TSG-6 protein is crucial for the development of pulmonary hyaluronan deposition, eosinophilia, and airway hyperresponsiveness in a murine model of asthma

Journal of Biological Chemistry

Volumn 288, Issue 1, 2013, Pages 412-422

  Swaidani, Shadi ^a   Cheng, Georgiana ^a   Lauer, Mark E ^a   Sharma, Manisha ^a   Mikecz, Katalin ^b   Hascall, Vincent C ^a   Aronica, Mark A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; ANTI-PLASMIN; CHEMOKINES; CYTOKINES; HYALURONAN; INFLAMMATORY RESPONSE; LUNG MECHANICS; LUNG TISSUE; METHACHOLINE; MURINE MODEL; PATHOLOGICAL RESPONSE; PATHOPHYSIOLOGICAL; WILD TYPES;

BIOLOGICAL ORGANS; DISEASES; MAMMALS; PROTEINS; TISSUE;

PATHOLOGY;

CHEMOKINE; CYTOKINE; HYALURONIC ACID; HYALURONIC ACID BINDING PROTEIN; METHACHOLINE; PROTEIN TSG 6; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; HUMORAL IMMUNITY; LOEFFLER PNEUMONIA; LUNG LAVAGE; LUNG MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RESPIRATORY TRACT ALLERGY; TH2 CELL; WILD TYPE;

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE; CELL ADHESION MOLECULES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; HYALURONIC ACID; INFLAMMATION; LUNG; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; TH2 CELLS;

MURINAE; MUS;

EID: 84872076777     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.389874     Document Type: Article

References (59)

1. Elias, J. A., Lee, C. G., Zheng, T., Ma, B., Homer, R. J., and Zhu, Z. (2003) New insights into the pathogenesis of asthma. J. Clin. Invest. 111, 291-297 (Pubitemid 36182201)
2. Laitinen, A., and Laitinen, L. A. (1994) Pathology of asthma. Allergy Proc. 15, 323-328
3. Holgate, S. T., and Davies, D. E. (2009) Rethinking the pathogenesis of asthma. Immunity 31, 362-367
4. Wills-Karp, M. (1999) Immunologic basis of antigen-induced airway hy- perresponsiveness. Annu. Rev. Immunol. 17, 255-281
5. Raines, E. W. (2000) The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int. J. Exp. Pathol. 81, 173-182
6. Vaday, G. G., and Lider, O. (2000) Extracellular matrix moieties, cytokines, and enzymes: dynamic effects on immune cell behavior and inflammation. J. Leukoc. Biol. 67, 149-159
7. Burgess, J. K. (2009) The role of the extracellular matrix and specific growth factors in the regulation of inflammation and remodelling in asthma. Pharmacol. Ther. 122, 19-29
8. Papakonstantinou, E., and Karakiulakis, G. (2009) The 'sweet' and 'bitter' involvement of glycosaminoglycans in lung diseases: pharmacotherapeutic relevance. Br. J. Pharmacol. 157, 1111-1127
9. Jiang, D., Liang, J., and Noble, P. W. (2007) Hyaluronan in tissue injury and repair. Annu. Rev. Cell Dev. Biol. 23, 435-461
10. Culley, F. J., Fadlon, E. J., Kirchem, A., Williams, T. J., Jose, P. J., and Pease, J. E. (2003) Proteoglycans are potent modulators of the biological responses of eosinophils to chemokines. Eur. J. Immunol. 33, 1302-1310 (Pubitemid 36609148)
11. Cantor, J. O., Cerreta, J. M., Armand, G., Osman, M., and Turino, G. M. (1999) The pulmonary matrix, glycosaminoglycans and pulmonary emphysema. Connect. Tissue Res. 40, 97-104 (Pubitemid 29298219)
12. Negrini, D., Passi, A., and Moriondo, A. (2008) The role of proteoglycans in pulmonary edema development. Intensive Care Med. 34, 610-618
13. Jiang, D., Liang, J., and Noble, P. W. (2010) Regulation of non-infectious lung injury, inflammation, and repair by the extracellular matrix glycosaminoglycan hyaluronan. Anat. Rec. 293, 982-985
14. Noble, P. W., and Jiang, D. (2006) Matrix regulation of lung injury, inflammation, and repair: the role of innate immunity. Proc. Am. Thorac. Soc. 3, 401-404 (Pubitemid 44033352)
15. Wisniewski, H. G., and Vilcek, J. (2004) Cytokine-induced gene expression at the crossroads of innate immunity, inflammation and fertility: TSG-6 and PTX3/TSG-14. Cytokine Growth Factor Rev. 15, 129-146
16. Blundell, C. D., Mahoney, D. J., Almond, A., DeAngelis, P. L., Kahmann, J. D., Teriete, P., Pickford, A. R., Campbell, I. D., and Day, A. J. (2003) The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. J. Biol. Chem. 278, 49261-49270
17. Stern, R. (2004) Hyaluronan catabolism: a new metabolic pathway. Eur. J. Cell Biol. 83, 317-325
18. Day, A. J., and de la Motte, C. A. (2005) Hyaluronan cross-linking: a protective mechanism in inflammation? Trends Immunol. 26, 637-643 (Pubitemid 41628196)
19. Jiang, D., Liang, J., Fan, J., Yu, S., Chen, S., Luo, Y., Prestwich, G. D., Mascarenhas, M. M., Garg, H. G., Quinn, D. A., Homer, R. J., Goldstein, D. R., Bucala, R., Lee, P. J., Medzhitov, R., and Noble, P. W. (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11, 1173-1179 (Pubitemid 43093664)
20. Monzon, M. E., Casalino-Matsuda, S. M., and Forteza, R. M. (2006) Identification of glycosaminoglycans in human airway secretions. Am. J. Respir. Cell Mol. Biol. 34, 135-141 (Pubitemid 43202459)
21. Sahu, S., and Lynn, W. S. (1978) Hyaluronic acid in the pulmonary secretions of patients with asthma. Biochem. J. 173, 565-568 (Pubitemid 8395173)
22. Bousquet, J., Chanez, P., Lacoste, J. Y., Enander, I., Venge, P., Peterson, C., Ahlstedt, S., Michel, F. B., and Godard, P. (1991) Indirect evidence of bronchial inflammation assessed by titration of inflammatory mediators in BAL fluid of patients with asthma. J. Allergy Clin. Immunol. 88, 649-660
23. Parkar, A. A., Kahmann, J. D., Howat, S. L., Bayliss, M. T., and Day, A. J. (1998) TSG-6 interacts with hyaluronan and aggrecan in a pH-dependent manner via a common functional element: implications for its regulation in inflamed cartilage. FEBS Lett. 428, 171-176 (Pubitemid 28319679)
24. Kohda, D., Morton, C. J., Parkar, A. A., Hatanaka, H., Inagaki, F. M., Campbell, I. D., and Day, A. J. (1996) Solution structure of the link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell 86, 767-775 (Pubitemid 26303445)
25. Parkar, A. A., and Day, A. J. (1997) Overlapping sites on the link module of human TSG-6 mediate binding to hyaluronan and chrondroitin 4-sulfate. FEBS Lett. 410, 413-417 (Pubitemid 27304107)
26. Blundell, C. D., Almond, A., Mahoney, D. J., DeAngelis, P. L., Campbell, I. D., and Day, A. J. (2005) Towards a structure for a TSG-6·hyaluronan complex by modeling and NMR spectroscopy: insights into other members of the link module superfamily. J. Biol. Chem. 280, 18189-18201 (Pubitemid 41389064)
27. Carrette, O., Nemade, R. V., Day, A. J., Brickner, A., and Larsen, W. J. (2001) TSG-6 is concentrated in the extracellular matrix of mouse cumulus oocyte complexes through hyaluronan and inter-α-inhibitor binding. Biol. Reprod. 65, 301-308 (Pubitemid 32574812)
28. Kahmann, J. D., O'Brien, R., Werner, J. M., Heinegârd, D., Ladbury, J. E., Campbell, I. D., and Day, A. J. (2000) Localization and characterization of the hyaluronan-binding site on the link module from human TSG-6. Structure 8, 763-774 (Pubitemid 30469994)
29. Milner, C. M., Higman, V. A., and Day, A. J. (2006) TSG-6: a pluripotent inflammatory mediator? Biochem. Soc. Trans. 34, 446-450 (Pubitemid 43954008)
30. Mahoney, D. J., Mulloy, B., Forster, M. J., Blundell, C. D., Fries, E., Milner, C. M., and Day, A. J. (2005) Characterization of the interaction between tumor necrosis factor-stimulated gene-6 and heparan: implications for the inhibition of plasmin in extracellular matrix microenvironments. J. Biol. Chem. 280, 27044-27055 (Pubitemid 41040741)
31. Lesley, J., Gál, I., Mahoney, D. J., Cordell, M. R., Rugg, M. S., Hyman, R., Day, A. J., and Mikecz, K. (2004) TSG-6 modulates the interaction between hyaluronan and cell surface CD44. J. Biol. Chem. 279, 25745-25754 (Pubitemid 38756838)
32. Sanggaard, K. W., Sonne-Schmidt, C. S., Krogager, T. P., Lorentzen, K. A., Wisniewski, H. G., Thøgersen, I. B., and Enghild, J. J. (2008) The transfer of heavy chains from bikunin proteins to hyaluronan requires both TSG-6 and HC2. J. Biol. Chem. 283, 18530-18537
33. Mukhopadhyay, D., Hascall, V. C., Day, A. J., Salustri, A., and Fülöp, C. (2001) Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes. Arch. Biochem. Biophys. 394, 173-181 (Pubitemid 32989326)
34. Mukhopadhyay, D., Asari, A., Rugg, M. S., Day, A. J., and Fülöp, C. (2004) Specificity of the tumor necrosis factor-induced protein 6-mediated heavy chain transfer from inter-α-trypsin inhibitor to hyaluronan: implications for the assembly of the cumulus extracellular matrix. J. Biol. Chem. 279, 11119-11128 (Pubitemid 38401605)
35. Fülöp, C., Szántó, S., Mukhopadhyay, D., Bárdos, T., Kamath, R. V., Rugg, M. S., Day, A. J., Salustri, A., Hascall, V. C., Glant, T. T., and Mikecz, K. (2003) Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6-deficient mice. Development 130, 2253-2261 (Pubitemid 36656719)
36. Lilly, C. M., Tateno, H., Oguma, T., Israel, E., and Sonna, L. A. (2005) Effects of allergen challenge on airway epithelial cell gene expression. Am. J. Respir. Crit. Care Med. 171, 579-586 (Pubitemid 40365412)
37. Forteza, R., Casalino-Matsuda, S. M., Monzon, M. E., Fries, E., Rugg, M. S., Milner, C. M., and Day, A. J. (2007) TSG-6 potentiates the antitissue kallikrein activity of inter-α-inhibitor through bikunin release. Am. J. Respir. Cell Mol. Biol. 36, 20-31 (Pubitemid 46067704)
38. Aronica, M. A., Mora, A. L., Mitchell, D. B., Finn, P. W., Johnson, J. E., Sheller, J. R., and Boothby, M. R. (1999) Preferential role for NF-κB/Rel signaling in the type 1 but not type 2 T cell-dependent immune response in vivo. J. Immunol. 163, 5116-5124 (Pubitemid 29501281)
39. Swaidani, S., Bulek, K., Kang, Z., Liu, C., Lu, Y., Yin, W., Aronica, M., and Li, X. (2009) The critical role of epithelial-derived Act1 in IL-17- and IL-25-mediated pulmonary inflammation. J. Immunol. 182, 1631-1640
40. Lauer, M. E., Fulop, C., Mukhopadhyay, D., Comhair, S., Erzurum, S. C., and Hascall, V. C. (2009) Airway smooth muscle cells synthesize hyaluronan cable structures independent of inter-α-inhibitor heavy chain attachment. J. Biol. Chem. 284, 5313-5323
41. Kumar, R. K., Herbert, C., and Foster, P. S. (2008) The "classical" ovalbumin challenge model of asthma in mice. Curr. Drug Targets 9, 485-494 (Pubitemid 352025205)
42. Fuchs, B., and Braun, A. (2008) Improved mouse models of allergy and allergic asthma-chances beyond ovalbumin. Curr. Drug Targets 9, 495-502 (Pubitemid 352025206)
43. Finkelman, F. D., Hogan, S. P., Hershey, G. K., Rothenberg, M. E., and Wills-Karp, M. (2010) Importance of cytokines in murine allergic airway disease and human asthma. J. Immunol. 184, 1663-1674
44. Irvin, C. G., and Bates, J. H. (2003) Measuring the lung function in the mouse: the challenge of size. Respir. Res. 4, 4
45. Cheng, G., Swaidani, S., Sharma, M., Lauer, M. E., Hascall, V. C., and Aronica, M. A. (2011) Hyaluronan deposition and correlation with inflammation in a murine ovalbumin model of asthma. Matrix Biol. 30, 126-134
46. Szántó, S., Bárdos, T., Gál, I., Glant, T. T., and Mikecz, K. (2004) Enhanced neutrophil extravasation and rapid progression of proteoglycan-induced arthritis in TSG-6-knockout mice. Arthritis Rheum. 50, 3012-3022 (Pubitemid 39209541)
47. Wisniewski, H. G., Hua, J. C., Poppers, D. M., Naime, D., Vilcek, J., and Cronstein, B. N. (1996) TNF/IL-1-inducible protein TSG-6 potentiates plasmin inhibition by inter-α-inhibitor and exerts a strong anti-inflammatory effect in vivo. J. Immunol. 156, 1609-1615
48. Cao, T. V., La, M., Getting, S. J., Day, A. J., and Perretti, M. (2004) Inhibitory effects of TSG-6 link module on leukocyte-endothelial cell interactions in vitro and in vivo. Microcirculation 11, 615-624 (Pubitemid 39618633)
49. Getting, S. J., Mahoney, D. J., Cao, T., Rugg, M. S., Fries, E., Milner, C. M., Perretti, M., and Day, A. J. (2002) The link module from human TSG-6 inhibits neutrophil migration in a hyaluronan- and inter-α-inhibitor- independent manner. J. Biol. Chem. 277, 51068-51076 (Pubitemid 36042279)
50. Mindrescu, C., Le, J., Wisniewski, H. G., and Vilcek, J. (2005) Up-regulation of cyclooxygenase-2 expression by TSG-6 protein in macrophage cell line. Biochem. Biophys. Res. Commun. 330, 737-745 (Pubitemid 40462149)
51. 2 receptors DP1 and CRTH2 in promoting allergic responses. Br. J. Pharmacol. 153, S191-S199
52. Herrerias, A., Torres, R., Serra, M., Marco, A., Pujols, L., Picado, C., and de Mora, F. (2009) Activity of the cyclooxygenase 2-prostaglandin E prostanoid receptor pathway in mice exposed to house dust mite aeroallergens, and impact of exogenous prostaglandin E2. J. Inflamm. 6, 30
53. 2 receptor DP2/CRTH2 increases allergic inflammation in mouse. J. Immunol. 174, 3703-3708
54. Hirai, H., Tanaka, K., Yoshie, O., Ogawa, K., Kenmotsu, K., Takamori, Y., Ichimasa, M., Sugamura, K., Nakamura, M., Takano, S., and Nagata, K. (2001) Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J. Exp. Med. 193, 255-261 (Pubitemid 32524457)
55. 2 reinforces Th2-type inflammatory responses of airways to low-dose antigen through bronchial expression of macrophage-derived chemokine. J. Exp. Med. 198, 533-543
56. Ney, P., and Schrör, K. (1991) PGD2 and its mimetic ZK 110.841 are potent inhibitors of receptor-mediated activation of human neutrophils. Eicosanoids 4, 21-28
57. Darius, H., Michael-Hepp, J., Thierauch, K. H., and Fisch, A. (1994) Inhibition of human platelets and polymorphonuclear neutrophils by the potent and metabolically stable prostaglandin D2 analog ZK 118.182. Eur. J. Pharmacol. 258, 207-213 (Pubitemid 24179982)
58. Garantziotis, S., Li, Z., Potts, E. N., Lindsey, J. Y., Stober, V. P., Polosukhin, V. V., Blackwell, T. S., Schwartz, D. A., Foster, W. M., and Hollingsworth, J. W. (2010) TLR4 is necessary for hyaluronan-mediated airway hyperresponsiveness after ozone inhalation. Am. J. Respir. Crit. Care Med. 181, 666-675
59. Lauer, M. E., Cheng, G., Swaidani, S., Aronica, M. A., Weigel, P. H., and Hascall, V. C. (2013) Tumor necrosis factor-stimulated gene-6 (TSG-6) amplifies hyaluronan synthesis by airway smooth muscle cells. J. Biol. Chem. 288, 423-431