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Erschienen in: Seminars in Immunopathology 3/2019

05.04.2019 | Review

A new therapeutic target: the CD69-Myl9 system in immune responses

verfasst von: Motoko Y. Kimura, Ryo Koyama-Nasu, Ryoji Yagi, Toshinori Nakayama

Erschienen in: Seminars in Immunopathology | Ausgabe 3/2019

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Abstract

CD69 is an activation marker on leukocytes. Early studies showed that the CD69+ cells were detected in the lung of patients with asthmatic and eosinophilic pneumonia, suggesting that CD69 might play crucial roles in the pathogenesis of such inflammatory diseases, rather than simply being an activation marker. Intensive studies using mouse models have since clarified that CD69 is a functional molecule regulating the immune responses. We discovered that Myosin light chain 9, 12a, 12b (Myl9/12) are ligands for CD69 and that platelet-derived Myl9 forms a net-like structure (Myl9 nets) that is strongly detected inside blood vessels in inflamed lung. CD69-expressing activated T cells attached to the Myl9 nets can thereby migrate into the inflamed tissues through a system known as the CD69-Myl9 system. In this review, we summarize the discovery of the CD69-Myl9 system and discuss how this system is important in inflammatory immune responses. In addition, we discuss our recent finding that CD69 controls the exhaustion status of tumor-infiltrating T cells and that the blockade of the CD69 function enhances anti-tumor immunity. Finally, we discuss the possibility of CD69 as a new therapeutic target for patients with intractable inflammatory disorders and tumors
Literatur
1.
Zurück zum Zitat Ziegler SF, Ramsdell F, Hjerrild KA, Armitage RJ, Grabstein KH, Hennen KB, Farrah T, Fanslow WC, Shevach EM, Alderson MR (1993) Molecular characterization of the early activation antigen CD69: a type II membrane glycoprotein related to a family of natural killer cell activation antigens. Eur J Immunol 23:1643–1648CrossRefPubMed Ziegler SF, Ramsdell F, Hjerrild KA, Armitage RJ, Grabstein KH, Hennen KB, Farrah T, Fanslow WC, Shevach EM, Alderson MR (1993) Molecular characterization of the early activation antigen CD69: a type II membrane glycoprotein related to a family of natural killer cell activation antigens. Eur J Immunol 23:1643–1648CrossRefPubMed
2.
Zurück zum Zitat Lopez-Cabrera M, Santis AG, Fernandez-Ruiz E, Blacher R, Esch F, Sanchez-Mateos P, Sanchez-Madrid F (1993) Molecular cloning, expression, and chromosomal localization of the human earliest lymphocyte activation antigen AIM/CD69, a new member of the C-type animal lectin superfamily of signal-transmitting receptors. J Exp Med 178:537–547CrossRefPubMed Lopez-Cabrera M, Santis AG, Fernandez-Ruiz E, Blacher R, Esch F, Sanchez-Mateos P, Sanchez-Madrid F (1993) Molecular cloning, expression, and chromosomal localization of the human earliest lymphocyte activation antigen AIM/CD69, a new member of the C-type animal lectin superfamily of signal-transmitting receptors. J Exp Med 178:537–547CrossRefPubMed
3.
Zurück zum Zitat Kimura MY, Hayashizaki K, Tokoyoda K, Takamura S, Motohashi S, Nakayama T (2017) Crucial role for CD69 in allergic inflammatory responses: CD69-Myl9 system in the pathogenesis of airway inflammation. Immunol Rev 278:87–100CrossRefPubMed Kimura MY, Hayashizaki K, Tokoyoda K, Takamura S, Motohashi S, Nakayama T (2017) Crucial role for CD69 in allergic inflammatory responses: CD69-Myl9 system in the pathogenesis of airway inflammation. Immunol Rev 278:87–100CrossRefPubMed
4.
Zurück zum Zitat Llera AS, Viedma F, Sanchez-Madrid F, Tormo J (2001) Crystal structure of the C-type lectin-like domain from the human hematopoietic cell receptor CD69. J Biol Chem 276:7312–7319CrossRefPubMed Llera AS, Viedma F, Sanchez-Madrid F, Tormo J (2001) Crystal structure of the C-type lectin-like domain from the human hematopoietic cell receptor CD69. J Biol Chem 276:7312–7319CrossRefPubMed
5.
Zurück zum Zitat Lin CR, Wei TY, Tsai HY, Wu YT, Wu PY, Chen ST (2015) Glycosylation-dependent interaction between CD69 and S100A8/S100A9 complex is required for regulatory T-cell differentiation. FASEB J 29:5006–5017CrossRefPubMed Lin CR, Wei TY, Tsai HY, Wu YT, Wu PY, Chen ST (2015) Glycosylation-dependent interaction between CD69 and S100A8/S100A9 complex is required for regulatory T-cell differentiation. FASEB J 29:5006–5017CrossRefPubMed
6.
Zurück zum Zitat de la Fuente H, Cruz-Adalia A, Martinez Del Hoyo G, Cibrian-Vera D, Bonay P, Perez-Hernandez D, Vazquez J, Navarro P, Gutierrez-Gallego R, Ramirez-Huesca M, Martin P, Sanchez-Madrid F (2014) The leukocyte activation receptor CD69 controls T cell differentiation through its interaction with galectin-1. Mol Cell Biol 34:2479–2487CrossRefPubMedPubMedCentral de la Fuente H, Cruz-Adalia A, Martinez Del Hoyo G, Cibrian-Vera D, Bonay P, Perez-Hernandez D, Vazquez J, Navarro P, Gutierrez-Gallego R, Ramirez-Huesca M, Martin P, Sanchez-Madrid F (2014) The leukocyte activation receptor CD69 controls T cell differentiation through its interaction with galectin-1. Mol Cell Biol 34:2479–2487CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Hayashizaki K, Kimura MY, Tokoyoda K, Hosokawa H, Shinoda K, Hirahara K, Ichikawa T, Onodera A, Hanazawa A, Iwamura C, Kakuta J, Muramoto K, Motohashi S, Tumes DJ, Iinuma T, Yamamoto H, Ikehara Y, Okamoto H, Nakayama T (2016) Myosin light chains 9 and 12 are functional ligands for CD69 that regulate airway inflammation. Sci Immunol 1:eaaf9154CrossRefPubMed Hayashizaki K, Kimura MY, Tokoyoda K, Hosokawa H, Shinoda K, Hirahara K, Ichikawa T, Onodera A, Hanazawa A, Iwamura C, Kakuta J, Muramoto K, Motohashi S, Tumes DJ, Iinuma T, Yamamoto H, Ikehara Y, Okamoto H, Nakayama T (2016) Myosin light chains 9 and 12 are functional ligands for CD69 that regulate airway inflammation. Sci Immunol 1:eaaf9154CrossRefPubMed
8.
Zurück zum Zitat Mendez-Huergo SP, Blidner AG, Rabinovich GA (2017) Galectins: emerging regulatory checkpoints linking tumor immunity and angiogenesis. Curr Opin Immunol 45:8–15CrossRefPubMed Mendez-Huergo SP, Blidner AG, Rabinovich GA (2017) Galectins: emerging regulatory checkpoints linking tumor immunity and angiogenesis. Curr Opin Immunol 45:8–15CrossRefPubMed
9.
Zurück zum Zitat Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 176:778–789CrossRefPubMed Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 176:778–789CrossRefPubMed
10.
Zurück zum Zitat Starossom SC, Mascanfroni ID, Imitola J, Cao L, Raddassi K, Hernandez SF, Bassil R, Croci DO, Cerliani JP, Delacour D, Wang Y, Elyaman W, Khoury SJ, Rabinovich GA (2012) Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 37:249–263CrossRefPubMedPubMedCentral Starossom SC, Mascanfroni ID, Imitola J, Cao L, Raddassi K, Hernandez SF, Bassil R, Croci DO, Cerliani JP, Delacour D, Wang Y, Elyaman W, Khoury SJ, Rabinovich GA (2012) Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration. Immunity 37:249–263CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Bonzi J, Bornet O, Betzi S, Kasper BT, Mahal LK, Mancini SJ, Schiff C, Sebban-Kreuzer C, Guerlesquin F, Elantak L (2015) Pre-B cell receptor binding to galectin-1 modifies galectin-1/carbohydrate affinity to modulate specific galectin-1/glycan lattice interactions. Nat Commun 6:6194CrossRefPubMed Bonzi J, Bornet O, Betzi S, Kasper BT, Mahal LK, Mancini SJ, Schiff C, Sebban-Kreuzer C, Guerlesquin F, Elantak L (2015) Pre-B cell receptor binding to galectin-1 modifies galectin-1/carbohydrate affinity to modulate specific galectin-1/glycan lattice interactions. Nat Commun 6:6194CrossRefPubMed
12.
Zurück zum Zitat Gebhardt C, Nemeth J, Angel P, Hess J (2006) S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72:1622–1631CrossRefPubMed Gebhardt C, Nemeth J, Angel P, Hess J (2006) S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72:1622–1631CrossRefPubMed
13.
Zurück zum Zitat Testi R, Pulcinelli F, Frati L, Gazzaniga PP, Santoni A (1990) CD69 is expressed on platelets and mediates platelet activation and aggregation. J Exp Med 172:701–707CrossRefPubMed Testi R, Pulcinelli F, Frati L, Gazzaniga PP, Santoni A (1990) CD69 is expressed on platelets and mediates platelet activation and aggregation. J Exp Med 172:701–707CrossRefPubMed
14.
Zurück zum Zitat Testi R, D’Ambrosio D, De Maria R, Santoni A (1994) The CD69 receptor: a multipurpose cell-surface trigger for hematopoietic cells. Immunol Today 15:479–483CrossRefPubMed Testi R, D’Ambrosio D, De Maria R, Santoni A (1994) The CD69 receptor: a multipurpose cell-surface trigger for hematopoietic cells. Immunol Today 15:479–483CrossRefPubMed
15.
Zurück zum Zitat Gonzalez-Amaro R, Cortes JR, Sanchez-Madrid F, Martin P (2013) Is CD69 an effective brake to control inflammatory diseases? Trends Mol Med 19:625–632CrossRefPubMedPubMedCentral Gonzalez-Amaro R, Cortes JR, Sanchez-Madrid F, Martin P (2013) Is CD69 an effective brake to control inflammatory diseases? Trends Mol Med 19:625–632CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Martin P, Gomez M, Lamana A, Cruz-Adalia A, Ramirez-Huesca M, Ursa MA, Yanez-Mo M, Sanchez-Madrid F (2010) CD69 association with Jak3/Stat5 proteins regulates Th17 cell differentiation. Mol Cell Biol 30:4877–4889CrossRefPubMedPubMedCentral Martin P, Gomez M, Lamana A, Cruz-Adalia A, Ramirez-Huesca M, Ursa MA, Yanez-Mo M, Sanchez-Madrid F (2010) CD69 association with Jak3/Stat5 proteins regulates Th17 cell differentiation. Mol Cell Biol 30:4877–4889CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Cyster JG, Schwab SR (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 30:69–94CrossRefPubMed Cyster JG, Schwab SR (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 30:69–94CrossRefPubMed
18.
Zurück zum Zitat Bankovich AJ, Shiow LR, Cyster JG (2010) CD69 suppresses sphingosine 1-phosophate receptor-1 (S1P1) function through interaction with membrane helix 4. J Biol Chem 285:22328–22337CrossRefPubMedPubMedCentral Bankovich AJ, Shiow LR, Cyster JG (2010) CD69 suppresses sphingosine 1-phosophate receptor-1 (S1P1) function through interaction with membrane helix 4. J Biol Chem 285:22328–22337CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4:397–407CrossRefPubMed Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4:397–407CrossRefPubMed
20.
Zurück zum Zitat Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544CrossRefPubMed Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544CrossRefPubMed
21.
Zurück zum Zitat Feng C, Woodside KJ, Vance BA, El-Khoury D, Canelles M, Lee J, Gress R, Fowlkes BJ, Shores EW, Love PE (2002) A potential role for CD69 in thymocyte emigration. Int Immunol 14:535–544CrossRefPubMed Feng C, Woodside KJ, Vance BA, El-Khoury D, Canelles M, Lee J, Gress R, Fowlkes BJ, Shores EW, Love PE (2002) A potential role for CD69 in thymocyte emigration. Int Immunol 14:535–544CrossRefPubMed
22.
Zurück zum Zitat Nakayama T, Kasprowicz DJ, Yamashita M, Schubert LA, Gillard G, Kimura M, Didierlaurent A, Koseki H, Ziegler SF (2002) The generation of mature, single-positive thymocytes in vivo is dysregulated by CD69 blockade or overexpression. J Immunol 168:87–94CrossRefPubMed Nakayama T, Kasprowicz DJ, Yamashita M, Schubert LA, Gillard G, Kimura M, Didierlaurent A, Koseki H, Ziegler SF (2002) The generation of mature, single-positive thymocytes in vivo is dysregulated by CD69 blockade or overexpression. J Immunol 168:87–94CrossRefPubMed
23.
Zurück zum Zitat Zachariah MA, Cyster JG (2010) Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328:1129–1135CrossRefPubMedPubMedCentral Zachariah MA, Cyster JG (2010) Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science 328:1129–1135CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Murata K, Inami M, Hasegawa A, Kubo S, Kimura M, Yamashita M, Hosokawa H, Nagao T, Suzuki K, Hashimoto K, Shinkai H, Koseki H, Taniguchi M, Ziegler SF, Nakayama T (2003) CD69-null mice protected from arthritis induced with anti-type II collagen antibodies. Int Immunol 15:987–992CrossRefPubMed Murata K, Inami M, Hasegawa A, Kubo S, Kimura M, Yamashita M, Hosokawa H, Nagao T, Suzuki K, Hashimoto K, Shinkai H, Koseki H, Taniguchi M, Ziegler SF, Nakayama T (2003) CD69-null mice protected from arthritis induced with anti-type II collagen antibodies. Int Immunol 15:987–992CrossRefPubMed
25.
Zurück zum Zitat Lauzurica P, Sancho D, Torres M, Albella B, Marazuela M, Merino T, Bueren JA, Martinez AC, Sanchez-Madrid F (2000) Phenotypic and functional characteristics of hematopoietic cell lineages in CD69-deficient mice. Blood 95:2312–2320PubMed Lauzurica P, Sancho D, Torres M, Albella B, Marazuela M, Merino T, Bueren JA, Martinez AC, Sanchez-Madrid F (2000) Phenotypic and functional characteristics of hematopoietic cell lineages in CD69-deficient mice. Blood 95:2312–2320PubMed
26.
Zurück zum Zitat Kimura MY, Igi A, Hayashizaki K, Mita Y, Shinzawa M, Kadakia T, Endo Y, Ogawa S, Yagi R, Motohashi S, Singer A, Nakayama T (2018) CD69 prevents PLZF(hi) innate precursors from prematurely exiting the thymus and aborting NKT2 cell differentiation. Nat Commun 9:3749CrossRefPubMedPubMedCentral Kimura MY, Igi A, Hayashizaki K, Mita Y, Shinzawa M, Kadakia T, Endo Y, Ogawa S, Yagi R, Motohashi S, Singer A, Nakayama T (2018) CD69 prevents PLZF(hi) innate precursors from prematurely exiting the thymus and aborting NKT2 cell differentiation. Nat Commun 9:3749CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Hall JG, Morris B (1965) The immediate effect of antigens on the cell output of a lymph node. Br J Exp Pathol 46:450–454PubMedPubMedCentral Hall JG, Morris B (1965) The immediate effect of antigens on the cell output of a lymph node. Br J Exp Pathol 46:450–454PubMedPubMedCentral
28.
Zurück zum Zitat Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci U S A 107:20447–20452CrossRefPubMedPubMedCentral Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci U S A 107:20447–20452CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Miki-Hosokawa T, Hasegawa A, Iwamura C, Shinoda K, Tofukuji S, Watanabe Y, Hosokawa H, Motohashi S, Hashimoto K, Shirai M, Yamashita M, Nakayama T (2009) CD69 controls the pathogenesis of allergic airway inflammation. J Immunol 183:8203–8215CrossRefPubMed Miki-Hosokawa T, Hasegawa A, Iwamura C, Shinoda K, Tofukuji S, Watanabe Y, Hosokawa H, Motohashi S, Hashimoto K, Shirai M, Yamashita M, Nakayama T (2009) CD69 controls the pathogenesis of allergic airway inflammation. J Immunol 183:8203–8215CrossRefPubMed
31.
Zurück zum Zitat Wang HY, Dai Y, Wang JL, Yang XY, Jiang XG (2015) Anti-CD69 monoclonal antibody treatment inhibits airway inflammation in a mouse model of asthma. J Zhejiang Univ Sci B 16:622–631CrossRefPubMedPubMedCentral Wang HY, Dai Y, Wang JL, Yang XY, Jiang XG (2015) Anti-CD69 monoclonal antibody treatment inhibits airway inflammation in a mouse model of asthma. J Zhejiang Univ Sci B 16:622–631CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Tsuyusaki J, Kuroda F, Kasuya Y, Ishizaki S, Yamauchi K, Sugimoto H, Kono T, Iwamura C, Nakayama T, Tatsumi K (2011) Cigarette smoke-induced pulmonary inflammation is attenuated in CD69-deficient mice. J Recept Signal Transduct Res 31:434–439CrossRefPubMed Tsuyusaki J, Kuroda F, Kasuya Y, Ishizaki S, Yamauchi K, Sugimoto H, Kono T, Iwamura C, Nakayama T, Tatsumi K (2011) Cigarette smoke-induced pulmonary inflammation is attenuated in CD69-deficient mice. J Recept Signal Transduct Res 31:434–439CrossRefPubMed
33.
Zurück zum Zitat Yamauchi K, Kasuya Y, Kuroda F, Tanaka K, Tsuyusaki J, Ishizaki S, Matsunaga H, Iwamura C, Nakayama T, Tatsumi K (2011) Attenuation of lung inflammation and fibrosis in CD69-deficient mice after intratracheal bleomycin. Respir Res 12:131CrossRefPubMedPubMedCentral Yamauchi K, Kasuya Y, Kuroda F, Tanaka K, Tsuyusaki J, Ishizaki S, Matsunaga H, Iwamura C, Nakayama T, Tatsumi K (2011) Attenuation of lung inflammation and fibrosis in CD69-deficient mice after intratracheal bleomycin. Respir Res 12:131CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Hasegawa A, Iwamura C, Kitajima M, Hashimoto K, Otsuyama K, Ogino H, Nakayama T, Shirai M (2013) Crucial role for CD69 in the pathogenesis of dextran sulphate sodium-induced colitis. PLoS One 8:e65494CrossRefPubMedPubMedCentral Hasegawa A, Iwamura C, Kitajima M, Hashimoto K, Otsuyama K, Ogino H, Nakayama T, Shirai M (2013) Crucial role for CD69 in the pathogenesis of dextran sulphate sodium-induced colitis. PLoS One 8:e65494CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Radulovic K, Manta C, Rossini V, Holzmann K, Kestler HA, Wegenka UM, Nakayama T, Niess JH (2012) CD69 regulates type I IFN-induced tolerogenic signals to mucosal CD4 T cells that attenuate their colitogenic potential. J Immunol 188:2001–2013CrossRefPubMed Radulovic K, Manta C, Rossini V, Holzmann K, Kestler HA, Wegenka UM, Nakayama T, Niess JH (2012) CD69 regulates type I IFN-induced tolerogenic signals to mucosal CD4 T cells that attenuate their colitogenic potential. J Immunol 188:2001–2013CrossRefPubMed
36.
Zurück zum Zitat Radulovic K, Rossini V, Manta C, Holzmann K, Kestler HA, Niess JH (2013) The early activation marker CD69 regulates the expression of chemokines and CD4 T cell accumulation in intestine. PLoS One 8:e65413CrossRefPubMedPubMedCentral Radulovic K, Rossini V, Manta C, Holzmann K, Kestler HA, Niess JH (2013) The early activation marker CD69 regulates the expression of chemokines and CD4 T cell accumulation in intestine. PLoS One 8:e65413CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Cortes JR, Sanchez-Diaz R, Bovolenta ER, Barreiro O, Lasarte S, Matesanz-Marin A, Toribio ML, Sanchez-Madrid F, Martin P (2014) Maintenance of immune tolerance by Foxp3+ regulatory T cells requires CD69 expression. J Autoimmun 55:51–62CrossRefPubMedPubMedCentral Cortes JR, Sanchez-Diaz R, Bovolenta ER, Barreiro O, Lasarte S, Matesanz-Marin A, Toribio ML, Sanchez-Madrid F, Martin P (2014) Maintenance of immune tolerance by Foxp3+ regulatory T cells requires CD69 expression. J Autoimmun 55:51–62CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Shinoda K, Tokoyoda K, Hanazawa A, Hayashizaki K, Zehentmeier S, Hosokawa H, Iwamura C, Koseki H, Tumes DJ, Radbruch A, Nakayama T (2012) Type II membrane protein CD69 regulates the formation of resting T-helper memory. Proc Natl Acad Sci U S A 109:7409–7414CrossRefPubMedPubMedCentral Shinoda K, Tokoyoda K, Hanazawa A, Hayashizaki K, Zehentmeier S, Hosokawa H, Iwamura C, Koseki H, Tumes DJ, Radbruch A, Nakayama T (2012) Type II membrane protein CD69 regulates the formation of resting T-helper memory. Proc Natl Acad Sci U S A 109:7409–7414CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Nakayama T, Yoshikawa M, Asaka D, Okushi T, Matsuwaki Y, Otori N, Hama T, Moriyama H (2011) Mucosal eosinophilia and recurrence of nasal polyps—new classification of chronic rhinosinusitis. Rhinology 49:392–396PubMed Nakayama T, Yoshikawa M, Asaka D, Okushi T, Matsuwaki Y, Otori N, Hama T, Moriyama H (2011) Mucosal eosinophilia and recurrence of nasal polyps—new classification of chronic rhinosinusitis. Rhinology 49:392–396PubMed
40.
Zurück zum Zitat Shinoda K, Hirahara K, Iinuma T, Ichikawa T, Suzuki AS, Sugaya K, Tumes DJ, Yamamoto H, Hara T, Tani-Ichi S, Ikuta K, Okamoto Y, Nakayama T (2016) Thy1+IL-7+ lymphatic endothelial cells in iBALT provide a survival niche for memory T-helper cells in allergic airway inflammation. Proc Natl Acad Sci U S A 113:E2842–E2851CrossRefPubMedPubMedCentral Shinoda K, Hirahara K, Iinuma T, Ichikawa T, Suzuki AS, Sugaya K, Tumes DJ, Yamamoto H, Hara T, Tani-Ichi S, Ikuta K, Okamoto Y, Nakayama T (2016) Thy1+IL-7+ lymphatic endothelial cells in iBALT provide a survival niche for memory T-helper cells in allergic airway inflammation. Proc Natl Acad Sci U S A 113:E2842–E2851CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Garcia BA, Smalley DM, Cho H, Shabanowitz J, Ley K, Hunt DF (2005) The platelet microparticle proteome. J Proteome Res 4:1516–1521CrossRefPubMed Garcia BA, Smalley DM, Cho H, Shabanowitz J, Ley K, Hunt DF (2005) The platelet microparticle proteome. J Proteome Res 4:1516–1521CrossRefPubMed
42.
Zurück zum Zitat Gilles L, Bluteau D, Boukour S, Chang Y, Zhang Y, Robert T, Dessen P, Debili N, Bernard OA, Vainchenker W, Raslova H (2009) MAL/SRF complex is involved in platelet formation and megakaryocyte migration by regulating MYL9 (MLC2) and MMP9. Blood 114:4221–4232CrossRefPubMed Gilles L, Bluteau D, Boukour S, Chang Y, Zhang Y, Robert T, Dessen P, Debili N, Bernard OA, Vainchenker W, Raslova H (2009) MAL/SRF complex is involved in platelet formation and megakaryocyte migration by regulating MYL9 (MLC2) and MMP9. Blood 114:4221–4232CrossRefPubMed
43.
Zurück zum Zitat Seri M, Cusano R, Gangarossa S, Caridi G, Bordo D, Lo Nigro C, Ghiggeri GM, Ravazzolo R, Savino M, Del Vecchio M, d’Apolito M, Iolascon A, Zelante LL, Savoia A, Balduini CL, Noris P, Magrini U, Belletti S, Heath KE, Babcock M, Glucksman MJ, Aliprandis E, Bizzaro N, Desnick RJ, Martignetti JA (2000) Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. The May-Heggllin/Fechtner Syndrome Consortium. Nat Genet 26:103–105CrossRefPubMed Seri M, Cusano R, Gangarossa S, Caridi G, Bordo D, Lo Nigro C, Ghiggeri GM, Ravazzolo R, Savino M, Del Vecchio M, d’Apolito M, Iolascon A, Zelante LL, Savoia A, Balduini CL, Noris P, Magrini U, Belletti S, Heath KE, Babcock M, Glucksman MJ, Aliprandis E, Bizzaro N, Desnick RJ, Martignetti JA (2000) Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. The May-Heggllin/Fechtner Syndrome Consortium. Nat Genet 26:103–105CrossRefPubMed
44.
Zurück zum Zitat Lopez-Cabrera M, Munoz E, Blazquez MV, Ursa MA, Santis AG, Sanchez-Madrid F (1995) Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-alpha-responsive elements. J Biol Chem 270:21545–21551CrossRefPubMed Lopez-Cabrera M, Munoz E, Blazquez MV, Ursa MA, Santis AG, Sanchez-Madrid F (1995) Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-alpha-responsive elements. J Biol Chem 270:21545–21551CrossRefPubMed
45.
Zurück zum Zitat Kohlmeier JE, Miller SC, Woodland DL (2007) Cutting edge: antigen is not required for the activation and maintenance of virus-specific memory CD8+ T cells in the lung airways. J Immunol 178:4721–4725CrossRefPubMed Kohlmeier JE, Miller SC, Woodland DL (2007) Cutting edge: antigen is not required for the activation and maintenance of virus-specific memory CD8+ T cells in the lung airways. J Immunol 178:4721–4725CrossRefPubMed
46.
Zurück zum Zitat Ledgerwood LG, Lal G, Zhang N, Garin A, Esses SJ, Ginhoux F, Merad M, Peche H, Lira SA, Ding Y, Yang Y, He X, Schuchman EH, Allende ML, Ochando JC, Bromberg JS (2008) The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol 9:42–53CrossRefPubMed Ledgerwood LG, Lal G, Zhang N, Garin A, Esses SJ, Ginhoux F, Merad M, Peche H, Lira SA, Ding Y, Yang Y, He X, Schuchman EH, Allende ML, Ochando JC, Bromberg JS (2008) The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol 9:42–53CrossRefPubMed
47.
Zurück zum Zitat Takamura S, Roberts AD, Jelley-Gibbs DM, Wittmer ST, Kohlmeier JE, Woodland DL (2010) The route of priming influences the ability of respiratory virus-specific memory CD8+ T cells to be activated by residual antigen. J Exp Med 207:1153–1160CrossRefPubMedPubMedCentral Takamura S, Roberts AD, Jelley-Gibbs DM, Wittmer ST, Kohlmeier JE, Woodland DL (2010) The route of priming influences the ability of respiratory virus-specific memory CD8+ T cells to be activated by residual antigen. J Exp Med 207:1153–1160CrossRefPubMedPubMedCentral
48.
Zurück zum Zitat Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, Lucas PJ, Artis D, Wherry EJ, Hogquist K, Vezys V, Masopust D (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188:4866–4875CrossRefPubMed Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, Lucas PJ, Artis D, Wherry EJ, Hogquist K, Vezys V, Masopust D (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188:4866–4875CrossRefPubMed
49.
Zurück zum Zitat Skon CN, Lee JY, Anderson KG, Masopust D, Hogquist KA, Jameson SC (2013) Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14:1285–1293CrossRefPubMedPubMedCentral Skon CN, Lee JY, Anderson KG, Masopust D, Hogquist KA, Jameson SC (2013) Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14:1285–1293CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Esplugues E, Sancho D, Vega-Ramos J, Martinez C, Syrbe U, Hamann A, Engel P, Sanchez-Madrid F, Lauzurica P (2003) Enhanced antitumor immunity in mice deficient in CD69. J Exp Med 197:1093–1106CrossRefPubMedPubMedCentral Esplugues E, Sancho D, Vega-Ramos J, Martinez C, Syrbe U, Hamann A, Engel P, Sanchez-Madrid F, Lauzurica P (2003) Enhanced antitumor immunity in mice deficient in CD69. J Exp Med 197:1093–1106CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Esplugues E, Vega-Ramos J, Cartoixa D, Vazquez BN, Salaet I, Engel P, Lauzurica P (2005) Induction of tumor NK-cell immunity by anti-CD69 antibody therapy. Blood 105:4399–4406CrossRefPubMed Esplugues E, Vega-Ramos J, Cartoixa D, Vazquez BN, Salaet I, Engel P, Lauzurica P (2005) Induction of tumor NK-cell immunity by anti-CD69 antibody therapy. Blood 105:4399–4406CrossRefPubMed
52.
Zurück zum Zitat Wei SM, Pan HL, Wang L, Yin GL, Zhong K, Zhou Y, Yang SJ, Xin ZL (2017) Combination therapy with dendritic cell-based vaccine and anti-CD69 antibody enhances antitumor efficacy in renal cell carcinoma-bearing mice. Turk J Med Sci 47:658–667CrossRefPubMed Wei SM, Pan HL, Wang L, Yin GL, Zhong K, Zhou Y, Yang SJ, Xin ZL (2017) Combination therapy with dendritic cell-based vaccine and anti-CD69 antibody enhances antitumor efficacy in renal cell carcinoma-bearing mice. Turk J Med Sci 47:658–667CrossRefPubMed
53.
Zurück zum Zitat Mita Y, Kimura MY, Hayashizaki K, Koyama-Nasu R, Ito T, Motohashi S, Okamoto Y, Nakayama T (2018) Crucial role of CD69 in anti-tumor immunity through regulating the exhaustion of tumor-infiltrating T cells. Int Immunol 30:559–567CrossRefPubMed Mita Y, Kimura MY, Hayashizaki K, Koyama-Nasu R, Ito T, Motohashi S, Okamoto Y, Nakayama T (2018) Crucial role of CD69 in anti-tumor immunity through regulating the exhaustion of tumor-infiltrating T cells. Int Immunol 30:559–567CrossRefPubMed
54.
Zurück zum Zitat Budhu S, Schaer DA, Li Y, Toledo-Crow R, Panageas K, Yang X, Zhong H, Houghton AN, Silverstein SC, Merghoub T, Wolchok JD (2017) Blockade of surface-bound TGF-beta on regulatory T cells abrogates suppression of effector T cell function in the tumor microenvironment. Sci Signal 10:eaak9702CrossRefPubMedPubMedCentral Budhu S, Schaer DA, Li Y, Toledo-Crow R, Panageas K, Yang X, Zhong H, Houghton AN, Silverstein SC, Merghoub T, Wolchok JD (2017) Blockade of surface-bound TGF-beta on regulatory T cells abrogates suppression of effector T cell function in the tumor microenvironment. Sci Signal 10:eaak9702CrossRefPubMedPubMedCentral
55.
Zurück zum Zitat Mariathasan S, Turley SJ, Nickles D, Castiglioni A, Yuen K, Wang Y, Kadel EE III, Koeppen H, Astarita JL, Cubas R, Jhunjhunwala S, Banchereau R, Yang Y, Guan Y, Chalouni C, Ziai J, Senbabaoglu Y, Santoro S, Sheinson D, Hung J, Giltnane JM, Pierce AA, Mesh K, Lianoglou S, Riegler J, Carano RAD, Eriksson P, Hoglund M, Somarriba L, Halligan DL, van der Heijden MS, Loriot Y, Rosenberg JE, Fong L, Mellman I, Chen DS, Green M, Derleth C, Fine GD, Hegde PS, Bourgon R, Powles T (2018) TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature 554:544–548CrossRefPubMedPubMedCentral Mariathasan S, Turley SJ, Nickles D, Castiglioni A, Yuen K, Wang Y, Kadel EE III, Koeppen H, Astarita JL, Cubas R, Jhunjhunwala S, Banchereau R, Yang Y, Guan Y, Chalouni C, Ziai J, Senbabaoglu Y, Santoro S, Sheinson D, Hung J, Giltnane JM, Pierce AA, Mesh K, Lianoglou S, Riegler J, Carano RAD, Eriksson P, Hoglund M, Somarriba L, Halligan DL, van der Heijden MS, Loriot Y, Rosenberg JE, Fong L, Mellman I, Chen DS, Green M, Derleth C, Fine GD, Hegde PS, Bourgon R, Powles T (2018) TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature 554:544–548CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Tauriello DVF, Palomo-Ponce S, Stork D, Berenguer-Llergo A, Badia-Ramentol J, Iglesias M, Sevillano M, Ibiza S, Canellas A, Hernando-Momblona X, Byrom D, Matarin JA, Calon A, Rivas EI, Nebreda AR, Riera A, Attolini CS, Batlle E (2018) TGFbeta drives immune evasion in genetically reconstituted colon cancer metastasis. Nature 554:538–543CrossRefPubMed Tauriello DVF, Palomo-Ponce S, Stork D, Berenguer-Llergo A, Badia-Ramentol J, Iglesias M, Sevillano M, Ibiza S, Canellas A, Hernando-Momblona X, Byrom D, Matarin JA, Calon A, Rivas EI, Nebreda AR, Riera A, Attolini CS, Batlle E (2018) TGFbeta drives immune evasion in genetically reconstituted colon cancer metastasis. Nature 554:538–543CrossRefPubMed
57.
Zurück zum Zitat Yang ZZ, Grote DM, Xiu B, Ziesmer SC, Price-Troska TL, Hodge LS, Yates DM, Novak AJ, Ansell SM (2014) TGF-beta upregulates CD70 expression and induces exhaustion of effector memory T cells in B-cell non-Hodgkin’s lymphoma. Leukemia 28:1872–1884CrossRefPubMedPubMedCentral Yang ZZ, Grote DM, Xiu B, Ziesmer SC, Price-Troska TL, Hodge LS, Yates DM, Novak AJ, Ansell SM (2014) TGF-beta upregulates CD70 expression and induces exhaustion of effector memory T cells in B-cell non-Hodgkin’s lymphoma. Leukemia 28:1872–1884CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH (2014) Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res 20:434–444CrossRefPubMed Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH (2014) Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin Cancer Res 20:434–444CrossRefPubMed
59.
Zurück zum Zitat Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, de Montpreville V, Validire P, Besse B, Mami-Chouaib F (2015) CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J Immunol 194:3475–3486CrossRefPubMed Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, de Montpreville V, Validire P, Besse B, Mami-Chouaib F (2015) CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J Immunol 194:3475–3486CrossRefPubMed
60.
Zurück zum Zitat Wang B, Wu S, Zeng H, Liu Z, Dong W, He W, Chen X, Dong X, Zheng L, Lin T, Huang J (2015) CD103+ tumor infiltrating lymphocytes predict a favorable prognosis in urothelial cell carcinoma of the bladder. J Urol 194:556–562CrossRefPubMed Wang B, Wu S, Zeng H, Liu Z, Dong W, He W, Chen X, Dong X, Zheng L, Lin T, Huang J (2015) CD103+ tumor infiltrating lymphocytes predict a favorable prognosis in urothelial cell carcinoma of the bladder. J Urol 194:556–562CrossRefPubMed
61.
Zurück zum Zitat Ganesan AP, Clarke J, Wood O, Garrido-Martin EM, Chee SJ, Mellows T, Samaniego-Castruita D, Singh D, Seumois G, Alzetani A, Woo E, Friedmann PS, King EV, Thomas GJ, Sanchez-Elsner T, Vijayanand P, Ottensmeier CH (2017) Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat Immunol 18:940–950CrossRefPubMedPubMedCentral Ganesan AP, Clarke J, Wood O, Garrido-Martin EM, Chee SJ, Mellows T, Samaniego-Castruita D, Singh D, Seumois G, Alzetani A, Woo E, Friedmann PS, King EV, Thomas GJ, Sanchez-Elsner T, Vijayanand P, Ottensmeier CH (2017) Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat Immunol 18:940–950CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat Koh J, Kim S, Kim MY, Go H, Jeon YK, Chung DH (2017) Prognostic implications of intratumoral CD103+ tumor-infiltrating lymphocytes in pulmonary squamous cell carcinoma. Oncotarget 8:13762–13769PubMedPubMedCentral Koh J, Kim S, Kim MY, Go H, Jeon YK, Chung DH (2017) Prognostic implications of intratumoral CD103+ tumor-infiltrating lymphocytes in pulmonary squamous cell carcinoma. Oncotarget 8:13762–13769PubMedPubMedCentral
63.
Zurück zum Zitat Edwards J, Wilmott JS, Madore J, Gide TN, Quek C, Tasker A, Ferguson A, Chen J, Hewavisenti R, Hersey P, Gebhardt T, Weninger W, Britton WJ, Saw RPM, Thompson JF, Menzies AM, Long GV, Scolyer RA, Palendira U (2018) CD103(+) tumor-resident CD8(+) T cells are associated with improved survival in immunotherapy-naive melanoma patients and expand significantly during anti-PD-1 treatment. Clin Cancer Res 24:3036–3045CrossRefPubMed Edwards J, Wilmott JS, Madore J, Gide TN, Quek C, Tasker A, Ferguson A, Chen J, Hewavisenti R, Hersey P, Gebhardt T, Weninger W, Britton WJ, Saw RPM, Thompson JF, Menzies AM, Long GV, Scolyer RA, Palendira U (2018) CD103(+) tumor-resident CD8(+) T cells are associated with improved survival in immunotherapy-naive melanoma patients and expand significantly during anti-PD-1 treatment. Clin Cancer Res 24:3036–3045CrossRefPubMed
64.
Zurück zum Zitat Duhen T, Duhen R, Montler R, Moses J, Moudgil T, de Miranda NF, Goodall CP, Blair TC, Fox BA, McDermott JE, Chang SC, Grunkemeier G, Leidner R, Bell RB, Weinberg AD (2018) Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors. Nat Commun 9:2724CrossRefPubMedPubMedCentral Duhen T, Duhen R, Montler R, Moses J, Moudgil T, de Miranda NF, Goodall CP, Blair TC, Fox BA, McDermott JE, Chang SC, Grunkemeier G, Leidner R, Bell RB, Weinberg AD (2018) Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors. Nat Commun 9:2724CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Simoni Y, Becht E, Fehlings M, Loh CY, Koo SL, Teng KWW, Yeong JPS, Nahar R, Zhang T, Kared H, Duan K, Ang N, Poidinger M, Lee YY, Larbi A, Khng AJ, Tan E, Fu C, Mathew R, Teo M, Lim WT, Toh CK, Ong BH, Koh T, Hillmer AM, Takano A, Lim TKH, Tan EH, Zhai W, Tan DSW, Tan IB, Newell EW (2018) Bystander CD8(+) T cells are abundant and phenotypically distinct in human tumour infiltrates. Nature 557:575–579CrossRefPubMed Simoni Y, Becht E, Fehlings M, Loh CY, Koo SL, Teng KWW, Yeong JPS, Nahar R, Zhang T, Kared H, Duan K, Ang N, Poidinger M, Lee YY, Larbi A, Khng AJ, Tan E, Fu C, Mathew R, Teo M, Lim WT, Toh CK, Ong BH, Koh T, Hillmer AM, Takano A, Lim TKH, Tan EH, Zhai W, Tan DSW, Tan IB, Newell EW (2018) Bystander CD8(+) T cells are abundant and phenotypically distinct in human tumour infiltrates. Nature 557:575–579CrossRefPubMed
66.
Zurück zum Zitat Park SL, Buzzai A, Rautela J, Hor JL, Hochheiser K, Effern M, McBain N, Wagner T, Edwards J, McConville R, Wilmott JS, Scolyer RA, Tuting T, Palendria U, Gyorki D, Mueller SN, Huntington ND, Bedoui S, Holzel M, Mackay LK, Waithman J, Gebhardt T (2019) Tissue-resident memory CD8(+) T cells promote melanoma-immune equilibrium in skin. Nature 565:366–371CrossRefPubMed Park SL, Buzzai A, Rautela J, Hor JL, Hochheiser K, Effern M, McBain N, Wagner T, Edwards J, McConville R, Wilmott JS, Scolyer RA, Tuting T, Palendria U, Gyorki D, Mueller SN, Huntington ND, Bedoui S, Holzel M, Mackay LK, Waithman J, Gebhardt T (2019) Tissue-resident memory CD8(+) T cells promote melanoma-immune equilibrium in skin. Nature 565:366–371CrossRefPubMed
67.
Zurück zum Zitat Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570CrossRefPubMed Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570CrossRefPubMed
Metadaten
Titel
A new therapeutic target: the CD69-Myl9 system in immune responses
verfasst von
Motoko Y. Kimura
Ryo Koyama-Nasu
Ryoji Yagi
Toshinori Nakayama
Publikationsdatum
05.04.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
Seminars in Immunopathology / Ausgabe 3/2019
Print ISSN: 1863-2297
Elektronische ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-019-00734-7

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