Interplay between β herpesviruses and fungal infections in transplant patients: From the bench to the bedside

Future Virology

Volumn 10, Issue 4, 2015, Pages 399-414

  Gentile, Giuseppe ^a   Antonelli, Guido ^b  

^a Department of Cellular Biotechnologies and Hematology ^*  (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

cytomegalovirus; fungal infection; human herpesvirus 6; human herpesvirus 7; innate immune system; microbiome; solid organ transplant; stem cell transplant; viral fungal interactions; herpesviruses

Indexed keywords

BETAHERPESVIRINAE; CYTOMEGALOVIRUS; GRAFT REJECTION; HERPES VIRUS INFECTION; HOST; HUMAN; HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 7; IMMUNE RESPONSE; IMMUNOCOMPROMISED PATIENT; INNATE IMMUNITY; META ANALYSIS (TOPIC); MICROBIOME; MYCOSIS; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYSTEMIC MYCOSIS;

CYTOMEGALOVIRUS; FUNGI; HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 7; SIMPLEXVIRUS;

EID: 84929082750     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.15.4     Document Type: Review

References (126)

1. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med. Virol. 20(4), 202-213 (2010).
2. Gentile G, Mele A, Ragona G et al. Human herpes virus-6 seroprevalence and leukaemias: a case-control study. GIMEMA (Gruppo Italiano Malattie Ematologiche dell'Adulto). Br. J. Cancer 80(7), 1103-1106 (1999).
3. Razonable RR. Human herpesviruses 6, 7 and 8 in solid organ transplant recipients. Am. J. Transplant. 13(S3), 67-78 (2013).
4. Agut H. Deciphering the clinical impact of acute human herpesvirus 6 (HHV-6) infections. J. Clin. Virol. 52, 164-171 (2011).
5. Fishman JA, Rubin RH. Infection in organ-transplant recipients. N. Engl. J. Med. 338(24), 1741-1751 (1998).
6. Gentile G. Post-transplant HHV-6 diseases. Herpes 7(1), 24-27 (2000).
7. Freeman RB. The indirect effects of cytomegalovirus infection. Am. J. Transplant. 9(11), 2453-2458 (2009)
8. Fishman JA. Opportunistic infections-coming to the limits of immunosuppression Cold Spring Harb. Perspect. Med. 3(10), a015669 (2013).
9. Marr K, Carter RA, Boeckh M et al. Invasive aspergilloisis in allogeneic stem cell transplant recipients: changes in epidemiology and risk factors. Blood 100(13), 4358-4366 (2002).
10. Fukuda T, Carter RA, Boeckh M et al. Risks and outcome of invasive fungal infections in recipients of allogeneic hematopoietic stem cell transplants recipients after non myeloablative conditioning. Blood 102(3), 827-833 (2003).
11. Garcia-Vidal C, Upton A, Kirby KA, Marr KA. Epidemiology of invasive mold infections in allogeneic stem cell transplant recipients: biological risk factors for infection according to time after transplantation. Clin. Infect. Dis. 47(8), 1041-1050 (2008).
12. Gavalda J, Len O, San Juan R et al. Risk factors for invasive aspergillosis in solid organ transplant recipients: a case-control study. Clin. Infect. Dis. 41(1), 52-59 (2005).
13. Pappas PG, Alexander BD, Andes DR et al. Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET). Clin. Infect. Dis. 50(8), 1101-1111 (2010).
14. Bitar D, Lortholary O, Le Strat Y et al. Population-based analysis of invasive fungal infections, france, 2001-2010. Emerg. Infect. Dis. 20(7), 1163-1169 (2014).
15. Chong AS, Alegre ML. The impact of infection and tissue damage in solid-organ transplantation. Nat. Rev. Immunol. 12(6), 459-471 (2012).
16. Alegre ML, Bartman C, Chong AS. Microbes and allogeneic transplantation. Transplantation 97(1), 5-11 (2014).
17. Alegre ML, Mannon RB, Mannon PJ. The microbiota, the immune system and the allograft. Am. J. Transplant. 14(6), 1236-1248 (2014).
18. Fishman JA. From the classic concepts to modern practice. Clin. Microbiol. Infect. doi: 10.1111/1469-0691.12593 (2014) (Epub ahead of print).
19. Smith C, Khanna R. Immune regulation of human herpesviruses and its implications for human transplantation. Am. J. Transplant. 13(Suppl. 3), 9-23 (2013).
20. Bego M, Jeor ST. Human cytomegalovirus infection of cells of hematopoietic origin: HCMV-induced immunosuppression, immune evasion, and latency. Exp. Hematol. 34(5), 555-570 (2006).
21. Capobianchi A, Iori AP, Micozzi A et al. Cytomegalovirus in bone marrow cells correlates with cytomegalovirus in peripheral blood leukocytes. J. Clin. Microbiol. 52(6), 2183-2185 (2014).
22. Kapasi K, Rice GP. Cytomegalovirus infection of peripheral blood mononuclear cells: effects on interleukin-1 and-2 production and responsiveness. J. Virol. 62(10), 3603-3607 (1988).
23. Schrier RD, Rice GP, Oldstone MB. Suppression of natural killer cell activity and T cell proliferation by fresh isolates of human cytomegalovirus. J. Infect. Dis. 153(6), 1084-1091 (1986).
24. Ng-Bautista CL, Sedmark DD. Cytomegalovirus infection is associated with absence of alveolar epithelial cell HLA class II antigen expression. Nat. Med. 5(9), 1039-1043 (1999).
25. Hopkins HA, Monick MM, Hunninghake GW. Cytomegalovirus inhibits CD14 expression on human alveolar macrophages. J. Infect. Dis. 174(1), 69-74 (1996).
26. Kapasi K, Rice GP. Role of the monocyte in cytomegalovirus-mediated immunosuppression in vitro. J. Infect. Dis. 154, 881-884 (1986).
27. Span AH, Van Boven CP, Bruggeman CA. The effect of cytomegalovirus infection on the adherence of polymorphonuclear leukocytes to endothelial cells. Eur. J. Clin. Invest. 19, 542-548 (1989).
28. Sparrelid E, Emanuel D, Fehniger T, Anderson U, Anderson J. Interstitial pneumonitis in bone marrow transplant recipients is associated with local production of TH 2-type cytokines and lack of T cell-mediated cytotoxicity. Transplantation 63, 1782-1789 (1997).
29. Cenci E, Mencacci A, de D'ostiani C et al. Cytokine-and T helper-dependent lung mucosal immunity in mice with invasive pulmonary aspergillosis. J. Infect. Dis. 178, 1750-1760 (1998).
30. Lockridge KM, Zhou SS, Kravitz RH et al. Primate cytomegalovirus encode and express an IL-10-like protein. Virology 268, 272-280 (2000).
31. Bochud P, Bochud M, Telenti A, Calandra T. Innate immunogenetics: a tool for exploring new frontiers of host defence. Lancet Infect. Dis. 7(8), 531-542 (2007).
32. Cervera C, Lozano F, Saval N et al. The influence of innate immunity gene receptors polymorphisms in renal transplant infections. Transplantation 83, 1493-1500 (2007).
33. Kijpittayarit S, Eid AJ, Brown RA et al. Relationship between Toll-like receptor 2 polymorphism and Cytomegalovirus disease after liver transplantation. J. Infect. Dis. 44, 1315-1320 (2007).
34. Xiao HW, Luo Y, Lai XY et al. Donor TLR9 gene tagSNPs influence susceptibility to aGVHD and CMV reactivation in the allo-HSCT setting without polymorphisms in TLR4 and NOD2 genes. Bone Marrow Transplant. 49, 241-247 (2014).
35. Kang SH, Abdel-Massih RC, Brown RA, Dierkhising RA, Kremers WK, Razonable RR. Homozygosity for the toll-like receptor 2 R753Q single-nucleotide polymorphism is a risk factor for cytomegalovirus disease after liver transplantation. J. Infect. Dis. 205(4), 639-646 (2012).
36. Boehme KW, Guerrero M, Compton T. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 177(10), 7094-7102 (2006).
37. Compton T, Kurt-Jones EA, Boehme KW et al. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77(8), 4588-4596 (2003).
38. Loré K, Betts MR, Brenchley JM et al. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus-and HIV-1-specific T cell responses. J. Immunol. 171(8), 4320-4328 (2003).
39. Tabeta K, Georgel P, Janssen E et al. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl Acad. Sci. USA 101(10), 3516-3521 (2004).
40. Hossain MS, Ramachandiran S, Gewirtz AT, Waller EK. Recombinant TLR5 agonist CBLB502 promotes NK cell-mediated anti-CMV immunity in mice. PLoS ONE 9(5), e96165 (2014).
41. Adams AB, Williams MA, Jones TR et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J. Clin. Invest. 111(12), 1887-1895 (2003).
42. Chen HD, Fraire AE, Joris I, Brehm MA, Welsh RM, Selin LK. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2(11), 1067-1076. 2001.
43. Heeger PS, Greenspan NS, Kuhlenschmidt S et al. Pretransplant frequency of donorspecific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J. Immunol. 163(4), 2267-2275 (1999).
44. Adams MJ, Carstens EB. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch. Virol. 157(7), 1411-1422 (2012).
45. Ljungman P, Singh N. Human herpesvirus-6 in solid organ and stem cell transplant recipients. J. Clin. Virol. 37(Suppl. 1), S87-S91 (2006).
46. Lautenschlager I, Razonable RR. Human herpesvirus 6 infections in kidney, liver, lung, and heart transplantation: review. Transplant. Int. 25, 493-502 (2012).
47. Lusso P. HHV-6 and the immune system: mechanisms of immunomodulation and viral escape. J. Clin. Virol. 37, S4-S10 (2006).
48. Santoro F, Kennedy PE, Locatelli G, Malnati MS, Berger EA, Lusso P. CD46 is a cellular receptor for human herpesvirus 6. Cell 99(7), 817-827 (1999).
49. Tang H, Serada S, Kawabata A et al. CD134 is a cellular receptor specific for human herpesvirus-6B entry. Proc. Natl Acad. Sci. USA 110(22), 9096-9099 (2013).
50. Ogata M, Satou T, Kadota J et al. Human herpesvirus 6 (HHV-6) reactivation and HHV-6 encephalitis after allogeneic hematopoietic cell transplantation: a multicenter, prospective study. Clin. Infect. Dis. 57(5), 671-681 (2013).
51. Chevallier P, Robillard N, Illiaquer M et al. HHV-6 cell receptor CD46 expression on various cell subsets of six blood and graft sources: a prospective series. J. Clin. Virol. 56(4), 331-335 (2013).
52. Becerra A, Gibson L, Stern LJ, Calvo-Calle JM. Immune response to HHV-6 and implications for immunotherapy. Curr. Opin. Virol. 9, 154-161 (2014).
53. Suga S, Yoshikawa T, Asano Y et al. IgM neutralizing antibody responses to human herpesvirus-6 in patients with exnthem subitum or organ transplantation. Microbiol. Immunol. 36, 495-506 (1992).
54. Nastke MD, Becerra A, Yin L et al. Human CD4+ T cell response to human herpesvirus 6. J. Virol. 86, 4776-4792 (2012).
55. Gedermann U, Keukens L, Keiman JM et al. Immunotherapeutic strategies to prevent and treat human herpesvirus 6 reactivation after allogeneic stem cell transplantation. Blood. 121, 207-218 (2013).
56. Sylvester AW, Mitchell BL, Edgar JB et al. Broadly targeted human cytomegalovirusspecific Cd4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202, 673-685 (2005).
57. Dagna L, Pritchett JC, Lusso P. Immunomodulation and immunosuppression by human herpesvirus 6A and 6B. Future Virol. 8(3), 273-287 (2013).
58. Lusso P. HHV-6 and the immune system: mechanisms of immunomodulation and viral escape. J. Clin. Virol. 37(Suppl. 1); S4-S10 (2006).
59. Wang F, Chi J, Peng G et al. Development of virus-specific CD4+ and CD8+ regulatory T cells induced by human herpesvirus 6 infection. J. Virol. 88(2), 1011-1024 (2014).
60. Murakami Y, Tanimoto K, Fujiwara H et al. Human herpesvirus 6 infection impairs Toll-like receptor signaling. Virol. J. 10(7), 91 (2010).
61. Chi J, Wang F, Li L et al. The role of MAPK in CD4(+) T cells toll-like receptor 9-mediated signaling following HHV-6 infection. Virology 422(1), 92-98 (2012).
62. Reynaud JM, Jègou JF, Welsch JC, Horvat B. Human herpesvirus 6A infection in CD46 transgenic mice: viral persistence in the brain and increased production of proinflammatory chemokines via Toll-like receptor 9. J. Virol. 88(10), 5421-5436 (2014).
63. Pellett PE, Ablashi DV, Ambros PF et al. Chromosomally integrated human herpesvirus 6: questions and answers. Rev. Med. Virol. 22(3), 144-155 (2012).
64. Endo A, Watanabe K, Ohye T et al. Molecular and virological evidence of viral activation from chromosomally integrated human herpesvirus 6A in a patient with X-linked severe combined immunodeficiency. Clin. Infect. Dis. 59(4), 545-548 2014).
65. Potenza L, Barozzi P, Rossi G et al. May indirect effects of CIHHV-6 in transplant patients be exerted through the reactivation of the viral replicative machinery Transplantation 92, e49-e51 (2011).
66. Flamand L. Pathogenesis from the reactivation of chromosomally integrated human herpesvirus type 6: facts rather than fiction. Clin. Infect. Dis. 59(4), 549-551 (2014).
67. Strenger V, Caselli E, Lautensclager I et al. Detection of HHV-6-specific mRNA and antigens in PBMCs of individuals with chromosomically integrated HHV-6 (ciHHV-6). Clin. Microbiol. Infect. 20(10), 1027-1032 (2014).
68. Lee SO, Brown RA, Razonable RR. Clinical significance of pretransplant chromosomally integrated human herpesvirus-6 in liver transplant recipients. Transplantation 92(2), 224-229 (2011).
69. Katsafanas GC, Schirmer EC, Wyatt LS, Frenkel N. In vitro activation of human herpesviruses 6 and 7 from latency. Proc. Natl Acad. Sci. USA 93(18), 9788-9792 (1996).
70. Hudson AW. Roseoloviruses and their modulation of host defenses. Curr. Opin. Virol. 9, 178-187 (2014).
71. Antón A, Cervera C, Pumarola T et al. Human herpesvirus 7 primary infection in kidney transplant recipients. Transplantation 85(2), 298-302 (2008).
72. Mendez JC, Dockrell DH, Espy MJ et al. Human beta-herpesvirus interactions in solid organ transplant recipients. J. Infect. Dis. 183(2), 179-184 (2001).
73. Boutolleau D, Fernandez C, André E et al. Human herpesvirus (HHV)-6 and HHV-7: two closely related viruses with different infection profiles in stem cell transplantation recipients. J. Infect. Dis. 187(2), 179-186 (2003).
74. Dockrell DH, Paya CV. Human herpesvirus-6 and-7 in transplantation. Rev. Med. Virol. 11(1), 23-36 (2001).
75. Boeckh M, Nichols WG. Immunosuppressive effects of beta-herpesviruses. Herpes 10, 12-16 (2003).
76. Singh N, Arnow PM, Bonham A et al. Invasive aspergillosis in liver transplant recipients in the 1990s. Transplantation 64, 716-720 (1997.
77. Legendre C, Pascual M. Improving outcomes for solid-organ transplant recipients at risk for cytomegalovirus infection: late onset disease and indirect consequences. Clin. Infect. Dis. 46, 732-740 (2008).
78. Broers AE, van Der Holt R, von Esser JW et al. Increased transplant-related morbidity and mortality in CMV-seropositive patients despite highly effective prevention of CMV disease after allogeneic T-cell-depleted stem cell transplantation. Blood 95, 2240-2245 (2000).
79. Nichols WG, Corey L, Gooley T, Davis C, Boeckh M. High risk of death due to bacterial and fungal infection among cytomegalovirus (CMV)-seronegative recipients of stem cell transplant from seropositive donors: evidence for indirect effects of primary CMV infection. J. Infect. Dis. 185, 273-282 (2002).
80. Leach CT, Detels R, Hennessy K et al. A longitudinal study of cytomegalovirus infection in human immunodeficiency virus type 1-seropositive homosexual men: molecular epidemiology and association with disease progression. J. Infect. Dis. 170, 293-298 (1994).
81. Laursen AL, Mogensen SC, Andersen HMK et al. The impact of CMV on the respiratory bursts of macrophages in response to Pneumocystis carinii. Clin. Exp. Immunol. 123, 239-246 (2001).
82. Qureshi MH, Garvy BA, Pomeroy C et al. A murine model of dual infection with cytomegalovirus and Pneumocystis carinii: effects of virus-induced immunomodulation on disease progression. Virus Res. 114, 35-44 (2005).
83. George MJ, Snydman DR, Werner BG et al. The independent role of cytomegalovirus as a risk factor for invasive fungal disease in orthotopic liver transplant recipients. Am. J. Med. 103, 106-113 (1997).
84. Husni RN, Gordon SM, Longworth DL et al. Cytomegalovirus infection is a risk factor for invasive aspergillosis in lung transplant recipients. Clin. Infect. Dis. 26, 753-755 (1998).
85. Collins LA, Samore MH, Roberts MS et al. Risk factors for invasive fungal infections complicating orthotopic liver transplantation. J. Infect. Dis. 170, 644-652 (1994).
86. Jacobs F, Knoop C, Brancart F et al. Human herpesvirus-6 infection after lung and heart-lung transplantation: a prospective longitudinal study. Transplantation 75, 1996-2001 (2003).
87. Ratnamohan VM, Chapman J, Howse H et al. Cytomegalovirus and human herpesvirus 6 both cause viral disease after renal transplantation. Transplantation 66(7), 877-882 (1998).
88. Herbein G, Strasswimmer J, Altieri M, Woehl-Jaegle ML, Wolf P, Obert G. Longitudinal study of human herpesvirus 6 infection in organ transplant recipients. Clin. Infect. Dis. 22(1), 171-173 (1996).
89. Boeckh M, Nichols G. The impact of Cytomegalovirus serostatus of donor and recipient before hematopoietic stem cell transplantation in the era of antiviral prophylaxis and preemptive therapy. Blood 103(6), 2003-2008 (2004).
90. Schmidt-Hieber M, Labopin M, Beelen D et al. CMV serostatus still has an important prognostic impact in de novo acute leukemia patients after allogeneic stem cell transplantation: a report from the Acute Leukemia Working Party of EBMT. Blood 122(19), 3359-3364 (2013).
91. Ljungman P, Brand R, Hoek J et al. Donor Cytomegalovirus status influences the outcome of allogeneic stem cell transplant: a study by the European Group for Blood and Marrow Transplantation. Clin. Infect. Dis. 59(4), 473-481 (2014).
92. Li L, Wang J, Zhang W, Yang J, Chen L, Lv S. Risk factors for invasive mold infections following allogeneic hematopoietic stem cell transplantation: a single center study of 190 recipients. Scand. J. Infect. Dis. 44(2), 100-107 (2012).
93. Martino R, Parody R, Fukuda T et al. Impact of the intensity of the pre transplantation conditioning regimen in patients with prior invasive aspergillosis undergoing allogeneic hematopoietic stem cell transplantation: a retrospective survey of the infections disease working party of the European group from blood and marrow transplantation. Blood 108(9), 2928-2936, (2006).
94. Panackal AA, Li H, Kontoyiannis DP et al. Geoclimatic influences on invasive aspergillosis after hematopoietic stem cell transplantation. Clin. Infect. Dis. 50(12), 1588-1597 (2010).
95. Mikulska M, Raiola AM, Bruno B et al. Risk factors for invasive aspergillosis and related mortality in recipients of allogeneic SCT from alternative donors: an analysis of 306 patients. Bone Marrow Transplant. 44, 361-370 (2009).
96. Martino R, Pinana JL, Parodi R et al. Lower respiratory tract respiratory virus infections increase the risk invasive aspergillosis after a reduced intensity allogeneic hematopoietic SCT. Bone Marrow Transplant. 44, 749-756 (2009).
97. Marr KA, Seidel K, White TC, Bowden RA. Candidemia in allogeneic blood and marrow transplant recipients: evolution of risk factor after adoption of prophylactic fluconazole. J. Infect. Dis. 181, 309-316 (2000).
98. Gentile G, Capobianchi A, Ferraironi M, Greco E, Martino P. Relationship of serum human herpesvirus 6 DNA with cytomegalovirus pp65 antigenemia in allogeneic bone marrow transplant recipients. Transplantation 77(12), 1907-1908 (2004).
99. Dockrell DH, Mendez JC, Jones M et al. Human herpesvirus-6 seronegativity before transplantation predicts the occurrence of fungal infection in liver transplant recipients. Transplantation 67(3), 399-403 (1999).
100. Rogers J, Rohal S, Carrigan D et al. Human herpesvirus 6 in liver transplant recipients: role in pathogenesis of fungal infections, neurologic complications and outcome. Transplantation 69, 2566-2577 (2000).
101. Miller W, Flynn P, McCullough J et al. Cytomegalovirus infection after bone marrow transplantation:an association with acute graft-vs.-host disease. Blood 67, 1162-1167 (1986).
102. Wingard JR, Chen DY, Burns WH et al. Cytomegalovirus infection after autologous bone marrow transplantation with comparison to infection after allogeneic bone marrow transplantation. Blood 71, 1432-1437 (1988).
103. Goodrich JM, Bowden RA, Fisher L et al. Ganciclovir prophylaxis to prevent cytomegalovirus disease after allogeneic marrow transplant. Ann. Intern. Med. 118, 173-178 (1993).
104. Boeckh M, Gooley TA, Myerson D et al. Cytomegalovirus pp65-antigenemia guided early treatment with ganciclovir versus ganciclovir at engraftment after allogeneic marrow transplant recipients: a randomized double-blind study. Blood 88, 4063-4071 (1996).
105. Humar A, Kumar D, Kaliendo AM et al. Clinical impact of human herpesvirus 6 infection after liver transplantation. Transplantation 73(4), 599-604 (2002).
106. DesJardin JA, Cho E, Supran S, Gibbons L, Werner BG, Snydman DR. Association of human herpesvirus 6 reactivation with severe cytomegalovirus-associated disease in orthotopic liver transplant recipients. Clin. Infect. Dis. 33, 1358-1362 (2001).
107. Zerr DM, Boeckh M, Delaney C et al. HHV-6 reactivation and associated sequelae after hematopoietic cell transplantation. Biol. Blood Marrow Transplant. 18(11), 1700-1708 (2012).
108. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 336(6086), 1268-1273 (2012).
109. Tanaka K, Sawamura S, Satoh T, Kobayashi K, Noda S. Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J. Immunol. 178, 5209-5216 (2007).
110. Onyeagocha C, Hossain MS, Kumar A, Jones R, Roback J, Gewirtz AT. Latent cytomegalovirus infection exacerbates experimental colitis. Am. J. Pathol. 175(5), 2034-2042 (2009).
111. Virgin HW. The virome in mammalian physiology and disease. Cell 157, 142-150 (2014).
112. Abeles SR, Pride DT. Molecular bases and role of viruses in the human microbiome. J. Mol. Biol. 426(23), 3892-3906 (2014).
113. De Vlaminck I, Khush KK, Strehl C et al. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell 155, 1178-1187 (2013).
114. Focosi D, Maggi F, Albani M et al. Torquetenovirus viremia kinetics after autologous stem cell transplantation are predictable and may serve as a surrogate marker of functional immune reconstitution. J. Clin. Virol. 47(2), 189-192 (2010).
115. Béland K, Dore-Nguyen M, Gagné MJ et al. Torque Teno virus in children who underwent orthotopic liver transplantation: new insights about a common pathogen. J. Infect. Dis. 209(2), 247-254 (2014).
116. Maggi F, Bendinelli M. Immunobiology of the Torque Teno viruses and other anelloviruses. Curr. Top. Microbiol. Immunol. 331, 65-90 (2009).
117. Norman JA, Handley SC, Virgin HW. Kindom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146, 1459-1469 (2014).
118. Osborne LC, Monticelli LA, Nice TJ et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345(6196), 578-582 (2014).
119. Kernbauer E, Ding Y, Cadwell K. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516(7529), 94-98 (2014)
120. This study, for the first time, shows the presence of a symbiotic virus in the mammalian gastrointestinal tract. 120 Martino R, Subira M, Rovira M et al. Invasive fungal infections after allogeneic peripheral blood stem cell transplantation: incidence and risk factors in 395 patients. Br. J. Haematol. 116, 475-482 (2002).
121. Grow WB, Moreb JS, Roque D et al. Late onset invasive aspergillus infection in bone marrow transplant patients at a university hospital. Bone Marrow Transplant. 29, 15-19 (2002).
122. Gimenez E, Solano C, Nieto J et al. An investigation on the relationship between the occurrence of CMV DNAemia and the development of invasive aspergillosis in the allogeneic stem cell transplantation setting. J. Med. Virol. 86(4), 568-575 (2014).
123. Prentice HG, Gluckman E, Powles RL et al. Impact of long-term acyclovir on cytomegalovirus infection and survival after allogeneic bone marrow transplantation. European Acyclovir for CMV study group. Lancet 343, 749-753 (1994).
124. Lowance D, Neumayer HH, Legendre CM et al. Valacyclovir for the prevention of cytomegalovirus disease after renal transplantation. International Valacyclovir propylaxis transplantation study group. N. Engl. J. Med. 340, 1462-1470 (1999).
125. Kalil AC, Levitsky J, Lyden E, Stoner J, Freifeld AG. Meta-analysis: the efficacy of strategies to prevent organ disease by cytomegalovirus in solid organ transplant recipients. Ann. Intern. Med. 143, 870-880 (2005).
126. Florescu DF, Qiu F, Schmidt CM, Kalil AC. A direct and indirect comparison metaanalysis on the efficacy of Cytomegalovirus preventive strategies in solid organ transplant. Clin. Infect. Dis. 58(6), 785-803 (2014).