ATM facilitates mouse gammaherpesvirus reactivation from myeloid cells during chronic infection

Virology

Volumn 483, Issue , 2015, Pages 264-274

  Kulinski, Joseph M ^a   Darrah, Eric J ^a   Broniowska, Katarzyna A ^b   Mboko, Wadzanai P ^a   Mounce, Bryan C ^a   Malherbe, Laurent P ^c   Corbett, John A ^b   Gauld, Stephen B ^d,e   Tarakanova, Vera L ^a,b  

^a Microbiology and Molecular Genetics   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c BLOOD RESEARCH INSTITUTE   (United States)

^d Division of Allergy and Clinical Immunology   (United States)

^e ABBVIE INC   (United States)

Author keywords

ATM; Gammaherpesvirus; Myeloid cell; Reactivation; T cell response

Indexed keywords

ATM PROTEIN; REACTIVE OXYGEN METABOLITE; VIRUS DNA; ATM PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DNA DAMAGE; DNA SYNTHESIS; GAMMAHERPESVIRINAE; HERPES VIRUS INFECTION; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS CELL INTERACTION; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS STRAIN; ADULT; ANIMAL; C57BL MOUSE; CHRONIC DISEASE; DEFICIENCY; HOST PATHOGEN INTERACTION; HUMAN; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

MUS;

ADULT; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CHRONIC DISEASE; GAMMAHERPESVIRINAE; HERPESVIRIDAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; VIRUS ACTIVATION;

EID: 84929458199     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.04.026     Document Type: Article

References (52)

1. Barlow C., Dennery P.A., Shigenaga M.K., Smith M.A., Morrow J.D., Roberts L.J., Wynshaw-Boris A., Levine R.L. Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9915-9919.
2. Ben-Zvi A., Soffer D., Yatziv S. Disseminated Herpes simplex virus infection in ataxia-telangiectasia. Acta Paediatr. Scand. 1978, 67:667-670.
3. Braaten D.C., Sparks-Thissen R.L., Kreher S., Speck S.H., Virgin H.W. An optimized CD8+ T-cell response controls productive and latent gammaherpesvirus infection. J. Virol. 2005, 79:2573-2583.
4. Broniowska K.A., Diers A.R., Corbett J.A., Hogg N. Effect of nitric oxide on naphthoquinone toxicity in endothelial cells: role of bioenergetic dysfunction and poly (ADP-ribose) polymerase activation. Biochemistry 2013, 52:4364-4372.
5. Campbell T.B., Borok M., Gwanzura L., MaWhinney S., White I.E., Ndemera B., Gudza I., Fitzpatrick L., Schooley R.T. Relationship of human herpesvirus 8 peripheral blood virus load and Kaposi's sarcoma clinical stage. AIDS 2000, 14:2109-2116.
6. Cesarman E. Gammaherpesvirus and lymphoproliferative disorders in immunocompromised patients. Cancer Lett. 2011, 305:163-174.
7. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265-277.
8. Coleman C.B., Nealy M.S., Tibbetts S.A. Immature and transitional B cells are latency reservoirs for a gammaherpesvirus. J. Virol. 2010, 84:13045-13052.
9. Collins C.M., Boss J.M., Speck S.H. Identification of infected B-cell populations by using a recombinant murine gammaherpesvirus 68 expressing a fluorescent protein. J. Virol. 2009, 83:6484-6493.
10. D'Souza A.D., Parish I.A., McKay S.E., Kaech S.M., Shadel G.S. Aberrant CD8 T-cell responses and memory differentiation upon viral infection of an ataxia-telangiectasia mouse model driven by hyper-activated Akt and mTORC1 signaling. Am. J. Pathol. 2011, 178:2740-2751.
11. D'Souza A.D., Parish I.A., McKay S.E., Kaech S.M., Shadel G.S. Aberrant CD8+ T-cell responses and memory differentiation upon viral infection of an ataxia-telangiectasia mouse model driven by hyper-activated Akt and mTORC1 signaling. Am. J. Pathol. 2011, 178:2740-2751.
12. Efstathiou S., Ho Y.M., Hall S., Styles C.J., Scott S.D., Gompels U.A. Murine herpesvirus 68 is genetically related to the gammaherpesviruses Epstein-Barr virus and herpesvirus saimiri. J. Gen. Virol. 1990, 71:1365-1372.
13. Ehtisham S., Sunil-Chandra N.P., Nash A.A. Pathogenesis of murine gammaherpesvirus infection in mice deficient in CD4 and CD8 T cells. J. Virol. 1993, 67:5247-5252.
14. Feng W.H., Cohen J.I., Fischer S., Li L., Sneller M., Goldbach-Mansky R., Raab-Traub N., Delecluse H.J., Kenney S.C. Reactivation of latent Epstein-Barr virus by methotrexate: a potential contributor to methotrexate-associated lymphomas. J. Natl. Cancer Inst. 2004, 96:1691-1702.
15. Folgori L., Scarselli A., Angelino G., Ferrari F., Antoccia A., Chessa L., Finocchi A. Cutaneous granulomatosis and combined immunodeficiency revealing Ataxia-Telangiectasia: a case report. Ital. J. Pediatr. 2010, 36:29.
16. Freeman M.L., Lanzer K.G., Cookenham T., Peters B., Sidney J., Wu T.T., Sun R., Woodland D.L., Sette A., Blackman M.A. Two kinetic patterns of epitope-specific CD8 T-cell responses following murine gammaherpesvirus 68 infection. J. Virol. 2010, 84:2881-2892.
17. Giovannetti A., Mazzetta F., Caprini E., Aiuti A., Marziali M., Pierdominici M., Cossarizza A., Chessa L., Scala E., Quinti I., Russo G., Fiorilli M. Skewed T-cell receptor repertoire, decreased thymic output, and predominance of terminally differentiated T cells in ataxia telangiectasia. Blood 2002, 100:4082-4089.
18. Gredmark-Russ S., Cheung E.J., Isaacson M.K., Ploegh H.L., Grotenbreg G.M. The CD8 T-cell response against murine gammaherpesvirus 68 is directed toward a broad repertoire of epitopes from both early and late antigens. J. Virol. 2008, 82:12205-12212.
19. Gregorek H., Chrzanowska K.H., Dzierzanowska-Fangrat K., Wakulinska A., Pietrucha B., Zapasnik A., Zborowska M., Pac M., Smolka-Afifi D., Kasztelewicz B., Piekutowska-Abramczuk D., Maldyk J. Nijmegen breakage syndrome: long-term monitoring of viral and immunological biomarkers in peripheral blood before development of malignancy. Clin. Immunol. 2010, 135:440-447.
20. Guo Z., Kozlov S., Lavin M.F., Person M.D., Paull T.T. ATM activation by oxidative stress. Science 2010, 330:517-521.
21. Hagemeier S.R., Barlow E.A., Meng Q., Kenney S.C. The cellular ataxia telangiectasia-mutated kinase promotes Epstein-Barr virus lytic reactivation in response to multiple different types of lytic reactivation-inducing stimuli. J. Virol. 2012, 86:13360-13370.
22. Hagemeier S.R., Barlow E.A., Meng Q., Kenney S.C. The cellular ataxia telangiectasia-mutated kinase promotes Epstein-Barr virus lytic reactivation in response to multiple different types of lytic reactivation-inducing stimuli. J. Virol. 2012, 86:13360-13370.
23. Ito K., Takubo K., Arai F., Satoh H., Matsuoka S., Ohmura M., Naka K., Azuma M., Miyamoto K., Hosokawa K., Ikeda Y., Mak T.W., Suda T., Hirao A. Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes. J. Immunol. 2007, 178:103-110.
24. Kalyanaraman B., Darley-Usmar V., Davies K.J., Dennery P.A., Forman H.J., Grisham M.B., Mann G.E., Moore K., Roberts L.J., Ischiropoulos H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free. Radic. Biol. Med. 2012, 52:1-6.
25. Kulinski J.M., Leonardo S.M., Mounce B.C., Malherbe L.P., Gauld S.B., Tarakanova V.L. Ataxia-Telangiectasia mutated kinase controls chronic gammaherpesvirus infection. J. Virol. 2012, 86:12826-12837.
26. Lankisch P., Adler H., Borkhardt A. Testing for herpesvirus infection is essential in children with chromosomal-instability syndromes. J. Virol. 2013, 87:3616-3617.
27. Lassoued S., Gargouri B., El Feki A.F., Attia H., Van P.J. Transcription of the Epstein-Barr virus lytic cycle activator BZLF-1 during oxidative stress induction. Biol. Trace Elem. Res. 2010, 137:13-22.
28. Lavin M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol. 2008, 9:759-769.
29. Li X., Feng J., Sun R. Oxidative stress induces reactivation of Kaposi's sarcoma-associated herpesvirus and death of primary effusion lymphoma cells. J. Virol. 2011, 85:715-724.
30. Masucci G., Berkel I., Masucci M.G., Ernberg I., Szigeti R., Ersoy F., Sanal O., Yegin O., Henle G., Henle W. Epstein-Barr virus (EBV)-specific cell-mediated and humoral immune responses in ataxia-telangectasia patients. J. Clin. Immunol. 1984, 4:369-382.
31. Matei I.R., Guidos C.J., Danska J.S. ATM-dependent DNA damage surveillance in T-cell development and leukemogenesis: the DSB connection. Immunol. Rev. 2006, 209:142-158.
32. Meerbach A., Wutzler P., Hafer R., Zintl F., Gruhn B. Monitoring of Epstein-Barr virus load after hematopoietic stem cell transplantation for early intervention in post-transplant lymphoproliferative disease. J. Med. Virol. 2008, 80:441-454.
33. Morio T., Takahashi N., Watanabe F., Honda F., Sato M., Takagi M., Imadome K.I., Miyawaki T., Delia D., Nakamura K., Gatti R.A., Mizutani S. Phenotypic variations between affected siblings with ataxia-telangiectasia: ataxia-telangiectasia in Japan. Int. J. Hematol. 2009, 90:455-462.
34. Mounce B.C., Tsan F.C., Droit L., Kohler S., Cirillo L.A., Tarakanova V.L. Gammaherpesvirus gene expression and DNA synthesis are facilitated by viral protein kinase and histone variant H2AX. Virology 2011, 420:73-81.
35. Mounce B.C., Tsan F.C., Kohler S., Cirillo L.A., Tarakanova V.L. Dynamic association of gammaherpesvirus DNA with core histone during de novo lytic infection of primary cells. Virology 2011, 421:167-172.
36. Nowak-Wegrzyn A., Crawford T.O., Winkelstein J.A., Carson K.A., Lederman H.M. Immunodeficiency and infections in ataxia-telangiectasia. J. Pediatr. 2004, 144:505-511.
37. Orlandi E., Paulli M., Viglio A., Pagnucco G., Riboni R., Baldanti F., Lazzarino M. Epstein-Barr virus-positive aggressive lymphoma as a consequence of immunosuppression after multiple salvage treatments for follicular lymphoma. Br. J. Haematol. 2001, 112:373-376.
38. Saemundsen A.K., Berkel A.I., Henle W., Henle G., Anvret M., Sanal O., Ersoy F., Caglar M., Klein G. Epstein-Barr-virus-carrying lymphoma in a patient with ataxia-telangiectasia. Br. Med. J. (Clin. Res.Ed.) 1981, 282:425-427.
39. Savitsky K., Bar-Shira A., Gilad S., Rotman G., Ziv Y., Vanagaite L., Tagle D.A., Smith S., Uziel T., Sfez S., Ashkenazi M., Pecker I., Frydman M., Harnik R., Patanjali S.R., Simmons A., Clines G.A., Sartiel A., Gatti R.A., Chessa L., Sanal O., Lavin M.F., Jaspers N.G., Taylor A.M., Arlett C.F., Miki T., Weissman S.M., Lovett M., Collins F.S., Shiloh Y. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 1995, 268:1749-1753.
40. Shiloh Y., Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 2013, 14:197-210.
41. Singh V.V., Dutta D., Ansari M.A., Dutta S., Chandran B. Kaposi's sarcoma-associated herpesvirus induces ATM and H2AX DNA damage response early during de novo infection of primary endothelial cells which play roles in latency establishment. J. Virol. 2013.
42. Tarakanova V.L., Leung-Pineda V., Hwang S., Yang C.-W., Matatall K., Basson M., Sun R., Piwnica-Worms H., Sleckman B.P., Virgin H.W. Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 2007, 1:275-286.
43. Tarakanova V.L., Molleston J.M., Goodwin M., Virgin H.W. MHV68 complement regulatory protein facilitates MHV68 replication in primary macrophages in a complement independent manner. Virology 2010, 405:50-61.
44. Tarakanova V.L., Stanitsa E., Leonardo S.M., Bigley T.M., Gauld S.B. Conserved gammaherpesvirus kinase and histone variant H2AX facilitate gammaherpesvirus latency in vivo. Virology 2010, 405:50-61.
45. Tarakanova V.L., Suarez F.S., Tibbetts S.A., Jacoby M., Weck K.E., Hess J.H., Speck S.H., Virgin H.W. Murine gammaherpesvirus 68 infection induces lymphoproliferative disease and lymphoma in BALB b2 microglobulin deficient mice. J. Virol. 2005, 79:14668-14679.
46. Tibbetts S.A., Van Dyk L., Speck S.H., Virgin H.W. Immune control of the number and reactivation phenotype of cells latently infected with a gamma-herpesvirus. J. Virol. 2002, 76:7125-7132.
47. Virgin H.W., Latreille P., Wamsley P., Hallsworth K., Weck K.E., Dal Canto A.J., Speck S.H. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J. Virol. 1997, 71:5894-5904.
48. Weck K.E., Kim S.S., Virgin H.W., Speck S.H. B cells regulate murine gammaherpesvirus 68 latency. J. Virol. 1999, 73:4651-4661.
49. Weck K.E., Kim S.S., Virgin H.W., Speck S.H. Macrophages are the major reservoir of latent murine gammaherpesvirus 68 in peritoneal cells. J. Virol. 1999, 73:3273-3283.
50. Ye F., Zhou F., Bedolla R.G., Jones T., Lei X., Kang T., Guadalupe M., Gao S.J. Reactive oxygen species hydrogen peroxide mediates Kaposi's sarcoma-associated herpesvirus reactivation from latency. PLoS. Pathog. 2011, 7:e1002054.
51. Zha S., Sekiguchi J., Brush J.W., Bassing C.H., Alt F.W. Complementary functions of ATM and H2AX in development and suppression of genomic instability. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9302-9306.
52. Zielonka J., Hardy M., Kalyanaraman B. HPLC study of oxidation products of hydroethidine in chemical and biological systems: ramifications in superoxide measurements. Free. Radic. Biol. Med. 2009, 46:329-338.