The immunoproteasome controls the availability of the cardioprotective pattern recognition molecule Pentraxin3

European Journal of Immunology

Volumn 46, Issue 3, 2016, Pages 619-633

  Paeschke, Anna ^a   Possehl, Anna ^a   Klingel, Karin ^b   Voss, Martin ^a,c   Voss, Karolin ^a   Kespohl, Meike ^a,c   Sauter, Martina ^b   Overkleeft, Hermen S ^d   Althof, Nadine ^a,c   Garlanda, Cecilia ^e   Voigt, Antje ^a,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d LEIDEN UNIVERSITY   (Netherlands)

^e HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Infection; Inflammation; Innate immunity; Myocarditis; Pentraxin3; Proteasome; Stress response; Virus

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOPROTEASOME; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PENTRAXIN 3; PROTEASOME; PROTEIN LMP7; UNCLASSIFIED DRUG; C REACTIVE PROTEIN; LMP7 PROTEIN; NERVE PROTEIN; NEURONAL PENTRAXIN;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CATALYSIS; CELL DEATH; CONTROLLED STUDY; COXSACKIEVIRUS B3; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; HEART INJURY; HEART PROTECTION; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANATOMY AND HISTOLOGY; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL CULTURE; COXSACKIE VIRUS INFECTION; DEFICIENCY; DISEASE MODEL; GENETICS; HEART; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; VIROLOGY; VIRUS LOAD;

ANIMALS; C-REACTIVE PROTEIN; CELLS, CULTURED; COXSACKIEVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; HEART; IMMUNITY, INNATE; INFLAMMATION; MAP KINASE SIGNALING SYSTEM; MICE; MYOCARDITIS; MYOCARDIUM; MYOCYTES, CARDIAC; NERVE TISSUE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; STRESS, PHYSIOLOGICAL; VIRAL LOAD;

EID: 84959320010     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545892     Document Type: Article

References (60)

1. Yajima, T. and Knowlton, K. U., Viral myocarditis: from the perspective of the virus. Circulation 2009. 119: 2615-2624.
2. Sagar, S., Liu, P. P. and Cooper, L. T., Jr., Myocarditis. Lancet 2012. 379: 738-747.
3. Epelman, S., Liu, P. P. and Mann, D. L., Role of innate and adaptive immune mechanisms in cardiac injury and repair. Nat. Rev. Immunol. 2015. 15: 117-129.
4. Whitton, J. L., Cornell, C. T. and Feuer, R., Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 2005. 3: 765-776.
5. Szalay, G., Meiners, S., Voigt, A., Lauber, J., Spieth, C., Speer, N., Sauter, M. et al., Ongoing coxsackievirus myocarditis is associated with increased formation and activity of myocardial immunoproteasomes. Am. J. Pathol. 2006. 168: 1542-1552.
6. Jakel, S., Kuckelkorn, U., Szalay, G., Plotz, M., Textoris-Taube, K., Opitz, E., Klingel, K. et al., Differential interferon responses enhance viral epitope generation by myocardial immunoproteasomes in murine enterovirus myocarditis. Am. J. Pathol. 2009. 175: 510-518.
7. Mishto, M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Weberruss, M., Dahlmann, B. et al., Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur. J. Immunol. 2014. 44: 3508-3521.
8. 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.
9. Strehl, B., Joeris, T., Rieger, M., Visekruna, A., Textoris-Taube, K., Kaufmann, S. H. E., Kloetzel, P. M. et al., Immunoproteasomes are essential for clearance of Listeria monocytogenes in nonlymphoid tissues but not for induction of bacteria-specific CD8(+) T cells. J. Immunol. 2006. 177: 6238-6244.
10. Schwarz, K., van den Broek, M., Kostka, S., Kraft, R., Soza, A., Schmidtke, G., Kloetzel, P. M. et al., Overexpression of the proteasome subunits LMP2, LMP7, and MECL-1, but not PA28 alpha/beta, enhances the presentation of an immunodominant lymphocytic choriomeningitis virus T cell epitope. J. Immunol. 2000. 165: 768-778.
11. Voigt, A., Jakel, S., Textoris-Taube, K., Keller, C., Drung, I., Szalay, G., Klingel, K. et al., Generation of in silico predicted coxsackievirus B3-derived MHC class I epitopes by proteasomes. Amino Acids 2010. 39: 243-255.
12. Strehl, B., Textoris-Taube, K., Jakel, S., Voigt, A., Henklein, P., Steinhoff, U., Kloetzel, P. M. et al., Antitopes define preferential proteasomal cleavage site usage. J. Biol. Chem. 2008. 283: 17891-17897.
13. Seifert, U., Bialy, L. P., Ebstein, F., Bech-Otschir, D., Voigt, A., Schroter, F., Prozorovski, T. et al., Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 2010. 142: 613-624.
14. 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.
15. 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.
16. 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.
17. Opitz, E., Koch, A., Klingel, K., Schmidt, F., Prokop, S., Rahnefeld, A., Sauter, M. et al., Impairment of immunoproteasome function by beta5i/LMP7 subunit deficiency results in severe enterovirus myocarditis. PLoS Pathog. 2011. 7: 1-13.
18. Ebstein, F., Voigt, A., Lange, N., Warnatsch, A., Schroter, F., Prozorovski, T., Kuckelkorn, U. et al., Immunoproteasomes are important for proteostasis in immune responses. Cell 2013. 152: 935-937.
19. Arima, K., Kinoshita, A., Mishima, H., Kanazawa, N., Kaneko, T., Mizushima, T., Ichinose, K. et al., Proteasome assembly defect due to a proteasome subunit beta type 8 (PSMB8) mutation causes the autoinflammatory disorder, Nakajo-Nishimura syndrome. Proc. Natl. Acad. Sci. USA 2011. 108: 14914-14919.
20. Kitamura, A., Maekawa, Y., Uehara, H., Izumi, K., Kawachi, I., Nishizawa, M., Toyoshima, Y. et al., A mutation in the immunoproteasome subunit PSMB8 causes autoinflammation and lipodystrophy in humans. J. Clin. Invest. 2011. 121: 4150-4160.
21. Garlanda, C., Bottazzi, B., Bastone, A. and Mantovani, A., Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 2005. 23: 337-366.
22. Deban, L., Jaillon, S., Garlanda, C., Bottazzi, B. and Mantovani, A., Pentraxins in innate immunity: lessons from PTX3. Cell Tissue Res. 2011. 343: 237-249.
23. Jaillon, S., Peri, G., Delneste, Y., Fremaux, I., Doni, A., Moalli, F., Garlanda, C. et al., The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J. Exp. Med. 2007. 204: 793-804.
24. Deban, L., Russo, R. C., Sironi, M., Moalli, F., Scanziani, M., Zambelli, V., Cuccovillo, I. et al., Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat. Immunol. 2010. 11: 328-334.
25. Salio, M., Chimenti, S., De Angelis, N., Molla, F., Maina, V., Nebuloni, M., Pasqualini, F. et al., Cardioprotective function of the long pentraxin PTX3 in acute myocardial infarction. Circulation 2008. 117: 1055-1064.
26. Pucci, S., Fisco, T., Zonetti, M. J., Bonanno, E., Mazzarelli, P. and Mauriello, A., PTX3: a modulator of human coronary plaque vulnerability acting by macrophages type 2. Int. J. Cardiol. 2014. 176: 710-717.
27. Nebuloni, M., Pasqualini, F., Zerbi, P., Lauri, E., Mantovani, A., Vago, L. and Garlanda, C., PTX3 expression in the heart tissues of patients with myocardial infarction and infectious myocarditis. Cardiovasc. Pathol. 2011. 20: e27-e35.
28. Suzuki, S., Takeishi, Y., Niizeki, T., Koyama, Y., Kitahara, T., Sasaki, T., Sagara, M. et al., Pentraxin 3, a new marker for vascular inflammation, predicts adverse clinical outcomes in patients with heart failure. Am. Heart. J. 2008. 155: 75-81.
29. Tomandlova, M., Jarkovsky, J., Tomandl, J., Kubkova, L., Kala, P., Littnerova, S., Gottwaldova, J. et al., Prognostic value of pentraxin-3 level in patients with STEMI and its relationship with heart failure and markers of oxidative stress. Dis. Markers 2015. 2015: doi: 10.1155/2015/159051.
30. Althof, N., Harkins, S., Kemball, C. C., Flynn, C. T., Alirezaei, M. and Whitton, J. L., In vivo ablation of type I interferon receptor from cardiomyocytes delays coxsackieviral clearance and accelerates myocardial disease. J. Virol. 2014. 88: 5087-5099.
31. Bozza, S., Bistoni, F., Gaziano, R., Pitzurra, L., Zelante, T., Bonifazi, P., Perruccio, K. et al., Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 2006. 108: 3387-3396.
32. 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.
33. 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.
34. Altmeyer, A., Klampfer, L., Goodman, A. R. and Vilcek, J., Promoter structure and transcriptional activation of the murine TSG-14 gene encoding a tumor necrosis factor/interleukin-1-inducible pentraxin protein. J. Biol. Chem. 1995. 270: 25584-25590.
35. 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.
36. Schmidt, N., Gonzalez, E., Visekruna, A., Kuhl, A. A., Loddenkemper, C., Mollenkopf, H., Kaufmann, S. H. E. et al., Targeting the proteasome: partial inhibition of the proteasome by bortezomib or deletion of the immunosubunit LMP7 attenuates experimental colitis. Gut 2010. 59: 896-906.
37. Visekruna, A., Joeris, T., Seidel, D., Kroesen, A., Loddenkemper, C., Zeitz, M., Kaufmann, S. H. E. et al., Proteasome-mediated degradation of I kappa B alpha and processing of p105 in Crohn disease and ulcerative colitis. J. Clin. Invest. 2006. 116: 3195-3203.
38. Arthur, J. S. and Ley, S. C., Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol. 2013. 13: 679-692.
39. Cooper, L. T., Medical progress: myocarditis. N. Engl. J. Med. 2009. 360: 1526-1538.
40. Rahnefeld, A., Klingel, K., Schuermann, A., Diny, N. L., Althof, N., Lindner, A., Bleienheuft, P. et al., Ubiquitin-like protein ISG15 (interferon-stimulated gene of 15 kDa) in host defense against heart failure in a mouse model of virus-induced cardiomyopathy. Circulation 2014. 130: 1589-1600.
41. Fuse, K., Chan, G., Liu, Y. A., Gudgeon, P., Husain, M., Chen, M. Y., Yeh, W. C. et al., Myeloid differentiation factor-88 plays a crucial role in the pathogenesis of coxsackievirus B3-induced myocarditis and influences type I interferon production. Circulation 2005. 112: 2276-2285.
42. Valaperti, A., Nishii, M., Liu, Y., Naito, K., Chan, M., Zhang, L., Skurk, C. et al., Innate immune interleukin-1 receptor-associated kinase 4 exacerbates viral myocarditis by reducing CCR5(+) CD11b(+) monocyte migration and impairing interferon production. Circulation 2013. 128: 1542-1554.
43. Reading, P. C., Bozza, S., Gilbertson, B., Tate, M., Moretti, S., Job, E. R., Crouch, E. C. et al., Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J. Immunol. 2008. 180: 3391-3398.
44. Rovere, P., Peri, G., Fazzini, F., Bottazzi, B., Doni, A., Bondanza, A., Zimmermann, V. S. et al., The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 2000. 96: 4300-4306.
45. Diniz, S. N., Nomizo, R., Cisalpino, P. S., Teixeira, M. M., Brown, G. D., Mantovani, A., Gordon, S. et al., PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. J. Leukoc. Biol. 2004. 75: 649-656.
46. Basile, A., Sica, A., d'Aniello, E., Breviario, F., Garrido, G., Castellano, M., Mantovani, A. et al., Characterization of the promoter for the human long pentraxin PTX3. Role of NF-kappaB in tumor necrosis factor-alpha and interleukin-1beta regulation. J. Biol. Chem. 1997. 272: 8172-8178.
47. 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.
48. 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.
49. Runnels, H. A., Watkins, W. A. and Monaco, J. J., LMP2 expression and proteasome activity in NOD mice. Nat. Med. 2000. 6: 1064-1065.
50. 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.
51. Jang, E. R., Lee, N. R., Han, S., Wu, Y., Sharma, L. K., Carmony, K. C., Marks, J. et al., Revisiting the role of the immunoproteasome in the activation of the canonical NF-kappaB pathway. Mol. Biosyst. 2012. 8: 2295-2302.
52. Mishto, M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Weberruss, M., Dahlmann, B. et al., Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur. J. Immunol. 2014. 44: 3508-3521.
53. Arciniega, M., Beck, P., Lange, O. F., Groll, M. and Huber, R., Differential global structural changes in the core particle of yeast and mouse proteasome induced by ligand binding. Proc. Natl. Acad. Sci. USA 2014. 111: 9479-9484.
54. Ronkina, N., Kotlyarov, A., Dittrich-Breiholz, O., Kracht, M., Hitti, E., Milarski, K., Askew, R. et al., The mitogen-activated protein kinase (MAPK)-activated protein kinases MK2 and MK3 cooperate in stimulation of tumor necrosis factor biosynthesis and stabilization of p38 MAPK. Mol. Cell. Biol. 2007. 27: 170-181.
55. Klingel, K., Hohenadl, C., Canu, A., Albrecht, M., Seemann, M., Mall, G. and Kandolf, R., Ongoing enterovirus-induced myocarditis is associated with persistent heart-muscle infection-quantitative-analysis of virus-replication, tissue-damage, and inflammation. Proc. Natl. Acad. Sci. USA 1992. 89: 314-318.
56. Garlanda, C., Hirsch, E., Bozza, S., Salustri, A., De, A. M., Nota, R., Maccagno, A. et al., Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 2002. 420: 182-186.
57. Rahnefeld, A., Ebstein, F., Albrecht, N., Opitz, E., Kuckelkorn, U., Stangl, K., Rehm, A. et al., Antigen-presentation capacity of dendritic cells is impaired in ongoing enterovirus myocarditis. Eur. J. Immunol. 2011. 41: 2774-2781.
58. Englen, M. D., Valdez, Y. E., Lehnert, N. M. and Lehnert, B. E., Granulocyte/macrophage colony-stimulating factor is expressed and secreted in cultures of murine L929 cells. J. Immunol. Methods 1995. 184: 281-283.
59. Bottazzi, B., Vouret-Craviari, V., Bastone, A., De Gioia, L., Matteucci, C., Peri, G., Spreafico, F. et al., Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. J. Biol. Chem. 1997. 272: 32817-32823.
60. Kindermann, I., Kindermann, M., Kandolf, R., Klingel, K., Bultmann, B., Muller, T., Lindinger, A. et al., Predictors of outcome in patients with suspected myocarditis. Circulation 2008. 118: 639-648.