Proteasome composition in immune cells implies special immune-cell-specific immunoproteasome function.
Expression
Immune cells
Immunoproteasome
Lymphoid tissue
Proteasome
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
08 Mar 2024
08 Mar 2024
Historique:
revised:
11
12
2023
received:
16
06
2023
accepted:
12
12
2023
medline:
9
3
2024
pubmed:
9
3
2024
entrez:
8
3
2024
Statut:
aheadofprint
Résumé
Immunoproteasomes are a special class of proteasomes, which can be induced with IFN-γ in an inflammatory environment. In recent years, it became evident that certain immune cell types constitutively express high levels of immunoproteasomes. However, information regarding the basal expression of proteolytically active immunoproteasome subunits in different types of immune cells is still rare. Hence, we quantified standard proteasome subunits (β1c, β2c, β5c) and immunoproteasome subunits (LMP2, MECL-1, LMP7) in the major murine (CD4
Identifiants
pubmed: 38458995
doi: 10.1002/eji.202350613
doi:
Types de publication
English Abstract
Journal Article
Langues
ita
Sous-ensembles de citation
IM
Pagination
e2350613Subventions
Organisme : Kezar Life Sciences
Organisme : Deutsche Forschungsgemeinschaft
ID : GR 1517/27-1
Informations de copyright
© 2024 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.
Références
Huber, E. M., Basler, M., Schwab, R., Heinemeyer, W., Kirk, C. J., Groettrup, M. and Groll, M., Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell. 2012. 148: 727-738.
Frantzeskakis, M., Takahama, Y. and Ohigashi, I., The role of proteasomes in the thymus. Front. Immunol. 2021. 12: 646209.
Gileadi, U., MoinsTeisserenc, H. T., Correa, I., Booth, B. L., Dunbar, P. R., Sewell, A. K., Trowsdale, J. et al., Generation of an immunodominant CTL epitope is affected by proteasome subunit composition and stability of the antigenic protein. J. Immunol. 1999. 163: 6045-6052.
Chen, W. S., Norbury, C. C., Cho, Y. J., Yewdell, J. W. and Bennink, J. R., Immunoproteasomes shape immunodominance hierarchies of antiviral CD8(+) T cells at the levels of T cell repertoire and presentation of viral antigens. J. Exp. Med. 2001. 193: 1319-1326.
Basler, M., Youhnovski, N., Van Den Broek, M., Przybylski, M. and Groettrup, M., Immunoproteasomes down-regulate presentation of a subdominant T cell epitope from lymphocytic choriomeningitis virus. J. Immunol. 2004. 173: 3925-3934.
Basler, M., Beck, U., Kirk, C. J. and Groettrup, M., The antiviral immune response in mice devoid of immunoproteasome activity. J. Immunol. 2011. 187: 5548-5557.
Basler, M., Lauer, C., Moebius, J., Weber, R., Przybylski, M., Kisselev, A. F., Tsu, C. et al., Why the structure but not the activity of the immunoproteasome subunit low molecular mass polypeptide 2 rescues antigen presentation. J. Immunol. 2012. 189: 1868-1877.
Basler, M., Mundt, S. and Groettrup, M., The immunoproteasome subunit LMP7 is required in the murine thymus for filling up a hole in the T cell repertoire. Eur. J. Immunol. 2018. 48: 419-429.
Basler, M., Moebius, J., Elenich, L., Groettrup, M. and Monaco, J. J., An altered T cell repertoire in MECL-1-deficient mice. J. Immunol. 2006. 176: 6665-6672.
Moebius, J., van den Broek, M., Groettrup, M. and Basler, M., Immunoproteasomes are essential for survival and expansion of T cells in virus-infected mice. Eur. J. Immunol. 2010. 40: 3439-3449.
Kalim, K. W., Basler, M., Kirk, C. J. and Groettrup, M., Immunoproteasome subunit LMP7 deficiency and inhibition suppresses Th1 and Th17 but enhances regulatory T cell differentiation. J. Immunol. 2012. 189: 4182-4193.
Vachharajani, N., Joeris, T., Luu, M., Hartmann, S., Pautz, S., Jenike, E., Pantazis, G. et al., Prevention of colitis-associated cancer by selective targeting of immunoproteasome subunit LMP7. Oncotarget. 2017. 8: 50447-50459.
Sula Karreci, E., Fan, H., Uehara, M., Mihali, A. B., Singh, P. K., Kurdi, A. T., Solhjou, Z. et al., Brief treatment with a highly selective immunoproteasome inhibitor promotes long-term cardiac allograft acceptance in mice. Proc. Natl. Acad. Sci. USA. 2016. 113: E8425-E8432.
Schmidt, C., Berger, T., Groettrup, M. and Basler, M., Immunoproteasome inhibition impairs T and B cell activation by restraining ERK signaling and proteostasis. Front. Immunol. 2018. 9: 2386.
Muchamuel, T., Basler, M., Aujay, M. A., Suzuki, E., Kalim, K. W., Lauer, C., Sylvain, C. et al., A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat. Med. 2009. 15: 781-787.
Basler, M., Mundt, S., Muchamuel, T., Moll, C., Jiang, J., Groettrup, M. and Kirk, C. J., Inhibition of the immunoproteasome ameliorates experimental autoimmune encephalomyelitis. EMBO Mol. Med. 2014. 6: 226-238.
Kremer, M., Henn, A., Kolb, C., Basler, M., Moebius, J., Guillaume, B., Leist, M., et al. Reduced immunoproteasome formation and accumulation of immunoproteasomal precursors in the brains of lymphocytic choriomeningitis virus-infected mice. J. Immunol. 2010. 185: 5549-5560.
Mundt, S., Engelhardt, B., Kirk, C. J., Groettrup, M. and Basler, M., Inhibition and deficiency of the immunoproteasome subunit LMP7 attenuates LCMV-induced meningitis. Eur. J. Immunol. 2016. 46: 104-113.
Li, J., Basler, M., Alvarez, G., Brunner, T., Kirk, C. J. and Groettrup, M., Immunoproteasome inhibition prevents chronic antibody-mediated allograft rejection in renal transplantation. Kidney Int. 2018. 93: 670-680.
Li, J., Koerner, J., Basler, M., Brunner, T., Kirk, C. J. and Groettrup, M., Immunoproteasome inhibition induces plasma cell apoptosis and preserves kidney allografts by activating the unfolded protein response and suppressing plasma cell survival factors. Kidney Int. 2019. 95: 611-623.
Li, J., Hu, S., Johnson, H. W. B., Kirk, C. J., Xian, P., Song, Y., Li, Y. et al., Co-inhibition of immunoproteasome subunits LMP2 and LMP7 enables prevention of transplant arteriosclerosis. Cardiovasc Res. 2023. 119: 1030-1045.
Basler, M., Li, J. and Groettrup, M., On the role of the immunoproteasome in transplant rejection. Immunogenetics. 2019. 71: 263-271.
Basler, M. and Groettrup, M., Recent insights how combined inhibition of immuno/proteasome subunits enables therapeutic efficacy. Genes Immun. 2020. 21: 273-287.
Basler, M., Mundt, S., Bitzer, A., Schmidt, C. and Groettrup, M., The immunoproteasome: a novel drug target for autoimmune diseases. Clin. Exp. Rheumatol. 2015. 33: S74-S79.
Basler, M., Dajee, M., Moll, C., Groettrup, M. and Kirk, C. J., Prevention of experimental colitis by a selective inhibitor of the immunoproteasome. J Immunol. 2010. 185: 634-641.
Basler, M., Maurits, E., de Bruin, G., Koerner, J., Overkleeft, H. S. and Groettrup, M., Amelioration of autoimmunity with an inhibitor selectively targeting all active centres of the immunoproteasome. Br. J. Pharmacol. 2018. 175: 38-52.
Ichikawa, H. T., Conley, T., Muchamuel, T., Jiang, J., Lee, S., Owen, T., Barnard, J. et al., Novel proteasome inhibitors have a beneficial effect in murine lupus via the dual inhibition of type i interferon and autoantibody secreting cells. Arthritis Rheum. 2012. 64: 493-503.
Muchamuel, T., Fan, R. A., Anderl, J. L., Bomba, D. J., Johnson, H. W. B., Lowe, E., Tuch, B. B. et al., Zetomipzomib (KZR-616) attenuates lupus in mice via modulation of innate and adaptive immune responses. Front. Immunol. 2023. 14: 1043680.
Basler, M., Lindstrom, M. M., LaStant, J. J., Bradshaw, J. M., Owens, T. D., Schmidt, C., Maurits, E. et al., Co-inhibition of immunoproteasome subunits LMP2 and LMP7 is required to block autoimmunity. EMBO Rep. 2018. 19: e46512.
Del Rio Oliva, M., Kirk, C. J., Groettrup, M. and Basler, M., Effective therapy of polymyositis in mice via selective inhibition of the immunoproteasome. Eur. J. Immunol. 2022. 52: 1510-1522.
Del Rio Oliva, M., Mellett, M. and Basler, M., Immunoproteasome inhibition attenuates experimental psoriasis. Front. Immunol. 2022. 13: 1075615.
Koerner, J., Brunner, T. and Groettrup, M., Inhibition and deficiency of the immunoproteasome subunit LMP7 suppress the development and progression of colorectal carcinoma in mice. Oncotarget. 2017. 8: 50873-50888.
Koerner, J., Horvath, D., Oliveri, F., Li, J. and Basler, M., Suppression of prostate cancer and amelioration of the immunosuppressive tumor microenvironment through selective immunoproteasome inhibition. Oncoimmunology. 2023. 12: 2156091.
Li, J., Liu, N., Zhou, H., Xian, P., Song, Y., Tang, X., Li, Y. et al., Immunoproteasome inhibition prevents progression of castration-resistant prostate cancer. Br. J. Cancer. 2023. 128: 1377-1390.
Furie, R., Parikh, S., Maiquez, A., Khan, A., Moreno, O., Soneira, M., Kirk, C. et al., AB0373 treatment of SLE with the immunoproteasome inhibitor KZR-616: results from the first 4 cohorts of the mission study, an open-label phase 1B dose escalation trial. Ann. Rheum. Dis. 2020. 79: 1486-1487.
Kirk, C. J., Muchamuel, T., Wang, J. and Fan, R. A., Discovery and early clinical development of selective immunoproteasome inhibitors. Cells. 2021. 11.
Stohwasser, R., Standera, S., Peters, I., Kloetzel, P-M and Groettrup, M., Molecular cloning of the mouse proteasome subunits MC14 and MECL-1: reciprocally regulated tissue expression of interferon-γ - modulated proteasome subunits. Eur. J. Immunol. 1997. 27: 1182-1187.
Murata, S., Sasaki, K., Kishimoto, T., Niwa, S., Hayashi, H., Takahama, Y. and Tanaka, K., Regulation of CD8+ T cell development by thymus-specific proteasomes. Science. 2007. 316: 1349-1353.
Boegel, S., Lower, M., Bukur, T., Sorn, P., Castle, J. C. and Sahin, U., HLA and proteasome expression body map. BMC Med. Genomics. 2018. 11: 36.
Guillaume, B., Chapiro, J., Stroobant, V., Colau, D., Van Holle, B., Parvizi, G., Bousquet-Dubouch, M. P. et al., Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proc. Natl. Acad. Sci. USA. 2010. 107: 18599-18604.
Boyum, A., Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab. Invest. Suppl. 1968. 97: 77-89.
Autissier, P., Soulas, C., Burdo, T. H. and Williams, K. C., Evaluation of a 12-color flow cytometry panel to study lymphocyte, monocyte, and dendritic cell subsets in humans. Cytometry A. 2010. 77: 410-419.
Sixt, S. U., Alami, R., Hakenbeck, J., Adamzik, M., Kloss, A., Costabel, U., Jungblut, P. R. et al., Distinct proteasome subpopulations in the alveolar space of patients with the acute respiratory distress syndrome. Mediators Inflamm. 2012. 2012: 204250.
Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature. 1998. 392: 245-252.
de Bruin, G., Xin, B. T., Kraus, M., van der Stelt, M., van der Marel, G. A., Kisselev, A. F., Driessen, C. et al., A set of activity-based probes to visualize human (immuno)proteasome activities. Angew Chem. Int. Ed. Engl. 2016. 55: 4199-4203.
Guilliams, M., Mildner, A. and Yona, S., Developmental and functional heterogeneity of monocytes. Immunity. 2018. 49: 595-613.
Basler, M. and Groettrup, M., Advances in prostate cancer immunotherapies. Drugs Aging. 2007. 24: 197-221.
Basler, M., Claus, M., Klawitter, M., Goebel, H. and Groettrup, M., Immunoproteasome inhibition selectively kills human CD14(+) monocytes and as a result dampens IL-23 secretion. J. Immunol. 2019. 203: 1776-1785.
Alculumbre, S. and Pattarini, L., Purification of human dendritic cell subsets from peripheral blood. Methods Mol. Biol. 2016. 1423: 153-167.
Macagno, A., Gilliet, M., Sallusto, F., Lanzavecchia, A., Nestle, F. O. and Groettrup, M., Dendritic cells upregulate immunoproteasomes and the proteasome regulator PA28 during maturation. Eur. J. Immunol. 1999. 29: 4037-4042.
Macagno, A., Kuehn, L., de Giuli, R. and Groettrup, M., Pronounced upregulation of the PA28α/β proteasome regulator but little increase in the steady state content of immunoproteasomes during dendritic cell maturation. Eur. J. Immunol. 2001. 31: 3271-3280.
Rieckmann, J. C., Geiger, R., Hornburg, D., Wolf, T., Kveler, K., Jarrossay, D., Sallusto, F. et al., Social network architecture of human immune cells unveiled by quantitative proteomics. Nat. Immunol. 2017. 18: 583-593.
Tanaka, K. and Kasahara, M., The MHC class I ligand-generating system: roles of immunoproteasomes and the interferon-gamma-inducible proteasome activator PA28. Immunol. Rev. 1998. 163: 161-176.
Groettrup, M., Kirk, C. J. and Basler, M., Proteasomes in immune cells: more than peptide producers? Nat. Rev. Immunol. 2010. 10: 73-78.
Lickliter, J., Anderl, J., Kirk, C. J., Wang, J. and Bomba, D., KZR-616, a selective inhibitor of the immunoproteasome, shows a promising safety and target inhibition profile in a phase I, double-blind, single (SAD) and multiple ascending dose (MAD) study in healthy volunteers [abstract]. Arthritis Rheumatol. 2017. 69: 2017.
Hensel, J. A., Khattar, V., Ashton, R. and Ponnazhagan, S., Characterization of immune cell subtypes in three commonly used mouse strains reveals gender and strain-specific variations. Lab. Invest. 2019. 99: 93-106.
Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M. and Chilvers E. R.. Neutrophil kinetics in health and disease. Trends Immunol. 2010. 31: 318-324.
Oliveri, F., Basler, M., Rao, T. N., Fehling, H. J. and Groettrup, M., Immunoproteasome inhibition reduces the T helper 2 response in mouse models of allergic airway inflammation. Front. Immunol. 2022. 13: 870720.
Kincaid, E. Z., Che, J. W., York, I., Escobar, H., Reyes-Vargas, E., Delgado, J. C., Welsh, R. M. et al., Mice completely lacking immunoproteasomes show major changes in antigen presentation. Nat. Immunol. 2012. 13: 129-135.
Kincaid, E. Z., Murata, S., Tanaka, K. and Rock, K. L., Specialized proteasome subunits have an essential role in the thymic selection of CD8(+) T cells. Nat. Immunol. 2016. 17: 938-945.
Ersching, J., Vasconcelos, J. R., Ferreira, C. P., Caetano, B. C., Machado, A. V., Bruna-Romero, O., Baron, M. A. et al., The combined deficiency of immunoproteasome subunits affects both the magnitude and quality of pathogen- and genetic vaccination-induced CD8+ T cell responses to the human protozoan parasite Trypanosoma cruzi. PLoS Pathog. 2016. 12: e1005593.
Groettrup, M., Khan, S., Schwarz, K. and Schmidtke, G., Interferon-γ inducible exchanges of 20S proteasome active site subunits: why? Biochimie. 2001. 83: 367-372.
Hayashi, T. and Faustman, D., NOD mice are defective in proteasome production and activation of NF-kappa B. Mol. Cell Biol. 1999. 19: 8646-8659.
Hayashi, T. and Faustman, D., Essential role of human leukocyte antigen-encoded proteasome subunits in NF-kappa B activation and prevention of tumor necrosis factor-alpha-induced apoptosis. J. Biol. Chem. 2000. 275: 5238-5247.
Visekruna, A., Joeris, T., Seidel, D., Kroesen, A., Loddenkemper, C., Zeitz, M., Kaufmann, S. H. et al., Proteasome-mediated degradation of IkappaBalpha and processing of p105 in Crohn disease and ulcerative colitis. J. Clin. Invest. 2006. 116: 3195-3203.
Hensley, S. E., Zanker, D., Dolan, B. P., David, A., Hickman, H. D., Embry, A. C., Skon, C. N. et al., Unexpected role for the immunoproteasome subunit LMP2 in antiviral humoral and innate immune responses. J. Immunol. 2010. 184: 4115-4122.
Maldonado, M., Kapphahn, R. J., Terluk, M. R., Heuss, N. D., Yuan, C., Gregerson, D. S. and Ferrington, D. A., Immunoproteasome deficiency modifies the alternative pathway of NFkappaB signaling. PLoS One. 2013. 8: e56187.
Kessler, B. M., Lennon-Dumenil, A. M., Shinohara, M. L., Lipes, M. A. and Ploegh, H. L., LMP2 expression and proteasome activity in NOD mice. Nat. Med. 2000. 6:1064; author reply 5-6.
Bitzer, A., Basler, M., Krappmann, D. and Groettrup, M., Immunoproteasome subunit deficiency has no influence on the canonical pathway of NF-kappaB activation. Mol Immunol. 2017. 83: 147-153.
Van Kaer, L., Ashton-Rickardt, P. G., Eichelberger, M., Gaczynska, M., Nagashima, K., Rock, K. L., Goldberg, A. L. et al., Altered peptidase and viral-specific T cell response in LMP 2 mutant mice. Immunity. 1994. 1: 533-541.
Fehling, H. J., Swat, W., Laplace, C., Kuhn, R., Rajewsky, K., Muller, U. and von Boehmer, H., MHC class I expression in mice lacking the proteasome subunit LMP-7. Science. 1994. 265: 1234-1237.
Salter, R. D. and Cresswell, P., Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid. EMBO J. 1986. 5: 943-949.
Basler, M. and Groettrup, M., Immunoproteasome-specific inhibitors and their application. Methods Mol. Biol. 2012. 832: 391-401.
Parlati, F., Lee, S. J., Aujay, M., Suzuki, E., Levitsky, K., Lorens, J. B., Micklem, D. R. et al., Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood. 2009. 114: 3439-3447.
Lee, S. J., Levitsky, K., Parlati, F., Bennett, M. K., Arastu-Kapur, S., Kellerman, L., Woo, T. F. et al., Clinical activity of carfilzomib correlates with inhibition of multiple proteasome subunits: application of a novel pharmacodynamic assay. Br. J. Haematol. 2016. 173: 884-895.