The Roles of Alternative Splicing in Tumor-immune Cell Interactions

Author(s): Yue Wang, Honglei Zhang*, Baowei Jiao*, Jianyun Nie*, Xiyin Li, Wenhuan Wang, Hairui Wang

Journal Name: Current Cancer Drug Targets

Volume 20 , Issue 10 , 2020


DOI : 10.2174/1568009620666200619123725

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Alternative splicing (AS) plays a significant role in the hallmarks of cancer and can provide neoantigens for immunotherapy. Here, we summarize recent advances in immune system associated tumor specific-antigens (TSAs) produced by AS. We further discuss the regulating mechanisms involved in AS-mediated innate and adaptive immune responses and the anti-tumoral and protumoral roles in different types of cancer. For example, ULBP1_RI, MLL5Δ21spe, NKp44-1Δ5, MHC-IΔ7, CD200SΔ1, 2, PVR α/β/γ/δ and IL-33 variants 1/2/3 act as regulators in solid tumors and IPAK4-L and, FOXP1ΔN100 exhibit functions in hematological cancers.

Keywords: Alternative splicing, tumor cells, immune system, immunotherapy, neoantigens, Tumor specific-antigens (TSAs).

[1]
Tran, E.; Robbins, P.F.; Rosenberg, S.A. Final common pathway’ of human cancer immunotherapy: Targeting random somatic mutations. Nat. Immunol., 2017, 18(3), 255-262.
[http://dx.doi.org/10.1038/ni.3682 ] [PMID: 28198830]
[2]
Paucek, R.D.; Baltimore, D.; Li, G. The cellular immunotherapy revolution: arming the immune system for precision therapy. Trends Immunol., 2019, 40(4), 292-309.
[http://dx.doi.org/10.1016/j.it.2019.02.002 ] [PMID: 30871979]
[3]
Rapoport, A.P.; Stadtmauer, E.A.; Binder-Scholl, G.K.; Goloubeva, O.; Vogl, D.T.; Lacey, S.F.; Badros, A.Z.; Garfall, A.; Weiss, B.; Finklestein, J.; Kulikovskaya, I.; Sinha, S.K.; Kronsberg, S.; Gupta, M.; Bond, S.; Melchiori, L.; Brewer, J.E.; Bennett, A.D.; Gerry, A.B.; Pumphrey, N.J.; Williams, D.; Tayton-Martin, H.K.; Ribeiro, L.; Holdich, T.; Yanovich, S.; Hardy, N.; Yared, J.; Kerr, N.; Philip, S.; Westphal, S.; Siegel, D.L.; Levine, B.L.; Jakobsen, B.K.; Kalos, M.; June, C.H. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat. Med., 2015, 21(8), 914-921.
[http://dx.doi.org/10.1038/nm.3910 ] [PMID: 26193344]
[4]
Robbins, P.F.; Morgan, R.A.; Feldman, S.A.; Yang, J.C.; Sherry, R.M.; Dudley, M.E.; Wunderlich, J.R.; Nahvi, A.V.; Helman, L.J.; Mackall, C.L.; Kammula, U.S.; Hughes, M.S.; Restifo, N.P.; Raffeld, M.; Lee, C.C.; Levy, C.L.; Li, Y.F.; El-Gamil, M.; Schwarz, S.L.; Laurencot, C.; Rosenberg, S.A. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol., 2011, 29(7), 917-924.
[http://dx.doi.org/10.1200/JCO.2010.32.2537 ] [PMID: 21282551]
[5]
Ott, P.A.; Hu, Z.; Keskin, D.B.; Shukla, S.A.; Sun, J.; Bozym, D.J.; Zhang, W.; Luoma, A.; Giobbie-Hurder, A.; Peter, L.; Chen, C.; Olive, O.; Carter, T.A.; Li, S.; Lieb, D.J.; Eisenhaure, T.; Gjini, E.; Stevens, J.; Lane, W.J.; Javeri, I.; Nellaiappan, K.; Salazar, A.M.; Daley, H.; Seaman, M.; Buchbinder, E.I.; Yoon, C.H.; Harden, M.; Lennon, N.; Gabriel, S.; Rodig, S.J.; Barouch, D.H.; Aster, J.C.; Getz, G.; Wucherpfennig, K.; Neuberg, D.; Ritz, J.; Lander, E.S.; Fritsch, E.F.; Hacohen, N.; Wu, C.J. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature, 2017, 547(7662), 217-221.
[http://dx.doi.org/10.1038/nature22991 ] [PMID: 28678778]
[6]
Carreno, B.M.; Magrini, V.; Becker-Hapak, M.; Kaabinejadian, S.; Hundal, J.; Petti, A.A.; Ly, A.; Lie, W.R.; Hildebrand, W.H.; Mardis, E.R.; Linette, G.P. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science, 2015, 348(6236), 803-808.
[http://dx.doi.org/10.1126/science.aaa3828 ] [PMID: 25837513]
[7]
Sahin, U.; Derhovanessian, E.; Miller, M.; Kloke, B.P.; Simon, P.; Löwer, M.; Bukur, V.; Tadmor, A.D.; Luxemburger, U.; Schrörs, B.; Omokoko, T.; Vormehr, M.; Albrecht, C.; Paruzynski, A.; Kuhn, A.N.; Buck, J.; Heesch, S.; Schreeb, K.H.; Müller, F.; Ortseifer, I.; Vogler, I.; Godehardt, E.; Attig, S.; Rae, R.; Breitkreuz, A.; Tolliver, C.; Suchan, M.; Martic, G.; Hohberger, A.; Sorn, P.; Diekmann, J.; Ciesla, J.; Waksmann, O.; Brück, A.K.; Witt, M.; Zillgen, M.; Rothermel, A.; Kasemann, B.; Langer, D.; Bolte, S.; Diken, M.; Kreiter, S.; Nemecek, R.; Gebhardt, C.; Grabbe, S.; Höller, C.; Utikal, J.; Huber, C.; Loquai, C.; Türeci, Ö. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature, 2017, 547(7662), 222-226.
[http://dx.doi.org/10.1038/nature23003 ] [PMID: 28678784]
[8]
Schumacher, T.N.; Schreiber, R.D. Neoantigens in cancer immunotherapy. Science, 2015, 348(6230), 69-74.
[http://dx.doi.org/10.1126/science.aaa4971 ] [PMID: 25838375]
[9]
Marcelino Meliso, F.; Hubert, C.G.; Favoretto Galante, P.A.; Penalva, L.O. RNA processing as an alternative route to attack glioblastoma. Hum. Genet., 2017, 136(9), 1129-1141.
[http://dx.doi.org/10.1007/s00439-017-1819-2 ] [PMID: 28608251]
[10]
Salton, M.; Misteli, T. Small molecule modulators of Pre-mRNA splicing in cancer therapy. Trends Mol. Med., 2016, 22(1), 28-37.
[http://dx.doi.org/10.1016/j.molmed.2015.11.005 ] [PMID: 26700537]
[11]
Lee, Y.; Rio, D.C. Mechanisms and regulation of alternative pre-mRNA splicing. Annu. Rev. Biochem., 2015, 84, 291-323.
[http://dx.doi.org/10.1146/annurev-biochem-060614-034316 ] [PMID: 25784052]
[12]
Nilsen, T.W.; Graveley, B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature, 2010, 463(7280), 457-463.
[http://dx.doi.org/10.1038/nature08909 ] [PMID: 20110989]
[13]
Oltean, S.; Bates, D.O. Hallmarks of alternative splicing in cancer. Oncogene, 2014, 33(46), 5311-5318.
[http://dx.doi.org/10.1038/onc.2013.533 ] [PMID: 24336324]
[14]
Todaro, M.; Gaggianesi, M.; Catalano, V.; Benfante, A.; Iovino, F.; Biffoni, M.; Apuzzo, T.; Sperduti, I.; Volpe, S.; Cocorullo, G.; Gulotta, G.; Dieli, F.; De Maria, R.; Stassi, G. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell, 2014, 14(3), 342-356.
[http://dx.doi.org/10.1016/j.stem.2014.01.009 ] [PMID: 24607406]
[15]
David, C.J.; Manley, J.L. Alternative pre-mRNA splicing regulation in cancer: Pathways and programs unhinged. Genes Dev., 2010, 24(21), 2343-2364.
[http://dx.doi.org/10.1101/gad.1973010 ] [PMID: 21041405]
[16]
Jayasinghe, R.G.; Cao, S.; Gao, Q.; Wendl, M.C.; Vo, N.S.; Reynolds, S.M.; Zhao, Y.; Climente-Gonzalez, H.; Chai, S.; Wang, F.; Varghese, R.; Huang, M.; Liang, W.W.; Wyczalkowski, M.A.; Sengupta, S.; Li, Z.; Payne, S.H.; Fenyo, D.; Miner, J.H.; Walter, M.J. Cancer Genome Atlas Research Network. Vincent B.; Eyras E.; Chen K.; Shmulevich I.; Chen F.; Ding L. Systematic analysis of splice-site-creating mutations in cancer. Cell Rep., 2018, 23(1), 270-281.
[17]
Hoyos, L.E.; Abdel-Wahab, O. Cancer-specific splicing changes and the potential for splicing-derived neoantigens. Cancer Cell, 2018, 34(2), 181-183.
[http://dx.doi.org/10.1016/j.ccell.2018.07.008 ] [PMID: 30107172]
[18]
Black, K.L.; Naqvi, A.S.; Asnani, M.; Hayer, K.E.; Yang, S.Y.; Gillespie, E.; Bagashev, A.; Pillai, V.; Tasian, S.K.; Gazzara, M.R.; Carroll, M.; Taylor, D.; Lynch, K.W.; Barash, Y.; Thomas-Tikhonenko, A. Aberrant splicing in B-cell acute lymphoblastic leukemia. Nucleic Acids Res., 2019, 47(2), 1043.
[http://dx.doi.org/10.1093/nar/gky1231 ] [PMID: 30517739]
[19]
Iwasaki, A.; Medzhitov, R. Control of adaptive immunity by the innate immune system. Nat. Immunol., 2015, 16(4), 343-353.
[http://dx.doi.org/10.1038/ni.3123 ] [PMID: 25789684]
[20]
Zhang, Y.; Lin, Z.; Wan, Y.; Cai, H.; Deng, L.; Li, R. the immunogenicity and anti-tumor efficacy of a rationally designed neoantigen vaccine for B16F10 mouse melanoma. Front. Immunol., 2019, 10, 2472.
[http://dx.doi.org/10.3389/fimmu.2019.02472 ] [PMID: 31749795]
[21]
Woo, S.R.; Corrales, L.; Gajewski, T.F. Innate immune recognition of cancer. Ann. Rev. Immunol., 2015, 33(undefined), 445-474.
[http://dx.doi.org/10.1146/annurev-immunol-032414-112043]
[22]
Moretta, A. Natural killer cells and dendritic cells: Rendezvous in abused tissues. Nat. Rev. Immunol., 2002, 2(12), 957-964.
[http://dx.doi.org/10.1038/nri956 ] [PMID: 12461568]
[23]
Grossenbacher, S.K.; Canter, R.J.; Murphy, W.J. Natural killer cell immunotherapy to target stem-like tumor cells. J. Immunother. Cancer, 2016, 4(undefined), 19.
[http://dx.doi.org/10.1186/s40425-016-0124-2]
[24]
Delgado, D.C.; Hank, J.A.; Kolesar, J.; Lorentzen, D.; Gan, J.; Seo, S.; Kim, K.; Shusterman, S.; Gillies, S.D.; Reisfeld, R.A.; Yang, R.; Gadbaw, B.; DeSantes, K.B.; London, W.B.; Seeger, R.C.; Maris, J.M.; Sondel, P.M. Genotypes of NK cell KIR receptors, their ligands, and Fcγ receptors in the response of neuroblastoma patients to Hu14.18-IL2 immunotherapy. Cancer Res., 2010, 70(23), 9554-9561.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2211 ] [PMID: 20935224]
[25]
Yang, R.K.; Kalogriopoulos, N.A.; Rakhmilevich, A.L.; Ranheim, E.A.; Seo, S.; Kim, K.; Alderson, K.L.; Gan, J.; Reisfeld, R.A.; Gillies, S.D.; Hank, J.A.; Sondel, P.M. Intratumoral treatment of smaller mouse neuroblastoma tumors with a recombinant protein consisting of IL-2 linked to the hu14.18 antibody increases intratumoral CD8+ T and NK cells and improves survival. Cancer Immunol. Immunother., 2013, 62(8), 1303-1313.
[http://dx.doi.org/10.1007/s00262-013-1430-x ] [PMID: 23661160]
[26]
Han, J.; Chu, J.; Keung Chan, W.; Zhang, J.; Wang, Y.; Cohen, J.B.; Victor, A.; Meisen, W.H.; Kim, S.H.; Grandi, P.; Wang, Q.E.; He, X.; Nakano, I.; Chiocca, E.A.; Glorioso Iii, J.C.; Kaur, B.; Caligiuri, M.A.; Yu, J. CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patientderived glioblastoma stem cells. Scientific Rep., 2015, 5(undefined), 11483.
[27]
Genßler, S.; Burger, M.C.; Zhang, C.; Oelsner, S.; Mildenberger, I.; Wagner, M.; Steinbach, J.P.; Wels, W.S. Dual targeting of glioblastoma with chimeric antigen receptor-engineered natural killer cells overcomes heterogeneity of target antigen expression and enhances antitumor activity and survival. OncoImmunology, 2015, 5(4), e1119354.
[http://dx.doi.org/10.1080/2162402X.2015.1119354 ] [PMID: 27141401]
[28]
Lee, Y.S.; Yeo, I.J.; Kim, K.C.; Han, S.B.; Hong, J.T. Inhibition of lung tumor development in ApoE knockout mice via enhancement of TREM-1 dependent NK cell cytotoxicity. Front. Immunol., 2019, 10, 1379.
[29]
Long, E.O.; Kim, H.S.; Liu, D.; Peterson, M.E.; Rajagopalan, S. Controlling natural killer cell responses: Integration of signals for activation and inhibition. Ann. Rev. Immunol., 2013, 31(undefined), 227-258.
[http://dx.doi.org/10.1146/annurev-immunol-020711-075005]
[30]
Vivier, E.; Raulet, D.H.; Moretta, A.; Caligiuri, M.A.; Zitvogel, L.; Lanier, L.L.; Yokoyama, W.M.; Ugolini, S. Innate or adaptive immunity? The example of natural killer cells. Science, 2011, 331(6013), 44-49.
[http://dx.doi.org/10.1126/science.1198687 ] [PMID: 21212348]
[31]
Shifrin, N.; Raulet, D.H.; Ardolino, M. NK cell self tolerance, responsiveness and missing self recognition. Semin. Immunol., 2014, 26(2), 138-144.
[http://dx.doi.org/10.1016/j.smim.2014.02.007 ] [PMID: 24629893]
[32]
Raulet, D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol., 2003, 3(10), 781-790.
[http://dx.doi.org/10.1038/nri1199 ] [PMID: 14523385]
[33]
Pende, D.; Cantoni, C.; Rivera, P.; Vitale, M.; Castriconi, R.; Marcenaro, S.; Nanni, M.; Biassoni, R.; Bottino, C.; Moretta, A.; Moretta, L. Role of NKG2D in tumor cell lysis mediated by human NK cells: Cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur. J. Immunol., 2001, 31(4), 1076-1086.
[http://dx.doi.org/10.1002/1521-4141(200104)31:4<1076:AID-IMMU1076>3.0.CO;2-Y ] [PMID: 11298332]
[34]
Raulet, D.H.; Gasser, S.; Gowen, B.G.; Deng, W.; Jung, H. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol., 2013, 31, 413-441.
[http://dx.doi.org/10.1146/annurev-immunol-032712-095951 ] [PMID: 23298206]
[35]
Gowen, B.G.; Chim, B.; Marceau, C.D.; Greene, T.T.; Burr, P.; Gonzalez, J.R.; Hesser, C.R.; Dietzen, P.A.; Russell, T.; Iannello, A.; Coscoy, L.; Sentman, C.L.; Carette, J.E.; Muljo, S.A.; Raulet, D.H. A forward genetic screen reveals novel independent regulators of ULBP1, an activating ligand for natural killer cells. eLife, 2015, 4, 4.
[http://dx.doi.org/10.7554/eLife.08474 ] [PMID: 26565589]
[36]
Wang, Y.; Chen, D.; Qian, H.; Tsai, Y.S.; Shao, S.; Liu, Q.; Dominguez, D.; Wang, Z. The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression. Cancer Cell, 2014, 26(3), 374-389.
[http://dx.doi.org/10.1016/j.ccr.2014.07.010 ] [PMID: 25203323]
[37]
Yong, H.; Zhu, H.; Zhang, S.; Zhao, W.; Wang, W.; Chen, C.; Ding, G.; Zhu, L.; Zhu, Z.; Liu, H.; Zhang, Y.; Wen, J.; Kang, X.; Zhu, J.; Feng, Z.; Liu, B. Prognostic value of decreased expression of RBM4 in human gastric cancer. Scientific reports, 2016, 6, 28222.
[http://dx.doi.org/10.1038/srep28222]
[38]
Cao, W.; Xi, X.; Hao, Z.; Li, W.; Kong, Y.; Cui, L.; Ma, C.; Ba, D.; He, W. RAET1E2, a soluble isoform of the UL16-binding protein RAET1E produced by tumor cells, inhibits NKG2D-mediated NK cytotoxicity. J. Biol. Chem., 2007, 282(26), 18922-18928.
[http://dx.doi.org/10.1074/jbc.M702504200 ] [PMID: 17470428]
[39]
Kruse, P.H.; Matta, J.; Ugolini, S.; Vivier, E. Natural cytotoxicity receptors and their ligands. Immunol. Cell Biol., 2014, 92(3), 221-229.
[http://dx.doi.org/10.1038/icb.2013.98 ] [PMID: 24366519]
[40]
Biassoni, R.; Cantoni, C.; Pende, D.; Sivori, S.; Parolini, S.; Vitale, M.; Bottino, C.; Moretta, A. Human natural killer cell receptors and co-receptors. Immunol. Rev., 2001, 181, 203-214.
[http://dx.doi.org/10.1034/j.1600-065X.2001.1810117.x]
[41]
Mathew, P.A. NKp44 and natural cytotoxicity receptors as damage- associated molecular pattern recognition receptors %. A Horton NC. Front. Immunol., 2015, 6(undefined), 31.
[42]
Vitale, M.; Bottino, C.; Sivori, S.; Sanseverino, L.; Castriconi, R.; Marcenaro, E.; Augugliaro, R.; Moretta, L.; Moretta, A. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J. Exp. Med., 1998, 187(12), 2065-2072.
[http://dx.doi.org/10.1084/jem.187.12.2065 ] [PMID: 9625766]
[43]
Cantoni, C.; Bottino, C.; Vitale, M.; Pessino, A.; Augugliaro, R.; Malaspina, A.; Parolini, S.; Moretta, L.; Moretta, A.; Biassoni, R. NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J. Exp. Med., 1999, 189(5), 787-796.
[http://dx.doi.org/10.1084/jem.189.5.787 ] [PMID: 10049942]
[44]
de Rham, C.; Ferrari-Lacraz, S.; Jendly, S.; Schneiter, G.; Dayer, J.M.; Villard, J. The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res. Ther., 2007, 9(6), R125.
[http://dx.doi.org/10.1186/ar2336 ] [PMID: 18053164]
[45]
Shemesh, A.; Kugel, A.; Steiner, N.; Yezersky, M.; Tirosh, D.; Edri, A.; Teltsh, O.; Rosental, B.; Sheiner, E.; Rubin, E.; Campbell, K.S.; Porgador, A. NKp44 and NKp30 splice variant profiles in decidua and tumor tissues: A comparative viewpoint. Oncotarget, 2016, 7(43), 70912-70923.
[http://dx.doi.org/10.18632/oncotarget.12292 ] [PMID: 27765926]
[46]
Shemesh, A.; Brusilovsky, M.; Kundu, K.; Ottolenghi, A.; Campbell, K.S.; Porgador, A. Splice variants of human natural cytotoxicity receptors: Novel innate immune checkpoints. Cancer Immunol. Immunother., 2018, 67(12), 1871-1883.
[http://dx.doi.org/10.1007/s00262-017-2104-x ] [PMID: 29264698]
[47]
Rosental, B.; Brusilovsky, M.; Hadad, U.; Oz, D.; Appel, M.Y.; Afergan, F.; Yossef, R.; Rosenberg, L.A.; Aharoni, A.; Cerwenka, A.; Campbell, K.S.; Braiman, A.; Porgador, A. Proliferating cell nuclear antigen is a novel inhibitory ligand for the natural cytotoxicity receptor NKp44. J. Immunol. (Baltimore, Md: 1950), 2011, 187(11), 5693-5702.
[http://dx.doi.org/10.4049/jimmunol.1102267]
[48]
Siewiera, J.; Gouilly, J.; Hocine, H.R.; Cartron, G.; Levy, C.; Al-Daccak, R.; Jabrane-Ferrat, N. Natural cytotoxicity receptor splice variants orchestrate the distinct functions of human natural killer cell subtypes. Nat. Commun., 2015, 6, 10183.
[http://dx.doi.org/10.1038/ncomms10183 ] [PMID: 26666685]
[49]
Shemesh, A.; Brusilovsky, M.; Hadad, U.; Teltsh, O.; Edri, A.; Rubin, E.; Campbell, K.S.; Rosental, B.; Porgador, A. Survival in acute myeloid leukemia is associated with NKp44 splice variants. Oncotarget, 2016, 7(22), 32933-32945.
[http://dx.doi.org/10.18632/oncotarget.8782 ] [PMID: 27102296]
[50]
Baychelier, F.; Sennepin, A.; Ermonval, M.; Dorgham, K.; Debré, P.; Vieillard, V. Identification of a cellular ligand for the natural cytotoxicity receptor NKp44. Blood, 2013, 122(17), 2935-2942.
[http://dx.doi.org/10.1182/blood-2013-03-489054 ] [PMID: 23958951]
[51]
Deng, L.W.; Chiu, I.; Strominger, J.L. MLL 5 protein forms intranuclear foci, and overexpression inhibits cell cycle progression. Proc. Natl. Acad. Sci. USA, 2004, 101(3), 757-762.
[http://dx.doi.org/10.1073/pnas.2036345100 ] [PMID: 14718661]
[52]
Yew, C.W.; Lee, P.; Chan, W.K.; Lim, V.K.; Tay, S.K.; Tan, T.M.; Deng, L.W. A novel MLL5 isoform that is essential to activate E6 and E7 transcription in HPV16/18-associated cervical cancers. Cancer Res., 2011, 71(21), 6696-6707.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-1271 ] [PMID: 21908553]
[53]
Smith, M.A.; Choudhary, G.S.; Pellagatti, A.; Choi, K.; Bolanos, L.C.; Bhagat, T.D.; Gordon-Mitchell, S.; Von Ahrens, D.; Pradhan, K.; Steeples, V.; Kim, S.; Steidl, U.; Walter, M.; Fraser, I.D.C.; Kulkarni, A.; Salomonis, N.; Komurov, K.; Boultwood, J.; Verma, A.; Starczynowski, D.T. U2AF1 mutations induce oncogenic IRAK4 isoforms and activate innate immune pathways in myeloid malignancies. Nat. Cell Biol., 2019, 21(5), 640-650.
[http://dx.doi.org/10.1038/s41556-019-0314-5 ] [PMID: 31011167]
[54]
Patra, M.C.; Choi, S. Recent progress in the molecular recognition and therapeutic importance of interleukin-1 receptor-associated Kinase 4. Molecules, 2016, 21(11), E1529.
[http://dx.doi.org/10.3390/molecules21111529 ] [PMID: 27845762]
[55]
Guillamot, M.; Aifantis, I. Splicing the innate immune signalling in leukaemia. Nat. Cell Biol., 2019, 21(5), 536-537.
[http://dx.doi.org/10.1038/s41556-019-0323-4 ] [PMID: 31011166]
[56]
De Obaldia, M.E.; Bhandoola, A. Transcriptional regulation of innate and adaptive lymphocyte lineages. Ann. Rev. Immunol., 2015, 33(undefined), 607-642.
[http://dx.doi.org/10.1146/annurev-immunol-032414-112032]
[57]
La Gruta, N.L.; Gras, S.; Daley, S.R.; Thomas, P.G.; Rossjohn, J. Understanding the drivers of MHC restriction of T cell receptors. Nat. Rev. Immunol., 2018, 18(7), 467-478.
[http://dx.doi.org/10.1038/s41577-018-0007-5 ] [PMID: 29636542]
[58]
Cyster, J.G.; Allen, C.D.C. B cell responses: cell interaction dynamics and decisions. Cell, 2019, 177(3), 524-540.
[http://dx.doi.org/10.1016/j.cell.2019.03.016 ] [PMID: 31002794]
[59]
Nutt, S.L.; Hodgkin, P.D.; Tarlinton, D.M.; Corcoran, L.M. The generation of antibody-secreting plasma cells. Nat. Rev. Immunol., 2015, 15(3), 160-171.
[http://dx.doi.org/10.1038/nri3795 ] [PMID: 25698678]
[60]
Gerner, M.Y.; Casey, K.A.; Kastenmuller, W.; Germain, R.N. Dendritic cell and antigen dispersal landscapes regulate T cell immunity. J. Exp. Med., 2017, 214(10), 3105-3122.
[http://dx.doi.org/10.1084/jem.20170335 ] [PMID: 28847868]
[61]
Lizée, G.; Basha, G.; Tiong, J.; Julien, J.P.; Tian, M.; Biron, K.E.; Jefferies, W.A. Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat. Immunol., 2003, 4(11), 1065-1073.
[http://dx.doi.org/10.1038/ni989 ] [PMID: 14566337]
[62]
Basha, G.; Lizée, G.; Reinicke, A.T.; Seipp, R.P.; Omilusik, K.D.; Jefferies, W.A. MHC class I endosomal and lysosomal trafficking coincides with exogenous antigen loading in dendritic cells. PLoS One, 2008, 3(9), e3247.
[http://dx.doi.org/10.1371/journal.pone.0003247 ] [PMID: 18802471]
[63]
Rodríguez-Cruz, T.G.; Liu, S.; Khalili, J.S.; Whittington, M.; Zhang, M.; Overwijk, W.; Lizée, G. Natural splice variant of MHC class I cytoplasmic tail enhances dendritic cell-induced CD8+ T-cell responses and boosts anti-tumor immunity. PLoS One, 2011, 6(8), e22939.
[http://dx.doi.org/10.1371/journal.pone.0022939 ] [PMID: 21860662]
[64]
Overwijk, W.W.; Theoret, M.R.; Finkelstein, S.E.; Surman, D.R.; de Jong, L.A.; Vyth-Dreese, F.A.; Dellemijn, T.A.; Antony, P.A.; Spiess, P.J.; Palmer, D.C.; Heimann, D.M.; Klebanoff, C.A.; Yu, Z.; Hwang, L.N.; Feigenbaum, L.; Kruisbeek, A.M.; Rosenberg, S.A.; Restifo, N.P. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med., 2003, 198(4), 569-580.
[http://dx.doi.org/10.1084/jem.20030590 ] [PMID: 12925674]
[65]
Lou, Y.; Wang, G.; Lizée, G.; Kim, G.J.; Finkelstein, S.E.; Feng, C.; Restifo, N.P.; Hwu, P. Dendritic cells strongly boost the antitumor activity of adoptively transferred T cells in vivo. Cancer Res., 2004, 64(18), 6783-6790.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-1621 ] [PMID: 15374997]
[66]
Cannon, M.J.; Block, M.S.; Morehead, L.C.; Knutson, K.L. The evolving clinical landscape for dendritic cell vaccines and cancer immunotherapy. Immunotherapy, 2019, 11(2), 75-79.
[http://dx.doi.org/10.2217/imt-2018-0129 ] [PMID: 30730268]
[67]
Rouas-Freiss, N.; Bruel, S.; Menier, C.; Marcou, C.; Moreau, P.; Carosella, E.D. Switch of HLA-G alternative splicing in a melanoma cell line causes loss of HLA-G1 expression and sensitivity to NK lysis. Int. J. Cancer, 2005, 117(1), 114-122.
[http://dx.doi.org/10.1002/ijc.21151 ] [PMID: 15880415]
[68]
Kuroki, K; Mio, K; Takahashi, A; Matsubara, H; Kasai, Y; Manaka, S; Kikkawa, M; Hamada, D; Sato, C; Maenaka, K. Cutting Edge: Class II-like structural features and strong receptor binding of the nonclassical HLA-G2 isoform homodimer. J. Immunol. (Baltimore, Md.1950), 2017, 198(9), 3399-3403.
[69]
Wright, G.J.; Puklavec, M.J.; Willis, A.C.; Hoek, R.M.; Sedgwick, J.D.; Brown, M.H.; Barclay, A.N. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity, 2000, 13(2), 233-242.
[http://dx.doi.org/10.1016/S1074-7613(00)00023-6 ] [PMID: 10981966]
[70]
Kobayashi, K.; Yano, H.; Umakoshi, A.; Matsumoto, S.; Mise, A.; Funahashi, Y.; Ueno, Y.; Kamei, Y.; Takada, Y.; Kumon, Y.; Ohnishi, T.; Tanaka, J. A truncated form of CD200 (CD200S) expressed on glioma cells prolonged survival in a rat glioma model by induction of a dendritic cell-like phenotype in tumor-associated macrophages. Neoplasia, 2016, 18(4), 229-241.
[http://dx.doi.org/10.1016/j.neo.2016.02.006 ] [PMID: 27108386]
[71]
Gorczynski, R.M.; Chen, Z.; Hu, J.; Kai, Y.; Lei, J. Evidence of a role for CD200 in regulation of immune rejection of leukaemic tumour cells in C57BL/6 mice. Clin. Exp. Immunol., 2001, 126(2), 220-229.
[http://dx.doi.org/10.1046/j.1365-2249.2001.01689.x ] [PMID: 11703364]
[72]
Kuwabara, J.; Umakoshi, A.; Abe, N.; Sumida, Y.; Ohsumi, S.; Usa, E.; Taguchi, K.; Choudhury, M.E.; Yano, H.; Matsumoto, S.; Kunieda, T.; Takahashi, H.; Yorozuya, T.; Watanabe, Y.; Tanaka, J. Truncated CD200 stimulates tumor immunity leading to fewer lung metastases in a novel Wistar rat metastasis model. Biochem. Biophys. Res. Commun., 2018, 496(2), 542-548.
[http://dx.doi.org/10.1016/j.bbrc.2018.01.065 ] [PMID: 29339155]
[73]
Holland, J.J. McLAREN, L.C. The location and nature of enterovirus receptors in susceptible cells. J. Exp. Med., 1961, 114(2), 161-171.
[http://dx.doi.org/10.1084/jem.114.2.161 ] [PMID: 13715283]
[74]
Strauss, M.; Filman, D.J.; Belnap, D.M.; Cheng, N.; Noel, R.T.; Hogle, J.M. Nectin-like interactions between poliovirus and its receptor trigger conformational changes associated with cell entry. J. Virol., 2015, 89(8), 4143-4157.
[http://dx.doi.org/10.1128/JVI.03101-14 ] [PMID: 25631086]
[75]
Sullivan, D.P.; Seidman, M.A.; Muller, W.A. Poliovirus receptor (CD155) regulates a step in transendothelial migration between PECAM and CD99. Am. J. Pathol., 2013, 182(3), 1031-1042.
[http://dx.doi.org/10.1016/j.ajpath.2012.11.037 ] [PMID: 23333754]
[76]
Tahara-Hanaoka, S.; Shibuya, K.; Onoda, Y.; Zhang, H.; Yamazaki, S.; Miyamoto, A.; Honda, S.; Lanier, L.L.; Shibuya, A. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). Int. Immunol., 2004, 16(4), 533-538.
[http://dx.doi.org/10.1093/intimm/dxh059 ] [PMID: 15039383]
[77]
Brown, M.C.; Dobrikova, E.Y.; Dobrikov, M.I.; Walton, R.W.; Gemberling, S.L.; Nair, S.K.; Desjardins, A.; Sampson, J.H.; Friedman, H.S.; Friedman, A.H.; Tyler, D.S.; Bigner, D.D.; Gromeier, M. Oncolytic polio virotherapy of cancer. Cancer, 2014, 120(21), 3277-3286.
[http://dx.doi.org/10.1002/cncr.28862 ] [PMID: 24939611]
[78]
Gong, J.; Fang, L.; Liu, R.; Wang, Y.; Xing, J.; Chen, Y.; Zhuang, R.; Zhang, Y.; Zhang, C.; Yang, A.; Zhang, X.; Jin, B.; Chen, L. UPR decreases CD226 ligand CD155 expression and sensitivity to NK cell-mediated cytotoxicity in hepatoma cells. Eur. J. Immunol., 2014, 44(12), 3758-3767.
[http://dx.doi.org/10.1002/eji.201444574 ] [PMID: 25209846]
[79]
Readler, J.M.; Sharma, P.K. Excoffon, poliovirus receptor: More than a simple viral receptor.%A Bowers JR. Virus Res., 2017, 242, 1-6.
[80]
Baury, B.; Masson, D.; McDermott, B.M., Jr; Jarry, A.; Blottière, H.M.; Blanchardie, P.; Laboisse, C.L.; Lustenberger, P.; Racaniello, V.R.; Denis, M.G. Identification of secreted CD155 isoforms. Biochem. Biophys. Res. Commun., 2003, 309(1), 175-182.
[http://dx.doi.org/10.1016/S0006-291X(03)01560-2 ] [PMID: 12943679]
[81]
Ohka, S.; Ohno, H.; Tohyama, K.; Nomoto, A. Basolateral sorting of human poliovirus receptor alpha involves an interaction with the mu1B subunit of the clathrin adaptor complex in polarized epithelial cells. Biochem. Biophys. Res. Commun., 2001, 287(4), 941-948.
[http://dx.doi.org/10.1006/bbrc.2001.5660 ] [PMID: 11573956]
[82]
Shibuya, A.; Campbell, D.; Hannum, C.; Yssel, H.; Franz-Bacon, K.; McClanahan, T.; Kitamura, T.; Nicholl, J.; Sutherland, G.R.; Lanier, L.L.; Phillips, J.H. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity, 1996, 4(6), 573-581.
[http://dx.doi.org/10.1016/S1074-7613(00)70060-4 ] [PMID: 8673704]
[83]
Iguchi-Manaka, A.; Okumura, G.; Kojima, H.; Cho, Y.; Hirochika, R.; Bando, H.; Sato, T.; Yoshikawa, H.; Hara, H.; Shibuya, A.; Shibuya, K. Increased soluble CD155 in the serum of cancer patients. PLoS One, 2016, 11(4), e0152982.
[http://dx.doi.org/10.1371/journal.pone.0152982 ] [PMID: 27049654]
[84]
Inozume, T.; Yaguchi, T.; Furuta, J.; Harada, K.; Kawakami, Y.; Shimada, S. Melanoma cells control antimelanoma CTL responses via interaction between TIGIT and CD155 in the effector phase. J. Invest. Dermatol., 2016, 136(1), 255-263.
[http://dx.doi.org/10.1038/JID.2015.404 ] [PMID: 26763445]
[85]
Desjardins, A.; Gromeier, M.; Herndon, J.E., II; Beaubier, N.; Bolognesi, D.P.; Friedman, A.H.; Friedman, H.S.; McSherry, F.; Muscat, A.M.; Nair, S.; Peters, K.B.; Randazzo, D.; Sampson, J.H.; Vlahovic, G.; Harrison, W.T.; McLendon, R.E.; Ashley, D.; Bigner, D.D. Recurrent glioblastoma treated with recombinant poliovirus. N. Engl. J. Med., 2018, 379(2), 150-161.
[http://dx.doi.org/10.1056/NEJMoa1716435 ] [PMID: 29943666]
[86]
Schmitz, J.; Owyang, A.; Oldham, E.; Song, Y.; Murphy, E.; McClanahan, T.K.; Zurawski, G.; Moshrefi, M.; Qin, J.; Li, X.; Gorman, D.M.; Bazan, J.F.; Kastelein, R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity, 2005, 23(5), 479-490.
[http://dx.doi.org/10.1016/j.immuni.2005.09.015 ] [PMID: 16286016]
[87]
Afferni, C.; Buccione, C.; Andreone, S.; Galdiero, M.R.; Varricchi, G.; Marone, G.; Mattei, F.; Schiavoni, G. The pleiotropic immunomodulatory functions of IL-33 and its implications in tumor immunity. Front. Immunol., 2018, 9, 2601.
[http://dx.doi.org/10.3389/fimmu.2018.02601 ] [PMID: 30483263]
[88]
Milosavljevic, M.Z.; Jovanovic, I.P.; Pejnovic, N.N.; Mitrovic, S.L.; Arsenijevic, N.N.; Simovic Markovic, B.J.; Lukic, M.L. Deletion of IL-33R attenuates VEGF expression and enhances necrosis in mammary carcinoma. Oncotarget, 2016, 7(14), 18106-18115.
[http://dx.doi.org/10.18632/oncotarget.7635 ] [PMID: 26919112]
[89]
Hu, H.; Sun, J.; Wang, C.; Bu, X.; Liu, X.; Mao, Y.; Wang, H. IL-33 facilitates endocrine resistance of breast cancer by inducing cancer stem cell properties. Biochem. Biophys. Res. Commun., 2017, 485(3), 643-650.
[http://dx.doi.org/10.1016/j.bbrc.2017.02.080 ] [PMID: 28216163]
[90]
Gao, X.; Wang, X.; Yang, Q.; Zhao, X.; Wen, W.; Li, G.; Lu, J.; Qin, W.; Qi, Y.; Xie, F.; Jiang, J.; Wu, C.; Zhang, X.; Chen, X.; Turnquist, H.; Zhu, Y.; Lu, B. Tumoral expression of IL-33 inhibits tumor growth and modifies the tumor microenvironment through CD8+ T and NK cells. J. Immunol. (Baltimore, Md.:1950), 2015, 194(1), 438-445.
[91]
Fang, M.; Li, Y.; Huang, K.; Qi, S.; Zhang, J.; Zgodzinski, W.; Majewski, M.; Wallner, G.; Gozdz, S.; Macek, P.; Kowalik, A.; Pasiarski, M.; Grywalska, E.; Vatan, L.; Nagarsheth, N.; Li, W.; Zhao, L.; Kryczek, I.; Wang, G.; Wang, Z.; Zou, W.; Wang, L. IL33 promotes colon cancer cell stemness via JNK activation and macrophage recruitment. Cancer Res., 2017, 77(10), 2735-2745.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-1602 ] [PMID: 28249897]
[92]
Zhang, Y.; Davis, C.; Shah, S.; Hughes, D.; Ryan, J.C.; Altomare, D.; Peña, M.M. IL-33 promotes growth and liver metastasis of colorectal cancer in mice by remodeling the tumor microenvironment and inducing angiogenesis. Mol. Carcinog., 2017, 56(1), 272-287.
[http://dx.doi.org/10.1002/mc.22491 ] [PMID: 27120577]
[93]
Eissmann, M.F.; Dijkstra, C.; Wouters, M.A.; Baloyan, D.; Mouradov, D.; Nguyen, P.M.; Davalos-Salas, M.; Putoczki, T.L.; Sieber, O.M.; Mariadason, J.M.; Ernst, M.; Masson, F. Interleukin 33 signaling restrains sporadic colon cancer in an interferon-γ-dependent manner. Cancer Immunol. Res., 2018, 6(4), 409-421.
[http://dx.doi.org/10.1158/2326-6066.CIR-17-0218 ] [PMID: 29463593]
[94]
Saranchova, I.; Han, J.; Huang, H.; Fenninger, F.; Choi, K.B.; Munro, L.; Pfeifer, C.; Welch, I.; Wyatt, A.W.; Fazli, L.; Gleave, M.E.; Jefferies, W.A. Discovery of a metastatic immune escape mechanism initiated by the loss of expression of the tumour biomarker interleukin-33. Scientific Rep., 2016, 6(undefined), 30555.
[http://dx.doi.org/10.1038/srep30555]
[95]
Yang, I.S.; Son, H.; Kim, S.; Kim, S. ISOexpresso: A web-based platform for isoform-level expression analysis in human cancer. BMC Genomics, 2016, 17(1), 631.
[http://dx.doi.org/10.1186/s12864-016-2852-6 ] [PMID: 27519173]
[96]
Koon, H.B.; Ippolito, G.C.; Banham, A.H.; Tucker, P.W. FOXP1: A potential therapeutic target in cancer. Expert Opin. Ther. Targets, 2007, 11(7), 955-965.
[http://dx.doi.org/10.1517/14728222.11.7.955 ] [PMID: 17614763]
[97]
Brown, P.J.; Ashe, S.L.; Leich, E.; Burek, C.; Barrans, S.; Fenton, J.A.; Jack, A.S.; Pulford, K.; Rosenwald, A.; Banham, A.H. Potentially oncogenic B-cell activation-induced smaller isoforms of FOXP1 are highly expressed in the activated B cell-like subtype of DLBCL. Blood, 2008, 111(5), 2816-2824.
[http://dx.doi.org/10.1182/blood-2007-09-115113 ] [PMID: 18077790]
[98]
van Keimpema, M.; Grüneberg, L.J.; Schilder-Tol, E.J.; Oud, M.E.; Beuling, E.A.; Hensbergen, P.J.; de Jong, J.; Pals, S.T.; Spaargaren, M. The small FOXP1 isoform predominantly expressed in activated B cell-like diffuse large B-cell lymphoma and full-length FOXP1 exert similar oncogenic and transcriptional activity in human B cells. Haematologica, 2017, 102(3), 573-583.
[http://dx.doi.org/10.3324/haematol.2016.156455 ] [PMID: 27909217]
[99]
Schrock, A.B.; Frampton, G.M.; Suh, J.; Chalmers, Z.R.; Rosenzweig, M.; Erlich, R.L.; Halmos, B.; Goldman, J.; Forde, P.; Leuenberger, K.; Peled, N.; Kalemkerian, G.P.; Ross, J.S.; Stephens, P.J.; Miller, V.A.; Ali, S.M.; Ou, S.H. Characterization of 298 Patients with Lung Cancer Harboring MET Exon 14 Skipping Alterations. J. Thoracic. Oncol., 2016, 11(9), 1493-502.
[100]
Gui, Y.; Yeganeh, M.; Donates, Y.C.; Tobelaim, W.S.; Chababi, W.; Mayhue, M.; Yoshimura, A.; Ramanathan, S.; Saucier, C.; Ilangumaran, S. Regulation of MET receptor tyrosine kinase signaling by suppressor of cytokine signaling 1 in hepatocellular carcinoma. Oncogene, 2015, 34(46), 5718-5728.
[http://dx.doi.org/10.1038/onc.2015.20 ] [PMID: 25728680]
[101]
Poulikakos, P.I.; Persaud, Y.; Janakiraman, M.; Kong, X.; Ng, C.; Moriceau, G.; Shi, H.; Atefi, M.; Titz, B.; Gabay, M.T.; Salton, M.; Dahlman, K.B.; Tadi, M.; Wargo, J.A.; Flaherty, K.T.; Kelley, M.C.; Misteli, T.; Chapman, P.B.; Sosman, J.A.; Graeber, T.G.; Ribas, A.; Lo, R.S.; Rosen, N.; Solit, D.B. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature, 2011, 480(7377), 387-390.
[http://dx.doi.org/10.1038/nature10662 ] [PMID: 22113612]
[102]
Brown, M.C.; Gromeier, M. Cytotoxic and immunogenic mechanisms of recombinant oncolytic poliovirus. Curr. Opin. Virol., 2015, 13, 81-85.
[http://dx.doi.org/10.1016/j.coviro.2015.05.007 ] [PMID: 26083317]
[103]
Dobrikova, E.Y.; Broadt, T.; Poiley-Nelson, J.; Yang, X.; Soman, G.; Giardina, S.; Harris, R.; Gromeier, M. Recombinant oncolytic poliovirus eliminates glioma in vivo without genetic adaptation to a pathogenic phenotype. Mol. Ther., 2008, 16(11), 1865-1872.
[http://dx.doi.org/10.1038/mt.2008.184 ] [PMID: 18766173]
[104]
Gromeier, M.; Lachmann, S.; Rosenfeld, M.R.; Gutin, P.H.; Wimmer, E. Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc. Natl. Acad. Sci. USA, 2000, 97(12), 6803-6808.
[http://dx.doi.org/10.1073/pnas.97.12.6803 ] [PMID: 10841575]
[105]
Martinez-Montiel, N.; Rosas-Murrieta, N.H.; Anaya Ruiz, M.; Monjaraz-Guzman, E.; Martinez-Contreras, R. Alternative splicing as a target for cancer treatment. Int. J. Mol. Sci., 2018, 19(2), E545.
[http://dx.doi.org/10.3390/ijms19020545 ] [PMID: 29439487]
[106]
Haferkamp, B.; Zhang, H.; Lin, Y.; Yeap, X.; Bunce, A.; Sharpe, J.; Xiang, J. BaxΔ2 is a novel bax isoform unique to microsatellite unstable tumors. J. Biol. Chem., 2012, 287(41), 34722-34729.
[http://dx.doi.org/10.1074/jbc.M112.374785 ] [PMID: 22910913]
[107]
Sadelain, M.; Rivière, I.; Riddell, S. Therapeutic T cell engineering. Nature, 2017, 545(7655), 423-431.
[http://dx.doi.org/10.1038/nature22395 ] [PMID: 28541315]
[108]
Souza-Fonseca-Guimaraes, F.; Cursons, J.; Huntington, N.D. The emergence of natural killer cells as a major target in cancer immunotherapy. Trends Immunol., 2019, 40(2), 142-158.
[http://dx.doi.org/10.1016/j.it.2018.12.003 ] [PMID: 30639050]
[109]
Ding, W.; Li, D.; Zhang, P.; Shi, L.; Dai, H.; Li, Y.; Bao, X.; Wang, Y.; Zhang, H.; Deng, L. Mutual editing of alternative splicing between breast cancer cells and macrophages. Oncol. Rep., 2019, 42(2), 629-656.
[http://dx.doi.org/10.3892/or.2019.7200 ] [PMID: 31233192]
[110]
Kahles, A.; Lehmann, K.V.; Toussaint, N.C.; Hüser, M.; Stark, S.G.; Sachsenberg, T.; Stegle, O.; Kohlbacher, O.; Sander, C.; Rätsch, G. Cancer Genome Atlas Research Network. Comprehensive analysis of alternative splicing across tumors from 8,705 Patients. Cancer Cell, 2018, 34(2), 211-224.
[http://dx.doi.org/10.1016/j.ccell.2018.07.001 ] [PMID: 30078747]
[111]
Frankiw, L.; Baltimore, D.; Li, G. Alternative mRNA splicing in cancer immunotherapy. Nat. Rev. Immunol., 2019, 19(11), 675-687.
[http://dx.doi.org/10.1038/s41577-019-0195-7 ] [PMID: 31363190]
[112]
Levin, A.A. Treating disease at the RNA level with oligonucleotides. N. Engl. J. Med., 2019, 380(1), 57-70.
[http://dx.doi.org/10.1056/NEJMra1705346 ] [PMID: 30601736]
[113]
Urbanski, L.M.; Leclair, N.; Anczuków, O. Alternative-splicing defects in cancer: Splicing regulators and their downstream targets, guiding the way to novel cancer therapeutics. Wiley Interdiscip. Rev. RNA, 2018, 9(4), e1476.
[http://dx.doi.org/10.1002/wrna.1476 ] [PMID: 29693319 ]


open access plus

Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 10
Year: 2020
Published on: 19 June, 2020
Page: [729 - 740]
Pages: 12
DOI: 10.2174/1568009620666200619123725

Article Metrics

PDF: 37
HTML: 9
PRC: 1