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Colorectal Cancer Immunotherapy: Current State and Prospects (Review)

Colorectal Cancer Immunotherapy: Current State and Prospects (Review)

Kit О.I., Kirichenko Е.Y., Novikova I.А., Maksimov А.Y., Filippova S.Y., Grankina А.О., Zlatnik Е.Y.
Key words: colorectal cancer; immunotherapy; monoclonal antibodies; adoptive cellular therapy; anticancer vaccine; cytokines.
2017, volume 9, issue 3, page 138.

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Currently, new knowledge on immunotherapy in solid tumors is being intensively accumulated and new promising techniques are originating. The most advanced are those in the field of searching for new immune checkpoints, development of highly efficient immune adjuvants based on recombinant viruses to improve the effect of anticancer vaccines, as well as design engineering of chimeric receptors of T cells used for adoptive immunotherapy. We have presented some clinical trial results of immunotherapeutic approaches, as well as experimental studies on animal models, which offer new prospects for colon cancer treatment.

  1. Burnet M. Cancer — a biological approach: III. Viruses associated with neoplastic conditions. IV. Practical applications. Br Med J 1957; 1(5023): 841–847, https://doi.org/10.1136/bmj.1.5023.841.
  2. Thomas L. Delayed hypersensitivity in health and disease. In: Cellular and humoral aspects of the hypersensitive states. Lawrence H.S. (editor). Hoeber-Harper; 1959; p. 529–532.
  3. Stutman O. Chemical carcinogenesis in nude mice: comparison between nude mice from homozygous and heterozygous matings and effect of age and carcinogen dose. J Natl Cancer Inst 1979; 2: 353–358, https://doi.org/10.1093/jnci/62.2.353.
  4. Hunig T. T-cell function and specificity in athymic mice. Immunol Today 1983; 4(3): 84–87, https://doi.org/10.1016/0167-5699(83)90125-1.
  5. Maleckar J.R., Sherman L.A. The composition of the T cell receptor repertoire in nude mice. J Immunol 1987; 138(11): 3873–3876.
  6. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001; 410(6832): 1107–1111, https://doi.org/10.1038/35074122.
  7. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., Schreiber R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002; 3(11): 991–998, https://doi.org/10.1038/ni1102-991.
  8. Tryakin A.A., Artamonova E.V., Besova N.S., Bolotina L.V., Gladkov O.A., Glebovskaya V.V., et al. Practical guidelines on medical therapy of rectal cancer. Zlokachestvennye opukholi 2015; 4(Special Issue): 230–246.
  9. Tryakin A.A., Artamonova E.V., Besova N.S., Bolotina L.V., Vladimirova L.Yu., Gladkov O.A., et al. Practical guidelines on medical therapy of colon cancer. Zlokachestvennye opukholi 2015; 4(Special Issue): 214–229.
  10. Grothey A., Flick E.D., Cohn A.L., Bekaii-Saab T.S., Bendell J.C., Kozloff M., Roach N., Mun Y., Fish S., Hurwitz H.I. Bevacizumab exposure beyond first disease progression in patients with metastatic colorectal cancer: analyses of the ARIES observational cohort study. Pharmacoepidemiol Drug Saf 2014; 23(7): 726–734, https://doi.org/10.1002/pds.3633.
  11. Hurwitz H.I., Tebbutt N.C., Kabbinavar F., Giantonio B.J., Guan Z.Z., Mitchell L., Waterkamp D., Tabernero J. Efficacy and safety of bevacizumab in metastatic colorectal cancer: pooled analysis from seven randomized controlled trials. Oncologist 2013; 18(9): 1004–1012, https://doi.org/10.1634/theoncologist.2013-0107.
  12. Price T.J., Peeters M., Kim T.W., Li J., Cascinu S., Ruff P., Suresh A.S., Thomas A., Tjulandin S., Zhang K., Murugappan S., Sidhu R. Panitumumab versus cetuximab in patients with chemotherapy-refractory wild-type KRAS exon 2 metastatic colorectal cancer (ASPECCT): a randomised, multicentre, open-label, non-inferiority phase 3 study. Lancet Oncol 2014; 15: 569–579, https://doi.org/10.1016/s1470-2045(14)70118-4.
  13. Van Cutsem E., Köhne C.H., Láng I., Folprecht G., Nowacki M.P., Cascinu S., Shchepotin I., Maurel J., Cunningham D., Tejpar S., Schlichting M., Zubel A., Celik I., Rougier P., Ciardiello F. Cetuximab plus irinotecan, fluorouracil, and leucovorin as first-line treatment for metastatic colorectal cancer: updated analysis of overall survival according to tumor KRAS and BRAF mutation status. J Clin Oncol 2011; 29(15): 2011–2019, https://doi.org/10.1200/jco.2010.33.5091.
  14. Vacchelli E., Aranda F., Eggermont A., Galon J., Sautès-Fridman C., Zitvogel L., Kroemer G., Galluzzi L. Trial Watch: Tumor-targeting monoclonal antibodies in cancer therapy. Oncoimmunology 2014; 3(1): e27048, https://doi.org/10.4161/onci.27048.
  15. Yang X., Zhang X., Mortenson E.D., Radkevich-Brown O., Wang Y., Fu Y.X. Cetuximab-mediated tumor regression depends on innate and adaptive immune responses. Mol Ther 2013; 21(1): 91–100, https://doi.org/10.1038/mt.2012.184.
  16. Kohrt H.E., Colevas A.D., Houot R., Weiskopf K., Goldstein M.J., Lund P., Mueller A., Sagiv-Barfi I., Marabelle A., Lira R., Troutner E., Richards L., Rajapaska A., Hebb J., Chester C., Waller E., Ostashko A., Weng W.K., Chen L., Czerwinski D., Fu Y.X., Sunwoo J., Levy R. Targeting CD137 enhances the efficacy of cetuximab. J Clin Invest 2014; 124(6): 2668–2682, https://doi.org/10.1172/jci73014.
  17. Calemma R., Ottaiano A., Trotta A.M., Nasti G., Romano C., Napolitano M., Galati D., Borrelli P., Zanotta S., Cassata A., Castello G., Iaffaioli V.R., Scala S. Fc gamma receptor IIIa polymorphisms in advanced colorectal cancer patients correlated with response to anti-EGFR antibodies and clinical outcome. J Transl Med 2012; 10: 232, https://doi.org/10.1186/1479-5876-10-232.
  18. Rodríguez J., Zarate R., Bandres E., Boni V., Hernández A., Sola J.J., Honorato B., Bitarte N., García-Foncillas J. Fc gamma receptor polymorphisms as predictive markers of cetuximab efficacy in epidermal growth factor receptor downstream-mutated metastatic colorectal cancer. Eur J Cancer 2012; 48(12): 1774–1780, https://doi.org/10.1016/j.ejca.2012.01.007.
  19. Riethmüller G., Schneider-Gädicke E., Schlimok G., Schmiegel W., Raab R., Höffken K., Gruber R., Pichlmaier H., Hirche H., Pichlmayr R., Witte J. Randomised trial of monoclonal antibody for adjuvant therapy of resected Dukes’ C colorectal carcinoma. German Cancer Aid 17-1A Study Group. Lancet 1994; 343(8907): 1177–1183, https://doi.org/10.1016/s0140-6736(94)92398-1.
  20. Punt C.J., Nagy A., Douillard J.Y., Figer A., Skovsgaard T., Monson J., Barone C., Fountzilas G., Riess H., Moylan E., Jones D., Dethling J., Colman J., Coward L., MacGregor S. Edrecolomab alone or in combination with fluorouracil and folinic acid in the adjuvant treatment of stage III colon cancer: a randomised study. Lancet 2002; 360(9334): 671–677, https://doi.org/10.1016/s0140-6736(02)09836-7.
  21. Han H., Ma J., Zhang K., Li W., Liu C., Zhang Y., Zhang G., Ma P., Wang L., Zhang G., Tao H., Gao B. Bispecific anti-CD3 x anti-HER2 antibody mediates T cell cytolytic activity to HER2-positive colorectal cancer in vitro and in vivo. Int J Oncol 2014; 45(6): 2446–2454, https://doi.org/10.3892/ijo.2014.2663.
  22. Schmohl J.U., Gleason M.K., Dougherty P.R., Miller J.S., Vallera D.A. Heterodimeric bispecific single chain variable fragments (scFv) killer engagers (BiKEs) enhance NK-cell activity against CD133+ colorectal cancer cells. Target Oncol 2015; 11(3): 353–361, https://doi.org/10.1007/s11523-015-0391-8.
  23. 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, https://doi.org/10.1146/annurev-immunol-032712-095951.
  24. Wu A.A., Drake V., Huang H.S., Chiu S., Zheng L. Reprogramming the tumor microenvironment: tumor-induced immunosuppressive factors paralyze T cells. Oncoimmunology 2015; 4(7): e1016700, https://doi.org/10.1080/2162402x.2015.1016700.
  25. Rothe A., Jachimowicz R.D., Borchmann S., Madlener M., Keßler J., Reiners K.S., Sauer M., Hansen H.P., Ullrich R.T., Chatterjee S., Borchmann P., Yazaki P., Koslowsky T.C., Engert A., Heukamp L.C., Hallek M., von Strandmann E.P. The bispecific immunoligand ULBP2-aCEA redirects natural killer cells to tumor cells and reveals potent anti-tumor activity against colon carcinoma. Int J Cancer 2014; 134(12): 2829–2840, https://doi.org/10.1002/ijc.28609.
  26. Kadagidze Z.G., Slavina E.G., Chertkova A.I. Lymphocyte receptors that regulate the immune response — the key to the management of antitumor immunity. Voprosy onkologii 2015; 61(4): 523–529.
  27. Walunas T.L., Lenschow D.J., Bakker C.Y., Linsley P.S., Freeman G.J., Green J.M., Thompson C.B., Bluestone J.A. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1994; 1(5): 405–413, https://doi.org/10.1016/1074-7613(94)90071-x.
  28. Freeman G.J., Long A.J., Iwai Y., Bourque K., Chernova T., Nishimura H., Fitz L.J., Malenkovich N., Okazaki T., Byrne M.C., Horton H.F., Fouser L., Carter L., Ling V., Bowman M.R., Carreno B.M., Collins M., Wood C.R., Honjo T. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192(7): 1027–1034, https://doi.org/10.1084/jem.192.7.1027.
  29. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., Roche P.C., Lu J., Zhu G., Tamada K., Lennon V.A., Celis E., Chen L. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002; 8(8): 793–800, https://doi.org/10.1038/nm730.
  30. Brahmer J.R., Tykodi S.S., Chow L.Q., Hwu W.J., Topalian S.L., Hwu P., Drake C.G., Camacho L.H., Kauh J., Odunsi K., Pitot H.C., Hamid O., Bhatia S., Martins R., Eaton K., Chen S., Salay T.M., Alaparthy S., Grosso J.F., Korman A.J., Parker S.M., Agrawal S., Goldberg S.M., Pardoll D.M., Gupta A., Wigginton J.M. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366(26): 2455–2465, https://doi.org/10.1056/nejmoa1200694.
  31. Hodi F.S., O’Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., Akerley W., van den Eertwegh A.J., Lutzky J., Lorigan P., Vaubel J.M., Linette G.P., Hogg D., Ottensmeier C.H., Lebbé C., Peschel C., Quirt I., Clark J.I., Wolchok J.D., Weber J.S., Tian J., Yellin M.J., Nichol G.M., Hoos A., Urba W.J. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8): 711–723, https://doi.org/10.1056/nejmoa1003466.
  32. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., Leming P.D., Spigel D.R., Antonia S.J., Horn L., Drake C.G., Pardoll D.M., Chen L., Sharfman W.H., Anders R.A., Taube J.M., McMiller T.L., Xu H., Korman A.J., Jure-Kunkel M., Agrawal S., McDonald D., Kollia G.D., Gupta A., Wigginton J.M., Sznol M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366(26): 2443–2454, https://doi.org/10.1056/nejmoa1200690.
  33. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., Segal N.H., Ariyan C.E., Gordon R.A., Reed K., Burke M.M., Caldwell A., Kronenberg S.A., Agunwamba B.U., Zhang X., Lowy I., Inzunza H.D., Feely W., Horak C.E., Hong Q., Korman A.J., Wigginton J.M., Gupta A., Sznol M. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369(2): 122–133, https://doi.org/10.1056/nejmoa1302369.
  34. Ge J., Zhu L., Zhou J., Li G., Li Y., Li S., Wu Z., Rong J., Yuan H., Liu Y., Chi Q., Piao D., Zhao Y., Cui B. Association between co-inhibitory molecule gene tagging single nucleotide polymorphisms and the risk of colorectal cancer in Chinese. J Cancer Res Clin Oncol 2015; 141(9): 1533–1544, https://doi.org/10.1007/s00432-015-1915-4.
  35. Mojtahedi Z., Mohmedi M., Rahimifar S., Erfani N., Hosseini S.V., Ghaderi A. Programmed death-1 gene polymorphism (PD-1.5 C/T) is associated with colon cancer. Gene 2012; 508(2): 229–232, https://doi.org/10.1016/j.gene.2012.07.059.
  36. Hua D., Sun J., Mao Y., Chen L.J., Wu Y.Y., Zhang X.G. B7-H1 expression is associated with expansion of regulatory T cells in colorectal carcinoma. World J Gastroenterol 2012; 18(9): 971–978, https://doi.org/10.3748/wjg.v18.i9.971.
  37. Droeser R.A., Hirt C., Viehl C.T., Frey D.M., Nebiker C., Huber X., Zlobec I., Eppenberger-Castori S., Tzankov A., Rosso R., Zuber M., Muraro M.G., Amicarella F., Cremonesi E., Heberer M., Iezzi G., Lugli A., Terracciano L., Sconocchia G., Oertli D., Spagnoli G.C., Tornillo L. Clinical impact of programmed cell death ligand 1 expression in colorectal cancer. Eur J Cancer 2013; 49(9): 2233–2242, https://doi.org/10.1016/j.ejca.2013.02.015.
  38. Le D.T., Uram J.N., Wang H., Bartlett B.R., Kemberling H., Eyring A.D., Skora A.D., Luber B.S., Azad N.S., Laheru D., Biedrzycki B., Donehower R.C., Zaheer A., Fisher G.A., Crocenzi T.S., Lee J.J., Duffy S.M., Goldberg R.M., de la Chapelle A., Koshiji M., Bhaijee F., Huebner T., Hruban R.H., Wood L.D., Cuka N., Pardoll D.M., Papadopoulos N., Kinzler K.W., Zhou S., Cornish T.C., Taube J.M., Anders R.A., Eshleman J.R., Vogelstein B., Diaz L.A. Jr.PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015; 372(26): 2509–2520, https://doi.org/10.1056/nejmoa1500596.
  39. Chung K.Y., Gore I., Fong L., Venook A., Beck S.B., Dorazio P., Criscitiello P.J., Healey D.I., Huang B., Gomez-Navarro J., Saltz L.B. Phase II study of the anti-cytotoxic T-lymphocyte-associated antigen 4 monoclonal antibody, tremelimumab, in patients with refractory metastatic colorectal cancer. J Clin Oncol 2010; 28(21): 3485–3490, https://doi.org/10.1200/jco.2010.28.3994.
  40. Xu B., Yuan L., Gao Q., Yuan P., Zhao P., Yuan H., Fan H., Li T., Qin P., Han L., Fang W., Suo Z. Circulating and tumor-infiltrating Tim-3 in patients with colorectal cancer. Oncotarget 2015; 6(24): 20592–20603, https://doi.org/10.18632/oncotarget.4112.
  41. Chen J., Chen Z. The effect of immune microenvironment on the progression and prognosis of colorectal cancer. Med Oncol 2014; 31(8): 82, https://doi.org/10.1007/s12032-014-0082-9.
  42. Weixler B., Cremonesi E., Sorge R., Muraro M.G., Delko T., Nebiker C.A., Däster S., Governa V., Amicarella F., Soysal S.D., Kettelhack C., von Holzen U.W., Eppenberger-Castori S., Spagnoli G.C., Oertli D., Iezzi G., Terracciano L., Tornillo L., Sconocchia G., Droeser R.A. OX40 expression enhances the prognostic significance of CD8 positive lymphocyte infiltration in colorectal cancer. Oncotarget 2015; 6(35): 37588–37599, https://doi.org/10.18632/oncotarget.5940.
  43. Keenan B.P., Jaffee E.M. Whole cell vaccines — past progress and future strategies. Semin Oncol 2012; 39(3): 276–286, https://doi.org/10.1053/j.seminoncol.2012.02.007.
  44. Schulze T., Kemmner W., Weitz J., Wernecke K.D., Schirrmacher V., Schlag P.M. Efficiency of adjuvant active specific immunization with Newcastle disease virus modified tumor cells in colorectal cancer patients following resection of liver metastases: results of a prospective randomized trial. Cancer Immunol Immunother 2009; 58(1): 61–69, https://doi.org/10.1007/s00262-008-0526-1.
  45. Becerra A.Z., Probst C.P., Tejani M.A., Aquina C.T., González M.G., Hensley B.J., Noyes K., Monson J.R., Fleming F.J. Evaluating the prognostic role of elevated preoperative carcinoembryonic antigen levels in colon cancer patients: results from the national cancer database. Ann Surg Oncol 2016; 23(5): 1554–1561, https://doi.org/10.1245/s10434-015-5014-1.
  46. Duncan T.J., Watson N.F., Al-Attar A.H., Scholefield J.H., Durrant L.G. The role of MUC1 and MUC3 in the biology and prognosis of colorectal cancer. World J Surg Oncol 2007; 5: 31, https://doi.org/10.1186/1477-7819-5-31.
  47. Lundin M., Nordling S., Lundin J., Alfthan H., Stenman U.H., Haglund C. Tissue expression of human chorionic gonadotropin beta predicts outcome in colorectal cancer: a comparison with serum expression. Int J Cancer 2001; 95(1): 18–22, https://doi.org/10.1002/1097-0215(20010120)95:1<18::aid-ijc1003>3.0.co;2-5.
  48. Kawasaki H., Altieri D.C., Lu C.D., Toyoda M., Tenjo T., Tanigawa N. Inhibition of apoptosis by survivin predicts shorter survival rates in colorectal cancer. Cancer Res 1998; 58(22): 5071–5074.
  49. Saito T., Masuda N., Miyazaki T., Kanoh K., Suzuki H., Shimura T., Asao T., Kuwano H. Expression of EphA2 and E-cadherin in colorectal cancer: correlation with cancer metastasis. Oncol Rep 2004; 11(3): 605–611, https://doi.org/10.3892/or.11.3.605.
  50. Sasatomi T., Suefuji Y., Matsunaga K., Yamana H., Miyagi Y., Araki Y., Ogata Y., Itoh K., Shirouzu K. Expression of tumor rejection antigens in colorectal carcinomas. Cancer 2002; 94(6): 1636–1641, https://doi.org/10.1002/cncr.10421.
  51. Moulton H.M., Yoshihara P.H., Mason D.H., Iversen P.L., Triozzi P.L. Active specific immunotherapy with a beta-human chorionic gonadotropin peptide vaccine in patients with metastatic colorectal cancer: antibody response is associated with improved survival. Clin Cancer Res 2002; 8(7): 2044–2051.
  52. Mukherjee P., Pathangey L.B., Bradley J.B., Tinder T.L., Basu G.D., Akporiaye E.T., Gendler S.J. MUC1-specific immune therapy generates a strong anti-tumor response in a MUC1-tolerant colon cancer model. Vaccine 2007; 25(9): 1607–1618, https://doi.org/10.1016/j.vaccine.2006.11.007.
  53. Kimura T., McKolanis J.R., Dzubinski L.A., Islam K., Potter D.M., Salazar A.M., Schoen R.E., Finn O.J. MUC1 vaccine for individuals with advanced adenoma of the colon: a cancer immunoprevention feasibility study. Cancer Prev Res (Phila) 2013; 6(1): 18–26, https://doi.org/10.1158/1940-6207.capr-12-0275.
  54. Hörig H., Lee D.S., Conkright W., Divito J., Hasson H., LaMare M., Rivera A., Park D., Tine J., Guito K., Tsang K.W., Schlom J., Kaufman H.L. Phase I clinical trial of a recombinant canarypoxvirus (ALVAC) vaccine expressing human carcinoembryonic antigen and the B7.1 co-stimulatory molecule. Cancer Immunol Immunother 2000; 49(9): 504–514, https://doi.org/10.1007/s002620000146.
  55. Kaufman H.L., Lenz H.J., Marshall J., Singh D., Garett C., Cripps C., Moore M., von Mehren M., Dalfen R., Heim W.J., Conry R.M., Urba W.J., Benson A.B. 3rd, Yu M., Caterini J., Kim-Schulze S., Debenedette M., Salha D., Vogel T., Elias I., Berinstein N.L. Combination chemotherapy and ALVAC-CEA/B7.1 vaccine in patients with metastatic colorectal cancer. Clin Cancer Res 2008; 14(15): 4843–4849, https://doi.org/10.1158/1078-0432.ccr-08-0276.
  56. Gameiro S.R., Higgins J.P., Dreher M.R., Woods D.L., Reddy G., Wood B.J., Guha C., Hodge J.W. Combination therapy with local radiofrequency ablation and systemic vaccine enhances antitumor immunity and mediates local and distal tumor regression. PLoS One 2013; 8(7): e70417, https://doi.org/10.1371/journal.pone.0070417.
  57. Gulley J.L., Madan R.A., Tsang K.Y., Arlen P.M., Camphausen K., Mohebtash M., Kamrava M., Schlom J., Citrin D. A pilot safety trial investigating a vector-based vaccine targeting carcinoembryonic antigen in combination with radiotherapy in patients with gastrointestinal malignancies metastatic to the liver. Expert Opin Biol Ther 2011; 11(11): 1409–1418, https://doi.org/10.1517/14712598.2011.615741.
  58. Liu Y., Zhang W., Zhang B., Yin X., Pang Y. DC vaccine therapy combined concurrently with oral capecitabine in metastatic colorectal cancer patients. Hepatogastroenterology 2013; 60(121): 23–27.
  59. Tamir A., Basagila E., Kagahzian A., Jiao L., Jensen S., Nicholls J., Tate P., Stamp G., Farzaneh F., Harrison P., Stauss H., George A.J., Habib N., Lechler R.I., Lombardi G. Induction of tumor-specific T cell responses by vaccination with tumor lysate-loaded dendritic cells in colorectal cancer patients with carcinoembryonic-antigen positive tumors. Cancer Immunol Immunother 2007; 56(12): 2003–2016, https://doi.org/10.1007/s00262-007-0299-y.
  60. Wu Y.G., Wu G.Z., Wang L., Zhang Y.Y., Li Z., Li D.C. Tumor cell lysate-pulsed dendritic cells induce a T cell response against colon cancer in vitro and in vivo. Med Oncol 2010; 27(3): 736–742, https://doi.org/10.1007/s12032-009-9277-x.
  61. Burgdorf S.K., Fischer A., Myschetzky P.S., Munksgaard S.B., Zocca M.B., Claesson M.H., Rosenberg J. Clinical responses in patients with advanced colorectal cancer to a dendritic cell based vaccine. Oncol Rep 2008; 20(6): 1305–1311, https://doi.org/10.3892/or_00000145.
  62. Toh H.C., Wang W.W., Chia W.K., Kvistborg P., Sun L., Teo K., Phoon Y.P., Soe Y., Tan S.H., Hee S.W., Foo K.F., Ong S., Koo W.H., Zocca M.B., Claesson M.H. Clinical benefit of allogeneic melanoma cell lysate-pulsed autologous dendritic cell vaccine in MAGE-positive colorectal cancer patients. Clin Cancer Res 2009; 15(24): 7726–7736, https://doi.org/10.1158/1078-0432.ccr-09-1537.
  63. Lesterhuis W.J., de Vries I.J., Schuurhuis D.H., Boullart A.C., Jacobs J.F., de Boer A.J., Scharenborg N.M., Brouwer H.M., van de Rakt M.W., Figdor C.G., Ruers T.J., Adema G.J., Punt C.J. Vaccination of colorectal cancer patients with CEA-loaded dendritic cells: antigen-specific T cell responses in DTH skin tests. Ann Oncol 2006; 17(6): 974–980, https://doi.org/10.1093/annonc/mdl072.
  64. Morse M.A., Niedzwiecki D., Marshall J.L., Garrett C., Chang D.Z., Aklilu M., Crocenzi T.S., Cole D.J., Dessureault S., Hobeika A.C., Osada T., Onaitis M., Clary B.M., Hsu D., Devi G.R., Bulusu A., Annechiarico R.P., Chadaram V., Clay T.M., Lyerly H.K. A randomized phase II study of immunization with dendritic cells modified with poxvectors encoding CEA and MUC1 compared with the same poxvectors plus GM-CSF for resected metastatic colorectal cancer. Ann Surg 2013; 258(6): 879–886, https://doi.org/10.1097/sla.0b013e318292919e.
  65. Nagorsen D., Thiel E. Clinical and immunologic responses to active specific cancer vaccines in human colorectal cancer. Clin Cancer Res 2006; 12(10): 3064–3069, https://doi.org/10.1158/1078-0432.ccr-05-2788.
  66. Rao B., Han M., Wang L., Gao X., Huang J., Huang M., Liu H., Wang J. Clinical outcomes of active specific immunotherapy in advanced colorectal cancer and suspected minimal residual colorectal cancer: a meta-analysis and system review. J Transl Med 2011; 9: 17, https://doi.org/10.1186/1479-5876-9-17.
  67. Simbirtsev A.S. Cytokines in allergy immunopathogenesis and therapy. Rossiyskiy allergologicheskiy zhurnal 2007; 1: 5–19.
  68. McAllister S.S., Weinberg R.A. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol 2014; 16(8): 717–727, https://doi.org/10.1038/ncb3015.
  69. Zlatnik E.Y., Nikipelova E.A., Terpugov A.L., Maksimov A.Y., Selyutina O.N., Zakora G.I. Cytokine content of colorectal polypous tissue. Fundamental’nye issledovaniya 2014; 5–5: 1016–1020.
  70. Kit O.I., Zlatnik E.Yu., Nikipelova E.A., Shaposhnikov A.V., Zakora G.I. Comparative characteristics of cytokines’ levels in tissues of gut adenoma and adenocarcinoma. Tsitokiny i vospalenie 2012; 11(3): 100–104.
  71. Gou H.F., Huang J., Shi H.S., Chen X.C., Wang Y.S. Chemo-immunotherapy with oxaliplatin and interleukin-7 inhibits colon cancer metastasis in mice. PloS One 2014; 9(1): e85789, https://doi.org/10.1371/journal.pone.0085789.
  72. Lu L., Li Z.J., Li L.F., Wu W.K., Shen J., Zhang L., Chan R.L., Yu L., Liu Y.W., Ren S.X., Chan K.M., Cho C.H. Vascular-targeted TNFα improves tumor blood vessel function and enhances antitumor immunity and chemotherapy in colorectal cancer. J Control Release 2015; 210: 134–146, https://doi.org/10.1016/j.jconrel.2015.05.282.
  73. Yang J.L., Qu X.J., Russell P.J., Goldstein D. Interferon-alpha promotes the anti-proliferative effect of erlotinib (OSI-774) on human colon cancer cell lines. Cancer Lett 2005; 225(1): 61–74, https://doi.org/10.1016/j.canlet.2004.11.041.
  74. Yang J.L., Qu X.J., Russell P.J., Goldstein D. Interferon-alpha promotes the anti-proliferative effect of gefitinib (ZD 1839) on human colon cancer cell lines. Oncology 2005; 69(3): 224–238, https://doi.org/10.1159/000088070.
  75. Slattery M.L., Lundgreen A., Bondurant K.L., Wolff R.K. Interferon-signaling pathway: associations with colon and rectal cancer risk and subsequent survival. Carcinogenesis 2011; 32(11): 1660–1667, https://doi.org/10.1093/carcin/bgr189.
  76. Molchanov O., Karelin M., Zharinov G. Current trends of recombinant interleukin 2 application in oncology. Tsitokiny i vospalenie 2002; 1(3): 38–47.
  77. Lu S., Pardini B., Cheng B., Naccarati A., Huhn S., Vymetalkova V., Vodickova L., Buchler T., Hemminki K., Vodicka P., Försti A. Single nucleotide polymorphisms within interferon signaling pathway genes are associated with colorectal cancer susceptibility and survival. PLoS One 2014; 9(10): e111061, https://doi.org/10.1371/journal.pone.0111061.
  78. Kjaer M. Combining 5-fluorouracil with interferon-alpha in the treatment of advanced colorectal cancer: optimism followed by disappointment. Anticancer Drugs 1996; 7: 35–42, https://doi.org/10.1097/00001813-199601000-00003.
  79. Link K.H., Kornmann M., Staib L., Redenbacher M., Kron M., Beger H.G.; Study Group Oncology of Gastrointestinal Tumors. Increase of survival benefit in advanced resectable colon cancer by extent of adjuvant treatment: results of a randomized trial comparing modulation of 5-FU + levamisole with folinic acid or with interferon-alpha. Ann Surg 2005; 242(2): 178–187, https://doi.org/10.1097/01.sla.0000171033.65639.a9.
  80. Joffe J.K., Perren T.J., Bradley C., Primrose J., Hallam S., Ward U., Illingworth J.M., Selby P.J. A phase II study of recombinant interferon-beta (r-hIFN-beta 1a) in combination with 5-fluorouracil (5-FU) in the treatment of patients with advanced colorectal carcinoma. Br J Cancer 1997; 75: 423–426, https://doi.org/10.1038/bjc.1997.69.
  81. Pavlidis N., Nicolaides C., Athanassiadis A., Beriatou K., Skarlos D., Giannakakis T., Kosmidis P., Karvounis N., Fountzilas G. Phase II study of 5-fluorouracil and interferon-gamma in patients with metastatic colorectal cancer. A Hellenic Cooperative Oncology Group Study. Oncology 1996; 53(2): 159–162.
  82. Correale P., Tagliaferri P., Fioravanti A., Del Vecchio M.T., Remondo C., Montagnani F., Rotundo M.S., Ginanneschi C., Martellucci I., Francini E., Cusi M.G., Tassone P., Francini G. Immunity feedback and clinical outcome in colon cancer patients undergoing chemoimmunotherapy with gemcitabine + FOLFOX followed by subcutaneous granulocyte macrophage colony-stimulating factor and aldesleukin (GOLFIG-1 Trial). Clin Cancer Res 2008; 14(13): 4192–4199, https://doi.org/10.1158/1078-0432.ccr-07-5278.
  83. Correale P., Botta C., Rotundo M.S., Guglielmo A., Conca R., Licchetta A., Pastina P., Bestoso E., Ciliberto D., Cusi M.G., Fioravanti A., Guidelli G.M., Bianco M.T., Misso G., Martino E., Caraglia M., Tassone P., Mini E., Mantovani G., Ridolfi R., Pirtoli L., Tagliaferri P. Gemcitabine, oxaliplatin, levofolinate, 5-fluorouracil, granulocyte-macrophage colony-stimulating factor, and interleukin-2 (GOLFIG) versus FOLFOX chemotherapy in metastatic colorectal cancer patients: the GOLFIG-2 multicentric open-label randomized phase III trial. J Immunother 2014; 37(1): 26–35, https://doi.org/10.1097/cji.0000000000000004.
  84. Goloshchapov R.S., Kokov L.S., Vishnevskiy V.A., Ionkin D.A., Elagina L.V. Regional arterial chemoembolization and chemoimmunoembolization in complex treatment of colon cancer with liver metastases. Khirurgiya 2003; 7: 66–71.
  85. Promzeleva N.V., Promzelev E.G., Shorokhova T.A., Dem’yanov V.S., Morozov V.P. Opyt primeneniya ronkoleykina — rekombinantnogo interleykina-2 — v khimioimmunoterapii rasprostranennogo kolorektal’nogo raka. V kn.: Materialy mezhregional’noy nauchno-prakticheskoy konferentsii “Kombinirovannye i kompleksnye metody lecheniya v onkologii” [Experience of Roncoleukin — recombinant interleukin-2 — application in chemoimmunotherapy of advanced colorectal cancer. In: Proceedings of interregional research and practice conference “Combined and complex treatment modalities in oncology”]. Barnaul; 2004; p. 106–109.
  86. Stupakova S.V., Teterin A.V. Regionarnaya vnutriarterial’naya khimioimmunoterapiya bol’nykh s metastazami kolorektal’nogo raka pecheni. V kn.: Materialy konferentsii “Sovremennye tekhnologii diagnostiki i lecheniya zlokachestvennykh opukholey” [Regional intraarterial chemoimmunotherapy of patients with liver metastases in colorectal cancer. In: Proceedings of the conference “Modern diagnostic and treatment technologies for malignant tumors”]. Saint Petersburg; 2005.
  87. Simbirtsev A.S. Achievements and perspectives of the recombinant cytokine therapy in clinical practice. Meditsinskiy akademicheskiy zhurnal 2013; 13(1): 7–22.
  88. Vigil A., Park M.S., Martinez O., Chua M.A., Xiao S., Cros J.F., Martínez-Sobrido L., Woo S.L., García-Sastre A. Use of reverse genetics to enhance the oncolytic properties of Newcastle disease virus. Cancer Res 2007; 67(17): 8285–8292, https://doi.org/10.1158/0008-5472.can-07-1025.
  89. Derubertis B.G., Stiles B.M., Bhargava A., Gusani N.J., Hezel M., D’Angelica M., Fong Y. Cytokine-secreting herpes viral mutants effectively treat tumor in a murine metastatic colorectal liver model by oncolytic and T-cell-dependent mechanisms. Cancer Gene Ther 2007; 14(6): 590–597, https://doi.org/10.1038/sj.cgt.7701053.
  90. Stephenson K.B., Barra N.G., Davies E., Ashkar A.A., Lichty B.D. Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of anti-tumor immunity. Cancer Gene Ther 2012; 19(4): 238–246, https://doi.org/10.1038/cgt.2011.81.
  91. Berezhnaya N.M., Chekhun V.F. Immunologiya zlokachestvennogo rosta [Malignant growth immunology]. Kiev: Naukova dumka; 2005; 792 p.
  92. Balkwill F. Tumour necrosis factor and cancer. Nat Rev Cancer 2009; 9(5): 361–371, https://doi.org/10.1038/nrc2628.
  93. Cui G., Yuan A., Goll R., Florholmen J. IL-17A in the tumor microenvironment of the human colorectal adenoma-carcinoma sequence. Scand J Gastroenterol 2012; 47(11): 1304–1312, https://doi.org/10.3109/00365521.2012.725089.
  94. Kryczek I., Lin Y., Nagarsheth N., Peng D., Zhao L., Zhao E., Vatan L., Szeliga W., Dou Y., Owens S., Zgodzinski W., Majewski M., Wallner G., Fang J., Huang E., Zou W. IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L. Immunity 2014; 40(5): 772–784, https://doi.org/10.1016/j.immuni.2014.03.010.
  95. Taniguchi K., Karin M. IL-6 and related cytokines as the critical lynchpins between inflammation and cancer. Semin Immunol 2014; 26(1): 54–74, https://doi.org/10.1016/j.smim.2014.01.001.
  96. Dai Y., Jiao H., Teng G., Wang W., Zhang R., Wang Y., Hebbard L., George J., Qiao L. Embelin reduces colitis-associated tumorigenesis through limiting IL-6/STAT3 signaling. Mol Cancer Ther 2014; 13(5): 1206–1216, https://doi.org/10.1158/1535-7163.mct-13-0378.
  97. Morris K.T., Castillo E.F., Ray A.L., Weston L.L., Nofchissey R.A., Hanson J.A., Samedi V.G., Pinchuk I.V., Hudson L.G., Beswick E.J. Anti-G-CSF treatment induces protective tumor immunity in mouse colon cancer by promoting protective NK cell, macrophage and T cell responses. Oncotarget 2015; 6(26): 22338–22347, https://doi.org/10.18632/oncotarget.4169.
  98. Kit O.I., Nabatova O.S., Zlatnik E.Y., Pavlenko S.G., Nistratova O.V. Dynamics of some parameters of cell-mediated ular immunity in patients with colorectal cancer in complex treatment by immunomodulators and antioxidants. Fundamental’nye issledovaniya 2014; 7–2: 286–289.
  99. Lake R.A., Robinson B.W. Immunotherapy and chemotherapy — a practical partnership. Nat Rev Cancer 2005; 5(5): 397–405, https://doi.org/10.1038/nrc1613.
  100. Rosenberg S.A., Lotze M.T., Muul L.M., Leitman S., Chang A.E., Vetto J.T., Seipp C.A., Simpson C. A new approach to the therapy of cancer based on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2. Surgery 1986; 100(2): 262–272.
  101. Schmidt-Wolf I.G., Negrin R.S., Kiem H.P., Blume K.G., Weissman I.L. Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med 1991; 174(1): 139–149, https://doi.org/10.1084/jem.174.1.139.
  102. Davydov M.I., Orazgel’dyev K.R., Volkov S.M., Kiselevskiy M.V. Adoptivnaya immunoterapiya opukholevykh plevritov. V kn.: Novoe v onkologii [Adoptive immunotherapy of tumor pleurites. In: New advances in incology]. Moscow; 2001; p. 75–78.
  103. Rosenberg S.A., Yang J.C., Sherry R.M., Kammula U.S., Hughes M.S., Phan G.Q., Citrin D.E., Restifo N.P., Robbins P.F., Wunderlich J.R., Morton K.E., Laurencot C.M., Steinberg S.M., White D.E., Dudley M.E. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17(13): 4550–4557, https://doi.org/10.1158/1078-0432.ccr-11-0116.
  104. Rosenberg S.A., Restifo N.P. Adoptive cell transfer as personalized immunotherapy for human cancer. Science 2015; 348(6230): 62–68, https://doi.org/10.1126/science.aaa4967.
  105. Zhang J., Zhu L., Zhang Q., He X., Yin Y., Gu Y., Guo R., Lu K., Liu L., Liu P., Shu Y. Effects of cytokine-induced killer cell treatment in colorectal cancer patients: a retrospective study. Biomed Pharmacother 2014; 68(6): 715–720, https://doi.org/10.1016/j.biopha.2014.07.010.
  106. Gao D., Li C., Xie X., Zhao P., Wei X., Sun W., Liu H.C., Alexandrou A.T., Jones J., Zhao R., Li J.J. Autologous tumor lysate-pulsed dendritic cell immunotherapy with cytokine-induced killer cells improves survival in gastric and colorectal cancer patients. PloS One 2014; 9(4): e93886, https://doi.org/10.1371/journal.pone.0093886.
  107. Niu J., Ren Y., Zhang T., Yang X., Zhu W., Zhu H., Li J., Li J., Pang Y. Retrospective comparative study of the effects of dendritic cell vaccine and cytokine-induced killer cell immunotherapy with that of chemotherapy alone and in combination for colorectal cancer. Biomed Res Int 2014; 2014: 214727, https://doi.org/10.1155/2014/214727.
  108. Zhu H., Yang X., Li J., Ren Y., Zhang T., Zhang C., Zhang J., Li J., Pang Y. Immune response, safety, and survival and quality of life outcomes for advanced colorectal cancer patients treated with dendritic cell vaccine and cytokine-induced killer cell therapy. Biomed Res Int 2014; 2014: 603871, https://doi.org/10.1155/2014/603871.
  109. Parkhurst M.R., Yang J.C., Langan R.C., Dudley M.E., Nathan D.N., Feldman S.A., Davis J.L., Morgan R.A., Merino M.J., Sherry R.M., Hughes M.S., Kammula U.S., Phan G.Q., Lim R.M., Wank S.A., Restifo N.P., Robbins P.F., Laurencot C.M., Rosenberg S.A. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011; 19(3): 620–626, https://doi.org/10.1038/mt.2010.272.
  110. Morgan R.A., Yang J.C., Kitano M., Dudley M.E., Laurencot C.M., Rosenberg S.A. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010; 18(4): 843–851, https://doi.org/10.1038/mt.2010.24.

Kit О.I., Kirichenko Е.Y., Novikova I.А., Maksimov А.Y., Filippova S.Y., Grankina А.О., Zlatnik Е.Y. Colorectal Cancer Immunotherapy: Current State and Prospects (Review). Sovremennye tehnologii v medicine 2017; 9(3): 138, https://doi.org/10.17691/stm2017.9.3.18


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