A ceramide analogue stimulates dendritic cells to promote T cell responses upon virus infections

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4339-4349

  Pritzl, Curtis J ^a   Seo, Young Jin ^a   Xia, Chuan ^a   Vijayan, Madhuvanthi ^a   Stokes, Zachary D ^a   Hahm, Bumsuk ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; IMMUNOLOGIC FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DENDRITIC CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA; INFLUENZA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS INFECTION; VIRUS STRAIN; ANIMAL; CYTOTOXICITY; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; METABOLISM; ORTHOMYXOVIRUS INFECTION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CERAMIDES; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; IMMUNOLOGIC FACTORS; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; ORTHOMYXOVIRIDAE INFECTIONS; T-LYMPHOCYTE SUBSETS; VIRUS DISEASES;

EID: 84928485431     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402672     Document Type: Article

References (72)

1. Park, J. W., W. J. Park, and A. H. Futerman. 2014. Ceramide synthases as potential targets for therapeutic intervention in human diseases. Biochim. Biophys. Acta 1841: 671-681.
2. Okazaki, T., A. Bielawska, R. M. Bell, and Y. A. Hannun. 1990. Role of ceramide as a lipid mediator of 1 α,25-dihydroxyvitamin D3-induced HL-60 cell differentiation. J. Biol. Chem. 265: 15823-15831.
3. Li, H., P. Junk, A. Huwiler, C. Burkhardt, T. Wallerath, J. Pfeilschifter, and U. Förstermann. 2002. Dual effect of ceramide on human endothelial cells: induction of oxidative stress and transcriptional upregulation of endothelial nitric oxide synthase. Circulation 106: 2250-2256.
4. Hartfield, P. J., G. C. Mayne, and A. W. Murray. 1997. Ceramide induces apoptosis in PC12 cells. FEBS Lett. 401: 148-152.
5. Jayadev, S., B. Liu, A. E. Bielawska, J. Y. Lee, F. Nazaire, L. M. Pushkareva MYu, Obeid, and Y. A. Hannun. 1995. Role for ceramide in cell cycle arrest. J. Biol. Chem. 270: 2047-2052.
6. Bourbon, N. A., J. Yun, and M. Kester. 2000. Ceramide directly activates protein kinase Cζ to regulate a stress-activated protein kinase signaling complex. J. Biol. Chem. 275: 35617-35623.
7. Zhu, X. F., Z. C. Liu, B. F. Xie, G. K. Feng, and Y. X. Zeng. 2003. Ceramide induces cell cycle arrest and upregulates p27kip in nasopharyngeal carcinoma cells. Cancer Lett. 193: 149-154.
8. Mizushima, N., R. Koike, H. Kohsaka, Y. Kushi, S. Handa, H. Yagita, and N. Miyasaka. 1996. Ceramide induces apoptosis via CPP32 activation. FEBS Lett. 395: 267-271.
9. Gill, J. S., and A. J. Windebank. 2000. Ceramide initiates NFκB-mediated caspase activation in neuronal apoptosis. Neurobiol. Dis. 7: 448-461.
10. Park, J. Y., M. J. Kim, Y. K. Kim, and J. S. Woo. 2011. Ceramide induces apoptosis via caspase-dependent and caspase-independent pathways in mesenchymal stem cells derived from human adipose tissue. Arch. Toxicol. 85: 1057-1065.
11. Yabu, T., H. Shiba, Y. Shibasaki, T. Nakanishi, S. Imamura, K. Touhata, and M. Yamashita. 2015. Stress-induced ceramide generation and apoptosis via the phosphorylation and activation of nSMase1 by JNK signaling. Cell Death Differ. 22: 258-273.
12. Bielawska, A., C. M. Linardic, and Y. A. Hannun. 1992. Modulation of cell growth and differentiation by ceramide. FEBS Lett. 307: 211-214.
13. Riboni, L., A. Prinetti, R. Bassi, A. Caminiti, and G. Tettamanti. 1995. A mediator role of ceramide in the regulation of neuroblastoma Neuro2a cell differentiation. J. Biol. Chem. 270: 26868-26875.
14. Józefowski, S., M. Czerkies, A. Łukasik, A. Bielawska, J. Bielawski, K. Kwiatkowska, and A. Sobota. 2010. Ceramide and ceramide 1-phosphate are negative regulators of TNF-α production induced by lipopolysaccharide. J. Immunol. 185: 6960-6973.
15. Herz, J., J. Pardo, H. Kashkar, M. Schramm, E. Kuzmenkina, E. Bos, K. Wiegmann, R. Wallich, P. J. Peters, S. Herzig, et al. 2009. Acid sphingomyelinase is a key regulator of cytotoxic granule secretion by primary T lymphocytes. Nat. Immunol. 10: 761-768.
16. Boucher, L. M., K. Wiegmann, A. Fütterer, K. Pfeffer, T. Machleidt, S. Schütze, T. W. Mak, and M. Krönke. 1995. CD28 signals through acidic sphingomyelinase. J. Exp. Med. 181: 2059-2068.
17. Santinha, D. R., D. R. Marques, E. A. Maciel, C. S. Simões, S. Rosa, B. M. Neves, B. Macedo, P. Domingues, M. T. Cruz, and M. R. Domingues. 2012. Profiling changes triggered during maturation of dendritic cells: a lipidomic approach. Anal. Bioanal. Chem. 403: 457-471.
18. Chiba, N., A. Masuda, Y. Yoshikai, and T. Matsuguchi. 2007. Ceramide inhibits LPS-induced production of IL-5, IL-10, and IL-13 from mast cells. J. Cell. Physiol. 213: 126-136.
19. Steinman, R. M. 2012. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30: 1-22.
20. Austyn, J. M., R. M. Steinman, D. E. Weinstein, A. Granelli-Piperno, and M. A. Palladino. 1983. Dendritic cells initiate a two-stage mechanism for T lymphocyte proliferation. J. Exp. Med. 157: 1101-1115.
21. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
22. Pasare, C., and R. Medzhitov. 2005. Toll-like receptors: linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560: 11-18.
23. Ng, C. T., B. M. Sullivan, and M. B. Oldstone. 2011. The role of dendritic cells in viral persistence. Curr. Opin. Virol. 1: 160-166.
24. Colonna, M. 2004. Viral immunosuppression: disabling the guards. J. Clin. Invest. 113: 660-662.
25. Pritzl, C. J., Y.-J. Seo, and B. Hahm. 2012. Viruses strive to suppress host immune responses and prolong persistence. In Recent Advances in Immunology to Target Cancer, Inflammation and Infections. J. R. Kanwar, ed. InTech, Rijeka, Croatia, p. 23-42.
26. Hahm, B. 2009. Hostile communication of measles virus with host innate immunity and dendritic cells. Curr. Top. Microbiol. Immunol. 330: 271-287.
27. Matloubian, M., T. Somasundaram, S. R. Kolhekar, R. Selvakumar, and R. Ahmed. 1990. Genetic basis of viral persistence: single amino acid change in the viral glycoprotein affects ability of lymphocytic choriomeningitis virus to persist in adult mice. J. Exp. Med. 172: 1043-1048.
28. 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. Invest. 113: 737-745.
29. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
30. + T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10: 29-37.
31. + T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
32. Jin, H. T., A. C. Anderson, W. G. Tan, E. E. West, S. J. Ha, K. Araki, G. J. Freeman, V. K. Kuchroo, and R. Ahmed. 2010. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 107: 14733-14738.
33. Brooks, D. G., M. J. Trifilo, K. H. Edelmann, L. Teyton, D. B. McGavern, and M. B. Oldstone. 2006. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12: 1301-1309.
34. Ejrnaes, M., C. M. Filippi, M. M. Martinic, E. M. Ling, L. M. Togher, S. Crotty, and M. G. von Herrath. 2006. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203: 2461-2472.
35. Teijaro, J. R., C. Ng, A. M. Lee, B. M. Sullivan, K. C. Sheehan, M. Welch, R. D. Schreiber, J. C. de la Torre, and M. B. Oldstone. 2013. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340: 207-211.
36. Wilson, E. B., D. H. Yamada, H. Elsaesser, J. Herskovitz, J. Deng, G. Cheng, B. J. Aronow, C. L. Karp, and D. G. Brooks. 2013. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202-207.
37. Seo, Y. J., and B. Hahm. 2014. Sphingosine analog AAL-R promotes activation of LCMV-infected dendritic cells. Viral Immunol. 27: 82-86.
38. Hahm, B., M. J. Trifilo, E. I. Zuniga, and M. B. Oldstone. 2005. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 22: 247-257.
39. Seo, Y. J., C. J. Pritzl, M. Vijayan, K. Bomb, M. E. McClain, S. Alexander, and B. Hahm. 2013. Sphingosine kinase 1 serves as a pro-viral factor by regulating viral RNA synthesis and nuclear export of viral ribonucleoprotein complex upon influenza virus infection. PLoS One 8: e75005.
40. Marsolais, D., B. Hahm, K. H. Edelmann, K. B. Walsh, M. Guerrero, Y. Hatta, Y. Kawaoka, E. Roberts, M. B. Oldstone, and H. Rosen. 2008. Local not systemic modulation of dendritic cell S1P receptors in lung blunts virus-specific immune responses to influenza. Mol. Pharmacol. 74: 896-903.
41. Marsolais, D., B. Hahm, K. B. Walsh, K. H. Edelmann, D. McGavern, Y. Hatta, Y. Kawaoka, H. Rosen, and M. B. Oldstone. 2009. A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc. Natl. Acad. Sci. USA 106: 1560-1565.
42. Seo, Y. J., C. J. Pritzl, M. Vijayan, C. R. Blake, M. E. McClain, and B. Hahm. 2012. Sphingosine analogue AAL-R increases TLR7-mediated dendritic cell responses via p38 and type I IFN signaling pathways. J. Immunol. 188: 4759-4768.
43. Hassett, D. E., J. Zhang, M. Slifka, and J. L. Whitton. 2000. Immune responses following neonatal DNA vaccination are long-lived, abundant, and qualitatively similar to those induced by conventional immunization. J. Virol. 74: 2620-2627.
44. Nayak, D., K. R. Johnson, S. Heydari, T. L. Roth, B. H. Zinselmeyer, and D. B. McGavern. 2013. Type I interferon programs innate myeloid dynamics and gene expression in the virally infected nervous system. PLoS Pathog. 9: e1003395.
45. Jeannet, G., C. Boudousquié, N. Gardiol, J. Kang, J. Huelsken, and W. Held. 2010. Essential role of the Wnt pathway effector Tcf-1 for the establishment of functional CD8 T cell memory. Proc. Natl. Acad. Sci. USA 107: 9777-9782.
46. Gulbins, E., R. Bissonnette, A. Mahboubi, S. Martin, W. Nishioka, T. Brunner, G. Baier, G. Baier-Bitterlich, C. Byrd, F. Lang, et al. 1995. FAS-induced apoptosis is mediated via a ceramide-initiated RAS signaling pathway. Immunity 2: 341-351.
47. Brugg, B., P. P. Michel, Y. Agid, and M. Ruberg. 1996. Ceramide induces apoptosis in cultured mesencephalic neurons. J. Neurochem. 66: 733-739.
48. Larocca, J. N., M. Farooq, and W. T. Norton. 1997. Induction of oligodendrocyte apoptosis by C2-ceramide. Neurochem. Res. 22: 529-534.
49. Siskind, L. J., and M. Colombini. 2000. The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. J. Biol. Chem. 275: 38640-38644.
50. Lavrentiadou, S. N., C. Chan, T. Kawcak, T. Ravid, A. Tsaba, A. van der Vliet, R. Rasooly, and T. Goldkorn. 2001. Ceramide-mediated apoptosis in lung epithelial cells is regulated by glutathione. Am. J. Respir. Cell Mol. Biol. 25: 676-684.
51. Kurinna, S. M., C. C. Tsao, A. F. Nica, T. Jiffar, and P. P. Ruvolo. 2004. Ceramide promotes apoptosis in lung cancer-derived A549 cells by a mechanism involving c-Jun NH2-terminal kinase. Cancer Res. 64: 7852-7856.
52. Finnegan, C. M., S. S. Rawat, A. Puri, J. M. Wang, F. W. Ruscetti, and R. Blumenthal. 2004. Ceramide, a target for antiretroviral therapy. Proc. Natl. Acad. Sci. USA 101: 15452-15457.
53. Voisset, C., M. Lavie, F. Helle, A. Op De Beeck, A. Bilheu, J. Bertrand-Michel, F. Tercé, L. Cocquerel, C. Wychowski, N. Vu-Dac, and J. Dubuisson. 2008. Ceramide enrichment of the plasma membrane induces CD81 internalization and inhibits hepatitis C virus entry. Cell. Microbiol. 10: 606-617.
54. Basu, S., and R. Kolesnick. 1998. Stress signals for apoptosis: ceramide and c-Jun kinase. Oncogene 17: 3277-3285.
55. Mazière, C., M. A. Conte, L. Leborgne, T. Levade, W. Hornebeck, R. Santus, and J. C. Mazière. 2001. UVA radiation stimulates ceramide production: relationship to oxidative stress and potential role in ERK, JNK, and p38 activation. Biochem. Biophys. Res. Commun. 281: 289-294.
56. Sanvicens, N., and T. G. Cotter. 2006. Ceramide is the key mediator of oxidative stress-induced apoptosis in retinal photoreceptor cells. J. Neurochem. 98: 1432-1444.
57. Raulet, D. H. 2004. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat. Immunol. 5: 996-1002.
58. Spaggiari, G. M., R. Carosio, D. Pende, S. Marcenaro, P. Rivera, M. R. Zocchi, L. Moretta, and A. Poggi. 2001. NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur. J. Immunol. 31: 1656-1665.
59. Wolff, R. A., R. T. Dobrowsky, A. Bielawska, L. M. Obeid, and Y. A. Hannun. 1994. Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem. 269: 19605-19609.
60. Sallusto, F., C. Nicolò, R. De Maria, S. Corinti, and R. Testi. 1996. Ceramide inhibits antigen uptake and presentation by dendritic cells. J. Exp. Med. 184: 2411-2416.
61. Tan, J. T., J. K. Whitmire, R. Ahmed, T. C. Pearson, and C. P. Larsen. 1999. 4-1BB ligand, a member of the TNF family, is important for the generation of antiviral CD8 T cell responses. J. Immunol. 163: 4859-4868.
62. + dendritic cells are protected from influenza virus infection. J. Clin. Invest. 122: 4037-4047.
63. Wakim, L. M., and M. J. Bevan. 2011. Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection. Nature 471: 629-632.
64. Alayoubi, A. M., J. C. Wang, B. C. Au, S. Carpentier, V. Garcia, S. Dworski, S. El-Ghamrasni, K. N. Kirouac, M. J. Exertier, Z. J. Xiong, et al. 2013. Systemic ceramide accumulation leads to severe and varied pathological consequences. EMBO Mol. Med. 5: 827-842.
65. Petrache, I., V. Natarajan, L. Zhen, T. R. Medler, A. T. Richter, C. Cho, W. C. Hubbard, E. V. Berdyshev, and R. M. Tuder. 2005. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 11: 491-498.
66. + T cell tolerance. J. Exp. Med. 196: 1627-1638.
67. Guo, M., S. Gong, S. Maric, Z. Misulovin, M. Pack, K. Mahnke, M. C. Nussenzweig, and R. M. Steinman. 2000. A monoclonal antibody to the DEC-205 endocytosis receptor on human dendritic cells. Hum. Immunol. 61: 729-738.
68. Mahnke, K., M. Guo, S. Lee, H. Sepulveda, S. L. Swain, M. Nussenzweig, and R. M. Steinman. 2000. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell Biol. 151: 673-684.
69. Copland, M. J., M. A. Baird, T. Rades, J. L. McKenzie, B. Becker, F. Reck, P. C. Tyler, and N. M. Davies. 2003. Liposomal delivery of antigen to human dendritic cells. Vaccine 21: 883-890.
70. Pietersz, G. A., V. Apostolopoulos, and I. F. McKenzie. 2000. Generation of cellular immune responses to antigenic tumor peptides. Cell. Mol. Life Sci. 57: 290-310.
71. Badiee, A., N. Davies, K. McDonald, K. Radford, H. Michiue, D. Hart, and M. Kato. 2007. Enhanced delivery of immunoliposomes to human dendritic cells by targeting the multilectin receptor DEC-205. Vaccine 25: 4757-4766.
72. van Broekhoven, C. L., C. R. Parish, C. Demangel, W. J. Britton, and J. G. Altin. 2004. Targeting dendritic cells with antigen-containing liposomes: a highly effective procedure for induction of antitumor immunity and for tumor immunotherapy. Cancer Res. 64: 4357-4365.