PI3K-dependent upregulation of Mcl-1 by human cytomegalovirus is mediated by epidermal growth factor receptor and inhibits apoptosis in short-lived monocytes

Journal of Immunology

Volumn 184, Issue 6, 2010, Pages 3213-3222

  Chan, Gary ^a   Nogalski, Maciej T ^a   Bentz, Gretchen L ^a,b   Smith, M Shane ^a,c   Parmater, Alexander ^a   Yurochko, Andrew D ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN MCL 1; SMALL INTERFERING RNA; TRANSCRIPTOME; APOPTOSIS REGULATORY PROTEIN; IMMEDIATE EARLY PROTEIN; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN;

APOPTOSIS; ARTICLE; CELL COMMUNICATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; EMBRYO; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MODULATION; MONOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SURVIVAL; UPREGULATION; VIRUS ATTACHMENT; BIOSYNTHESIS; CELL CULTURE; CELL DEATH; CYTOLOGY; CYTOMEGALOVIRUS; DRUG ANTAGONISM; ENZYME INDUCTION; ENZYMOLOGY; IMMUNOLOGY; IMMUNOPHENOTYPING; MACROPHAGE; METABOLISM; PATHOGENICITY; PHYSIOLOGY; VIROLOGY; VIRULENCE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS REGULATORY PROTEINS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CYTOMEGALOVIRUS; ENZYME INDUCTION; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNOPHENOTYPING; MACROPHAGES; MONOCYTES; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, EPIDERMAL GROWTH FACTOR; UP-REGULATION; VIRULENCE;

EID: 77951911859     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903025     Document Type: Article

References (47)

1. Fowler, K. B., and R. F. Pass. 1991. Sexually transmitted diseases in mothers of neonates with congenital cytomegalovirus infection. J. Infect. Dis. 164: 259-264.
2. Jordan, M. C., W. Rousseau, J. A. Stewart, G. R. Noble, and T. D. Chin. 1973. Spontaneous cytomegalovirus mononucleosis. Clinical and laboratory observations in nine cases. Ann. Intern. Med. 79: 153-160.
3. Rahbar, A., L. Boström, U. Lagerstedt, I. Magnusson, C. Söderberg-Naucler, and V. A. Sundqvist. 2003. Evidence of active cytomegalovirus infection and increased production of IL-6 in tissue specimens obtained from patients with inflammatory bowel diseases. Inflamm. Bowel Dis. 9: 154-161.
4. Streblow, D. N., J. Dumortier, A. V. Moses, S. L. Orloff, and J. A. Nelson. 2008. Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr. Top. Microbiol. Immunol. 325: 397-415.
5. Masur, H., S. M. Whitcup, C. Cartwright, M. Polis, and R. Nussenblatt. 1996. Advances in the management of AIDS-related cytomegalovirus retinitis. Ann. Intern. Med. 125: 126-136.
6. Ho, M. 1977. Virus infections after transplantation in man. Brief review. Arch. Virol. 55: 1-24.
7. Stagno, S., R. F. Pass, M. E. Dworsky, R. E. Henderson, E. G. Moore, P. D. Walton, and C. A. Alford. 1982. Congenital cytomegalovirus infection: The relative importance of primary and recurrent maternal infection. N. Engl. J. Med. 306: 945-949.
8. Bissinger, A. L., C. Sinzger, E. Kaiserling, and G. Jahn. 2002. Human cytomegalovirus as a direct pathogen: correlation of multiorgan involvement and cell distribution with clinical and pathological findings in a case of congenital inclusion disease. J. Med. Virol. 67: 200-206.
9. Mocarski, E. S., T. Shenk, and R. F. Pass. 2007. Cytomegalovirus. In Fields Virology. D. M. Knipe, and P. M. Howley, eds. Lippincott, Williams and Wilkins, Philadelphia, p. 2701-2772.
10. Yurochko, A. D. 2008. Human cytomegalovirus modulation of signal transduction. In Human cytomegaloviruses. M. F. Stinski, and T. Shenk, eds. Springer-Verlag, Berlin Heidelberg, p. 205-220.
11. Manez, R., S. Kusne, C. Rinaldo, J. M. Aguado, K. St George, P. Grossi, B. Frye, J. J. Fung, and G. D. Ehrlich. 1996. Time to detection of cytomegalovirus (CMV) DNA in blood leukocytes is a predictor for the development of CMV disease in CMV-seronegative recipients of allografts from CMV-seropositive donors following liver transplantation. J. Infect. Dis. 173: 1072-1076.
12. Taylor-Wiedeman, J., P. Sissons, and J. Sinclair. 1994. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68: 1597-1604.
13. Pulliam, L. 1991. Cytomegalovirus preferentially infects a monocyte derived macrophage/microglial cell in human brain cultures: neuropathology differs between strains. J. Neuropathol. Exp. Neurol. 50: 432-440.
14. Booss, J., P. R. Dann, B. P. Griffith, and J. H. Kim. 1989. Host defense response to cytomegalovirus in the central nervous system. Predominance of the monocyte. Am. J. Pathol. 134: 71-78.
15. Chan, G., E. R. Bivins-Smith, M. S. Smith, P. M. Smith, and A. D. Yurochko. 2008. Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage. J. Immunol. 181: 698-711.
16. Smith, M. S., G. L. Bentz, J. S. Alexander, and A. D. Yurochko. 2004. Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J. Virol. 78: 4444-4453.
17. Yurochko, A. D., and E. S. Huang. 1999. Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression. J. Immunol. 162: 4806-4816.
18. Whitelaw, D. M. 1972. Observations on human monocyte kinetics after pulse labeling. Cell Tissue Kinet. 5: 311-317.
19. Goldmacher, V. S. 2005. Cell death suppression by cytomegaloviruses. Apoptosis 10: 251-265.
20. Chan, G., M. T. Nogalski, and A. D. Yurochko. 2009. Activation of EGFR on monocytes is required for human cytomegalovirus entry and mediates cellular motility. Proc. Natl. Acad. Sci. USA 106: 22369-22374.
21. Smith, M. S., G. L. Bentz, P. M. Smith, E. R. Bivins, and A. D. Yurochko. 2004. HCMV activates PI(3)K in monocytes and promotes monocyte motility and transendothelial migration in a PI(3)K-dependent manner. J. Leukoc. Biol. 76: 65-76.
22. Smith, M. S., E. R. Bivins-Smith, A. M. Tilley, G. L. Bentz, G. Chan, J. Minard, and A. D. Yurochko. 2007. Roles of phosphatidylinositol 3-kinase and NF-kappaB in human cytomegalovirus-mediated monocyte diapedesis and adhesion: strategy for viral persistence. J. Virol. 81: 7683-7694.
23. Chan, G., E. R. Bivins-Smith, M. S. Smith, and A. D. Yurochko. 2008. Transcriptome analysis of NF-kappaB- and phosphatidylinositol 3-kinase-regulated genes in human cytomegalovirus-infected monocytes. J. Virol. 82: 1040-1046.
24. Liu, H., H. Perlman, L. J. Pagliari, and R. M. Pope. 2001. Constitutively activated Akt-1 is vital for the survival of human monocyte-differentiated macrophages. Role of Mcl-1, independent of nuclear factor (NF)-kappaB, Bad, or caspase activation. J. Exp. Med. 194: 113-126.
25. Liu, H., Q. Huang, B. Shi, P. Eksarko, V. Temkin, and R. M. Pope. 2006. Regulation of Mcl-1 expression in rheumatoid arthritis synovial macrophages. Arthritis Rheum. 54: 3174-3181.
26. Opferman, J. T., H. Iwasaki, C. C. Ong, H. Suh, S. Mizuno, K. Akashi, and S. J. Korsmeyer. 2005. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307: 1101-1104.
27. Haughn, L., R. G. Hawley, D. K. Morrison, H. von Boehmer, and D. M. Hockenbery. 2003. BCL-2 and BCL-XL restrict lineage choice during hematopoietic differentiation. J. Biol. Chem. 278: 25158-25165.
28. Triglia, T., G. F. Burns, and J. A. Werkmeister. 1985. Rapid changes in surface antigen expression by blood monocytes cultured in suspension or adherent to plastic. Blood 65: 921-928.
29. Hashimoto, S. I., I. Komuro, M. Yamada, and K. S. Akagawa. 2001. IL-10 inhibits granulocyte-macrophage colony-stimulating factor-dependent human monocyte survival at the early stage of the culture and inhibits the generation of macrophages. J. Immunol. 167: 3619-3625.
30. Yurochko, A. D., D. Y. Liu, D. Eierman, and S. Haskill. 1992. Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction. Proc. Natl. Acad. Sci. USA 89: 9034-9038.
31. Chan, G., D. G. Hemmings, A. D. Yurochko, and L. J. Guilbert. 2002. Human cytomegalovirus-caused damage to placental trophoblasts mediated by immediate-early gene-induced tumor necrosis factor-alpha. Am. J. Pathol. 161: 1371-1381.
32. Perlman, H., L. J. Pagliari, N. Nguyen, K. Bradley, H. Liu, and R. M. Pope. 2001. The Fas-FasL death receptor and PI3K pathways independently regulate monocyte homeostasis. Eur. J. Immunol. 31: 2421-2430.
33. Han, Z., E. A. Hendrickson, T. A. Bremner, and J. H. Wyche. 1997. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J. Biol. Chem. 272: 13432-13436.
34. Castillo, J. P., and T. F. Kowalik. 2002. Human cytomegalovirus immediate early proteins and cell growth control. Gene 290: 19-34.
35. Clemens, M. J. 2003. Interferons and apoptosis. J. Interferon Cytokine Res. 23: 277-292.
36. Yang, T., H. L. Buchan, K. J. Townsend, and R. W. Craig. 1996. MCL-1, a member of the BLC-2 family, is induced rapidly in response to signals for cell differentiation or death, but not to signals for cell proliferation. J. Cell. Physiol. 166: 523-536.
37. Reynolds, J. E., T. Yang, L. Qian, J. D. Jenkinson, P. Zhou, A. Eastman, and R. W. Craig. 1994. Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res. 54: 6348-6352.
38. Adams, K. W., and G. M. Cooper. 2007. Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J. Biol. Chem. 282: 6192-6200.
39. Michels, J., P. W. Johnson, and G. Packham. 2005. Mcl-1. Int. J. Biochem. Cell Biol. 37: 267-271.
40. Moulding, D. A., R. V. Giles, D. G. Spiller, M. R. White, D. M. Tidd, and S. W. Edwards. 2000. Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood 96: 1756-1763.
41. Zhou, P., L. Qian, C. K. Bieszczad, R. Noelle, M. Binder, N. B. Levy, and R. W. Craig. 1998. Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage. Blood 92: 3226-3239.
42. Sly, L. M., S. M. Hingley-Wilson, N. E. Reiner, and W. R. McMaster. 2003. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J. Immunol. 170: 430-437.
43. Hasan, Z., M. Ashraf, A. Tayyebi, and R. Hussain. 2006. M. leprae inhibits apoptosis in THP-1 cells by downregulation of Bad and Bak and upregulation of Mcl-1 gene expression. BMC Microbiol. 6: 78.
44. Swingler, S., A. M. Mann, J. Zhou, C. Swingler, and M. Stevenson. 2007. Apoptotic killing of HIV-1-infected macrophages is subverted by the viral envelope glycoprotein. PLoS Pathog. 3: 1281-1290.
45. Wang, X., D. Y. Huang, S. M. Huong, and E. S. Huang. 2005. Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat. Med. 11: 515-521.
46. Feire, A. L., H. Koss, and T. Compton. 2004. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. USA 101: 15470-15475.
47. Edick, M. J., L. Tesfay, L. E. Lamb, B. S. Knudsen, and C. K. Miranti. 2007. Inhibition of integrin-mediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol. Biol. Cell 18: 2481-2490.