The role of the CCL2/CCR2 axis in mouse mast cell migration in vitro and in vivo

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6114-6123

  Collington, Sarah J ^a,e   Hallgren, Jenny ^c,f   Pease, James E ^a   Jones, Tatiana G ^c   Rollins, Barrett J ^c,d   Westwick, John ^b   Austen, K Frank ^c   Williams, Timothy J ^a   Gurish, Michael F ^c   Weller, Charlotte L ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; INTERLEUKIN 3; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; STEM CELL FACTOR; ALLERGEN; CCR2 PROTEIN, MOUSE; OVALBUMIN;

AFFINITY LABELING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHIOLE; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MAST CELL; MIGRATION; MOUSE; MOUSE STRAIN; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; STATISTICAL SIGNIFICANCE; STROMA; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; LUNG LAVAGE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; RESPIRATORY TRACT ALLERGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ALLERGENS; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINE CCL2; CHEMOTAXIS, LEUKOCYTE; FEMALE; HEMATOPOIETIC STEM CELLS; MAST CELLS; MICE; MICE, INBRED BALB C; OVALBUMIN; RECEPTORS, CCR2; RESPIRATORY HYPERSENSITIVITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELL FACTOR;

EID: 77953414965     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0904177     Document Type: Article

References (48)

1. Marshall, J. S. 2004. Mast-cell responses to pathogens. Nat. Rev. Immunol. 4: 787-799.
2. Kitamura, Y., S. Go, and K. Hatanaka. 1978. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 52: 447-452.
3. Jamur, M. C., A. C. Grodzki, E. H. Berenstein, M. M. Hamawy, R. P. Siraganian, and C. Oliver. 2005. Identification and characterization of undifferentiated mast cells in mouse bone marrow. Blood 105: 4282-4289.
4. Chen, C. C., M. A. Grimbaldeston, M. Tsai, I. L. Weissman, and S. J. Galli. 2005. Identification of mast cell progenitors in adult mice. Proc. Natl. Acad. Sci. USA 102: 11408-11413.
5. Arinobu, Y., H. Iwasaki, M. F. Gurish, S. Mizuno, H. Shigematsu, H. Ozawa, D. G. Tenen, K. F. Austen, and K. Akashi. 2005. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. Proc. Natl. Acad. Sci. USA 102: 18105-18110.
6. Rodewald, H. R., M. Dessing, A. M. Dvorak, and S. J. Galli. 1996. Identification of a committed precursor for the mast cell lineage. Science 271: 818-822.
7. Gurish, M. F., W. S. Pear, R. L. Stevens, M. L. Scott, K. Sokol, N. Ghildyal, M. J. Webster, X. Hu, K. F. Austen, D. Baltimore, et al. 1995. Tissue-regulated differentiation and maturation of a v-abl-immortalized mast cell-committed progenitor. Immunity 3: 175-186.
8. Friend, D. S., N. Ghildyal, K. F. Austen, M. F. Gurish, R. Matsumoto, and R. L. Stevens. 1996. Mast cells that reside at different locations in the jejunum of mice infected with Trichinella spiralis exhibit sequential changes in their granule ultrastructure and chymase phenotype. J. Cell Biol. 135: 279-290.
9. Befus, A. D., and J. Bienenstock. 1979. Immunologically mediated intestinal mastocytosis in Nippostrongylus brasiliensis-infected rats. Immunology 38: 95-101.
10. Pipkorn, U., G. Karlsson, and L. Enerbäck. 1988. Phenotypic expression of proteoglycan in mast cells of the human nasal mucosa. Histochem. J. 20: 519-525.
11. Fokkens, W. J., T. Godthelp, A. F. Holm, H. Blom, P. G. Mulder, T. M. Vroom, and E. Rijntjes. 1992. Dynamics of mast cells in the nasal mucosa of patients with allergic rhinitis and non-allergic controls: a biopsy study. Clin. Exp. Allergy 22: 701-710.
12. Nouri-Aria, K. T., C. Pilette, M. R. Jacobson, H. Watanabe, and S. R. Durham. 2005. IL-9 and c-Kit+ mast cells in allergic rhinitis during seasonal allergen exposure: effect of immunotherapy. J. Allergy Clin. Immunol. 116: 73-79.
13. Brightling, C. E., P. Bradding, F. A. Symon, S. T. Holgate, A. J. Wardlaw, and I. D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346: 1699-1705.
14. Carroll, N. G., S. Mutavdzic, and A. L. James. 2002. Increased mast cells and neutrophils in submucosal mucous glands and mucus plugging in patients with asthma. Thorax 57: 677-682.
15. Mwamtemi, H. H., K. Koike, T. Kinoshita, S. Ito, S. Ishida, Y. Nakazawa, Y. Kurokawa, K. Shinozaki, K. Sakashita, K. Takeuchi, et al. 2001. An increase in circulating mast cell colony-forming cells in asthma. J. Immunol. 166: 4672-4677.
16. Ikeda, R. K., M. Miller, J. Nayar, L. Walker, J. Y. Cho, K. McElwain, S. McElwain, E. Raz, and D. H. Broide. 2003. Accumulation of peribronchial mast cells in a mouse model of ovalbumin allergen induced chronic airway inflammation: modulation by immunostimulatory DNA sequences. J. Immunol. 171: 4860-4867.
17. Yu, M., M. Tsai, S. Y. Tam, C. Jones, J. Zehnder, and S. J. Galli. 2006. Mast cells can promote the development of multiple features of chronic asthma in mice. J. Clin. Invest. 116: 1633-1641.
18. Abonia, J. P., K. F. Austen, B. J. Rollins, S. K. Joshi, R. A. Flavell, W. A. Kuziel, P. A. Koni, and M. F. Gurish. 2005. Constitutive homing of mast cell progenitors to the intestine depends on autologous expression of the chemokine receptor CXCR2. Blood 105: 4308-4313.
19. Gurish, M. F., H. Tao, J. P. Abonia, A. Arya, D. S. Friend, C. M. Parker, and K. F. Austen. 2001. Intestinal mast cell progenitors require CD49dbeta7 (alpha4beta7 integrin) for tissue-specific homing. J. Exp. Med. 194: 1243-1252.
20. Artis, D., N. E. Humphreys, C. S. Potten, N. Wagner, W. Müller, J. R. McDermott, R. K. Grencis, and K. J. Else. 2000. Beta7 integrin-deficient mice: delayed leukocyte recruitment and attenuated protective immunity in the small intestine during enteric helminth infection. Eur. J. Immunol. 30: 1656-1664.
21. Abonia, J. P., J. Hallgren, T. Jones, T. Shi, Y. Xu, P. Koni, R. A. Flavell, J. A. Boyce, K. F. Austen, and M. F. Gurish. 2006. Alpha-4 integrins and VCAM-1, but not MAdCAM-1, are essential for recruitment of mast cell progenitors to the inflamed lung. Blood 108: 1588-1594.
22. Hallgren, J., T. G. Jones, J. P. Abonia, W. Xing, A. Humbles, K. F. Austen, and M. F. Gurish. 2007. Pulmonary CXCR2 regulates VCAM-1 and antigen-induced recruitment of mast cell progenitors. Proc. Natl. Acad. Sci. USA 104: 20478-20483.
23. Weller, C. L., S. J. Collington, J. K. Brown, H. R. Miller, A. Al-Kashi, P. Clark, P. J. Jose, A. Hartnell, and T. J. Williams. 2005. Leukotriene B4, an activation product of mast cells, is a chemoattractant for their progenitors. J. Exp. Med. 201: 1961-1971.
24. Weller, C. L., S. J. Collington, A. Hartnell, D. M. Conroy, T. Kaise, J. E. Barker, M. S. Wilson, G. W. Taylor, P. J. Jose, and T. J. Williams. 2007. Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proc. Natl. Acad. Sci. USA 104: 11712-11717.
25. Lu, B., B. J. Rutledge, L. Gu, J. Fiorillo, N. W. Lukacs, S. L. Kunkel, R. North, C. Gerard, and B. J. Rollins. 1998. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med. 187: 601-608.
26. Williams, C. M., and S. J. Galli. 2000. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. J. Exp. Med. 192: 455-462.
27. Crapper, R. M., and J. W. Schrader. 1983. Frequency of mast cell precursors in normal tissues determined by an in vitro assay: antigen induces parallel increases in the frequency of P cell precursors and mast cells. J. Immunol. 131: 923-928.
28. Brown, J. K., P. A. Knight, S. H. Wright, E. M. Thornton, and H. R. Miller. 2003. Constitutive secretion of the granule chymase mouse mast cell protease-1 and the chemokine, CCL2, by mucosal mast cell homologues. Clin. Exp. Allergy 33: 132-146.
29. Pemberton, A. D., J. K. Brown, S. H. Wright, P. A. Knight, M. L. McPhee, A. R. McEuen, P. A. Forse, and H. R. Miller. 2003. Purification and characterization of mouse mast cell proteinase-2 and the differential expression and release of mouse mast cell proteinase-1 and -2 in vivo. Clin. Exp. Allergy 33: 1005-1012.
30. Martinelli, R., I. Sabroe, G. LaRosa, T. J. Williams, and J. E. Pease. 2001. The CC chemokine eotaxin (CCL11) is a partial agonist of CC chemokine receptor 2b. J. Biol. Chem. 276: 42957-42964.
31. Miller, H. R., S. H. Wright, P. A. Knight, and E. M. Thornton. 1999. A novel function for transforming growth factor-beta1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1. Blood 93: 3473-3486.
32. Terashima, Y., N. Onai, M. Murai, M. Enomoto, V. Poonpiriya, T. Hamada, K. Motomura, M. Suwa, T. Ezaki, T. Haga, et al. 2005. Pivotal function for cytoplasmic protein FROUNT in CCR2-mediated monocyte chemotaxis. Nat. Immunol. 6: 827-835.
33. Belema-Bedada, F., S. Uchida, A. Martire, S. Kostin, and T. Braun. 2008. Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2: 566-575.
34. Eklund, K. K., N. Ghildyal, K. F. Austen, D. S. Friend, V. Schiller, and R. L. Stevens. 1994. Mouse bone marrow-derived mast cells (mBMMC) obtained in vitro from mice that are mast cell-deficient in vivo express the same panel of granule proteases as mBMMC and serosal mast cells from their normal littermates. J. Exp. Med. 180: 67-73.
35. Serbina, N. V., T. Jia, T. M. Hohl, and E. G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26: 421-452.
36. Oliveira, S. H., and N. W. Lukacs. 2001. Stem cell factor and igE-stimulated murine mast cells produce chemokines (CCL2, CCL17, CCL22) and express chemokine receptors. Inflamm. Res. 50: 168-174.
37. Baghestanian, M., R. Hofbauer, H. P. Kiener, H. C. Bankl, F. Wimazal, M. Willheim, O. Scheiner, W. Füreder, M. R. Müller, D. Bevec, et al. 1997. The c-kit ligand stem cell factor and anti-IgE promote expression of monocyte chemoattractant protein-1 in human lung mast cells. Blood 90: 4438-4449.
38. Lin, D. A., and J. A. Boyce. 2005. IL-4 regulates MEK expression required for lysophosphatidic acid-mediated chemokine generation by human mast cells. J. Immunol. 175: 5430-5438.
39. Gonzalo, J. A., C. M. Lloyd, D. Wen, J. P. Albar, T. N. Wells, A. Proudfoot, C. Martinez-A, M. Dorf, T. Bjerke, A. J. Coyle, and J. C. Gutierrez-Ramos. 1998. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J. Exp. Med. 188: 157-167.
40. Lukacs, N. W., R. M. Strieter, K. Warmington, P. Lincoln, S. W. Chensue, and S. L. Kunkel. 1997. Differential recruitment of leukocyte populations and alteration of airway hyperreactivity by C-C family chemokines in allergic airway inflammation. J. Immunol. 158: 4398-4404.
41. -/- mice: the role of mast cells. J. Immunol. 163: 2160-2167.
42. Alam, R., J. York, M. Boyars, S. Stafford, J. A. Grant, J. Lee, P. Forsythe, T. Sim, and N. Ida. 1996. Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am. J. Respir. Crit. Care Med. 153: 1398-1404.
43. Holgate, S. T., K. S. Bodey, A. Janezic, A. J. Frew, A. P. Kaplan, and L. M. Teran. 1997. Release of RANTES, MIP-1 alpha, and MCP-1 into asthmatic airways following endobronchial allergen challenge. Am. J. Respir. Crit. Care Med. 156: 1377-1383.
44. Sanchez, O., E. Marcos, F. Perros, E. Fadel, L. Tu, M. Humbert, P. Dartevelle, G. Simonneau, S. Adnot, and S. Eddahibi. 2007. Role of endothelium-derived CC chemokine ligand 2 in idiopathic pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 176: 1041-1047.
45. Dzenko, K. A., L. Song, S. Ge, W. A. Kuziel, and J. S. Pachter. 2005. CCR2 expression by brain microvascular endothelial cells is critical for macrophage transendothelial migration in response to CCL2. Microvasc. Res. 70: 53-64.
46. Christensen, P. J., M. Du, B. Moore, S. Morris, G. B. Toews, and R. Paine, III. 2004. Expression and functional implications of CCR2 expression on murine alveolar epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 286: L68-L72.
47. Hogaboam, C. M., C. L. Bone-Larson, S. Lipinski, N. W. Lukacs, S. W. Chensue, R. M. Strieter, and S. L. Kunkel. 1999. Differential monocyte chemoattractant protein-1 and chemokine receptor 2 expression by murine lung fibroblasts derived from Th1- and Th2-type pulmonary granuloma models. J. Immunol. 163: 2193-2201.
48. Taub, D., J. Dastych, N. Inamura, J. Upton, D. Kelvin, D. Metcalfe, and J. Oppenheim. 1995. Bone marrow-derived murine mast cells migrate, but do not degranulate, in response to chemokines. J. Immunol. 154: 2393-2402.