The adipocyte fatty acid-binding protein aP2 is required in allergic airway inflammation

Journal of Clinical Investigation

Volumn 116, Issue 8, 2006, Pages 2183-2192

  Shum, Bennett O V ^a,b,c   Mackay, Charles R ^a,b,c   Gorgun, Cem Z ^d   Frost, Melinda J ^a,b   Kumar, Rakesh K ^c   Hotamisligil, Gökhan S ^d   Rolph, Michael S ^a,b,c  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Cooperative Research Centre for Asthma and Airways ^*  (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTE FATTY ACID BINDING PROTEIN; CYTOKINE; FATTY ACID BINDING PROTEIN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 4; STAT6 PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRONCHUS MUCOSA; CELL INFILTRATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; EOSINOPHIL; EPITHELIUM CELL; GENE CONTROL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY TRACT INFLAMMATION; T LYMPHOCYTE; UPREGULATION;

3T3 CELLS; ADIPOCYTES; ANIMALS; ASTHMA; BRONCHI; CELL CULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; HYPERSENSITIVITY; INFLAMMATION; INTERLEUKIN-12; INTERLEUKIN-4; MICE; MICE, KNOCKOUT; RESPIRATORY MUCOSA; RNA, MESSENGER; TH2 CELLS; TRANSCRIPTION, GENETIC;

EID: 33746758322     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI24767     Document Type: Article

References (56)

1. Bochner, B.S., Undem, B.J., and Lichtenstein, L.M. 1994. Immunological aspects of allergic asthma. Annu. Rev. Immunol. 12:295-335.
2. Woolcock, A.J., Bastiampillai, S.A., Marks, G.B., and Keena, V.A. 2001. The burden of asthma in Australia. Med. J. Aust. 175:141-145.
3. Centers for Disease Control. 2002. Surveillance for asthma - United States, 1980-1999. MMWR Surveill. Summ. 51:1-13.
4. Strachan, D.P. 1989. Hay fever, hygiene, and household size. BMJ. 299:1259-1260.
5. Tattersfield, A.E., Knox, A.J., Britton, J.R., and Hall, I.P. 2002. Asthma. Lancet. 360:1313-1322.
6. Brusselle, G., Kips, J., Joos, G., Bluethmann, H., and Pauwels, R. 1995. Allergen-induced airway inflammation and bronchial responsiveness in wild-type and interleukin-4-deficient mice. Am. J. Respir. Cell Mol. Biol. 12:254-259.
7. Grunig, G., et al. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 282:2261-2263.
8. Shore, S.A. 2004. Direct effects of Th2 cytokines on airway smooth muscle. Curr. Opin. Pharmacol. 4:235-240.
9. Davies, D.E. 2001. The bronchial epithelium in chronic and severe asthma. Curr. Allergy Asthma Rep. 1:127-133.
10. Matsukura, S., et al. 2001. Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 24:755-761.
11. Dabbagh, K., et al. 1999. IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. J. Immunol. 162:6233-6237.
12. Striz, I., et al. 1999. IL-4 induces ICAM-1 expression in human bronchial epithelial cells and potentiates TNF-alpha. Am. J. Physiol. 277:L58-L64.
13. Ponath, P.D., et al. 1996. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 97:604-612.
14. Rothenberg, M.E., Luster, A.D., and Leder, P. 1995. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc. Natl. Acad. Sci. U. S. A. 92:8960-8964.
15. Rolph, M.S., Sisavanh, M., Liu, S.M., and Mackay, C.R. 2006. Clues to asthma pathogenesis from microarray expression studies. Pharmacol. Ther. 109:284-294.
16. Jeffrey, K.L., et al. 2006. Positive regulation of immune cell function and inflammatory responses by phosphatase PAC-1. Nat. Immunol. 7:274-283.
17. Chtanova, T., et al. 2005. Identification of T cell-restricted genes, and signatures for different T cell responses, using a comprehensive collection of microarray datasets. J. Immunol. 175:7837-7847.
18. Liu, S.M., et al. 2006. "Immune cell transcriptome" datasets reveal novel leukocyte subset-specific genes, and genes associated with allergic processes. J. Allergy Clin. Immunol. In press.
19. Boord, J.B., et al. 2002. Adipocyte fatty acid-binding protein, aP2, alters late atherosclerotic lesion formation in severe hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 22:1686-1691.
20. Makowski, L., et al. 2001. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat. Med. 7:699-705.
21. Scheja, L., et al. 1999. Altered insulin secretion associated with reduced lipolytic efficiency in aP2-/-mice. Diabetes. 48:1987-1994.
22. Zimmerman, A.W., and Veerkamp, J.H. 2002. New insights into the structure and function of fatty acid-binding proteins. Cell. Mol. Life Sci. 59:1096-1116.
23. Hertzel, A.V., and Bernlohr, D.A. 2000. The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol. Metab. 11:175-180.
24. Makowski, L., and Hotamisligil, G.S. 2005. The role of fatty acid binding proteins in metabolic syndrome and atherosclerosis. Curr. Opin. Lipidol. 16:543-548.
25. Maeda, K., et al. 2003. Role of the fatty acid binding protein mal1 in obesity and insulin resistance. Diabetes. 52:300-307.
26. Tontonoz, P., Hu, E., Graves, R.A., Budavari, A.I., and Spiegelman, B.M. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8:1224-1234.
27. Pelton, P.D., Zhou, L., Demarest, K.T., and Burris, T.P. 1999. PPARgamma activation induces the expression of the adipocyte fatty acid binding protein gene in human monocytes. Biochem. Biophys. Res. Commun. 261:456-458.
28. Chawla, A., et al. 2001. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7:48-52.
29. Yu, S., et al. 2003. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor gamma1 (PPARgamma1) overexpression. J. Biol. Chem. 278:498-505.
30. Kelly-Welch, A.E., Hanson, E.M., Boothby, M.R., and Keegan, A.D. 2003. Interleukin-4 and interleukin-13 signaling connections maps. Science. 300:1527-1528.
31. Kotanides, H., and Reich, N.C. 1996. Interleukin-4-induced STAT6 recognizes and activates a target site in the promoter of the interleukin-4 receptor gene. J. Biol. Chem. 271:25555-25561.
32. Matsukura, S., et al. 1999. Activation of eotaxin gene transcription by NF-kappa B and STAT6 in human airway epithelial cells. J. Immunol. 163:6876-6883.
33. Lee, J.H., et al. 2001. Interleukin-13 induces dramatically different transcriptional programs in three human airway cell types. Am. J. Respir. Cell Mol. Biol. 25:474-485.
34. Leung, D.Y., et al. 1995. Dysregulation of interleukin 4, interleukin 5, and interferon gamma gene expression in steroid-resistant asthma. J. Exp. Med. 181:33-40.
35. Shirakawa, T., Enomoto, T., Shimazu, S., and Hopkin, J.M. 1997. The inverse association between tuberculin responses and atopic disorder. Science. 275:77-79.
36. Zimmermann, N., et al. 2003. Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J. Clin. Invest. 111:1863-1874. doi:10.1172/JCI200317912.
37. Fulkerson, P.C., Zimmermann, N., Hassman, L.M., Finkelman, F.D., and Rothenberg, M.E. 2004. Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-gamma. J. Immunol. 173:7565-7574.
38. Welch, J.S., Ricote, M., Akiyama, T.E., Gonzalez, F.J., and Glass, C.K. 2003. PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc. Natl. Acad. Sci. U. S. A. 100:6712-6717.
39. Makowski, L., and Hotamisligil, G.S. 2004. Fatty acid binding proteins - the evolutionary cross-roads of inflammatory and metabolic responses. J. Nutr. 134:2464S-2468S.
40. Hotamisligil, G.S., et al. 1996. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science. 274:1377-1379.
41. Hertzel, A.V., and Bernlohr, D.A. 1998. Regulation of adipocyte gene expression by polyunsaturated fatty acids. Mol. Cell. Biochem. 188:33-39.
42. Kuperman, D.A., et al. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8:885-889.
43. Zimmermann, N., Hershey, G.K., Foster, P.S., and Rothenberg, M.E. 2003. Chemokines in asthma: cooperative interaction between chemokines and IL-13. J. Allergy Clin. Immunol. 111:227-242; quiz 243.
44. Makowski, L., Brittingham, K.C., Reynolds, J.M., Suttles, J., and Hotamisligil, G.S. 2005. The fatty acid-binding protein, aP2, coordinates macrophage cholesterol trafficking and inflammatory activity. Macrophage expression of aP2 impacts peroxisome proliferator-activated receptor gamma and IkappaB kinase activities. J. Biol. Chem. 280:12888-12895.
45. Helledie, T., et al. 2000. Lipid-binding proteins modulate ligand-dependent trans-activation by peroxisome proliferator-activated receptors and localize to the nucleus as well as the cytoplasm. J. Lipid Res. 41:1740-1751.
46. Veerkamp, J.H., van Moerkerk, H.T., Prinsen, C.F., and van Kuppevelt, T.H. 1999. Structural and functional studies on different human FABP types. Mol. Cell. Biochem. 192:137-142.
47. Zimmer, J.S., Dyckes, D.F., Bernlohr, D.A., and Murphy, R.C. 2004. Fatty acid binding proteins stabilize leukotriene A4: competition with arachidonic acid but not other lipoxygenase products. J. Lipid Res. 45:2138-2144.
48. Mehrabian, M., et al. 2002. Identification of 5-lipoxygenase as a major gene contributing to atherosclerosis susceptibility in mice. Circ. Res. 91:120-126.
49. Dwyer, J.H., et al. 2004. Arachidonate 5-lipoxygenase promoter genotype, dietary arachidonic acid, and atherosclerosis. N. Engl. J. Med. 350:29-37.
50. De Caterina, R., and Zampolli, A. 2004. From asthma to atherosclerosis - 5-lipoxygenase, leukotrienes, and inflammation. N. Engl. J. Med. 350:4-7.
51. Serhan, C.N., Takano, T., Chiang, N., Gronert, K., and Clish, C.B. 2000. Formation of endogenous "antiinflammatory" lipid mediators by transcellular biosynthesis. Lipoxins and aspirin-triggered lipoxins inhibit neutrophil recruitment and vascular permeability. Am. J. Respir. Crit. Care Med. 161:S95-S101.
52. Davidson, D.J., Kilanowski, F.M., Randell, S.H., Sheppard, D.N., and Dorin, J.R. 2000. A primary culture model of differentiated murine tracheal epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 279:L766-L778.
53. Chtanova, T., Kemp, R.A., Sutherland, A.P., Ronchese, F., and Mackay, C.R. 2001. Gene microarrays reveal extensive differential gene expression in both CD4(+) and CD8(+) type 1 and type 2 T cells. J. Immunol. 167:3057-3063.
54. Rozen, S., and Skaletsky, H.J. 2000. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics methods and protocols: methods in molecular biology. S. Misener and S.A. Krawetz, editors. Humana Press. Totowa, New Jersey, USA. 365-386.
55. Yokoyama, W.M. 1995. Production of monoclonal antibodies. In Current protocols in immunology. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober, editors. John Wiley and Sons. New York, New York, USA. 2.5.1-2.5.17.
56. Temelkovski, J., Hogan, S.P., Shepherd, D.P., Foster, P.S., and Kumar, R.K. 1998. An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolized allergen. Thorax. 53:849-856.