Constitutive expression of pentraxin 3 (PTX3) protein by human amniotic membrane cells leads to formation of the heavy chain (HC)-hyaluronan (HA)-PTX3 complex

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13531-13542

  Zhang, Suzhen ^a   Zhu, Ying Ting ^a   Chen, Szu Yu ^a   He, Hua ^a   Tseng, Scheffer C G ^a,b  

^a TISSUETECH INC   (United States)

^b OCULAR SURFACE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHAINS; CYTOLOGY; GENE EXPRESSION; LASER TISSUE INTERACTION;

AMNIOTIC MEMBRANES; ANTI-INFLAMMATORIES; BIOLOGICAL FUNCTIONS; CONSTITUTIVE EXPRESSIONS; HUMAN SKIN FIBROBLAST; INTEGRAL COMPONENTS; ULTRACENTRIFUGATION; WESTERN-BLOT ANALYSIS;

HYALURONIC ACID;

HEAVY CHAIN HYALURONAN PENTRAXIN 3 COMPLEX; HYALURONIC ACID; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; PENTRAXIN 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

AMNION CELL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; HEAVY CHAIN; HUMAN; HUMAN CELL; M2 MACROPHAGE; MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; STROMA CELL; UPREGULATION;

AMNIOTIC MEMBRANE CELLS; CELL BIOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HEAVY CHAIN-HYALURONAN COMPLEX; PENTRAXIN 3; PROTEIN SYNTHESIS; STROMAL CELL;

ADULT; AMNION; C-REACTIVE PROTEIN; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; HYALURONIC ACID; INTERLEUKIN-1BETA; SERUM AMYLOID P-COMPONENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900428521     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.525287     Document Type: Article

References (54)

1. Inforzato, A., Baldock, C., Jowitt, T. A., Holmes, D. F., Lindstedt, R., Marcellini, M., Rivieccio, V., Briggs, D. C., Kadler, K. E., Verdoliva, A., Bottazzi, B., Mantovani, A., Salvatori, G., and Day, A. J. (2010) The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. J. Biol. Chem. 285, 17681-17692
2. Bottazzi, B., Doni, A., Garlanda, C., and Mantovani, A. (2010) An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu. Rev. Immunol. 28, 157-183
3. Inforzato, A., Jaillon, S., Moalli, F., Barbati, E., Bonavita, E., Bottazzi, B., Mantovani, A., and Garlanda, C. (2011) The long pentraxin PTX3 at the crossroads between innate immunity and tissue remodelling. Tissue Antigens 77, 271-282
4. Manfredi, A. A., Rovere-Querini, P., Bottazzi, B., Garlanda, C., and Mantovani, A. (2008) Pentraxins, humoral innate immunity and tissue injury. Curr. Opin. Immunol. 20, 538-544
5. Nauta, A. J., Daha, M. R., Van Kooten, C., and Roos, A. (2003) Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends Immunol. 24, 148-154
6. Rovere, P., Peri, G., Fazzini, F., Bottazzi, B., Doni, A., Bondanza, A., Zimmermann, V. S., Garlanda, C., Fascio, U., Sabbadini, M. G., Rugarli, C., Mantovani, A., and Manfredi, A. A. (2000) The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 96, 4300-4306
7. Garlanda, C., Bottazzi, B., Bastone, A., and Mantovani, A. (2005) Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 23, 337-366
8. Garlanda, C., Hirsch, E., Bozza, S., Salustri, A., De Acetis, M., Nota, R., Maccagno, A., Riva, F., Bottazzi, B., Peri, G., Doni, A., Vago, L., Botto, M., De Santis, R., Carminati, P., Siracusa, G., Altruda, F., Vecchi, A., Romani, L., and Mantovani, A. (2002) Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420, 182-186
9. Han, B., Ma, X., Zhang, J., Zhang, Y., Bai, X., Hwang, D. M., Keshavjee, S., Levy, G. A., McGilvray, I., and Liu, M. (2012) Protective effects of long pentraxin PTX3 on lung injury in a severe acute respiratory syndrome model in mice. Lab. Invest. 92, 1285-1296
10. Soares, A. C., Souza, D. G., Pinho, V., Vieira, A. T., Nicoli, J. R., Cunha, F. Q., Mantovani, A., Reis, L. F., Dias, A. A., and Teixeira, M. M. (2006) Dual function of the long pentraxin PTX3 in resistance against pulmonary infection with Klebsiella pneumoniae in transgenic mice. Microbes Infect. 8, 1321-1329
11. Goodman, A. R., Cardozo, T., Abagyan, R., Altmeyer, A., Wisniewski, H. G., and Vilcek, J. (1996) Long pentraxins: an emerging group of proteins with diverse functions. Cytokine Growth Factor Rev. 7, 191-202
12. Maina, V., Cotena, A., Doni, A., Nebuloni, M., Pasqualini, F., Milner, C. M., Day, A. J., Mantovani, A., and Garlanda, C. (2009) Coregulation in human leukocytes of the long pentraxin PTX3 and TSG-6. J. Leukocyte Biol. 86, 123-132
13. Camozzi, M., Rusnati, M., Bugatti, A., Bottazzi, B., Mantovani, A., Bastone, A., Inforzato, A., Vincenti, S., Bracci, L., Mastroianni, D., and Presta, M. (2006) Identification of an antiangiogenic FGF2-binding site in the N terminus of the soluble pattern recognition receptor PTX3. J. Biol. Chem. 281, 22605-22613
14. Scarchilli, L., Camaioni, A., Bottazzi, B., Negri, V., Doni, A., Deban, L., Bastone, A., Salvatori, G., Mantovani, A., Siracusa, G., and Salustri, A. (2007) PTX3 interacts with inter-α-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion. J. Biol. Chem. 282, 30161-30170
15. Salustri, A., Garlanda, C., Hirsch, E., De Acetis, M., Maccagno, A., Bottazzi, B., Doni, A., Bastone, A., Mantovani, G., Beck Peccoz, P., Salvatori, G., Mahoney, D. J., Day, A. J., Siracusa, G., Romani, L., and Mantovani, A. (2004) PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131, 1577-1586
16. 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
17. Jessen, T. E., and Ødum, L. (2003) Role of tumour necrosis factor stimulated gene 6 (TSG-6) in the coupling of inter-α-trypsin inhibitor to hyaluronan in human follicular fluid. Reproduction. 125, 27-31
18. Rugg, M. S., Willis, A. C., Mukhopadhyay, D., Hascall, V. C., Fries, E., Fülöp, C., Milner, C. M., and Day, A. J. (2005) Characterization of complexes formed between TSG-6 and inter-α-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 280, 25674-25686
19. Sato, H., Kajikawa, S., Kuroda, S., Horisawa, Y., Nakamura, N., Kaga, N., Kakinuma, C., Kato, K., Morishita, H., Niwa, H., and Miyazaki, J. (2001) Impaired fertility in female mice lacking urinary trypsin inhibitor. Biochem. Biophys. Res. Commun. 281, 1154-1160
20. Zhuo, L., Yoneda, M., Zhao, M., Yingsung, W., Yoshida, N., Kitagawa, Y., Kawamura, K., Suzuki, T., and Kimata, K. (2001) Defect in SHAP-hyaluronan complex causes severe female infertility: a study by inactivation of the bikunin gene in mice. J. Biol. Chem. 276, 7693-7696
21. He, H., Li, W., Tseng, D. Y., Zhang, S., Chen, S. Y., Day, A. J., and Tseng, S. C. (2009) Biochemical characterization and function of complexes formed by hyaluronan and the heavy chains of inter-α-inhibitor (HC·HA) purified from extracts of human amniotic membrane. J. Biol. Chem. 284, 20136-20146
22. Shay, E., He, H., Sakurai, S., and Tseng, S. C. (2011) Inhibition of angiogenesis by HC·HA, a complex of hyaluronan and the heavy chain of inter-α-inhibitor, purified from human amniotic membrane. Invest Ophthalmol. Vis. Sci. 52, 2669-2678
23. Zhang, S., He, H., Day, A. J., and Tseng, S. C. (2012) Constitutive expression of inter-α-inhibitor (IαI) family proteins and tumor necrosis factorstimulated gene-6 (TSG-6) by human amniotic membrane epithelial and stromal cells supporting formation of the heavy chain-hyaluronan (HCHA) complex. J. Biol. Chem. 287, 12433-12444
24. He, H., Zhang, S., Tighe, S., Son, J., and Tseng, S. C. (2013) Immobilized HC-HA polarizes LPS-Activated macrophages toward M2 phenotype. J. Biol. Chem. 288, 25792-25803
25. Blom, A. M., Mörgelin, M., Oyen, M., Jarvet, J., and Fries, E. (1999) Structural characterization of inter-α-inhibitor: evidence for an extended shape. J. Biol. Chem. 274, 298-304
26. Muramatu, M., Mori, S., Matsuzawa, Y., Horiguchi, Y., Nakanishi, Y., and Tanaka, M. (1980) Purification and characterization of urinary trypsin inhibitor, UTI68, from normal human urine, and its cleavage by human uropepsin. J. Biochem. 88, 1317-1329
27. Chen, Y. T., Li, W., Hayashida, Y., He, H., Chen, S. Y., Tseng, D. Y., Kheirkhah, A., and Tseng, S. C. (2007) Human amniotic epithelial cells as novel feeder layers for promoting ex vivo expansion of limbal epithelial progenitor cells. Stem Cells 25, 1995-2005
28. Li, W., He, H., Chen, Y. T., Hayashida, Y., and Tseng, S. C. (2008) Reversal of myofibroblasts by amniotic membrane stromal extract. J. Cell. Physiol. 215, 657-664
29. Chen, S. Y., Hayashida, Y., Chen, M. Y., Xie, H. T., and Tseng, S. C. (2011) A new isolation method of human limbal progenitor cells by maintaining close association with their niche cells. Tissue Eng. Part C Methods 17, 537-548
30. He, H., Li, W., Chen, S. Y., Zhang, S., Chen, Y. T., Hayashida, Y., Zhu, Y. T., and Tseng, S. C. (2008) Suppression of activation and induction of apoptosis in RAW264.7 cells by amniotic membrane extract. Invest. Ophthalmol. Vis. Sci. 49, 4468-4475
31. Yoneda, M., Suzuki, S., and Kimata, K. (1990) Hyaluronic acid associated with the surfaces of cultured fibroblasts is linked to a serum-derived 85-kDa protein. J. Biol. Chem. 265, 5247-5257
32. Colón, E., Shytuhina, A., Cowman, M. K., Band, P. A., Sanggaard, K. W., Enghild, J. J., and Wisniewski, H. G. (2009) Transfer of inter-α-inhibitor heavy chains to hyaluronan by surface-linked hyaluronan-TSG-6 complexes. J. Biol. Chem. 284, 2320-2331
33. Rovere-Querini, P., Antonacci, S., Dell'Antonio, G., Angeli, A., Almirante, G., Cin, E. D., Valsecchi, L., Lanzani, C., Sabbadini, M. G., Doglioni, C., Manfredi, A. A., and Castiglioni, M. T. (2006) Plasma and tissue expression of the long pentraxin 3 during normal pregnancy and preeclampsia. Obstet. Gynecol. 108, 148-155
34. Jessen, T. E., Odum, L., and Johnsen, A. H. (1994) In vivo binding of human inter-α-trypsin inhibitor free heavy chains to hyaluronic acid. Biol. Chem. Hoppe-Seyler 375, 521-526
35. Zhao, M., Yoneda, M., Ohashi, Y., Kurono, S., Iwata, H., Ohnuki, Y., and Kimata, K. (1995) Evidence for the covalent binding of SHAP, heavy chains of inter-α-trypsin inhibitor, to hyaluronan. J. Biol. Chem. 270, 26657-26663
36. Inforzato, A., Rivieccio, V., Morreale, A. P., Bastone, A., Salustri, A., Scarchilli, L., Verdoliva, A., Vincenti, S., Gallo, G., Chiapparino, C., Pacello, L., Nucera, E., Serlupi-Crescenzi, O., Day, A. J., Bottazzi, B., Mantovani, A., De Santis, R., and Salvatori, G. (2008) Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J. Biol. Chem. 283, 10147-10161
37. Lee, G. W., Lee, T. H., and Vilcek, J. (1993) TSG-14, a tumor necrosis factor- and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J. Immunol. 150, 1804-1812
38. Lee, T. H., Lee, G. W., Ziff, E. B., and Vilcek, J. (1990) Isolation and characterization of eight tumor necrosis factor-induced gene sequences from human fibroblasts. Mol. Cell. Biol. 10, 1982-1988
39. Luchetti, M. M., Sambo, P., Majlingová, P., Svegliati Baroni, S., Peri, G., Paroncini, P., Introna, M., Stoppacciaro, A., Mantovani, A., and Gabrielli, A. (2004) Scleroderma fibroblasts constitutively express the long pentraxin PTX3. Clin. Exp. Rheumatol. 22, S66-S72
40. Huang, L., Yoneda, M., and Kimata, K. (1993) A serum-derived hyaluronanassociated protein (SHAP) is the heavy chain of the inter α-trypsin inhibitor. J. Biol. Chem. 268, 26725-26730
41. Hassell, J. R., Kane, B. P., Etheredge, L. T., Valkov, N., and Birk, D. E. (2008) Increased stromal extracellular matrix synthesis and assembly by insulin activated bovine keratocytes cultured under agarose. Exp. Eye Res. 87, 604-611
42. Etheredge, L., Kane, B. P., Valkov, N., Adams, S., Birk, D. E., and Hassell, J. R. (2010) Enhanced cell accumulation and collagen processing by keratocytes cultured under agarose and in media containing IGF-I, TGF-κ or PDGF. Matrix Biol. 29, 519-524
43. Yingsung, W., Zhuo, L., Morgelin, M., Yoneda, M., Kida, D., Watanabe, H., Ishiguro, N., Iwata, H., and Kimata, K. (2003) Molecular heterogeneity of the SHAP-hyaluronan complex: isolation and characterization of the complex in synovial fluid from patients with rheumatoid arthritis. J. Biol. Chem. 278, 32710-32718
44. Wisniewski, H. G., Snitkin, E. S., Mindrescu, C., Sweet, M. H., and Vilcek, J. (2005) TSG-6 protein binding to glycosaminoglycans: formation of stable complexes with hyaluronan and binding to chondroitin sulfates. J. Biol. Chem. 280, 14476-14484
45. Baranova, N. S., Foulcer, S. J., Briggs, D. C., Tilakaratna, V., Enghild, J. J., Milner, C. M., Day, A. J., and Richter, R. P. (2013) Inter-α-inhibitor impairs TSG-6-induced hyaluronan cross-linking. J. Biol. Chem. 288, 29642-29653
46. Anderson, C. F., and Mosser, D. M. (2002) A novel phenotype for an activated macrophage: the type 2 activated macrophage. J. Leukocyte Biol. 72, 101-106
47. Edwards, J. P., Zhang, X., Frauwirth, K. A., and Mosser, D. M. (2006) Biochemical and functional characterization of three activated macrophage populations. J. Leukocyte Biol. 80, 1298-1307
48. Mosser, D. M. (2003) The many faces of macrophage activation. J. Leukocyte Biol. 73, 209-212
49. Jaillon, S., Peri, G., Delneste, Y., Frémaux, I., Doni, A., Moalli, F., Garlanda, C., Romani, L., Gascan, H., Bellocchio, S., Bozza, S., Cassatella, M. A., Jeannin, P., and Mantovani, A. (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J. Exp. Med. 204, 793-804
50. Nauta, A. J., De Haij, S., Bottazzi, B., Mantovani, A., Borrias, M. C., Aten, J., Rastaldi, M. P., Daha, M. R., Van Kooten, C., and Roos, A. (2005) Human renal epithelial cells produce the long pentraxin PTX3. Kidney Int. 67, 543-553
51. Bouchard, C. S., and John, T. (2004) Amniotic membrane transplantation in the management of severe ocular surface disease: indications and outcomes. Ocul. Surf. 2, 201-211
52. Dua, H. S., Gomes, J. A., King, A. J., and Maharajan, V. S. (2004) The amniotic membrane in ophthalmology. Surv. Ophthalmol. 49, 51-77
53. Tseng, S. C. (2001) Amniotic membrane transplantation for ocular surface reconstruction. Biosci. Rep. 21, 481-489
54. Tseng, S. C., Espana, E. M., Kawakita, T., Di Pascuale, M. A., Li, W., He, H., Liu, T. S., Cho, T. H., Gao, Y. Y., Yeh, L. K., and Liu, C. Y. (2004) How does amniotic membrane work? Ocul. Surf. 2, 177-187