Autocrine CCL3 and CCL4 induced by the oncoprotein LMP1 promote epstein-barr virus-triggered B cell proliferation

Journal of Virology

Volumn 87, Issue 16, 2013, Pages 9041-9052

  Tsai, Shu Chun ^a   Lin, Sue Jane ^b   Lin, Cheau Jye ^a   Chou, Ya Ching ^a   Lin, Jiun Han ^a   Yeh, Te Huei ^c   Chen, Mei Ru ^a   Huang, Li Min ^c   Lu, Meng You ^c   Huang, Ya Chi ^a   Chen, Huan Yun ^a   Tsai, Ching Hwa ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE ANTIBODY; LATENT MEMBRANE PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE;

ADOLESCENT; ARTICLE; AUTOCRINE EFFECT; B LYMPHOCYTE ACTIVATION; CELL GROWTH; CELL IMMORTALIZATION; CELL SURVIVAL; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EPSTEIN BARR VIRUS INFECTION; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPROMISED PATIENT; IN VIVO STUDY; LYMPHOBLASTOID CELL LINE; LYMPHOCYTE PROLIFERATION; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCHOOL CHILD; UPREGULATION;

B-LYMPHOCYTES; CELL PROLIFERATION; CHEMOKINE CCL3; CHEMOKINE CCL4; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS;

EID: 84881219446     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00541-13     Document Type: Article

References (47)

1. Thorley-Lawson DA, Allday MJ. 2008. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6:913-924.
2. Dawson CW, Port RJ, Young LS. 2012. The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharyngeal carcinoma (NPC). Semin. Cancer Biol. 22:144-153.
3. Martin D, Gutkind JS. 2008. Human tumor-associated viruses and new insights into the molecular mechanisms of cancer. Oncogene 27(Suppl 2):S31-S42.
4. Jabs WJ, Wagner HJ, Maurmann S, Hennig H, Kreft B. 2002. Inhibition of macrophage inflammatory protein-1α production by Epstein-Barr virus. Blood 99:1512-1516.
5. Gaudreault E, Fiola S, Olivier M, Gosselin J. 2007. Epstein-barr virus induces MCP-1 secretion by human monocytes via TLR2. J. Virol. 81: 8016-8024.
6. Ehlin-Henriksson B, Liang W, Cagigi A, Mowafi F, Klein G, Nilsson A. 2009. Changes in chemokines and chemokine receptor expression on tonsillar B cells upon Epstein-Barr virus infection. Immunology 127:549- 557.
7. Nakayama T, Hieshima K, Nagakubo D, Sato E, Nakayama M, Kawa K, Yoshie O. 2004. Selective induction of Th2-attracting chemokines CCL17 and CCL22 in human B Cells by latent membrane protein 1 of EpsteinBarr virus. J. Virol. 78:1665-1674.
8. Miyauchi K, Urano E, Yoshiyama H, Komano J. 2011. Cytokine signatures of transformed B cells with distinct Epstein-Barr virus latencies as a potential diagnostic tool for B cell lymphoma. Cancer Sci. 102:1236-1241.
9. Tsai SC, Lin SJ, Chen PW, Luo WY, Yeh TH, Wang HW, Chen CJ, Tsai CH. 2009. EBV Zta protein induces the expression of interleukin-13, promoting the proliferation of EBV-infected B cells and lymphoblastoid cell lines. Blood 114:109-118.
10. Chou YC, Lin SJ, Lu J, Yeh TH, Chen CL, Weng PL, Lin JH, Yao M, Tsai CH. 2011. Requirement for LMP1-induced RON receptor tyrosine kinase in Epstein-Barr virus-mediated B-cell proliferation. Blood 118: 1340-1349.
11. Lo YM, Chan LY, Lo KW, Leung SF, Zhang J, Chan AT, Lee JC, Hjelm NM, Johnson PJ, Huang DP. 1999. Quantitative analysis of cell-free Epstein-Barr virus DNA in plasma of patients with nasopharyngeal carcinoma. Cancer Res. 59:1188-1191.
12. Shair KHY, Bendt KM, Edwards RH, Bedford EC, Nielsen JN, Raab-Traub N. 2007. EBV latent membrane protein 1 activates Akt, NFκB, and Stat3 in B cell lymphomas. PLoS Pathog. 3:e166. doi:10.1371/journal.ppat .0030166.
13. Morris MA, Dawson CW, Young LS. 2009. Role of the Epstein-Barr virus-encoded latent membrane protein-1, LMP1, in the pathogenesis of nasopharyngeal carcinoma. Future Oncol. 5:811-825.
14. Lentzsch S, Gries M, Janz M, Bargou R, Dorken B, Mapara MY. 2003. Macrophage inflammatory protein 1-alpha (MIP-1 alpha) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood 101:3568-3573.
15. Kuppers R. 2003. B cells under influence: transformation of B cells by Epstein-Barr virus. Nat. Rev. Immunol. 3:801-812.
16. Counter CM, Botelho FM, Wang P, Harley CB, Bacchetti S. 1994. Stabilization of short telomeres and telomerase activity accompany immortalization of Epstein-Barr virus-transformed human B lymphocytes. J. Virol. 68:3410-3414.
17. Sugimoto M, Tahara H, Ide T, Furuichi Y. 2004. Steps involved in immortalization and tumorigenesis in human B-lymphoblastoid cell lines transformed by Epstein-Barr virus. Cancer Res. 64:3361-3364.
18. Dorsam RT, Gutkind JS. 2007. G-protein-coupled receptors and cancer. Nat. Rev. Cancer 7:79-94.
19. Damania B. 2004. Oncogenic gamma-herpesviruses: comparison of viral proteins involved in tumorigenesis. Nat. Rev. Microbiol. 2:656-668.
20. Holst PJ, Rosenkilde MM, Manfra D, Chen S-C, Wiekowski MT, Holst B, Cifire F, Lipp M, Schwartz TW, Lira SA. 2001. Tumorigenesis induced by the HHV8-encoded chemokine receptor requires ligand modulation of high constitutive activity. J. Clin. Invest. 108:1789-1796.
21. Chow KYC, Brotin M, Ben Khalifa Y, Carthagena L, Teissier S, Danckaert A, Galzi J-L, Arenzana-Seisdedos F, Thierry F, Bachelerie F. 2010. A pivotal role for CXCL12 signaling in HPV-mediated transformation of keratinocytes: clues to understanding HPV-pathogenesis in WHIM syndrome. Cell Host Microbe 8:523-533.
22. Burger JA, Quiroga MP, Hartmann E, Burkle A, Wierda WG, Keating MJ, Rosenwald A. 2009. High-level expression of the T-cell chemokines CCL3 and CCL4 by chronic lymphocytic leukemia B cells in nurselike cell cocultures and after BCR stimulation. Blood 113:3050-3058.
23. Zucchetto A, Benedetti D, Tripodo C, Bomben R, Dal Bo M, Marconi D, Bossi F, Lorenzon D, Degan M, Rossi FM, Rossi D, Bulian P, Franco V, Del Poeta G, Deaglio S, Gaidano G, Tedesco F, Malavasi F, Gattei V. 2009. CD38/CD31, the CCL3 and CCL4 chemokines, and CD49d/vascular cell adhesion molecule-1 are interchained by sequential events sustaining chronic lymphocytic leukemia cell survival. Cancer Res. 69:4001-4009.
24. Bogunia-Kubik K, Jaskula E, Lange A. 2007. The presence of functional CCR5 and EBV reactivation after allogeneic haematopoietic stem cell transplantation. Bone Marrow Transplant. 40:145-150.
25. Lai HC, Hsiao JR, Chen CW, Wu SY, Lee CH, Su IJ, Takada K, Chang Y. 2010. Endogenous latent membrane protein 1 in Epstein-Barr virusinfected nasopharyngeal carcinoma cells attracts T lymphocytes through upregulation of multiple chemokines. Virology 405:464-473.
26. Kung CP, Raab-Traub N. 2008. Epstein-Barr virus latent membrane protein 1 induces expression of the epidermal growth factor receptor through effects on Bcl-3 and STAT3. J. Virol. 82:5486-5493.
27. Huang YT, Liu MY, Tsai CH, Yeh TH. 2010. Upregulation of interleukin-1 by Epstein-Barr virus latent membrane protein 1 and its possible role in nasopharyngeal carcinoma cell growth. Head Neck 32:869-876.
28. Eliopoulos AG, Stack M, Dawson CW, Kaye KM, Hodgkin L, Sihota S, Rowe M, Young LS. 1997. Epstein-Barr virus-encoded LMP1 and CD40 mediate IL-6 production in epithelial cells via an NF-kappaB pathway involving TNF receptor-associated factors. Oncogene 14:2899-2916.
29. Lambert SL, Martinez OM. 2007. Latent membrane protein 1 of EBV activates phosphatidylinositol 3-kinase to induce production of IL-10. J. Immunol. 179:8225-8234.
30. Fries KL, Miller WE, Raab-Traub N. 1996. Epstein-Barr virus latent membrane protein 1 blocks p53-mediated apoptosis through the induction of the A20 gene. J. Virol. 70:8653-8659.
31. Rowe M, Peng-Pilon M, Huen DS, Hardy R, Croom-Carter D, Lundgren E, Rickinson AB. 1994. Upregulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers. J. Virol. 68:5602-5612.
32. 1/S cell cycle progression in nasopharyngeal carcinoma. Int. J. Mol. Med. 29:574-580.
33. Wu HC, Lu TY, Lee JJ, Hwang JK, Lin YJ, Wang CK, Lin CT. 2004. MDM2 expression in EBV-infected nasopharyngeal carcinoma cells. Lab. Invest. 84:1547-1556.
34. Li L, Guo L, Tao Y, Zhou S, Wang Z, Luo W, Hu D, Li Z, Xiao L, Tang M, Yi W, Tsao SW, Cao Y. 2007. Latent membrane protein 1 of EpsteinBarr virus regulates p53 phosphorylation through MAP kinases. Cancer Lett. 255:219-231.
35. Lu J, Chua HH, Chen SY, Chen JY, Tsai CH. 2003. Regulation of matrix metalloproteinase-1 by Epstein-Barr virus proteins. Cancer Res. 63:256- 262.
36. Yoshizaki T, Sato H, Furukawa M, Pagano JS. 1998. The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1. Proc. Natl. Acad. Sci. U. S. A. 95:3621-3626.
37. Tsai CN, Tsai CL, Tse KP, Chang HY, Chang YS. 2002. The Epstein-Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc. Natl. Acad. Sci. U. S. A. 99:10084-10089.
38. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I, Furukawa M, Pagano JS. 2007. Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res. 67:1970- 1978.
39. Fahraeus R, Chen W, Trivedi P, Klein G, Obrink B. 1992. Decreased expression of E-cadherin and increased invasive capacity in EBV-LMPtransfected human epithelial and murine adenocarcinoma cells. Int. J. Cancer 52:834-838.
40. Horikawa T, Yoshizaki T, Kondo S, Furukawa M, Kaizaki Y, Pagano JS. 2011. Epstein-Barr virus latent membrane protein 1 induces Snail and epithelial-mesenchymal transition in metastatic nasopharyngeal carcinoma. Br. J. Cancer 104:1160-1167.
41. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, Raab-Traub N. 1998. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 95:11963-11968.
42. Zhang B, Kracker S, Yasuda T, Casola S, Vanneman M, Hömig-Hölzel C, Wang Z, Derudder E, Li S, Chakraborty T, Cotter SE, Koyama S, Currie T, Freeman GJ, Kutok JL, Rodig SJ, Dranoff G, Rajewsky K. 2012. Immune surveillance and therapy of lymphomas driven by EpsteinBarr virus protein LMP1 in a mouse model. Cell 148:739-751.
43. Sodhi A, Montaner S, Gutkind JS. 2004. Viral hijacking of G-proteincoupled-receptor signalling networks. Nat. Rev. Mol. Cell Biol. 5:998- 1012.
44. Alcami A. 2003. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3:36-50.
45. Nicholas J. 2005. Human gammaherpesvirus cytokines and chemokine receptors. J. Interferon Cytokine Res. 25:373-383.
46. Nijmeijer S, Leurs R, Smit MJ, Vischer HF. 2010. The Epstein-Barr virus-encoded G protein-Coupled Receptor BILF1 hetero-oligomerizes with human CXCR4, scavenges G alpha i proteins, and constitutively impairs CXCR4 functioning. J. Biol. Chem. 285:29632-29641.
47. Zuo J, Currin A, Griffin BD, Shannon-Lowe C, Thomas WA, Ressing ME, Wiertz EJ, Rowe M. 2009. The Epstein-Barr virus G-proteincoupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog. 5:e1000255. doi:10.1371 /journal.ppat.1000255.