IFN-α-driven CCL2 production recruits inflammatory monocytes to infection site in mice

Mucosal Immunology

Volumn 6, Issue 1, 2013, Pages 45-55

  Conrady, C D ^a   Zheng, M ^a   Mandal, N A ^a   Van Rooijen, N ^b   Carr, D J J ^a  

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

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CLODRONIC ACID; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; POLYVINYLPYRIDINE 1 OXIDE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORNEA CELL; FEMALE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; MALE; MOLECULAR RECOGNITION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS INHIBITION;

EID: 84874089105     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.46     Document Type: Article

References (54)

1. Conrady, C. D., Drevets, D. A. & Carr, D. J. Herpes simplex type I (HSV-1) infection of the nervous system: is an immune response a good thing? J. Neuroimmunol. 220, 1-9 (2010).
2. Khanna, K. M., Lepisto, A. J. & Hendricks, R. L. Immunity to latent viral infection: many skirmishes but few fatalities. Trends Immunol. 25, 230-234 (2004). (Pubitemid 38501668)
3. Duan, R., de Vries, R. D., Osterhaus, A. D., Remeijer, L. & Verjans, G. M. Acyclovir-resistant corneal HSV-1 isolates from patients with herpetic keratitis. J. Infect Dis. 198, 659-663 (2008).
4. Larkin, D. F. Corneal transplantation for herpes simplex keratitis. Br. J. Ophthalmol. 82, 107-108 (1998). (Pubitemid 28176982)
5. Smith, R. L., Morroni, J. & Wilcox, C. L. Lack of effect of treatment with penciclovir or acyclovir on the establishment of latent HSV-1 in primary sensory neurons in culture. Antiviral Res. 52, 19-24 (2001). (Pubitemid 32800688)
6. Wakim, L. M., Jones, C. M., Gebhardt, T., Preston, C. M. & Carbone, F. R. CD8(+) T-cell attenuation of cutaneous herpes simplex virus infection reduces the average viral copy number of the ensuing latent infection. Immunol. Cell Biol. 86, 666-675 (2008).
7. Conrady, C. D., Thapa, M., Wuest, T. & Carr, D. J. Loss of mandibular lymph node integrity is associated with an increase in sensitivity to HSV-1 infection in CD118-deficient mice. J. Immunol. 182, 3678-3687 (2009).
8. Leib, D. A., Harrison, T. E., Laslo, K. M., Machalek, M. A., Moorman, N. J. & Virgin, H. W. Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. J. Exp. Med. 189, 663-672 (1999). (Pubitemid 29193367)
9. Conrady, C. D., Zheng, M., Fitzgerald, K. A., Liu, C. & Carr, D. J. Resistance to HSV-1 infection in the epithelium resides with the novel innate sensor, IFI-16. Mucosal Immunol. 5, 173-183 (2012).
10. Reading, P. C., Whitney, P. G., Barr, D. P., Smyth, M. J. & Brooks, A. G. NK cells contribute to the early clearance of HSV-1 from the lung but cannot control replication in the central nervous system following intranasal infection. Eur. J. Immunol. 36, 897-905 (2006).
11. van Lint, A., Ayers, M., Brooks, A. G., Coles, R. M., Heath, W. R. & Carbone, F. R. Herpes simplex virus-specific CD8+ T cells can clear established lytic infections from skin and nerves and can partially limit the early spread of virus after cutaneous inoculation. J. Immunol. 172, 392-397 (2004). (Pubitemid 38020493)
12. Knickelbein, J. E., Khanna, K. M., Yee, M. B., Baty, C. J., Kinchington, P. R. & Hendricks, R. L. Noncytotoxic lytic granule-mediated CD8+ T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322, 268-271 (2008).
13. Chisholm, S. E., Howard, K., Gomez, M. V. & Reyburn, H. T. Expression of ICP0 is sufficient to trigger natural killer cell recognition of herpes simplex virus-infected cells by natural cytotoxicity receptors. J. Infect Dis. 195, 1160-1168 (2007). (Pubitemid 46543447)
14. Croen, K. D. Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. J. Clin. Invest. 91, 2446-2452 (1993). (Pubitemid 23182495)
15. Kodukula, P., Liu, T., Rooijen, N. V., Jager, M. J. & Hendricks, R. L. Macrophage control of herpes simplex virus type 1 replication in the peripheral nervous system. J. Immunol. 162, 2895-2905 (1999). (Pubitemid 29309317)
16. Fernandez, E. J. & Lolis, E. Structure, function, and inhibition of chemokines. Annu. Rev. Pharmacol. Toxicol. 42, 469-499 (2002).
17. Morrison, B. E., Park, S. J., Mooney, J. M. & Mehrad, B. Chemokinemediated recruitment of NK cells is a critical host defense mechanism in invasive aspergillosis. J. Clin. Invest. 112, 1862-1870 (2003). (Pubitemid 38063709)
18. Yoshimura, T., Robinson, E. A., Tanaka, S., Appella, E., Kuratsu, J. & Leonard, E. J. Purification and amino acid analysis of two human gliomaderived monocyte chemoattractants. J. Exp. Med. 169, 1449-1459 (1989). (Pubitemid 19104974)
19. Taub, D. D., Sayers, T. J., Carter, C. R. & Ortaldo, J. R. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J. Immunol. 155, 3877-3888 (1995).
20. Ho, E. L., Heusel, J. W., Brown, M. G., Matsumoto, K., Scalzo, A. A. & Yokoyama, W. M. Murine Nkg2d and Cd94 are clustered within the natural killer complex and are expressed independently in natural killer cells. Proc. Natl. Acad. Sci. USA 95, 6320-6325 (1998). (Pubitemid 28249010)
21. Yu, J. et al. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood 115, 274-281 (2010).
22. Wojtasiak, M. et al. Depletion of Gr-1+, but not Ly6G+, immune cells exacerbates virus replication and disease in an intranasal model of herpes simplex virus type 1 infection. J. Gen. Virol. 91, 2158-2166 (2010).
23. Cheng, H., Tumpey, T. M., Staats, H. F., van Rooijen, N., Oakes, J. E. & Lausch, R. N. Role of macrophages in restricting herpes simplex virus type 1 growth after ocular infection. Invest. Ophthalmol. Vis. Sci. 41, 1402-1409 (2000). (Pubitemid 30261863)
24. Benencia, F., Courreges, M. C., Gamba, G., Cavalieri, H. & Massouh, E. J. Effect of aminoguanidine, a nitric oxide synthase inhibitor, on ocular infection with herpes simplex virus in Balb/c mice. Invest. Ophthalmol. Vis. Sci. 42, 1277-1284 (2001). (Pubitemid 32381970)
25. Farlik, M. et al. Nonconventional initiation complex assembly by STAT and NF-kappaB transcription factors regulates nitric oxide synthase expression. Immunity 33, 25-34 (2010).
26. Fantuzzi, L. et al. Phosphatidylcholine-specific phospholipase C activation is required for CCR5-dependent, NF-kB-driven CCL2 secretion elicited in response to HIV-1 gp120 in human primary macrophages. Blood 111, 3355-3363 (2008).
27. Unterholzner, L. et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11, 997-1004 (2010).
28. Metelitsa, L. S. et al. Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J. Exp. Med. 199, 1213-1221 (2004). (Pubitemid 38620258)
29. Huang, D. R., Wang, J., Kivisakk, P., Rollins, B. J. & Ransohoff, R. M. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193, 713-726 (2001).
30. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222-225 (2011).
31. Eugenin, E. A., Osiecki, K., Lopez, L., Goldstein, H., Calderon, T. M. & Berman, J. W. CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: a potential mechanism of HIV-CNS invasion and NeuroAIDS. J. Neurosci. 26, 1098-1106 (2006). (Pubitemid 43237041)
32. Lu, H., Huang, D., Ransohoff, R. M. & Zhou, L. Acute skeletal muscle injury: CCL2 expression by both monocytes and injured muscle is required for repair. FASEB J. 25, 3344-3355 (2011).
33. Khorooshi, R., Babcock, A. A. & Owens, T. NF-kappaB-driven STAT2 and CCL2 expression in astrocytes in response to brain injury. J. Immunol. 181, 7284-7291 (2008).
34. Bonello, G. B., Pham, M. H., Begum, K., Sigala, J., Sataranatarajan, K. & Mummidi, S. An evolutionarily conserved TNF-alpha-responsive enhancer in the far upstream region of human CCL2 locus influences its gene expression. J. Immunol. 186, 7025-7038 (2011).
35. van Lint, A. L. et al. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-kappaB signaling. J. Virol. 84, 10802-10811 (2010).
36. Dunay, I. R. et al. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29, 306-317 (2008).
37. Kim, Y. G. et al. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34, 769-780 (2011).
38. Tumpey, T. M., Chen, S. H., Oakes, J. E. & Lausch, R. N. Neutrophilmediated suppression of virus replication after herpes simplex virus type 1 infection of the murine cornea. J. Virol. 70, 898-904 (1996). (Pubitemid 26029006)
39. Siebens, H., Tevethia, S. S. & Babior, B. M. Neutrophil-mediated antibodydependent killing of herpes-simplex-virus-infected cells. Blood 54, 88-94 (1979). (Pubitemid 9228089)
40. Frank, G. M., Buela, K. A., Maker, D. M., Harvey, S. A. & Hendricks, R. L. Early responding dendritic cells direct the local NK response to control herpes simplex virus 1 infection within the cornea. J. Immunol. 188, 1350-1359 (2012).
41. Rossol-Voth, R., Rossol, S., Schutt, K. H., Corridori, S., de Cian, W. & Falke, D. In vivo protective effect of tumour necrosis factor alpha against experimental infection with herpes simplex virus type 1. J. Gen. Virol. 72 (Pt 1), 143-147 (1991).
42. Karupiah, G., Xie, Q. W., Buller, R. M., Nathan, C., Duarte, C. & MacMicking, J. D. Inhibition of viral replication by interferon-gammainduced nitric oxide synthase. Science 261, 1445-1448 (1993). (Pubitemid 23334265)
43. Yan, X. T., Tumpey, T. M., Kunkel, S. L., Oakes, J. E. & Lausch, R. N. Role of MIP-2 in neutrophil migration and tissue injury in the herpes simplex virus-1-infected cornea. Invest. Ophthalmol. Vis. Sci. 39, 1854-1862 (1998).
44. Nishikado, H., Mukai, K., Kawano, Y., Minegishi, Y. & Karasuyama, H. NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo. J. Immunol. 186, 5766-5771 (2011).
45. Belshe, R. B. et al. Efficacy results of a trial of a herpes simplex vaccine. N. Engl. J. Med. 366, 34-43 (2012).
46. Corey, L. et al. Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: two randomized controlled trials. Chiron HSV Vaccine Study Group. JAMA 282, 331-340 (1999). (Pubitemid 29350487)
47. Halford, W. P., Puschel, R., Gershburg, E., Wilber, A., Gershburg, S. & Rakowski, B. A live-attenuated HSV-2 ICP0 virus elicits 10 to 100 times greater protection against genital herpes than a glycoprotein D subunit vaccine. PLoS One 6, e17748 (2011).
48. Lin, W. R., Jennings, R., Smith, T. L., Wozniak, M. A. & Itzhaki, R. F. Vaccination prevents latent HSV1 infection of mouse brain. Neurobiol. Aging 22, 699-703 (2001). (Pubitemid 33055606)
49. Marichal, T. et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat. Med. 17, 996-1002 (2011).
50. Liu, C. J., Wang, H. & Lengyel, P. The interferon-inducible nucleolar p204 protein binds the ribosomal RNA-specific UBF1 transcription factor and inhibits ribosomal RNA transcription. EMBO J. 18, 2845-2854 (1999). (Pubitemid 29233956)
51. Garvey, T. L. et al. Inflammatory responses to pneumovirus infection in IFN-alpha beta R gene-deleted mice. J. Immunol. 175, 4735-4744 (2005). (Pubitemid 41362015)
52. Sauer, J. D. et al. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79, 688-694 (2011).
53. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150 (1998). (Pubitemid 28361303)
54. Esplin, B. L., Welner, R. S., Zhang, Q., Borghesi, L. A. & Kincade, P. W. A differentiation pathway for B1 cells in adult bone marrow. Proc. Natl. Acad. Sci. USA 106, 5773-5778 (2009).