MCPIP1 regulates alveolar macrophage apoptosis and pulmonary fibroblast activation after in vitro exposure to silica

Toxicological Sciences

Volumn 151, Issue 1, 2016, Pages 126-138

  Wang, Xingang ^a   Zhang, Yuxia ^a   Zhang, Wei ^a   Liu, Haijun ^a,b   Zhou, Zewei ^a   Dai, Xiaoniu ^a   Cheng, Yusi ^a   Fang, Shencun ^c   Zhang, Yingming ^c   Yao, Honghong ^a,d   Chao, Jie ^a,d  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b CHINA PHARMACEUTICAL UNIVERSITY   (China)

^c NANJING CHEST HOSPITAL   (China)

^d SOUTHEAST UNIVERSITY   (China)

Author keywords

Apoptosis; Fibroblast; Macrophage; MCPIP1; Silicosis

Indexed keywords

MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN INDUCED PROTEIN 1; SILICON DIOXIDE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; COLLAGEN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RIBONUCLEASE; ZC3H12A PROTEIN, RAT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTRACTION ASSAY; CULTURE MEDIUM; DOWN REGULATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROBLAST; MACROPHAGE ACTIVATION; MALE; NONHUMAN; RAT; SILICOSIS; UPREGULATION; ANIMAL; CELL CULTURE; CELL MOTION; CONDITIONED MEDIUM; DRUG EFFECTS; FIBROBLAST; GENETIC TRANSFECTION; GENETICS; LUNG; METABOLISM; PARACRINE SIGNALING; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; CULTURE MEDIA, CONDITIONED; FIBROBLASTS; LUNG; MACROPHAGES, ALVEOLAR; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; PARACRINE COMMUNICATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS, SPRAGUE-DAWLEY; RIBONUCLEASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SILICON DIOXIDE; SILICOSIS; TIME FACTORS; TRANSFECTION;

EID: 84978863636     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfw029     Document Type: Article

References (65)

1. Baggiolini, M., and Dahinden, C. A. (1994). CC chemokines in allergic inflammation. Immunol. Today 15, 127-133.
2. Bell, E., Ivarsson, B., and Merrill, C. (1979). Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. U S A 76, 1274-1278.
3. Bhandary, Y. P., Shetty, S. K., Marudamuthu, A. S., Fu, J., Pinson, B. M., Levin, J., and Shetty, S. (2015). Role of p53-fibrinolytic system cross-talk in the regulation of quartz-induced lung injury. Toxicol. Appl. Pharmacol. 283, 92-98.
4. Borges, V. M., Falcao, H., Leite-Junior, J. H., Alvim, L., Teixeira, G. P., Russo, M., Nobrega, A. F., Lopes, M. F., Rocco, P. M., Davidson, W. F., et al. (2001). Fas ligand triggers pulmonary silicosis. J. Exp. Med. 194, 155-164.
5. Brown, J. M., Swindle, E. J., Kushnir-Sukhov, N. M., Holian, A., and Metcalfe, D. D. (2007). Silica-directed mast cell activation is enhanced by scavenger receptors. Am. J. Respir. Cell Mol. Biol. 36, 43-52.
6. Carlson, M. A., Longaker, M. T., and Thompson, J. S. (2004). Modulation of FAK, Akt, and p53 by stress release of the fibroblast-populated collagen matrix. J. Surg. Res. 120, 171-177.
7. Carlson, M. A., Prall, A. K., and Gums, J. J. (2007). RNA interference in human foreskin fibroblasts within the three-dimensional collagen matrix. Mol. Cell. Biochem. 306, 123-132.
8. Chao, J., Wood, J. G., Blanco, V. G., and Gonzalez, N. C. (2009). The systemic inflammation of alveolar hypoxia is initiated by alveolar macrophage-borne mediator(s). Am. J. Respir. Cell Mol. Biol. 41, 573-582.
9. Chao, J., Donham, P., van Rooijen, N., Wood, J. G., and Gonzalez, N. C. (2011). Monocyte chemoattractant protein-1 released from alveolar macrophages mediates the systemic inflammation of acute alveolar hypoxia. Am. J. Respir. Cell Mol. Biol. 45, 53-61.
10. Chao, J., Pena, T., Heimann, D. G., Hansen, C., Doyle, D. A., Yanala, U. R., Guenther, T. M., and Carlson, M. A. (2014). Expression of green fluorescent protein in human foreskin fibroblasts for use in 2D and 3D culture models. Wound Repair Regen. 22, 134-140.
11. Delgado, L., Parra, E. R., and Capelozzi, V. L. (2006). Apoptosis and extracellular matrix remodelling in human silicosis. Histopathology 49, 283-289.
12. Even-Ram, S., and Yamada, K. M. (2005). Cell migration in 3D matrix. Curr. Opin. Cell. Biol. 17, 524-532.
13. Fazzi, F., Njah, J., Di Giuseppe, M., Winnica, D. E., Go, K., Sala, E., St Croix, C. M., Watkins, S. C., Tyurin, V. A., Phinney, D. G., et al. (2014). TNFR1/phox interaction and TNFR1 mitochondrial translocation Thwart silica-induced pulmonary fibrosis. J. Immunol. 192, 3837-3846.
14. Fujimura, N. (2000). Pathology and pathophysiology of pneumoconiosis. Curr. Opin. Pulm. Med. 6, 140-144.
15. Genin, M., Clement, F., Fattaccioli, A., Raes, M., and Michiels, C. (2015). M1 and M2 macrophages derived from THP-1 cells differentially modulate the response of cancer cells to etopo-side. BMC Cancer 15, 577
16. Gharaee-Kermani, M., Denholm, E. M., and Phan, S. H. (1996). Costimulation of fibroblast collagen and transforming growth factor beta1 gene expression by monocyte chemoattractant protein-1 via specific receptors. J. Biol. Chem. 271, 17779-17784.
17. Goldsmith, E. C., Hoffman, A., Morales, M. O., Potts, J. D., Price, R. L., McFadden, A., Rice, M., and Borg, T. K. (2004). Organization of fibroblasts in the heart. Dev. Dyn. 230, 787-794.
18. Gordon, S. (2003). Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35.
19. Grinnell, F. (1994). Fibroblasts, myofibroblasts, and wound contraction. J. Cell. Biol. 124, 401-404.
20. Grinnell, F., Zhu, M., Carlson, M. A., and Abrams, J. M. (1999). Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp. Cell. Res. 248, 608-619.
21. Grinnell, F. (2003). Fibroblast biology in three-dimensional collagen matrices. Trends Cell. Biol. 13, 264-269.
22. Grinnell, F., Rocha, L. B., Iucu, C., Rhee, S., and Jiang, H. (2006). Nested collagen matrices: a new model to study migration of human fibroblast populations in three dimensions. Exp. Cell. Res. 312, 86-94.
23. Grinnell, F., and Petroll, W. M. (2010). Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell. Dev. Biol. 26, 335-361.
24. Gu, W., Song, J., Cao, Y., Sun, Q., Yao, H., Wu, Q., Chao, J., Zhou, J., Xue, W., and Duan, J. (2013). Application of the ITS2 region for barcoding medicinal plants of selaginellaceae in pteridophyta. PLoS One 8, e67818
25. Hamilton, R. F., Jr., Thakur, S. A., and Holian, A. (2008). Silica binding and toxicity in alveolar macrophages. Free Radic. Biol. Med. 44, 1246-1258.
26. Hao, C. F., Li, X. F., and Yao, W. (2013). Role of insulin-like growth factor II receptor in transdifferentiation of free silica-induced primary rat lung fibroblasts. Biomed. Environ. Sci. 26, 979-985.
27. Huang, S., Qi, D., Liang, J., Miao, R., Minagawa, K., Quinn, T., Matsui, T., Fan, D., Liu, J., and Fu, M. (2012). The putative tumor suppressor Zc3h12d modulates toll-like receptor signaling in macrophages. Cell. Signal. 24, 569-576.
28. Huaux, F. (2007). New developments in the understanding of immunology in silicosis. Curr. Opin. Allergy Clin. Immunol. 7, 168-173.
29. Jain, R. K. (2005). Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58-62.
30. Jawad, H., Boccaccini, A. R., Ali, N. N., and Harding, S. E. (2011). Assessment of cellular toxicity of TiO2 nanoparticles for cardiac tissue engineering applications. Nanotoxicology 5, 372-380.
31. Kessler, D., Dethlefsen, S., Haase, I., Plomann, M., Hirche, F., Krieg, T., and Eckes, B. (2001). Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J. Biol. Chem. 276, 36575-36585.
32. Langevin, H. M., Bouffard, N. A., Badger, G. J., Iatridis, J. C., and Howe, A. K. (2005). Dynamic fibroblast cytoskeletal response to subcutaneous tissue stretch ex vivo and in vivo. Am. J. Physiol. Cell Physiol. 288, C747-C756.
33. Lee, D. J., Rosenfeldt, H., and Grinnell, F. (2000). Activation of ERK and p38 MAP kinases in human fibroblasts during collagen matrix contraction. Exp. Cell Res. 257, 190-197.
34. Lee, J. K., Sayers, B. C., Chun, K. S., Lao, H. C., Shipley-Phillips, J. K., Bonner, J. C., and Langenbach, R. (2012). Multi-walled carbon nanotubes induce COX-2 and iNOS expression via MAP kinase-dependent and-independent mechanisms in mouse RAW264.7 macrophages. Part. Fibre Toxicol. 9,14
35. Leung, C. C., Yu, I. T., and Chen, W. (2012). Silicosis. Lancet 379, 2008-2018.
36. Liang, J., Wang, J., Azfer, A., Song, W., Tromp, G., Kolattukudy, P. E., and Fu, M. (2008). A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J. Biol. Chem. 283, 6337-6346.
37. Lim, Y., Kim, J. H., Kim, K. A., Chang, H. S., Park, Y. M., Ahn, B. Y., and Phee, Y. G. (1999). Silica-induced apoptosis in vitro and in vivo. Toxicol. Lett. 108, 335-339.
38. Liu, H., Dai, X., Cheng, Y., Fang, S., Zhang, Y., Wang, X., Zhang, W., Liao, H., Yao, H., and Chao, J. (2015a). MCPIP1 mediates silica-induced cell migration in human pulmonary fibro-blasts. Am. J. Physiol. Lung Cell. Mol. Physiol. ajplung 00278 2015.
39. Liu, X., Fang, S., Liu, H., Wang, X., Dai, X., Yin, Q., Yun, T., Wang, W., Zhang, Y., Liao, H., et al. (2015b). Role of human pulmonary fibroblast-derived MCP-1 in cell activation and migration in experimental silicosis. Toxicol. Appl. Pharmacol. 288, 152-160.
40. Low, Q. E., Drugea, I. A., Duffner, L. A., Quinn, D. G., Cook, D. N., Rollins, B. J., Kovacs, E. J., and DiPietro, L. A. (2001). Wound healing in MIP-1alpha(-/-) and MCP-1(-/-) mice. Am. J. Pathol. 159, 457-463.
41. Martinez, F. O., Helming, L., and Gordon, S. (2009). Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27, 451-483.
42. Matsushita, K., Takeuchi, O., Standley, D. M., Kumagai, Y., Kawagoe, T., Miyake, T., Satoh, T., Kato, H., Tsujimura, T., Nakamura, H., and Akira, S. (2009). Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature 458, 1185-1190.
43. Moore, B. B., Paine, R., 3rd, Christensen, P. J., Moore, T. A., Sitterding, S., Ngan, R., Wilke, C. A., Kuziel, W. A., and Toews, G. B. (2001). Protection from pulmonary fibrosis in the absence of CCR2 signaling. J. Immunol. 167, 4368-4377.
44. Moore, B. B., Peters-Golden, M., Christensen, P. J., Lama, V., Kuziel, W. A., Paine, R., 3rd., and Toews, G. B. (2003). Alveolar epithelial cell inhibition of fibroblast proliferation is regulated by MCP-1/CCR2 and mediated by PGE2. Am. J. Physiol. Lung Cell Mol. Physiol. 284, L342-L349.
45. Mossman, B. T., and Churg, A. (1998). Mechanisms in the pathogenesis of asbestosis and silicosis. Am. J. Respir. Crit. Care Med. 157, 1666-1680.
46. Niu, J., Azfer, A., Zhelyabovska, O., Fatma, S., and Kolattukudy, P. E. (2008). Monocyte chemotactic protein (MCP)-1 promotes angiogenesis via a novel transcription factor, MCP-1-induced protein (MCPIP). The. J. Biol. Chem. 283, 14542-14551.
47. Pampaloni, F., Reynaud, E. G., and Stelzer, E. H. (2007). The third dimension bridges the gap between cell culture and live tissue. Nat. Rev. Mol. Cell. Biol. 8, 839-845.
48. Pfau, J. C., Brown, J. M., and Holian, A. (2004). Silica-exposed mice generate autoantibodies to apoptotic cells. Toxicology 195, 167-176.
49. Qi, D., Huang, S., Miao, R., She, Z. G., Quinn, T., Chang, Y., Liu, J., Fan, D., Chen, Y. E., and Fu, M. (2011). Monocyte chemotactic protein-induced protein 1 (MCPIP1) suppresses stress granule formation and determines apoptosis under stress. J. Biol. Chem. 286, 41692-41700.
50. Ransohoff, R. M., Glabinski, A., and Tani, M. (1996). Chemokines in immune-mediated inflammation of the central nervous system. Cytokine Growth Factor Rev. 7, 35-46.
51. Rao, K. M., Porter, D. W., Meighan, T., and Castranova, V. (2004). The sources of inflammatory mediators in the lung after silica exposure. Environ. Health Perspect. 112, 1679-1686.
52. Rao, K. M., Ma, J. Y., Meighan, T., Barger, M. W., Pack, D., and Vallyathan, V. (2005). Time course of gene expression of inflammatory mediators in rat lung after diesel exhaust particle exposure. Environ. Health Perspect. 113, 612-617.
53. Rhee, S., and Grinnell, F. (2007). Fibroblast mechanics in 3D collagen matrices. Adv. Drug Deliv. Rev. 59, 1299-1305.
54. Rhee, S. (2009). Fibroblasts in three dimensional matrices: cell migration and matrix remodeling. Exp. Mol. Med. 41, 858-865.
55. Rodriguez-Menocal, L., Salgado, M., Ford, D., and Van Badiavas, E. (2012). Stimulation of skin and wound fibroblast migration by mesenchymal stem cells derived from normal donors and chronic wound patients. Stem Cells Trans. Med. 1, 221-229.
56. Silva, D., Caceres, M., Arancibia, R., Martinez, C., Martinez, J., and Smith, P. C. (2012). Effects of cigarette smoke and nicotine on cell viability, migration and myofibroblastic differentiation. J. Periodontal. Res. 47, 599-607.
57. Thakur, S. A., Hamilton, R., Jr., Pikkarainen, T., and Holian, A. (2009). Differential binding of inorganic particles to MARCO. Toxicol. Sci. 107, 238-246.
58. Van Ginderachter, J. A., Movahedi, K., Hassanzadeh Ghassabeh, G., Meerschaut, S., Beschin, A., Raes, G., and De Baetselier, P. (2006). Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 211, 487-501.
59. Wang, W., Liu, H., Dai, X., Fang, S., Wang, X., Zhang, Y., Yao, H., Zhang, X., and Chao, J. (2015). p53/PUMA expression in human pulmonary fibroblasts mediates cell activation and migration in silicosis. Sci. Rep. 5, 16900
60. Yao, H., Ma, R., Yang, L., Hu, G., Chen, X., Duan, M., Kook, Y., Niu, F., Liao, K., Fu, M., et al. (2014). MiR-9 promotes microglial activation by targeting MCPIP1. Nat. Commun. 5, 4386
61. Younce, C. W., and Kolattukudy, P. E. (2010). MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP. Biochem. J. 426, 43-53.
62. Zhou, C., and Petroll, W. M. (2010). Rho kinase regulation of fibro-blast migratory mechanics in fibrillar collagen matrices. Cell. Mol. Bioeng. 3, 76-83.
63. Zhou, L., Azfer, A., Niu, J., Graham, S., Choudhury, M., Adamski, F. M., Younce, C., Binkley, P. F., and Kolattukudy, P. E. (2006). Monocyte chemoattractant protein-1 induces a novel transcription factor that causes cardiac myocyte apoptosis and ventricular dysfunction. Circ. Res. 98, 1177-1185.
64. Zhu, T., Yao, Q., Hu, X., Chen, C., Yao, H., and Chao, J. (2015). The Role of MCPIP1 in Ischemia/Reperfusion Injury-Induced HUVEC Migration and Apoptosis. Cell. Physiol. Biochem. 37, 577-591.
65. Zickus, C., Kunkel, S. L., Simpson, K., Evanoff, H., Glass, M., Strieter, R. M., and Lukacs, N. W. (1998). Differential regulation of C-C chemokines during fibroblast-monocyte interactions: adhesion vs. inflammatory cytokine pathways. Mediators Inflamm 7, 269-274.