1,537
Views
26
CrossRef citations to date
0
Altmetric
Original Research

p38 MAPK differentially controls NK activating ligands at transcriptional and post-transcriptional level on multiple myeloma cells

, , , , , , , , , , , , , , , & show all
Article: e1264564 | Received 16 Aug 2016, Accepted 17 Nov 2016, Published online: 02 Dec 2016

References

  • Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013; 31:51-72; PMID:23157435; http://dx.doi.org/10.1146/annurev-immunol-032712-100008
  • Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 2013; 31:413-41; PMID:23298206; http://dx.doi.org/10.1146/annurev-immunol-032712-095951
  • Cerboni C, Fionda C, Soriani A, Zingoni A, Doria M, Cippitelli M, Santoni A. The DNA Damage Response: A Common Pathway in the Regulation of NKG2D and DNAM-1 Ligand Expression in Normal, Infected, and Cancer Cells. Front Immunol 2014; 4:508 ; PMID:24432022; http://dx.doi.org/10.3389/fimmu.2013.00508
  • Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003; 3:781-90; PMID:14523385; http://dx.doi.org/10.1038/nri1199
  • Coudert JD, Held W. The role of the NKG2D receptor for tumor immunity. Semin Cancer Biol 2006; 16:333-43; PMID:16914326; http://dx.doi.org/10.1016/j.semcancer.2006.07.008
  • Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, Kitamura T, Nicholl J, Sutherland GR, Lanier LL et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 1996; 4:573-81; PMID:8673704; http://dx.doi.org/10.1016/S1074-7613(00)70060-4
  • Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, Cantoni C, Grassi J, Marcenaro S, Reymond N et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med 2003; 198:557-67; PMID:12913096; http://dx.doi.org/10.1084/jem.20030788
  • Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 1996; 93:12445-50; PMID:8901601; http://dx.doi.org/10.1073/pnas.93.22.12445
  • Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005; 436:1186-90; PMID:15995699; http://dx.doi.org/10.1038/nature03884
  • Soriani A, Zingoni A, Cerboni C, Iannitto ML, Ricciardi MR, Di Gialleonardo V, Cippitelli M, Fionda C, Petrucci MT, Guarini A et al. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 2009; 113:3503-11; PMID:19098271; http://dx.doi.org/10.1182/blood-2008-08-173914
  • Fionda C, Soriani A, Malgarini G, Iannitto ML, Santoni A, Cippitelli M. Heat shock protein-90 inhibitors increase MHC class I-related chain A and B ligand expression on multiple myeloma cells and their ability to trigger NK cell degranulation. J Immunol 2009; 183:4385-94; PMID:19748980; http://dx.doi.org/10.4049/jimmunol.0901797
  • Raulet DH, Guerra N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009; 9:568-80; PMID:19629084; http://dx.doi.org/10.1038/nri2604
  • Zingoni A, Cecere F, Vulpis E, Fionda C, Molfetta R, Soriani A, Petrucci MT, Ricciardi MR, Fuerst D, Amendola MG et al. Genotoxic stress induces senescence-associated ADAM10-dependent release of NKG2D MIC ligands in multiple myeloma cells. J Immunol 2015; 195:736-48; PMID:26071561; http://dx.doi.org/10.4049/jimmunol.1402643
  • Soriani A, Iannitto ML, Ricci B, Fionda C, Malgarini G, Morrone S, Peruzzi G, Ricciardi MR, Petrucci MT, Cippitelli M, Santoni A. Reactive oxygen species- and DNA damage response-dependent NK cell activating ligand upregulation occurs at transcriptional levels and requires the transcriptional factor E2F1. J Immunol 2014; 193:950-60; PMID:24913980; http://dx.doi.org/10.4049/jimmunol.1400271
  • Venkataraman GM, Suciu D, Groh V, Boss JM, Spies T. Promoter region architecture and transcriptional regulation of the genes for the MHC class I-related chain A and B ligands of NKG2D. J Immunol 2007; 178:961-9; PMID:17202358; http://dx.doi.org/10.4049/jimmunol.178.2.961
  • Unni AM, Bondar T, Medzhitov R. Intrinsic sensor of oncogenic transformation induces a signal for innate immunosurveillance. Proc Natl Acad Sci U S A 2008; 105:1686-91; PMID:18223157; http://dx.doi.org/10.1073/pnas.0701675105
  • Liu XV, Ho SS, Tan JJ, Kamran N, Gasser S. Ras activation induces expression of Raet1 family NK receptor ligands. J Immunol 2012; 189:1826-34; PMID:22798674; http://dx.doi.org/10.4049/jimmunol.1200965
  • Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res 2011; 71:5998-6009; PMID:21764762; http://dx.doi.org/10.1158/0008-5472.CAN-10-3211
  • Li H, Lakshmikanth T, Garofalo C, Enge M, Spinnler C, Anichini A, Szekely L, Karre K, Carbone E, Selivanova G. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle 2011; 10:3346-58; PMID:21941086; http://dx.doi.org/10.4161/cc.10.19.17630
  • Zitvogel L, Apetoh L, Ghiringhelli F, André F, Tesniere A, Kroemer G. The anticancer immune response: indispensable for therapeutic success? J Clin Invest 2008; 118:1991-2001; PMID:18523649; http://dx.doi.org/10.1172/JCI35180
  • Spear P, Wu MR, Sentman ML, Sentman CL. NKG2D ligands as therapeutic targets. Cancer Immun 2013; 13:8; PMID:23833565
  • Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene 2008; 27:5944-58; PMID:18836475; http://dx.doi.org/10.1038/onc.2008.272
  • Fionda C, Soriani A, Zingoni A, Santoni A, Cippitelli M. NKG2D and DNAM-1 ligands: molecular targets for NK cell-mediated immunotherapeutic intervention in Multiple Myeloma. Biomed Res Int 2015; 2015:1786982015; PMID:26161387; http://dx.doi.org/10.1155/2015/178698
  • Fionda C, Abruzzese MP, Zingoni A, Cecere F, Vulpis E, Peruzzi G, Soriani A, Molfetta R, Paolini R, Ricciardi MR et al. The IMiDs targets IKZF-1/3 and IRF4 as novel negative regulators of NK cell-activating ligands expression in multiple myeloma. Oncotarget 2015; 6:23609-30; PMID:26269456; http://dx.doi.org/10.18632/oncotarget.4603
  • Parker AL, Kavallaris M, McCarroll JA. Microtubules and Their Role in Cellular Stress in Cancer. Front Oncol 2014; 4:153; PMID:24995158; http://dx.doi.org/10.3389/fonc.2014.00153
  • Chun-Te H, Yu-Jia C, Li-Xi Y, Po-Li W, Tsan-Zon L, Jun-Jen L. A Novel Microtubule-Disrupting Agent Induces Endoplasmic Reticular Stress-Mediated Cell Death in Human Hepatocellular Carcinoma Cells. PLoS One 2015; 10:e0136340; PMID:26355599; http://dx.doi.org/10.1371/journal.pone.0136340
  • Yi JM, Zhang XF, Huan XJ, Song SS, Wang W, Tian QT, Sun YM, Chen Y, Ding J, Wang YQ, Yang CH, Miao ZH. Dual targeting of microtubule and topoisomerase II by α-carboline derivative YCH337 for tumor proliferation and growth inhibition. Oncotarget 2015; 6:8960-73; PMID:25840421; http://dx.doi.org/10.18632/oncotarget.3264
  • Colin DJ, Hain KO, Allan LA, Clarke PR. Cellular responses to a prolonged delay in mitosis are determined by a DNA damage response controlled by Bcl-2 family proteins. Open Biol 2015; 5:140156; PMID:25761368; http://dx.doi.org/10.1098/rsob.140156
  • Osterborg A, Nilsson B, Bjorkholm M, Holm G, Mellstedt H. Natural killer cell activity in monoclonal gammopathies: relation to disease activity. Eur J Haematol 1990; 45:153-7; PMID:1699786; http://dx.doi.org/10.1111/j.1600-0609.1990.tb00443.x
  • Jinushi M, Vanneman M, Munshi NC, Tai YT, Prabhala RH, Ritz J, Neuberg D, Anderson KC, Carrasco DR, Dranoff G. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc Natl Acad Sci U S A 2008; 105:1285-90; PMID:18202175; http://dx.doi.org/10.1073/pnas.0711293105
  • Moudi MI, Go R, Yien CY, Nazre M. Vinca alkaloids. Int J Prev Med 2013; 4:231-5
  • Lazaryan A, Hussein MA, Reu FJ, Faiman B, Habecker B, Ann Karam M, Reed J, Hamilton K, Waksman J, Bruening K et al. Mature results of MM-011: a phase I/II trial of liposomal doxorubicin, vincristine, dexamethasone, and lenalidomide combination therapy followed by lenalidomide maintenance for relapsed/refractory multiple myeloma. Am J Hematol 2014; 89:349-54; PMID:24404355; PMID:24273135; http://dx.doi.org/10.1002/ajh.23639
  • Kyriakis JM, Avruch J. Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 1996; 18:567-77; PMID:8757935; http://dx.doi.org/10.1002/bies.950180708
  • Quan H, Xu Y, Lou L. p38 MAPK, but not ERK1/2, is critically involved in the cytotoxicity of the novel vascular disrupting agent combretastatin A4. Int J Cancer 2008; 122:1730-7; PMID:18074350; http://dx.doi.org/10.1002/ijc.23262
  • Deacon K, Mistry P, Chernoff J, Blank JL, Patel R. p38 Mitogen-activated protein kinase mediates cell death and p21-activated kinase mediates cell survival during chemo-therapeutic drug-induced mitotic arrest. Mol Biol Cell 2003; 14:2071-87; PMID:12802076; http://dx.doi.org/10.1091/mbc.E02-10-0653
  • Jung H, Hsiung B, Pestal K, Procyk E, Raulet DH. RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry. J Exp Med 2012; 209:2409-22; PMID:23166357; http://dx.doi.org/10.1084/jem.20120565
  • de Olano N, Koo CY, Monteiro LJ, Pinto PH, Gomes AR, Aligue R, Lam EW. The p38 MAPK-MK2 axis regulates E2F1 and FOXM1 expression after epirubicin treatment. Mol Cancer Res 2012; 10:1189-202; PMID:22802261; http://dx.doi.org/10.1158/1541-7786.MCR-11-0559
  • Stevens C, Smith L, La Thangue NB. Chk2 activates E2F-1 in response to DNA damage. Nat Cell Biol 2003; 5:401-9; PMID:12717439; http://dx.doi.org/10.1038/ncb974
  • Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med 2005; 202:1001-1012; PMID:16203869; http://dx.doi.org/10.1084/jem.20051143
  • Molinero LL, Fuertes MB, Fainboim L, Rabinovich GA, Zwirner NW. Up-regulated expression of MICA on activated T lymphocytes involves Lck and Fyn kinases and signaling through MEK1/ERK, p38 MAP kinase, and calcineurin. J Leukoc Biol 2003; 73(6):815-22; PMID:12773514
  • Liu XV, Ho SS, Tan JJ, Kamran N, Gasser S. Ras activation induces expression of Raet1 family NK receptor ligands. J Immunol 2012; 189:1826-34; PMID:22798674; http://dx.doi.org/10.4049/jimmunol.1200965
  • Chauveau A, Tonnerre P, Pabois A, Gavlovsky PJ, Chatelais M, Coupel S, Charreau B. Endothelial cell activation and proliferation modulate NKG2D activity by regulating MICA expression and shedding. J Innate Immun 2014; 6:89-104; PMID:23860405; http://dx.doi.org/10.1159/000351605
  • Vantourout P, Willcox C, Turner A, Swanson CM, Haque Y, Sobolev O, Grigoriadis A, Tutt A, Hayday A. Immunological visibility: posttranscriptional regulation of human NKG2D ligands by the EGF receptor pathway. Sci Transl Med 2014; 6:231ra49; PMID:24718859; http://dx.doi.org/10.1126/scitranslmed.3007579
  • Jung H, Hsiung B, Pestal K, Procyk E. D.H. RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry. J Exp Med 2012; 209:2409-22; PMID:23166357; http://dx.doi.org/10.1084/jem.20120565
  • Solecki D, Schwarz S, Wimmer E, Lipp M, Bernhardt G. The promoters for human and monkey poliovirus receptors. Requirements for basic and cell type-specific activity. J Biol Chem 1997; 272:5579-86; PMID:9038165; http://dx.doi.org/10.1074/jbc.272.9.5579
  • Hirota T, Irie K, Okamoto R, Ikeda W, Takai Y. Transcriptional activation of the mouse Necl-5/Tage4/PVR/CD155 gene by fibroblast growth factor or oncogenic Ras through the Raf-MEK-ERK-AP-1 pathway. Oncogene 2005; 24:2229-35; PMID:15688018; http://dx.doi.org/10.1038/sj.onc.1208409
  • Himmelreich H, Mathys A, Wodnar-Filipowicz A, Kalberer CP. Post-transcriptional regulation of ULBP1 ligand for the activating immunoreceptor NKG2D involves 3′ untranslated region. Hum Immunol 2011; 72:470-8; PMID:21406206; http://dx.doi.org/10.1016/j.humimm.2011.03.005
  • Antic D, Keene JD. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J Cell Sci 1998; 111:183-97; PMID:9405302
  • Fionda C, Malgarini G, Soriani A, Zingoni A, Cecere F, Iannitto ML, Ricciardi MR, Federico V, Petrucci MT, Santoni A, Cippitelli M. Inhibition of glycogen synthase kinase-3 increases NKG2D ligand MICA expression and sensitivity to NK cell-mediated cytotoxicity in multiple myeloma cells: role of STAT3. J Immunol 2013; 190:6662-72; PMID:23686482; http://dx.doi.org/10.4049/jimmunol.1201426
  • Quatrini L, Molfetta R, Zitti B, Peruzzi G, Fionda C, Capuano C, Galandrini R, Cippitelli M, Santoni A, Paolini R. Ubiquitin-dependent endocytosis of NKG2D-DAP10 receptor complexes activates signaling and functions in human NK cells. Sci Signal 2015; 8(400):ra108; PMID:26508790; http://dx.doi.org/10.1126/scisignal.aab2724

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.