5,583
Views
4
CrossRef citations to date
0
Altmetric
Research Article

T cell-mediated elimination of cancer cells by blocking CEACAM6–CEACAM1 interaction

, , , , , , , , , , , , , , , , , , , , , , , , , , , , , & show all
Article: 2008110 | Received 17 Jun 2021, Accepted 15 Nov 2021, Published online: 30 Dec 2021

References

  • Horna P, Sotomayor EM. Cellular and molecular mechanisms of tumor-induced T-cell tolerance. Curr Cancer Drug Targets. 2007;7(1):41–17. doi:10.2174/156800907780006940.
  • Pardoll DM. Immunology beats cancer: a blueprint for successful translation. Nat Immunol. 2012;13(12):1129–1132. doi:10.1038/ni.2392.
  • Yang L, Carbone DP. Tumor-host immune interactions and dendritic cell dysfunction. Adv Cancer Res. 2004;92:13–27.
  • Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348(6230):56–61. doi:10.1126/science.aaa8172.
  • Henick BS, Herbst RS, Goldberg SB. The PD-1 pathway as a therapeutic target to overcome immune escape mechanisms in cancer. Expert Opin Ther Targets. 2014;18(12):1407–1420. doi:10.1517/14728222.2014.955794.
  • Beauchemin N, Arabzadeh A. Carcinoembryonic antigen-related cell adhesion molecules (CEACAMs) in cancer progression and metastasis. Cancer Metastasis Rev. 2013;32(3–4):643–671. doi:10.1007/s10555-013-9444-6.
  • Obrink B. CEA adhesion molecules: multifunctional proteins with signal-regulatory properties. Curr Opin Cell Biol. 1997;9(5):616–626. doi:10.1016/S0955-0674(97)80114-7.
  • Kuespert K, Pils S, Hauck CR. CEACAMs: their role in physiology and pathophysiology. Curr Opin Cell Biol. 2006;18(5):565–571. doi:10.1016/j.ceb.2006.08.008.
  • Gur C, Maalouf N, Gerhard M, Singer BB, Emgard J, Temper V, Neuman T, Mandelboim O, Bachrach G. The Helicobacter pylori HopQ outermembrane protein inhibits immune cell activities. Oncoimmunology. 2019;8(4):e1553487. doi:10.1080/2162402X.2018.1553487.
  • Gur C, Maalouf N, Shhadeh A, Berhani O, Singer BB, Bachrach G, Mandelboim O. Fusobacterium nucleatum supresses anti-tumor immunity by activating CEACAM1. Oncoimmunology. 2019;8(6):e1581531. doi:10.1080/2162402X.2019.1581531.
  • Gray-Owen SD, Blumberg RS. CEACAM1: contact-dependent control of immunity. Nat Rev Immunol. 2006;6(6):433–446. doi:10.1038/nri1864.
  • Kammerer R, Hahn S, Singer BB, Luo JS, Von Kleist S, Von Kleist S. Biliary glycoprotein (CD66a), a cell adhesion molecule of the immunoglobulin superfamily, on human lymphocytes: structure, expression and involvement in T cell activation. Eur J Immunol. 1998;28(11):3664–3674. doi:10.1002/(SICI)1521-4141(199811)28:11<3664::AID-IMMU3664>3.0.CO;2-D.
  • Singer BB, Scheffrahn I, Heymann R, Sigmundsson K, Kammerer R, Obrink B. Carcinoembryonic antigen-related cell adhesion molecule 1 expression and signaling in human, mouse, and rat leukocytes: evidence for replacement of the short cytoplasmic domain isoform by glycosylphosphatidylinositol-linked proteins in human leukocytes. J Immunol. 2002;168(10):5139–5146. doi:10.4049/jimmunol.168.10.5139.
  • Witzens-Harig M, Hose D, Junger S, Pfirschke C, Khandelwal N, Umansky L, Seckinger A, Conrad H, Brackertz B, Rème T, et al. Tumor cells in multiple myeloma patients inhibit myeloma-reactive T cells through carcinoembryonic antigen-related cell adhesion molecule-6. Blood. 2013;121(22):4493–4503. doi:10.1182/blood-2012-05-429415.
  • Blumenthal RD, Leon E, Hansen HJ, Goldenberg DM. Expression patterns of CEACAM5 and CEACAM6 in primary and metastatic cancers. BMC Cancer. 2007;7(1):2. doi:10.1186/1471-2407-7-2.
  • Deng X, Liu P, Zhao Y, Wang Q Expression profiling of CEACAM6 associated with the tumorigenesis and progression in gastric adenocarcinoma. Genet Mol Res. 2014;13(3):7686–7697. doi:10.4238/2014.September.26.6.
  • Duxbury MS, Matros E, Clancy T, Bailey G, Doff M, Zinner MJ, Ashley SW, Maitra A, Redston M, Whang EE, et al. CEACAM6 is a novel biomarker in pancreatic adenocarcinoma and PanIN lesions. Ann Surg. 2005;241(3):491–496. doi:10.1097/01.sla.0000154455.86404.e9.
  • Jantscheff P, Terracciano L, Lowy A, Glatz-Krieger K, Grunert F, Micheel B, Brümmer J, Laffer U, Metzger U, Herrmann R, et al. Expression of CEACAM6 in resectable colorectal cancer: a factor of independent prognostic signi ficance. J Clin Oncol. 2003;21(19):3638–3646. doi:10.1200/JCO.2003.55.135.
  • Strickland LA, Ross J, Williams S, Ross S, Romero M, Spencer S, Erickson R, Sutcliffe J, Verbeke C, Polakis P, et al. Preclinical evaluation of carcinoembryonic cell adhesion molecule (CEACAM) 6 as potential therapy target for pancreatic adenocarcinoma. J Pathol. 2009;218(3):380–390. doi:10.1002/path.2545.
  • Kim KS, Kim JT, Lee SJ, Kang MA, Choe IS, Kang YH, Kim S-Y, Yeom YI, Lee Y-H, Kim JH, et al. Overexpression and clinical significance of carcinoembryonic antigen-related cell adhesion molecule 6 in colorectal cancer. Clin Chim Acta. 2013;415:12–19. doi:10.1016/j.cca.2012.09.003.
  • Kobayashi M, Miki Y, Ebina M, Abe K, Mori K, Narumi S, Suzuki T, Sato I, Maemondo M, Endo C, et al. Carcinoembryonic antigen-related cell adhesion molecules as surrogate markers for EGFR inhibitor sensitivity in human lung adenocarcinoma. Br J Cancer. 2012;107(10):1745–1753. doi:10.1038/bjc.2012.422.
  • Zang M, Hu L, Cao S, Fan Z, Pang L, Li J, Su L, Li C, Liu W, Gu Q, et al. Dual role of carcinoembryonic antigen-related cell adhesion molecule 6 expression in predicting the overall survival of gastric cancer patients. Sci Rep. 2017;7(1):10773. doi:10.1038/s41598-017-11482-9.
  • Zang M, Zhang B, Zhang Y, Li J, Su L, Zhu Z, Gu Q, Liu B, Yan M. CEACAM6 promotes gastric cancer invasion and metastasis by inducing epithelial-mesenchymal transition via PI3K/AKT signaling pathway. PLoS One. 2014;9(11):e112908. doi:10.1371/journal.pone.0112908.
  • Burtin P, Quan PC, Sabine MC Nonspecific cross reacting antigen as a marker for human polymorphs, macrophages and monocytes. Nature. 1975;255(5511):714–716. doi:10.1038/255714a0.
  • Liu Y, Xia T, Jin C, Gu D, Yu J, Shi W, Zhang KE, Zhang L, Ye J, Li L, et al. FOXP3 and CEACAM6 expression and T cell infiltration in the occurrence and development of colon cancer. Oncol Lett. 2016;11(6):3693–3701. doi:10.3892/ol.2016.4439.
  • Kuroki M, Matsuo Y, Kinugasa T, Matsuoka Y Three different NCA species, CGM6/CD67, NCA-95, and NCA-90, are comprised in the major 90 to 100-kDa band of granulocyte NCA detectable upon SDS-polyacrylamide gel electrophoresis. Biochem Biophys Res Commun. 1992;182(2):501–506. doi:10.1016/0006-291X(92)91760-N.
  • Kolla V, Gonzales LW, Bailey NA, Wang P, Angampalli S, Godinez MH, Madesh M, Ballard PL Carcinoembryonic cell adhesion molecule 6 in human lung: regulated expression of a multifunctional type II cell protein. Am J Physiol Lung Cell Mol Physiol. 2009;296(6):L1019–30. doi:10.1152/ajplung.90596.2008.
  • Chan CH, Stanners CP Novel mouse model for carcinoembryonic antigen-based therapy. Mol Ther. 2004;9(6):775–785. doi:10.1016/j.ymthe.2004.03.009.
  • Scholzel S, Zimmermann W, Schwarzkopf G, Grunert F, Rogaczewski B, Thompson J Carcinoembryonic antigen family members CEACAM6 and CEACAM7 are differentially expressed in normal tissues and oppositely deregulated in hyperplastic colorectal polyps and early adenomas. Am J Pathol. 2000;156(2):595–605. doi:10.1016/S0002-9440(10)64764-5.
  • Kammerer R, Zimmermann W. Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol. 2010;8(1):12. doi:10.1186/1741-7007-8-12.
  • Pavlopoulou A, Scorilas A A comprehensive phylogenetic and structural analysis of the carcinoembryonic antigen (CEA) gene family. Genome Biol Evol. 2014;6(6):1314–1326. doi:10.1093/gbe/evu103.
  • Daniel S, Nagel G, Johnson JP, Lobo FM, Hirn M, Jantscheff P, Kuroki, M, von Kleist, S, Grunert, F. Determination of the specificities of monoclonal antibodies recognizing members of the CEA family using a panel of transfectants. Int J Cancer. 1993;55(2):303–310. doi:10.1002/ijc.2910550222.
  • Jantscheff P, Nagel G, Thompson J, Kleist SV, Embleton MJ, Price MR, Grunert, F.A CD66a-specific, activation-dependent epitope detected by recombinant human single chain fragments (scFvs) on CHO transfectants and activated granulocytes. J Leukoc Biol. 1996;59(6):891–901. doi:10.1002/jlb.59.6.891.
  • Du X, Luka J, Stafford LJ, Semenuk M, Wang X-P, Kantor J, Bristol , AJ.Colon and pancreas cancer specific antigens and antibodies. Patent US20130189268. 2013.
  • Fantini M, David JM, Saric O, Dubeykovskiy A, Cui Y, Mavroukakis SA, Bristol A, Annunziata CM, Tsang KY, Arlen PM, et al. Preclinical characterization of a novel monoclonal antibody NEO-201 for the treatment of human carcinomas. Front Immunol. 2018;8:1899. doi:10.3389/fimmu.2017.01899.
  • Zeligs K, Arlen PM, Tsang K, Hernandez L, Fantini M, Annunziata CM. Preclinical characterization of a novel monoclonal antibody targeting a neo-antigen expressed in ovarian and GI malignancies. Cancer Res. 2017; 77:3025.
  • Markel G inventor. Antibodies to carcinoembryonic antigen-related cell adhesion molecule (CEACAM). Patent WO2013054320. 2013.
  • Brackertz B, Conrad H, Daniel J, Kast B, Kronig H, Busch DH, Adamski, J, Peschel, C, Bernhard, H.FLT3-regulated antigens as targets for leukemia-reactive cytotoxic T lymphocytes. Blood Cancer J. 2011;1(3):e11. doi:10.1038/bcj.2011.12.
  • Moosmann A. Gezielte Reaktivierung spezifischer zytotoxischer T-Zellen mit Epstein-Barr-Virus-Vektoren. Germany: Ludwig-Maximilians-University Munich; 2002.
  • Kuroki M, Matsuo Y, Kinugasa T, Matsuoka Y Augmented expression and release of nonspecific cross-reacting antigens (NCAs), members of the CEA family, by human neutrophils during cell activation. J Leukoc Biol. 1992;52(5):551–557. doi:10.1002/jlb.52.5.551.
  • Poschke I, Faryna M, Bergmann F, Flossdorf M, Lauenstein C, Hermes J, Hinz, U, Hank, T, Ehrenberg, R, Volkmar, M, et al. Identification of a tumor-reactive T-cell repertoire in the immune infiltrate of patients with resectable pancreatic ductal adenocarcinoma. Oncoimmunology. 2016;5(12):e1240859. doi:10.1080/2162402X.2016.1240859.
  • Guo X, Zhang Y, Zheng L, Zheng C, Song J, Zhang Q, Kang, B, Liu, Z, Jin, L, Xing, R, et al. Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing. Nat Med. 2018;24(7):978–985. doi:10.1038/s41591-018-0045-3.
  • Jerby-Arnon L, Shah P, Cuoco MS, Rodman C, Su MJ, Melms JC, Leeson R, Kanodia A, Mei S, Lin J-R, et al. A cancer cell program promotes T cell exclusion and resistance to checkpoint blockade. Cell. 2018;175(4):984–97 e24. doi:10.1016/j.cell.2018.09.006.
  • Chen Z, Chen L, Qiao SW, Nagaishi T, Blumberg RS Carcinoembryonic antigen-related cell adhesion molecule 1 inhibits proximal TCR signaling by targeting ZAP-70. J Immunol. 2008;180(9):6085–6093. doi:10.4049/jimmunol.180.9.6085.
  • Reissfelder C, Stamova S, Gossmann C, Braun M, Bonertz A, Walliczek U, Grimm M, Rahbari NN, Koch M, Saadati M, et al. Tumor-specific cytotoxic T lymphocyte activity determines colorectal cancer patient prognosis. J Clin Invest. 2015;125(2):739–751. doi:10.1172/JCI74894.
  • Slevogt H, Zabel S, Opitz B, Hocke A, Eitel J, N’Guessan PD, Lucka L, Riesbeck K, Zimmermann W, Zweigner J, et al. CEACAM1 inhibits Toll-like receptor 2-triggered antibacterial responses of human pulmonary epithelial cells. Nat Immunol. 2008;9(11):1270–1278. doi:10.1038/ni.1661.
  • Khairnar V, Duhan V, Maney SK, Honke N, Shaabani N, Pandyra AA, Seifert M, Pozdeev V, Xu HC, Sharma P, et al. CEACAM1 induces B-cell survival and is essential for protective antiviral antibody production. Nat Commun. 2015;6:6217. doi:10.1038/ncomms7217.
  • Xydia M, Rahbari R, Ruggiero E, Macaulay I, Tarabichi M, Lohmayer R, Wilkening S, Michels T, Brown D, Vanuytven S, et al. Common clonal origin of conventional T cells and induced regulatory T cells in breast cancer patients. Nat Commun. 2021;12(1):1119. doi:10.1038/s41467-021-21297-y.
  • Ramani SR, Tom I, Lewin-Koh N, Wranik B, Depalatis L, Zhang J, Eaton D, Gonzalez LC A secreted protein microarray platform for extracellular protein interaction discovery. Anal Biochem. 2012;420(2):127–138. doi:10.1016/j.ab.2011.09.017.
  • Nagaishi T, Pao L, Lin SH, Iijima H, Kaser A, Qiao SW, Chen Z, Glickman J, Najjar SM, Nakajima A, et al. SHP1 phosphatase-dependent T cell inhibition by CEACAM1 adhesion molecule isoforms. Immunity. 2006;25(5):769–781. doi:10.1016/j.immuni.2006.08.026.
  • Shapira R, Weber JS, Geva R, Sznol M, Kluger HM, Wong DJL, Liang BC A phase I, open-label, multicenter, single-dose escalation and multi-dose study of a monoclonal antibody targeting CEACAM1 in subjects with selected advanced or recurrent malignancies. Journal of Clinical Oncology. 2020;38(15suppl). doi:10.1200/JCO.2020.38.15_suppl.3094.
  • De La Rochere P, Guil-Luna S, Decaudin D, Azar G, Sidhu SS, Piaggio E Humanized mice for the study of immuno-oncology. Trends Immunol. 2018;39(9):748–763. doi:10.1016/j.it.2018.07.001.
  • Stripecke R, Munz C, Schuringa JJ, Bissig KD, Soper B, Meeham T, Yao, L-C, Di Santo, JP, Brehm, M, Rodriguez, E, et al. Innovations, challenges, and minimal information for standardization of humanized mice. EMBO Mol Med. 2020;12(7):e8662. doi:10.15252/emmm.201708662.