Group V secretory phospholipase A2 is involved in macrophage activation and is sufficient for macrophage effector functions in allergic pulmonary inflammation

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 5927-5938

  Ohta, Shin ^a,b   Imamura, Mitsuru ^a,b   Xing, Wei ^a,b   Boyce, Joshua A ^a,b,c   Balestrieri, Barbara ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c SHOWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; CHEMOKINE; INTERLEUKIN 4; MACROPHAGE DERIVED CHEMOKINE; PHOSPHOLIPASE A2 GROUP V; SECRETORY PHOSPHOLIPASE A2; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ADOPTIVE TRANSFER; ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELL ISOLATION; CELL TRANSFER; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATOPHAGOIDES FARINAE; DISEASE COURSE; DISEASE SEVERITY; EFFECTOR CELL; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INDUCTION; ENZYME LOCALIZATION; EOSINOPHILIA; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LOEFFLER PNEUMONIA; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PATHOGENESIS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVOCATION TEST; SENSITIZATION; T LYMPHOCYTE; TH2 CELL;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; GROUP V PHOSPHOLIPASES A2; HUMANS; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PNEUMONIA; T-LYMPHOCYTES;

EID: 84879126252     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203202     Document Type: Article

References (53)

1. Burke, J. E., and E. A. Dennis. 2009. Phospholipase A2 structure/function, mechanism, and signaling. J. Lipid Res. 50(Suppl): S237-S242.
2. Okunishi, K., and M. Peters-Golden. 2011. Leukotrienes and airway inflammation. Biochim. Biophys. Acta 1810: 1096-1102.
3. Boyce, J. A. 2008. Eicosanoids in asthma, allergic inflammation, and host defense. Curr. Mol. Med. 8: 335-349.
4. Gijón, M. A., D. M. Spencer, A. R. Siddiqi, J. V. Bonventre, and C. C. Leslie. 2000. Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that Do and Do not mobilize calcium. Novel role of mitogen-activated protein kinase pathways in cytosolic phospholipase A2 regulation. J. Biol. Chem. 275: 20146-20156. (Pubitemid 30441626)
5. Lambeau, G., and M. H. Gelb. 2008. Biochemistry and physiology of mammalian secreted phospholipases A2. Annu. Rev. Biochem. 77: 495-520.
6. Balestrieri, B., and J. P. Arm. 2006. Group V sPLA2: classical and novel functions. Biochim. Biophys. Acta 1761: 1280-1288. (Pubitemid 44738704)
7. Murakami, M., Y. Taketomi, H. Sato, and K. Yamamoto. 2011. Secreted phospholipase A2 revisited. J. Biochem. 150: 233-255.
8. Aloulou, A., Y. B. Ali, S. Bezzine, Y. Gargouri, and M. H. Gelb. 2012. Phospholipases: an overview. Methods Mol. Biol. 861: 63-85.
9. Chilton, F. H., F. J. Averill, W. C. Hubbard, A. N. Fonteh, M. Triggiani, and M. C. Liu. 1996. Antigen-induced generation of lyso-phospholipids in human airways. J. Exp. Med. 183: 2235-2245. (Pubitemid 26158915)
10. Seeds, M. C., K. A. Jones, R. Duncan Hite, M. C. Willingham, H. M. Borgerink, R. D. Woodruff, D. L. Bowton, and D. A. Bass. 2000. Cell-specific expression of group X and group V secretory phospholipases A(2) in human lung airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 23: 37-44. (Pubitemid 30597093)
11. Hallstrand, T. S., Y. Lai, Z. Ni, R. C. Oslund, W. R. Henderson, Jr., M. H. Gelb, and S. E. Wenzel. 2011. Relationship between levels of secreted phospholipase A(2) groups IIA and X in the airways and asthma severity. Clin. Exp. Allergy. 41: 801-810.
12. Muñoz, N. M., A. Y. Meliton, J. P. Arm, J. V. Bonventre,W. Cho, and A. R. Leff. 2007. Deletion of secretory group V phospholipase A2 attenuates cell migration and airway hyperresponsiveness in immunosensitized mice. J. Immunol. 179: 4800-4807.
13. Henderson, W. R., Jr., E. Y. Chi, J. G. Bollinger, Y. T. Tien, X. Ye, L. Castelli, Y. P. Rubtsov, A. G. Singer, G. K. Chiang, T. Nevalainen, et al. 2007. Importance of group X-secreted phospholipase A2 in allergen-induced airway inflammation and remodeling in a mouse asthma model. J. Exp. Med. 204: 865-877. (Pubitemid 46631615)
14. Martinez, F. O., L. Helming, and S. Gordon. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27: 451-483.
15. Mosser, D. M., and J. P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
16. Mantovani, A., and M. Locati. 2009. Orchestration of macrophage polarization. Blood 114: 3135-3136.
17. Murray, P. J., and T. A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11: 723-737.
18. Gordon, S., and F. O. Martinez. 2010. Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
19. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686. (Pubitemid 39457982)
20. Kurowska-Stolarska, M., B. Stolarski, P. Kewin, G. Murphy, C. J. Corrigan, S. Ying, N. Pitman, A. Mirchandani, B. Rana, N. van Rooijen, et al. 2009. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 183: 6469-6477.
21. Loke, P., I. Gallagher, M. G. Nair, X. Zang, F. Brombacher, M. Mohrs, J. P. Allison, and J. E. Allen. 2007. Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J. Immunol. 179: 3926-3936.
22. Niese, K. A., A. R. Collier, A. R. Hajek, S. D. Cederbaum, W. E. O'Brien, M.Wills-Karp, M. E. Rothenberg, and N. Zimmermann. 2009. Bone marrow cell derived arginase I is the major source of allergen-induced lung arginase but is not required for airway hyperresponsiveness, remodeling and lung inflammatory responses in mice. BMC Immunol. 10: 33.
23. Pesce, J. T., T. R. Ramalingam, M. M. Mentink-Kane, M. S. Wilson, K. C. ElKasmi, A.M. Smith, R.W. Thompson, A. W. Cheever, P. J. Murray, and T. A. Wynn. 2009. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 5: e1000371.
24. Thomas, G. D., D. Rückerl, B. H. Maskrey, P. D. Whitfield, M. L. Blaxter, and J. E. Allen. 2012. The biology of nematode- and IL4Rα-dependent murine macrophage polarization in vivo as defined by RNA-Seq and targeted lipidomics. Blood 120: e93-e104.
25. Holcomb, I. N., R. C. Kabakoff, B. Chan, T. W. Baker, A. Gurney, W. Henzel, C. Nelson, H. B. Lowman, B. D. Wright, N. J. Skelton, et al. 2000. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J. 19: 4046-4055. (Pubitemid 30608543)
26. Nieuwenhuizen, N. E., F. Kirstein, J. Jayakumar, B. Emedi, R. Hurdayal, W. G. Horsnell, A. L. Lopata, and F. Brombacher. 2012. Allergic airway disease is unaffected by the absence of IL-4Ralpha-dependent alternatively activated macrophages. J. Allergy Clin. Immunol. 130: 743-750.e748.
27. Loke, P., M. G. Nair, J. Parkinson, D. Guiliano, M. Blaxter, and J. E. Allen. 2002. IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol. 3: 7.
28. Sica, A., and A. Mantovani. 2012. Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122: 787-795.
29. Raes, G., P. De Baetselier, W. Noël, A. Beschin, F. Brombacher, and G. Hassanzadeh Gh. 2002. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J. Leukoc. Biol. 71: 597-602.
30. Kim, E. Y., J. T. Battaile, A. C. Patel, Y. You, E. Agapov, M. H. Grayson, L. A. Benoit, D. E. Byers, Y. Alevy, J. Tucker, et al. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14: 633-640. (Pubitemid 351809546)
31. Di Valentin, E., C. Crahay, N. Garbacki, B. Hennuy, M. Guéders, A. Noël, J. M. Foidart, J. Grooten, A. Colige, J. Piette, and D. Cataldo. 2009. New asthma biomarkers: lessons from murine models of acute and chronic asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 296: L185-L197.
32. Zimmermann, N., N. E. King, J. Laporte, M. Yang, A. Mishra, S. M. Pope, E. E. Muntel, D. P. Witte, A. A. Pegg, P. S. Foster, et al. 2003. Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J. Clin. Invest. 111: 1863-1874. (Pubitemid 38057731)
33. Agapov, E., J. T. Battaile, R. Tidwell, R. Hachem, G. A. Patterson, R. A. Pierce, J. J. Atkinson, and M. J. Holtzman. 2009. Macrophage chitinase 1 stratifies chronic obstructive lung disease. Am. J. Respir. Cell Mol. Biol. 41: 379-384.
34. Chupp, G. L., C. G. Lee, N. Jarjour, Y. M. Shim, C. T. Holm, S. He, J. D. Dziura, J. Reed, A. J. Coyle, P. Kiener, et al. 2007. A chitinase-like protein in the lung and circulation of patients with severe asthma. N. Engl. J. Med. 357: 2016-2027. (Pubitemid 350106709)
35. Melgert, B. N., N. H. ten Hacken, B. Rutgers, W. Timens, D. S. Postma, and M. N. Hylkema. 2011. More alternative activation of macrophages in lungs of asthmatic patients. J. Allergy Clin. Immunol. 127: 831-833.
36. Munitz, A., E. T. Cole, D. Karo-Atar, F. D. Finkelman, and M. E. Rothenberg. 2012. Resistin-like molecule-α regulates IL-13-induced chemokine production but not allergen-induced airway responses. Am. J. Respir. Cell Mol. Biol. 46: 703-713.
37. Giannattasio, G., D. Fujioka, W. Xing, H. R. Katz, J. A. Boyce, and B. Balestrieri. 2010. Group V secretory phospholipase A2 reveals its role in house dust mite-induced allergic pulmonary inflammation by regulation of dendritic cell function. J. Immunol. 185: 4430-4438.
38. Balestrieri, B., V. W. Hsu, H. Gilbert, C. C. Leslie, W. K. Han, J. V. Bonventre, and J. P. Arm. 2006. Group V secretory phospholipase A2 translocates to the phagosome after zymosan stimulation of mouse peritoneal macrophages and regulates phagocytosis. J. Biol. Chem. 281: 6691-6698. (Pubitemid 43847604)
39. Balestrieri, B., A. Maekawa, W. Xing, M. H. Gelb, H. R. Katz, and J. P. Arm. 2009. Group V secretory phospholipase A2 modulates phagosome maturation and regulates the innate immune response against Candida albicans. J. Immunol. 182: 4891-4898.
40. Satake, Y., B. L. Diaz, B. Balestrieri, B. K. Lam, Y. Kanaoka, M. J. Grusby, and J. P. Arm. 2004. Role of group V phospholipase A2 in zymosan-induced eicosanoid generation and vascular permeability revealed by targeted gene disruption. J. Biol. Chem. 279: 16488-16494. (Pubitemid 38509347)
41. Grünig, G., M. Warnock, A. E.Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263. (Pubitemid 29004075)
42. Martinez, F. O., S. Gordon, M. Locati, and A. Mantovani. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177: 7303-7311. (Pubitemid 44715100)
43. Simarro, M., G. Giannattasio, M. A. De la Fuente, C. Benarafa, K. K. Subramanian, R. Ishizawar, B. Balestrieri, E. M. Andersson, H. R. Luo, A. Orduña, et al. 2010. Fas-activated serine/threonine phosphoprotein promotes immune-mediated pulmonary inflammation. J. Immunol. 184: 5325-5332.
44. Barrett, N. A., O. M. Rahman, J. M. Fernandez, M. W. Parsons, W. Xing, K. F. Austen, and Y. Kanaoka. 2011. Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes. J. Exp. Med. 208: 593-604.
45. Lacey, D. C., A. Achuthan, A. J. Fleetwood, H. Dinh, J. Roiniotis, G. M. Scholz, M. W. Chang, S. K. Beckman, A. D. Cook, and J. A. Hamilton. 2012. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J. Immunol. 188: 5752-5765.
46. Bisset, L. R., and P. Schmid-Grendelmeier. 2005. Chemokines and their receptors in the pathogenesis of allergic asthma: progress and perspective. Curr. Opin. Pulm. Med. 11: 35-42. (Pubitemid 40189249)
47. Medoff, B. D., S. Y. Thomas, and A. D. Luster. 2008. T cell trafficking in allergic asthma: the ins and outs. Annu. Rev. Immunol. 26: 205-232. (Pubitemid 351600375)
48. Willment, J. A., H. H. Lin, D. M. Reid, P. R. Taylor, D. L. Williams, S. Y. Wong, S. Gordon, and G. D. Brown. 2003. Dectin-1 expression and function are enhanced on alternatively activated and GM-CSF-treated macrophages and are negatively regulated by IL-10, dexamethasone, and lipopolysaccharide. J. Immunol. 171: 4569-4573. (Pubitemid 37310572)
49. Galès, A., A. Conduché, J. Bernad, L. Lefevre, D. Olagnier, M. Béraud, G. Martin-Blondel, M. D. Linas, J. Auwerx, A. Coste, and B. Pipy. 2010. PPARgamma controls dectin-1 expression required for host antifungal defense against Candida albicans. PLoS Pathog. 6: e1000714.
50. Nair, M. G., Y. Du, J. G. Perrigoue, C. Zaph, J. J. Taylor, M. Goldschmidt, G. P. Swain, G. D. Yancopoulos, D. M. Valenzuela, A. Murphy, et al. 2009. Alternatively activated macrophage-derived RELM-alpha is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 206: 937-952.
51. Wills-Karp, M., R. Rani, K. Dienger, I. Lewkowich, J. G. Fox, C. Perkins, L. Lewis, F. D. Finkelman, D. E. Smith, P. J. Bryce, et al. 2012. Trefoil factor 2 rapidly induces interleukin 33 to promote type 2 immunity during allergic asthma and hookworm infection. J. Exp. Med. 209: 607-622.
52. Medoff, B. D., E. Seung, S. Hong, S. Y. Thomas, B. P. Sandall, J. S. Duffield, D. A. Kuperman, D. J. Erle, and A. D. Luster. 2009. CD11b+ myeloid cells are the key mediators of Th2 cell homing into the airway in allergic inflammation. J. Immunol. 182: 623-635.
53. Pilette, C., J. N. Francis, S. J. Till, and S. R. Durham. 2004. CCR4 ligands are up-regulated in the airways of atopic asthmatics after segmental allergen challenge. Eur. Respir. J. 23: 876-884. (Pubitemid 38807362)