Analysis of the differential host cell nuclear proteome induced by attenuated and virulent hemorrhagic arenavirus infection

Journal of Virology

Volumn 83, Issue 2, 2009, Pages 687-700

  Bowick, Gavin C ^a,b   Spratt, Heidi M ^b   Hogg, Alison E ^a   Endsley, Janice J ^a   Wiktorowicz, John E ^a,b   Kurosky, Alexander ^a,b   Luxon, Bruce A ^a,b   Gorenstein, David G ^a,b   Herzog, Norbert K ^a,b,c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NUCLEAR PROTEIN; NUCLEAR RNA; PROTEOME; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; DNA BINDING; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; INFLAMMATION; MOUSE; NONHUMAN; PATHOGENESIS; PICHINDE ARENAVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; TWO DIMENSIONAL GEL ELECTROPHORESIS; VIRUS INFECTION;

ANIMALS; ARENAVIRIDAE; ARENAVIRIDAE INFECTIONS; CELL LINE; CELL NUCLEUS; CYTOPLASM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; IMMUNOBLOTTING; MACROPHAGES; MICE; PROTEIN BINDING; PROTEOME; TANDEM MASS SPECTROMETRY;

ARENAVIRUS; CAVIA; LASSA VIRUS; MURINAE; PICHINDE VIRUS;

EID: 58149517736     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01281-08     Document Type: Article

References (75)

1. Althage, A., B. Odermatt, D. Moskophidis, T. Kundig, U. Hoffman-Rohrer, H. Hengartner, and R. M. Zinkernagel. 1992. Immunosuppression by lymphocytic choriomeningitis virus infection: competent effector T and B cells but impaired antigen presentation. Eur. J. Immunol. 22:1803-1812.
2. Amlie-Lefond, C., D. A. Paz, M. P. Connelly, G. B. Huffnagle, K. S. Dunn, N. T. Whelan, and H. T. Whelan. 2005. Innate immunity for biodefense: a strategy whose time has come. J. Allergy Clin. Immunol. 116:1334-1342.
3. Amman, B. R. 2007. Pet rodents and fatal lymphocytic choriomeningitis in transplant patients. Emerg. Infect. Dis. 13:719-725.
4. Andrade, A. A., P. N. Silva, A. C. Pereira, L. P. De Sousa, P. C. Ferreira, R. T. Gazzinelli, E. G. Kroon, C. Ropert, and C. A. Bonjardim. 2004. The vaccinia virus-stimulated mitogen-activated protein kinase (MAPK) pathway is required for virus multiplication. Biochem. J. 381:437-446.
5. Aronson, J. F., N. K. Herzog, and T. R. Jerrells. 1994. Pathological and virological features of arenavirus disease in guinea-pigs: comparison of 2 Pichinde virus-strains. Am. J. Pathol. 145:228-235.
6. Aronson, J. F., N. K. Herzog, and T. R. Jerrells. 1995. Tumor-necrosis-factor and the pathogenesis of Pichinde virus-infection in guinea-pigs. Am. J. Trop. Med. Hyg. 52:262-269.
7. Ben-Israel, H., and T. Kleinberger. 2002. Adenovirus and cell cycle control. Front. Biosci. 7:d1369-d1395.
8. Bowick, G. C., S. M. Fennewald, B. L. Elsom, J. F. Aronson, B. A. Luxon, D. G. Gorenstein, and N. K. Herzog. 2006. Differential signaling networks induced by mild and lethal hemorrhagic fever virus infections. J. Virol. 80:10248-10252.
9. Bowick, G. C., S. M. Fennewald, E. P. Scott, L. Zhang, B. L. Elsom, J. F. Aronson, H. M. Spratt, B. A. Luxon, D. G. Gorenstein, and N. K. Herzog. 2007. Identification of differentially activated cell-signaling networks associated with Pichinde virus pathogenesis by using systems kinomics. J. Virol. 81:1923-1933.
10. Caldenhoven, E., J. Liden, S. Wissink, A. Van de Stolpe, J. Raaijmakers, L. Koenderman, S. Okret, J. A. Gustafsson, and P. T. Van der Saag. 1995. Negative cross-talk between RelA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol. Endocrinol. 9:401-412.
11. Calvano, S. E., W. Z. Xiao, D. R. Richards, R. M. Felciano, H. V. Baker, R. J. Cho, R. O. Chen, B. H. Brownstein, J. P. Cobb, S. K. Tschoeke, C. Miller-Graziano, L. L. Moldawer, M. N. Mindrinos, R. W. Davis, R. G. Tompkins, and S. F. Lowry. 2005. A network-based analysis of systemic inflammation in humans. Nature 437:1032-1037.
12. Cao, W., M. D. Henry, P. Borrow, H. Yamada, J. H. Elder, E. V. Ravkov, S. T. Nichol, R. W. Compans, K. P. Campbell, and M. B. Oldstone. 1998. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079-2081.
13. Centers for Disease Control and Prevention. 2005. Lymphocytic choriomeningitis virus infection in organ transplant recipients-Massachusetts, Rhode Island, 2005. MMWR Morb. Mortal. Wkly. Rep. 54:537-539.
14. Chu, A., N. Matusiewicz, and U. Stochaj. 2001. Heat-induced nuclear accumulation of hsc70s is regulated by phosphorylation and inhibited in confluent cells. FASEB J. 15:1478-1480.
15. Clark, M. E., P. M. Lieberman, A. J. Berk, and A. Dasgupta. 1993. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro. Mol. Cell. Biol. 13:1232-1237.
16. Colle, J. H., M. F. Saron, B. Shidani, M. P. Lembezat, and P. Truffa-Bachi. 1993. High frequency of T lymphocytes committed to interferon-gamma transcription upon polyclonal activation in spleen from lymphocytic choriomeningitis virus-infected mice. Int. Immunol. 5:435-441.
17. Colle, J. H., M. F. Saron, and P. Truffa-Bachi. 1993. Altered cytokine genes expression by conA-activated spleen cells from mice infected by lymphocytic choriomeningitis virus. Immunol. Lett. 35:247-253.
18. Dai, R. M., E. Chen, D. L. Longo, C. M. Gorbea, and C. C. Li. 1998. Involvement of valosin-containing protein, an ATPase co-purified with IkappaBalpha and 26 S proteasome, in ubiquitin-proteasome-mediated degradation of IkappaBalpha. J. Biol. Chem. 273:3562-3573.
19. Dai, R. M., and C. C. Li. 2001. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 3:740-744.
20. Dastoor, Z., and J. Dreyer. 2000. Nuclear translocation and aggregate formation of heat shock cognate protein 70 (Hsc70) in oxidative stress and apoptosis. J. Cell Sci. 113:2845-2854.
21. Dhar, S. K., B. C. Lynn, C. Daosukho, and D. K. St. Clair. 2004. Identification of nucleophosmin as an NF-kappaB co-activator for the induction of the human SOD2 gene. J. Biol. Chem. 279:28209-28219.
22. Djavani, M. M., O. R. Crasta, J. C. Zapata, Z. Fei, O. Folkerts, B. Sobral, M. Swindells, J. Bryant, H. Davis, C. D. Pauza, I. S. Lukashevich, R. Hammamieh, M. Jett, and M. S. Salvato. 2007. Early blood profiles of virus infection in a monkey model for Lassa fever. J. Virol. 81:7960-7973.
23. Dyer, R. B., and N. K. Herzog. 1995. Isolation of intact nuclei for nuclear extract preparation from a fragile B-lymphocyte cell-line. BioTechniques 19:192.
24. Fennewald, S. M., J. F. Aronson, L. Zhang, and N. K. Herzog. 2002. Alterations in NF-κB and RBP-Jκ by arenavirus infection of macrophages in vitro and in vivo. J. Virol. 76:1154-1162.
25. Fennewald, S. M., E. P. Scott, L. H. Zhang, X. Yang, J. F. Aronson, D. G. Gorenstein, B. A. Luxon, R. E. Shope, D. W. C. Beasley, A. D. T. Barrett, and N. K. Herzog. 2007. Thioaptamer decoy targeting of AP-1 proteins influences cytokine gene expression and the outcome of arenavirus infections. J. Gen. Virol. 88:981-990.
26. Fischer, S. A., M. B. Graham, M. J. Kuehnert, C. N. Kotton, A. Srinivasan, F. M. Marty, J. A. Comer, J. Guarner, C. D. Paddock, D. L. DeMeo, W. J. Shieh, B. R. Erickson, U. Bandy, A. DeMaria, Jr., J. P. Davis, F. L. Delmonico, B. Pavlin, A. Likos, M. J. Vincent, T. K. Sealy, C. S. Goldsmith, D. B. Jernigan, P. E. Rollin, M. M. Packard, M. Patel, C. Rowland, R. F. Helfand, S. T. Nichol, J. A. Fishman, T. Ksiazek, and S. R. Zaki. 2006. Transmission of lymphocytic choriomeningitis virus by organ transplantation. N. Engl. J. Med. 354:2235-2249.
27. Gamel-Didelon, K., C. Corsi, G. Pepeu, H. Jung, M. Gratzl, and A. Mayerhofer. 2002. An autocrine role for pituitary GABA: activation of GABA-B receptors and regulation of growth hormone levels. Neuroendocrinology 76:170-177.
28. Garcia, M. A., E. F. Meurs, and M. Esteban. 2007. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811.
29. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81:2341-2364.
30. Gustin, K. E., and P. Sarnow. 2001. Effects of poliovirus infection on nucleocytoplasmic trafficking and nuclear pore complex composition. EMBO J. 20:240-249.
31. Hay, D. C., G. D. Kemp, C. Dargemont, and R. T. Hay. 2001. Interaction between hnRNPA1 and IκBα is required for maximal activation of NF-κB-dependent transcription. Mol. Cell. Biol. 21:3482-3490.
32. Hutchison, K. A., K. D. Dittmar, L. F. Stancato, and W. B. Pratt. 1996. Ability of various members of the hsp70 family of chaperones to promote assembly of the glucocorticoid receptor into a functional heterocomplex with hsp90. J. Steroid Biochem. Mol. Biol. 58:251-258.
33. Jahrling, P. B., R. A. Hesse, J. B. Rhoderick, M. A. Elwell, and J. B. Moe. 1981. Pathogenesis of a Pichinde virus strain adapted to produce lethal infections in guinea pigs. Infect. Immun. 32:872-880.
34. Johnson, K. M., J. B. McCormick, P. A. Webb, E. S. Smith, L. H. Elliott, and I. J. King. 1987. Clinical virology of Lassa fever in hospitalized patients. J. Infect. Dis. 155:456-464.
35. Kim, E. K., K. B. Kwon, B. S. Koo, M. J. Han, M. Y. Song, E. K. Song, M. K. Han, J. W. Park, D. G. Ryu, and B. H. Park. 2007. Activation of peroxisome proliferator-activated receptor-gamma protects pancreatic beta-cells from cytokine-induced cytotoxicity via NF kappaB pathway. Int. J. Biochem. Cell Biol. 39:1260-1275.
36. Kodiha, M., A. Chu, O. Lazrak, and U. Stochaj. 2005. Stress inhibits nucleocytoplasmic shuttling of heat shock protein hsc70. Am. J. Physiol. Cell Physiol. 289:C1034-C1041.
37. Kondo, T., N. Minamino, T. Nagamura-Inoue, M. Matsumoto, T. Taniguchi, and N. Tanaka. 1997. Identification and characterization of nucleophosmin/B23/numatrin which binds the anti-oncogenic transcription factor IRF-1 and manifests oncogenic activity. Oncogene 15:1275-1281.
38. Lagunas, L., C. M. Bradbury, A. Laszlo, C. R. Hunt, and D. Gius. 2004. Indomethacin and ibuprofen induce Hsc70 nuclear localization and activation of the heat shock response in HeLa cells. Biochem. Biophys. Res. Commun. 313:863-870.
39. Li, H. P., X. Zhang, R. Duncan, L. Comai, and M. M. Lai. 1997. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc. Natl. Acad. Sci. USA 94:9544-9549.
40. Lin, C. Y., Y. C. Liang, and B. Y. Yung. 2006. Nucleophosmin/B23 regulates transcriptional activation of E2F1 via modulating the promoter binding of NF-kappaB, E2F1 and pRB. Cell. Signal. 18:2041-2048.
41. Liou, H. C., M. R. Boothby, P. W. Finn, R. Davidon, N. Nabavi, N. J. Zeleznik-Le, J. P. Ting, and L. H. Glimcher. 1990. A new member of the leucine zipper class of proteins that binds to the HLA DR alpha promoter. Science 247:1581-1584.
42. Lisowska, K., and J. M. Witkowski. 2003. Viral strategies in modulation of NF-kappaB activity. Arch. Immunol. Ther. Exp. (Warsaw). 51:367-375.
43. Lukashevich, I. S., R. Maryankova, A. S. Vladyko, N. Nashkevich, S. Koleda, M. Djavani, D. Horejsh, N. N. Voitenok, and M. S. Salvato. 1999. Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. J. Med. Virol. 59:552-560.
44. Martin, T. E., S. C. Barghusen, G. P. Leser, and P. G. Spear. 1987. Redistribution of nuclear ribonucleoprotein antigens during herpes simplex virus infection. J. Cell Biol. 105:2069-2082.
45. Martinez-Sobrido, L., E. I. Zuniga, D. Rosario, A. Garcia-Sastre, and J. C. de la Torre. 2006. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 80:9192-9199.
46. Mayerhofer, A., B. Hohne-Zell, K. Gamel-Didelon, H. Jung, P. Redecker, D. Grube, H. F. Urbanski, B. Gasnier, J. M. Fritschy, and M. Gratzl. 2001. Gamma-aminobutyric acid (GABA): a para- and/or autocrine hormone in the pituitary. FASEB J. 15:1089-1091.
47. McCormick, J. B., I. J. King, P. A. Webb, C. L. Scribner, R. B. Craven, K. M. Johnson, L. H. Elliott, and R. Belmont-Williams. 1986. Lassa fever. Effective therapy with ribavirin. N. Engl. J. Med. 314:20-26.
48. McKay, L. I., and J. A. Cidlowski. 1998. Cross-talk between nuclear factor-kappa B and the steroid hormone receptors: mechanisms of mutual antagonism. Mol. Endocrinol. 12:45-56.
49. McKay, L. I., and J. A. Cidlowski. 2000. CBP (CREB binding protein) integrates NF-kappaB (nuclear factor-kappaB) and glucocorticoid receptor physical interactions and antagonism. Mol. Endocrinol. 14:1222-1234.
50. Ohgitani, E., K. Kobayashi, K. Takeshita, and J. Imanishi. 1999. Biphasic translocation of a 70 kDa heat shock protein in human cytomegalovirus-infected cells. J. Gen. Virol. 80:63-68.
51. Oldstone, M. B., M. Rodriguez, W. H. Daughaday, and P. W. Lampert. 1984. Viral perturbation of endocrine function: disordered cell function leads to disturbed homeostasis and disease. Nature 307:278-281.
52. Oldstone, M. B., Y. N. Sinha, P. Blount, A. Tishon, M. Rodriguez, R. von Wedel, and P. W. Lampert. 1982. Virus-induced alterations in homeostasis: alteration in differentiated functions of infected cells in vivo. Science 218:1125-1127.
53. Ono, S. J., H. C. Liou, R. Davidon, J. L. Strominger, and L. H. Glimcher. 1991. Human X-box-binding protein 1 is required for the transcription of a subset of human class II major histocompatibility genes and forms a heterodimer with c-fos. Proc. Natl. Acad. Sci. USA 88:4309-4312.
54. Peters, C. J., C. T. Liu, G. W. Anderson, Jr., J. C. Morrill, and P. B. Jahrling. 1989. Pathogenesis of viral hemorrhagic fevers: Rift Valley fever and Lassa fever contrasted. Rev. Infect. Dis. 11(Suppl. 4):S743-S749.
55. Pinol-Roma, S., and G. Dreyfuss. 1991. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science 253:312-314.
56. Radoshitzky, S. R., J. Abraham, C. F. Spiropoulou, J. H. Kuhn, D. Nguyen, W. Li, J. Nagel, P. J. Schmidt, J. H. Nunberg, N. C. Andrews, M. Farzan, and H. Choe. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96.
57. Rao, R. V., K. S. Poksay, S. Castro-Obregon, B. Schilling, R. H. Row, G. del Rio, B. W. Gibson, H. M. Ellerby, and D. E. Bredesen. 2004. Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J. Biol. Chem. 279:177-187.
58. Richmond, J. K., and D. J. Baglole. 2003. Lassa fever: epidemiology, clinical features, and social consequences. Brit. Med. J. 327:1271-1275.
59. Saron, M. F., J. H. Colle, A. utry-Varsat, and P. Truffa-Bachi. 1991. Activated T lymphocytes from mice infected by lymphocytic choriomeningitis virus display high affinity IL-2 receptors but do not proliferate in response to IL-2. J. Immunol. 147:4333-4337.
60. Scheinman, R. I., A. Gualberto, C. M. Jewell, J. A. Cidlowski, and A. S. Baldwin, Jr. 1995. Characterization of mechanisms involved in transrepression of NF-kappa B by activated glucocorticoid receptors. Mol. Cell. Biol. 15:943-953.
61. Schwab, M., V. Reynders, S. Loitsch, D. Steinhilber, J. Stein, and O. Schroder. 2007. Involvement of different nuclear hormone receptors in butyrate-mediated inhibition of inducible NF kappa B signalling. Mol. Immunol. 44:3625-3632.
62. Seow, H. F. 1998. Pathogen interactions with cytokines and host defense: an overview. Vet. Immunol. Immunopathol. 63:139-148.
63. Sevilla, N., S. Kunz, D. McGavern, and M. B. Oldstone. 2003. Infection of dendritic cells by lymphocytic choriomeningitis virus. Curr. Top. Microbiol. Immunol. 276:125-144.
64. Sevilla, N., D. B. McGavern, C. Teng, S. Kunz, and M. B. Oldstone. 2004. Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Investig. 113:737-745.
65. Shi, S. T., P. Huang, H. P. Li, and M. M. Lai. 2000. Heterogeneous nuclear ribonucleoprotein A1 regulates RNA synthesis of a cytoplasmic virus. EMBO J. 19:4701-4711.
66. Shi, S. T., G. Y. Yu, and M. M. Lai. 2003. Multiple type A/B heterogeneous nuclear ribonucleoproteins (hnRNPs) can replace hnRNP A1 in mouse hepatitis virus RNA synthesis. J. Virol. 77:10584-10593.
67. Vanden Berghe, W., K. De Bosscher, E. Boone, S. Plaisance, and G. Haegeman. 1999. The nuclear factor-kappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J. Biol. Chem. 274:32091-32098.
68. Vandermoere, F., I. El Yazidi-Belkoura, C. Slomianny, Y. Demont, G. Bidaux, E. Adriaenssens, J. Lemoine, and H. Hondermarck. 2006. The valosin-containing protein (VCP) is a target of Akt signaling required for cell survival. J. Biol. Chem. 281:14307-14313.
69. Wang, H., X. Yang, G. C. Bowick, N. K. Herzog, B. A. Luxon, L. O. Lomas, and D. G. Gorenstein. 2006. Identification of proteins bound to a thioaptamer probe on a proteomics array. Biochem. Biophys. Res. Commun. 347:586-593.
70. Wang, Y., and X. Zhang. 1999. The nucleocapsid protein of coronavirus mouse hepatitis virus interacts with the cellular heterogeneous nuclear ribonucleoprotein A1 in vitro and in vivo. Virology 265:96-109.
71. Yoo, C. G., S. Lee, C. T. Lee, Y. W. Kim, S. K. Han, and Y. S. Shim. 2000. Anti-inflammatory effect of heat shock protein induction is related to stabilization of I kappa B alpha through preventing I kappa B kinase activation in respiratory epithelial cells. J. Immunol. 164:5416-5423.
72. Zhang, L. H., K. Marriott, and J. F. Aronson. 1999. Sequence analysis of the small RNA segment of guinea pig-passaged Pichinde virus variants. Am. J. Trop. Med. Hyg. 61:220-225.
73. Zhang, W., J. M. Navenot, N. M. Frilot, N. Fujii, and S. C. Peiper. 2007. Association of nucleophosmin negatively regulates CXCR4-mediated G protein activation and chemotaxis. Mol. Pharmacol. 72:1310-1321.
74. Zhou, H., X. Wang, W. K. Ko, and A. O. Wong. 2004. Evidence for a novel intrapituitary autocrine/paracrine feedback loop regulating growth hormone synthesis and secretion in grass carp pituitary cells by functional interactions between gonadotrophs and somatotrophs. Endocrinology 145:5548-5559.
75. Zhu, Y., B. Singh, S. Hewitt, A. Liu, B. Gomez, A. Wang, and R. Clarke. 2006. Expression patterns among interferon regulatory factor-1, human X-box binding protein-1, nuclear factor kappa B, nucleophosmin, estrogen receptor-alpha and progesterone receptor proteins in breast cancer tissue microarrays. Int. J. Oncol. 28:67-76.