Kandolf R., Bock T., Wutzler P., Figulla H.R. Low level myocardial parvovirus B19 persistence is a frequent finding in patients with heart disease but unrelated to ongoing myocardial injury. J. Med. Virol. 2010, 82(8):1449-1457.
104. Lotze U., Egerer R., Tresselt C., Gluck B., Dannberg G., Stelzner A., Figulla H.R. Frequent detection of parvovirus B19 genome in the myocardium of adult patients with idiopathic dilated cardiomyopathy. Med. Microbiol. Immunol. (Berl.) 2004, 193(2-3):75-82.
105. Lundqvist A., Tolfvenstam T., Brytting M., Stolt C.M., Hedman K., Broliden K. Prevalence of parvovirus B19 DNA in bone marrow of patients with haematological disorders. Scand. J. Infect. Dis. 1999, 31(2):119-122.
106. Mahrholdt H., Wagner A., Deluigi C.C., Kispert E., Hager S., Meinhardt G., Vogelsberg H., Fritz P., Dippon J., Bock C.T., Klingel K., Kandolf R., Sechtem U. Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 2006, 114(15):1581-1590.
107. Mantke O.D., Meyer R., Prösch S., Niedrig M. Frequent detection of viral nucleic acids in heart valve tissue. J. Clin. Microbiol. 2004, 42(5):2298-2300.
108. Nakashima A., Tanaka N., Tamai K., Kyuuma M., Ishikawa Y., Sato H., Yoshimori T., Saito S., Sugamura K. Survival of parvovirus B19-infected cells by cellular autophagy. Virology 2006, 349(2):254-263.
109. Nguyen Y., Renois F., Leveque N., Giusti D., Picard-Maureau M., Bruneval P., Fornes P., Andreoletti L. Virus detection and semiquantitation in explanted heart tissues of idiopathic dilated cardiomyopathy adult patients by use of PCR coupled with mass spectrometry analysis. J. Clin. Microbiol. 2013, 51(7):2288-2294.
110. Ohtsuka T., Yamazaki S. Increased prevalence of human parvovirus B19 DNA in systemic sclerosis skin. Br. J. Dermatol. 2004, 150(6):1091-1095.
111. Pankuweit S., Moll R., Baandrup U., Portig I., Hufnagel G., Maisch B. Prevalence of the parvovirus B19 genome in endomyocardial biopsy specimens. Hum. Pathol. 2003, 34(5):497-503.
112. Peterlana D., Puccetti A., Beri R., Ricci M., Simeoni S., Borgato L., Scilanga L., Ceru S., Corrocher R., Lunardi C. The presence of parvovirus B19 VP and NS1 genes in the synovium is not correlated with rheumatoid arthritis. J. Rheumatol. 2003, 30(9):1907-1910.
113. Pfrepper K.I., Enders M., Motz M. Human parvovirus B19 serology and avidity using a combination of recombinant antigens enables a differentiated picture of the current state of infection. J. Vet. Med. Ser. B 2005, 52(7-8):362-365.
114. Saal J., Steidle M., Einsele H., Müller C., Fritz P., Zacher J. Persistence of B19 parvovirus in synovial membranes of patients with rheumatoid arthritis. Rheumatol. Int. 1992, 12(4):147-151.
115. Schenk T., Enders M., Pollak S., Hahn R., Huzly D. High prevalence of human parvovirus B19 DNA in myocardial autopsy samples from subjects without myocarditis or dilative cardiomyopathy. J. Clin. Microbiol. 2009, 47(1):106-110.
116. Schmid S., Bossart W., Michel B.A., Bruhlmann P. Outcome of patients with arthritis and parvovirus B19 DNA in synovial membranes. Rheumatol. Int. 2007, 27(8):747-751.
117. Schneider B., Höne A., Tolba R.H., Fischer H.-P., Blümel J., Eis-Hübinger A.M. Simultaneous persistence of multiple genome variants of human parvovirus B19. J. Gen. Virol. 2008, 89(Pt 1):164-176.
118. Söderlund M., von Essen R., Haapasaari J., Kiistala U., Kiviluoto O., Hedman K. Persistence of parvovirus B19 DNA in synovial membranes of young patients with and without chronic arthropathy. Lancet 1997, 349(9058):1063-1065.
119. Stewart G.C., Lopez-Molina J., Gottumukkala R.V., Rosner G.F., Anello M.S., Hecht J.L., Winters G.L., Padera R.F., Baughman K.L., Lipes M.A. Myocardial parvovirus B19 persistence: lack of association with clinicopathologic phenotype in adults with heart failure. Circ. Heart Fail. 2011, 4(1):71-78.
120. Tomasini D., Tomasini C.F., Cerri A., Sangalli G., Palmedo G., Hantschke M., Kutzner H. Pityriasis lichenoides: a cytotoxic T-cell-mediated skin disorder. Evidence of human parvovirus B19 DNA in nine cases. J. Cutan. Pathol. 2004, 31(8):531-538.
121. Tschöpe C., Bock C.T., Kasner M., Noutsias M., Westermann D., Schwimmbeck P.L., Pauschinger M., Poller W.C., Kühl U., Kandolf R., Schultheiss H.P. High prevalence of cardiac parvovirus B19 infection in patients with isolated left ventricular diastolic dysfunction. Circulation 2005, 111(7):879-886.
122. Vallbracht K.B., Schwimmbeck P.L., Kühl U., Seeberg B., Schultheiss H.P. Endothelium-dependent flow-mediated vasodilation of systemic arteries is impaired in patients with myocardial virus persistence. Circulation 2004, 110(18):2938-2945.
123. Vuorinen T., Lammintausta K., Kotilainen P., Nikkari S. Presence of parvovirus B19 DNA in chronic urticaric and healthy human skin. J. Clin. Virol. 2002, 25(2):217-221.
124. Wang C., Heim A., Schlaphoff V., Suneetha P.V., Stegmann K.A., Jiang H., Krueger M., Fytili P., Schulz T., Cornberg M., Kandolf R., Manns M.P., Bock C.T., Wedemeyer H. Intrahepatic long-term persistence of parvovirus B19 and its role in chronic viral hepatitis. J. Med. Virol. 2009, 81(12):2079-2088.
125. Wang X., Zhang G., Han M., Chao Q., Xu D. Investigation of parvovirus B19 in cardiac tissue from patients with congenital heart disease. Chin. Med. J. (Engl.) 1999, 112(11):995-997.
126. Yilmaz A., Mahrholdt H., Athanasiadis A., Vogelsberg H., Meinhardt G., Voehringer M., Kispert E.M., Deluigi C., Baccouche H., Spodarev E., Klingel K., Kandolf R., Sechtem U. Coronary vasospasm as the underlying cause for chest pain in patients with PVB19 myocarditis. Heart 2008, 94(11):1456-1463.
127. Zakrzewska K., Azzi A., De Biasi E., Radossi P., De Santis R., Davoli P.G., Tagariello G. Persistence of parvovirus B19 DNA in synovium of patients with haemophilic arthritis. J. Med. Virol. 2001, 65(2):402-407.