Skip to main content
Erschienen in: Inflammation 3/2015

01.06.2015

NOD1 and NOD2 Interact with the Phagosome Cargo in Mast Cells: A Detailed Morphological Evidence

verfasst von: Giuliano Zabucchi, Elisa Trevisan, Francesca Vita, Maria Rosa Soranzo, Violetta Borelli

Erschienen in: Inflammation | Ausgabe 3/2015

Einloggen, um Zugang zu erhalten

ABSTRACT

Mast cells (MC) play a key role in triggering the inflammatory process and share some functions with professional phagocytes. It is not clear whether or not the phagocytic process in MC follows the same route and has the same meaning of that of professional phagocytes. Herein we analyze in detail the structure of the phagosome in rat peritoneal mast cells (RPMC). The ultrastructural analysis of the phagosome, containing either model particles or bacteria, reveals that these vacuoles are very tight, and in several areas, their membrane seems to have dissolved. RPMC express NOD1 and NOD2 proteins whose role is to recognize intracellular foreign components and induce the production of pro-inflammatory mediators. Following Escherichia coli ingestion, both these molecules are found on the phagosome membrane and on ingested pathogens, together with phagosome maturation markers. These findings suggest that in RPMC the ingested cargo can, through interruptions of the phagosome membrane, interact directly with NODs, which act as switches in the process of cytokine production.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Frossi, B., M. De Carli, and C. Pucillo. 2004. The mast cell: an antenna of the microenvironment that directs the immune response. Journal of Leukocyte Biology 75: 579–585.CrossRefPubMed Frossi, B., M. De Carli, and C. Pucillo. 2004. The mast cell: an antenna of the microenvironment that directs the immune response. Journal of Leukocyte Biology 75: 579–585.CrossRefPubMed
2.
Zurück zum Zitat Metz, M., M.A. Grimbaldeston, S. Nakae, A.M. Piliponsky, M. Tsai, and S.J. Galli. 2007. Mast cells in the promotion and limitation of chronic inflammation. Immunological Reviews 217: 304–328.CrossRefPubMed Metz, M., M.A. Grimbaldeston, S. Nakae, A.M. Piliponsky, M. Tsai, and S.J. Galli. 2007. Mast cells in the promotion and limitation of chronic inflammation. Immunological Reviews 217: 304–328.CrossRefPubMed
3.
Zurück zum Zitat Galli, S.J., and M. Tsai. 2010. Mast cells in allergy and infection: versatile effector and regulatory cells in innate and adaptive immunity. European Journal of Immunology 40: 1843–1851.CrossRefPubMedCentralPubMed Galli, S.J., and M. Tsai. 2010. Mast cells in allergy and infection: versatile effector and regulatory cells in innate and adaptive immunity. European Journal of Immunology 40: 1843–1851.CrossRefPubMedCentralPubMed
4.
Zurück zum Zitat Marshall, J.S. 2004. Mast-cell responses to pathogens. Nature Reviews Immunology 4: 787–799.CrossRefPubMed Marshall, J.S. 2004. Mast-cell responses to pathogens. Nature Reviews Immunology 4: 787–799.CrossRefPubMed
5.
Zurück zum Zitat Galli, S.J., S. Nakae, and M. Tsai. 2005. Mast cells in the development of adaptive immune responses. Nature Immunology 6: 35–42.CrossRef Galli, S.J., S. Nakae, and M. Tsai. 2005. Mast cells in the development of adaptive immune responses. Nature Immunology 6: 35–42.CrossRef
6.
Zurück zum Zitat Malaviya, R., N.J. Twesten, E.A. Ross, S.N. Abraham, and J.D. Pfeifer. 1996. Mast cells process bacterial Ags through a phagocytic route for class I MHC presentation to T cells. Journal of Immunology 156: 1490–1496. Malaviya, R., N.J. Twesten, E.A. Ross, S.N. Abraham, and J.D. Pfeifer. 1996. Mast cells process bacterial Ags through a phagocytic route for class I MHC presentation to T cells. Journal of Immunology 156: 1490–1496.
7.
Zurück zum Zitat Frandji, P.C., C. Tkaczyk, B. Oskeritzian, C. David, C. Desaymard, and S. Mécheri. 1996. Exogenous and endogenous antigens are differentially presented by mast cells to CD4+ T lymphocytes. European Journal of Immunology 26: 2517–2528.CrossRefPubMed Frandji, P.C., C. Tkaczyk, B. Oskeritzian, C. David, C. Desaymard, and S. Mécheri. 1996. Exogenous and endogenous antigens are differentially presented by mast cells to CD4+ T lymphocytes. European Journal of Immunology 26: 2517–2528.CrossRefPubMed
8.
Zurück zum Zitat Villa, I.D., C. Skokos, R. Tkaczyk, B. Peronet, M. Huerre David, and S. Mécheri. 2001. Capacity of mouse mast cells to prime T cells and to induce specific antibody responses in vivo. Immunology 102: 165–172.CrossRefPubMedCentralPubMed Villa, I.D., C. Skokos, R. Tkaczyk, B. Peronet, M. Huerre David, and S. Mécheri. 2001. Capacity of mouse mast cells to prime T cells and to induce specific antibody responses in vivo. Immunology 102: 165–172.CrossRefPubMedCentralPubMed
9.
Zurück zum Zitat Lin, T.J., Z. Gao, M. Arock, and S.N. Abraham. 1999. Internalization of FimH+ Escherichia coli by the human mast cell line (HMC-1 5C6) involves protein kinase C. Journal of Leucocyte Biology 66: 1031–1038. Lin, T.J., Z. Gao, M. Arock, and S.N. Abraham. 1999. Internalization of FimH+ Escherichia coli by the human mast cell line (HMC-1 5C6) involves protein kinase C. Journal of Leucocyte Biology 66: 1031–1038.
10.
Zurück zum Zitat Malaviya, R., E.A. Ross, J.I. MacGregor, T. Ikeda, J.R. Little, B.A. Jakschik, and S.N. Abraham. 1994. Mast cell phagocytosis of FimH-expressing enterobacteria. Journal of Immunology 152: 1907–1914. Malaviya, R., E.A. Ross, J.I. MacGregor, T. Ikeda, J.R. Little, B.A. Jakschik, and S.N. Abraham. 1994. Mast cell phagocytosis of FimH-expressing enterobacteria. Journal of Immunology 152: 1907–1914.
11.
Zurück zum Zitat Malaviya, R., T. Ikeda, E.A. Ross, B.A. Jakschik, and S.N. Abraham. 1995. Bacteria-mast cell interactions in inflammatory disease. American Journal of Therapeutics 2: 787–792.CrossRefPubMed Malaviya, R., T. Ikeda, E.A. Ross, B.A. Jakschik, and S.N. Abraham. 1995. Bacteria-mast cell interactions in inflammatory disease. American Journal of Therapeutics 2: 787–792.CrossRefPubMed
12.
Zurück zum Zitat Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S.N. Abraham. 1998. Phagocytic and tumor necrosis factor alpha response of human mast cells following exposure to gram-negative and gram-positive bacteria. Infection and Immunity 66: 6030–6034.PubMedCentralPubMed Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S.N. Abraham. 1998. Phagocytic and tumor necrosis factor alpha response of human mast cells following exposure to gram-negative and gram-positive bacteria. Infection and Immunity 66: 6030–6034.PubMedCentralPubMed
13.
Zurück zum Zitat Malaviya, R., C. Navara, and F.M. Uckun. 2002. Augmentation of mast cell bactericidal activity by the anti-leukemic drug, 4-(3′bromo-4′-hydroxylphenyl)-amino-6,7-dimethoxyquinazoline. Leukemia and Lymphoma 43: 1329–1332.PubMed Malaviya, R., C. Navara, and F.M. Uckun. 2002. Augmentation of mast cell bactericidal activity by the anti-leukemic drug, 4-(3′bromo-4′-hydroxylphenyl)-amino-6,7-dimethoxyquinazoline. Leukemia and Lymphoma 43: 1329–1332.PubMed
14.
Zurück zum Zitat Wei, O.L., A. Hilliard, D. Kalman, and M. Sherman. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infection and Immunity 73: 1978–1985.CrossRefPubMedCentralPubMed Wei, O.L., A. Hilliard, D. Kalman, and M. Sherman. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infection and Immunity 73: 1978–1985.CrossRefPubMedCentralPubMed
15.
Zurück zum Zitat Henderson, W.R., and M. Kaliner. 1978. Immunologic and non-immunologic generation of superoxide from mast cells and basophils. Journal of Clinical Investigation 61: 187–196.CrossRefPubMedCentralPubMed Henderson, W.R., and M. Kaliner. 1978. Immunologic and non-immunologic generation of superoxide from mast cells and basophils. Journal of Clinical Investigation 61: 187–196.CrossRefPubMedCentralPubMed
16.
Zurück zum Zitat Mannaioni, P.F., E. Masini, A. Pistelli, D. Salvemini, and J.R. Vane. 1991. Mast cells as a source of superoxide anions and nitric oxide-like factor: relevance to histamine release. International Journal of Tissue Reactions 13: 271–278.PubMed Mannaioni, P.F., E. Masini, A. Pistelli, D. Salvemini, and J.R. Vane. 1991. Mast cells as a source of superoxide anions and nitric oxide-like factor: relevance to histamine release. International Journal of Tissue Reactions 13: 271–278.PubMed
17.
Zurück zum Zitat Schinetti, M.L., A. Mazzini, R. Greco, and A. Bertelli. 1984. Inhibiting effect of levamisole on superoxide production from rat mast cells. Pharmacological Research Communications 16: 101–107.CrossRefPubMed Schinetti, M.L., A. Mazzini, R. Greco, and A. Bertelli. 1984. Inhibiting effect of levamisole on superoxide production from rat mast cells. Pharmacological Research Communications 16: 101–107.CrossRefPubMed
18.
Zurück zum Zitat Fukuishi, N., M. Sakaguchi, S. Matsuura, C. Nakagawa, R. Akagi, and M. Akagi. 1997. The mechanisms of compound 48/80-induced superoxide generation mediated by A-kinase in rat peritoneal mast cells. Biochemical and Molecular Medicine 61: 107–113.CrossRefPubMed Fukuishi, N., M. Sakaguchi, S. Matsuura, C. Nakagawa, R. Akagi, and M. Akagi. 1997. The mechanisms of compound 48/80-induced superoxide generation mediated by A-kinase in rat peritoneal mast cells. Biochemical and Molecular Medicine 61: 107–113.CrossRefPubMed
19.
Zurück zum Zitat Sakaguchi, M., N. Fukuishi, K. Teramoto, M. Miyazaki, N.H. Huh, M. Namba, and M. Akagi. 2003. Involvement of arachidonic acid in nonimmunologic production of superoxide in mast cells. International Archives of Allergy and Immunology 130: 288–299.CrossRefPubMed Sakaguchi, M., N. Fukuishi, K. Teramoto, M. Miyazaki, N.H. Huh, M. Namba, and M. Akagi. 2003. Involvement of arachidonic acid in nonimmunologic production of superoxide in mast cells. International Archives of Allergy and Immunology 130: 288–299.CrossRefPubMed
20.
Zurück zum Zitat Swindle, E.J., and D.D. Metcalfe. 2007. The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory processes. Immunological Reviews 217: 186–205.CrossRefPubMed Swindle, E.J., and D.D. Metcalfe. 2007. The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory processes. Immunological Reviews 217: 186–205.CrossRefPubMed
21.
Zurück zum Zitat Trevisan, E., F. Vita, N. Medic, M.R. Soranzo, G. Zabucchi, and V. Borelli. 2014. Mast cells kill Candida albicans in the extracellular environment but spare ingested fungi from death. Inflammation 2014 Jun 21. [Epub ahead of print] Trevisan, E., F. Vita, N. Medic, M.R. Soranzo, G. Zabucchi, and V. Borelli. 2014. Mast cells kill Candida albicans in the extracellular environment but spare ingested fungi from death. Inflammation 2014 Jun 21. [Epub ahead of print]
22.
Zurück zum Zitat Padawer, J., and G.J. Fruhman. 1968. Phagocytosis of zymosan particles by mast cells. Experientia 24: 471–472.CrossRefPubMed Padawer, J., and G.J. Fruhman. 1968. Phagocytosis of zymosan particles by mast cells. Experientia 24: 471–472.CrossRefPubMed
23.
Zurück zum Zitat Otani, I., D.H. Conrad, J.R. Carlo, D.M. Segal, and S. Ruddy. 1982. Phagocytosis by rat peritoneal mast cells: independence of IgG Fc mediated and C3-mediated signals. Journal of Immunology 129: 2109–2112. Otani, I., D.H. Conrad, J.R. Carlo, D.M. Segal, and S. Ruddy. 1982. Phagocytosis by rat peritoneal mast cells: independence of IgG Fc mediated and C3-mediated signals. Journal of Immunology 129: 2109–2112.
24.
Zurück zum Zitat Féger, F., S. Varadaradjalou, Z. Gao, S.N. Abraham, and M. Arock. 2002. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends in Immunology 23: 151–158.CrossRefPubMed Féger, F., S. Varadaradjalou, Z. Gao, S.N. Abraham, and M. Arock. 2002. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends in Immunology 23: 151–158.CrossRefPubMed
25.
Zurück zum Zitat Wu, L., B.S. Feng, S.H. He, P.Y. Zheng, K. Croitoru, and P.C. Yang. 2007. Bacterial peptidoglycan breaks down intestinal tolerance via mast cell activation: the role of TLR2 and NOD2. Immunology and Cell Biology 85: 538–545.CrossRefPubMed Wu, L., B.S. Feng, S.H. He, P.Y. Zheng, K. Croitoru, and P.C. Yang. 2007. Bacterial peptidoglycan breaks down intestinal tolerance via mast cell activation: the role of TLR2 and NOD2. Immunology and Cell Biology 85: 538–545.CrossRefPubMed
26.
Zurück zum Zitat Feng, B.S., S.H. He, P.Y. Zheng, L. Wu, and P.C. Yang. 2007. Mast cells play a crucial role in Staphylococcus aureus peptidoglycan induced diarrhea. American Journal of Pathology 171: 537–547.CrossRefPubMedCentralPubMed Feng, B.S., S.H. He, P.Y. Zheng, L. Wu, and P.C. Yang. 2007. Mast cells play a crucial role in Staphylococcus aureus peptidoglycan induced diarrhea. American Journal of Pathology 171: 537–547.CrossRefPubMedCentralPubMed
27.
Zurück zum Zitat Xie, X., L. Wang, F. Gong, C. Xia, J. Chen, Y. Song, A. Shen, and J. Song. 2012. Intracellular Staphylococcus aureus-induced NF-κB activation and proinflammatory responses of P815 cells are mediated by NOD2. Journal of Huazhong University of Science and Technology Medical Science 32: 317–323.CrossRef Xie, X., L. Wang, F. Gong, C. Xia, J. Chen, Y. Song, A. Shen, and J. Song. 2012. Intracellular Staphylococcus aureus-induced NF-κB activation and proinflammatory responses of P815 cells are mediated by NOD2. Journal of Huazhong University of Science and Technology Medical Science 32: 317–323.CrossRef
28.
Zurück zum Zitat Enoksson, M., K.F. Ejendal, S. McAlpine, G. Nilsson, and C. Lunderius-Andersson. 2011. Human cord blood-derived mast cells are activated by the Nod1 agonist M-TriDAP to release pro-inflammatory cytokines and chemokines. Journal of Innate Immunity 3: 142–149.CrossRefPubMed Enoksson, M., K.F. Ejendal, S. McAlpine, G. Nilsson, and C. Lunderius-Andersson. 2011. Human cord blood-derived mast cells are activated by the Nod1 agonist M-TriDAP to release pro-inflammatory cytokines and chemokines. Journal of Innate Immunity 3: 142–149.CrossRefPubMed
29.
Zurück zum Zitat Shaw, M.H., T. Reimer, Y.G. Kim, and G. Nunez. 2008. NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Current Opinion in Immunology 20: 377–382.CrossRefPubMedCentralPubMed Shaw, M.H., T. Reimer, Y.G. Kim, and G. Nunez. 2008. NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Current Opinion in Immunology 20: 377–382.CrossRefPubMedCentralPubMed
30.
Zurück zum Zitat Magalhaes, J.G., M.T. Sorbara, S.E. Girardin, and D.J. Philpott. 2010. What is new with Nods? Current Opinion in Immunology 23: 1–6. Magalhaes, J.G., M.T. Sorbara, S.E. Girardin, and D.J. Philpott. 2010. What is new with Nods? Current Opinion in Immunology 23: 1–6.
31.
Zurück zum Zitat Antosz, H., and M. Osiak. 2013. NOD1 and NOD2 receptors: integral members of the innate and adaptive immunity system. Acta Biochimica Polonica 60: 351–360.PubMed Antosz, H., and M. Osiak. 2013. NOD1 and NOD2 receptors: integral members of the innate and adaptive immunity system. Acta Biochimica Polonica 60: 351–360.PubMed
32.
Zurück zum Zitat Philpott, D.J., M.T. Sorbara, S.J. Robertson, K. Croitoru, and S.E. Girardin. 2014. NOD proteins: regulators of inflammation in health and disease. Nature Reviews Immunology 14: 9–23.CrossRefPubMed Philpott, D.J., M.T. Sorbara, S.J. Robertson, K. Croitoru, and S.E. Girardin. 2014. NOD proteins: regulators of inflammation in health and disease. Nature Reviews Immunology 14: 9–23.CrossRefPubMed
33.
Zurück zum Zitat Shin, J.S., Z. Gao, and S.N. Abraham. 2000. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289: 785–788.CrossRefPubMed Shin, J.S., Z. Gao, and S.N. Abraham. 2000. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289: 785–788.CrossRefPubMed
34.
Zurück zum Zitat Abraham, S.N., and R. Malaviya. 1997. Mast cells in infection and immunity. Infection and Immunity 65: 3501–3508.PubMedCentralPubMed Abraham, S.N., and R. Malaviya. 1997. Mast cells in infection and immunity. Infection and Immunity 65: 3501–3508.PubMedCentralPubMed
35.
Zurück zum Zitat Medic, N., F. Vita, R. Abbate, M.R. Soranzo, S. Pacor, E. Fabbretti, V. Borelli, and G. Zabucchi. 2008. Mast cell activation by myelin through scavenger receptor. Journal of Neuroimmunology 200: 27–40.CrossRefPubMed Medic, N., F. Vita, R. Abbate, M.R. Soranzo, S. Pacor, E. Fabbretti, V. Borelli, and G. Zabucchi. 2008. Mast cell activation by myelin through scavenger receptor. Journal of Neuroimmunology 200: 27–40.CrossRefPubMed
36.
Zurück zum Zitat Minai-Fleminger, Y., M. Elishmereni, F. Vita, M.R. Soranzo, D. Mankuta, G. Zabucchi, and F. Levi-Schaffer. 2010. Ultrastructural evidence for human mast cell-eosinophil interactions in vitro. Cell and Tissue Research 341: 405–415.CrossRefPubMed Minai-Fleminger, Y., M. Elishmereni, F. Vita, M.R. Soranzo, D. Mankuta, G. Zabucchi, and F. Levi-Schaffer. 2010. Ultrastructural evidence for human mast cell-eosinophil interactions in vitro. Cell and Tissue Research 341: 405–415.CrossRefPubMed
37.
Zurück zum Zitat Zabucchi, G., M.R. Soranzo, R. Menegazzi, M. Vecchio, A. Knowles, C. Piccinini, P. Spessotto, and P. Patriarca. 1992. Eosinophil peroxidase deficiency: morphological and immunocytochemical studies of the eosinophil-specific granules. Blood 80: 2903–2910.PubMed Zabucchi, G., M.R. Soranzo, R. Menegazzi, M. Vecchio, A. Knowles, C. Piccinini, P. Spessotto, and P. Patriarca. 1992. Eosinophil peroxidase deficiency: morphological and immunocytochemical studies of the eosinophil-specific granules. Blood 80: 2903–2910.PubMed
38.
Zurück zum Zitat Straus, W.J. 1983. Mannose-specific binding sites for horseradish peroxidase in various cells of the rat. Journal of Histochemistry and Cytochemistry 31: 78–84.CrossRefPubMed Straus, W.J. 1983. Mannose-specific binding sites for horseradish peroxidase in various cells of the rat. Journal of Histochemistry and Cytochemistry 31: 78–84.CrossRefPubMed
39.
Zurück zum Zitat Knapp, S., U. Matt, N. Leitinger, and T. van der Poll. 2007. Oxidized phospholipids inhibit phagocytosis and impair outcome in Gram-negative sepsis in vivo. Journal of Immunology 178: 993–1001.CrossRef Knapp, S., U. Matt, N. Leitinger, and T. van der Poll. 2007. Oxidized phospholipids inhibit phagocytosis and impair outcome in Gram-negative sepsis in vivo. Journal of Immunology 178: 993–1001.CrossRef
40.
Zurück zum Zitat Fairn, G.D., and S. Grinstein. 2012. How nascent phagosomes mature to become phagolysosomes. Trends in Immunology 33: 397–405.CrossRefPubMed Fairn, G.D., and S. Grinstein. 2012. How nascent phagosomes mature to become phagolysosomes. Trends in Immunology 33: 397–405.CrossRefPubMed
41.
Zurück zum Zitat Gru¨tzkau, A., A. Smorodchenko, U. Lippert, L. Kirchhof, M. Artuc, and B.M. Henz. 2004. LAMP-1 and LAMP-2, but not LAMP-3, are reliable markers for activation-induced secretion of human mast cells. Cytometry Part A 61A: 62–68.CrossRef Gru¨tzkau, A., A. Smorodchenko, U. Lippert, L. Kirchhof, M. Artuc, and B.M. Henz. 2004. LAMP-1 and LAMP-2, but not LAMP-3, are reliable markers for activation-induced secretion of human mast cells. Cytometry Part A 61A: 62–68.CrossRef
42.
Zurück zum Zitat Puri, N., and P.A. Roche. 2008. Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proceedings of the National Academy of Sciences of the United States of America 105: 2580–2585.CrossRefPubMedCentralPubMed Puri, N., and P.A. Roche. 2008. Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proceedings of the National Academy of Sciences of the United States of America 105: 2580–2585.CrossRefPubMedCentralPubMed
43.
Zurück zum Zitat Mirghomizadeh, F., S. Winoto-Morbach, Z. Orinska, K.H. Lee, S. Schütze, and S. Bulfone-Paus. 2009. Intracellular IL-15 controls mast cell survival. Experimental Cell Research 315: 3064–3075.CrossRefPubMed Mirghomizadeh, F., S. Winoto-Morbach, Z. Orinska, K.H. Lee, S. Schütze, and S. Bulfone-Paus. 2009. Intracellular IL-15 controls mast cell survival. Experimental Cell Research 315: 3064–3075.CrossRefPubMed
44.
Zurück zum Zitat Beyenbach, K.W., and H. Wieczorek. 2006. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. The Journal of Experimental Biology 209: 577–589.CrossRefPubMed Beyenbach, K.W., and H. Wieczorek. 2006. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. The Journal of Experimental Biology 209: 577–589.CrossRefPubMed
45.
Zurück zum Zitat Vieira, O.V., R.J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochemical Journal 366: 689–704.PubMedCentralPubMed Vieira, O.V., R.J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochemical Journal 366: 689–704.PubMedCentralPubMed
46.
Zurück zum Zitat Dvorak, A.M. 2002. Ultrastructure of human mast cells. International Archives of Allergy and Immunology 127: 100–105.CrossRefPubMed Dvorak, A.M. 2002. Ultrastructure of human mast cells. International Archives of Allergy and Immunology 127: 100–105.CrossRefPubMed
47.
Zurück zum Zitat Hafez, M., and M.E. Costlow. 1988. Prolactin binding and localization in rat mammary tumor mast cells. Cancer Research 48: 3765–3771.PubMed Hafez, M., and M.E. Costlow. 1988. Prolactin binding and localization in rat mammary tumor mast cells. Cancer Research 48: 3765–3771.PubMed
48.
Zurück zum Zitat Xu, K., R.M. Williams, D. Holowka, and B. Baird. 1998. Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. Journal of Cell Science 111: 2385–2396.PubMed Xu, K., R.M. Williams, D. Holowka, and B. Baird. 1998. Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. Journal of Cell Science 111: 2385–2396.PubMed
49.
Zurück zum Zitat Raposo, G., D. Tenza, S. Mecheri, R. Peronet, C. Bonnerot, and C. Desaymard. 1997. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Molecular Biology of the Cell 8: 2631–2645.CrossRefPubMedCentralPubMed Raposo, G., D. Tenza, S. Mecheri, R. Peronet, C. Bonnerot, and C. Desaymard. 1997. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Molecular Biology of the Cell 8: 2631–2645.CrossRefPubMedCentralPubMed
50.
Zurück zum Zitat Dvorak, A.M. 2005. Piecemeal degranulation of basophils and mast cells is effected by vesicular transport of stored secretory granule contents. Chemical Immunology and Allergy 85: 135–184.CrossRefPubMed Dvorak, A.M. 2005. Piecemeal degranulation of basophils and mast cells is effected by vesicular transport of stored secretory granule contents. Chemical Immunology and Allergy 85: 135–184.CrossRefPubMed
51.
Zurück zum Zitat Olszewski, M.B., A.J. Groot, J. Dastych, and E.F. Knol. 2007. TNF trafficking to human mast cell granules: mature chain-dependent endocytosis. Journal of Immunology 178: 5701–5709.CrossRef Olszewski, M.B., A.J. Groot, J. Dastych, and E.F. Knol. 2007. TNF trafficking to human mast cell granules: mature chain-dependent endocytosis. Journal of Immunology 178: 5701–5709.CrossRef
52.
Zurück zum Zitat Simons, M., and G. Raposo. 2009. Exosomes vesicular carriers for intercellular communication. Current Opinion in Cell Biology 21: 575–581.CrossRefPubMed Simons, M., and G. Raposo. 2009. Exosomes vesicular carriers for intercellular communication. Current Opinion in Cell Biology 21: 575–581.CrossRefPubMed
53.
Zurück zum Zitat Nakano, H., and H. Ushio. 2011. An unexpected role for autophagy in degranulation of mast cells. Autophagy 7: 657–659.CrossRefPubMed Nakano, H., and H. Ushio. 2011. An unexpected role for autophagy in degranulation of mast cells. Autophagy 7: 657–659.CrossRefPubMed
54.
Zurück zum Zitat Madewell, B.R., R.J. Munn, and L.P. Phillips. 1987. Endocytosis of erythrocytes in vivo and particulate substances in vitro by feline neoplastic mast cells. Canadian Journal of Veterinary Research 51: 517–520.PubMedCentralPubMed Madewell, B.R., R.J. Munn, and L.P. Phillips. 1987. Endocytosis of erythrocytes in vivo and particulate substances in vitro by feline neoplastic mast cells. Canadian Journal of Veterinary Research 51: 517–520.PubMedCentralPubMed
55.
Zurück zum Zitat Bingham, C.O., R.J. Fijneman, D.S. Friend, R.P. Goddeau, R.A. Rogers, K.F. Austen, and J.P. Arm. 1999. Low molecular weight group IIA and group V phospholipase A(2) enzymes have different intracellular locations in mouse bone marrow-derived mast cells. Journal of Biological Chemistry 274: 31476–31484. Bingham, C.O., R.J. Fijneman, D.S. Friend, R.P. Goddeau, R.A. Rogers, K.F. Austen, and J.P. Arm. 1999. Low molecular weight group IIA and group V phospholipase A(2) enzymes have different intracellular locations in mouse bone marrow-derived mast cells. Journal of Biological Chemistry 274: 31476–31484.
56.
Zurück zum Zitat Fernández-Arenas, E., C.K.E. Bleck, C. Nombela, C. Gil, G. Griffiths, and R. Diez-Orejas. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cellular Microbiology 11: 560–589.CrossRefPubMed Fernández-Arenas, E., C.K.E. Bleck, C. Nombela, C. Gil, G. Griffiths, and R. Diez-Orejas. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cellular Microbiology 11: 560–589.CrossRefPubMed
57.
Zurück zum Zitat Clemens, D.L., B.Y. Lee, and M.A. Horwitz. 2004. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infection and Immunity 72: 3204–3217.CrossRefPubMedCentralPubMed Clemens, D.L., B.Y. Lee, and M.A. Horwitz. 2004. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infection and Immunity 72: 3204–3217.CrossRefPubMedCentralPubMed
58.
Zurück zum Zitat Barnich, N., J. E. Aguirre, H.C. Reinecker, R. Xavier, and D. K. Podolsky. 2005. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-B activation in muramyl dipeptide recognition. Journal of Cell Biology 170: 21–26. Barnich, N., J. E. Aguirre, H.C. Reinecker, R. Xavier, and D. K. Podolsky. 2005. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-B activation in muramyl dipeptide recognition. Journal of Cell Biology 170: 21–26.
59.
Zurück zum Zitat Lécine, P., S. Esmiol, J.Y. Métais, C. Nicoletti, C. Nourry, C. McDonald, G. Nunez, J.P. Hugot, J.P. Borg, and V. Ollendorff. 2007. The NOD2-RICK complex signals from the plasma membrane. Journal of Biological Chemistry 282: 15197–15207.CrossRefPubMed Lécine, P., S. Esmiol, J.Y. Métais, C. Nicoletti, C. Nourry, C. McDonald, G. Nunez, J.P. Hugot, J.P. Borg, and V. Ollendorff. 2007. The NOD2-RICK complex signals from the plasma membrane. Journal of Biological Chemistry 282: 15197–15207.CrossRefPubMed
60.
Zurück zum Zitat Kufer, T.A., E. Kremmer, A.C. Adam, D.J. Philpott, and P.J. Sansonetti. 2008. The pattern-recognition molecule Nod1 is localized at the plasma membrane at sites of bacterial interaction. Cellular Microbiology 10: 477–486.PubMed Kufer, T.A., E. Kremmer, A.C. Adam, D.J. Philpott, and P.J. Sansonetti. 2008. The pattern-recognition molecule Nod1 is localized at the plasma membrane at sites of bacterial interaction. Cellular Microbiology 10: 477–486.PubMed
61.
Zurück zum Zitat Izushi, K., Y. Fujiwara, and K. Tasaka. 1992. Identification of vimentin in rat peritoneal mast cells and its phosphorylation in association with histamine release. Immunopharmacology 23: 153–161.CrossRefPubMed Izushi, K., Y. Fujiwara, and K. Tasaka. 1992. Identification of vimentin in rat peritoneal mast cells and its phosphorylation in association with histamine release. Immunopharmacology 23: 153–161.CrossRefPubMed
62.
Zurück zum Zitat Tasaka, K. 1994. Molecular mechanism of histamine release: the role of intermediate filaments and membrane skeletons. Journal of Physiology and Pharmacology 45: 479–492.PubMed Tasaka, K. 1994. Molecular mechanism of histamine release: the role of intermediate filaments and membrane skeletons. Journal of Physiology and Pharmacology 45: 479–492.PubMed
63.
Zurück zum Zitat Di Nardo, A., A. Vitiello, and R.L. Gallo. 2003. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. Journal of Immunology 170: 2274–2278.CrossRef Di Nardo, A., A. Vitiello, and R.L. Gallo. 2003. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. Journal of Immunology 170: 2274–2278.CrossRef
64.
Zurück zum Zitat von Köckritz-Blickwede, M., O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, and E. Medina. 2008. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111: 3070–3080.CrossRef von Köckritz-Blickwede, M., O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, and E. Medina. 2008. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111: 3070–3080.CrossRef
Metadaten
Titel
NOD1 and NOD2 Interact with the Phagosome Cargo in Mast Cells: A Detailed Morphological Evidence
verfasst von
Giuliano Zabucchi
Elisa Trevisan
Francesca Vita
Maria Rosa Soranzo
Violetta Borelli
Publikationsdatum
01.06.2015
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 3/2015
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-014-0077-x

Weitere Artikel der Ausgabe 3/2015

Inflammation 3/2015 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.