Versican deficiency significantly reduces lung inflammatory response induced by polyinosine-polycytidylic acidstimulation

Journal of Biological Chemistry

Volumn 292, Issue 1, 2017, Pages 51-63

  Kang, Inkyung ^a   Harten, Ingrid A ^a   Chang, Mary Y ^b   Braun, Kathleen R ^a   Sheih, Alyssa ^a   Nivison, Mary P ^a,d   Johnson, Pamela Y ^a   Workman, Gail ^a   Kaber, Gernot ^a   Evanko, Stephen P ^a   Chan, Christina K ^a   Merrilees, Mervyn J ^c   Ziegler, Steven F ^a   Kinsella, Michael G ^a   Frevert, Charles W ^b   Wight, Thomas N ^a  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; CELL CULTURE; FIBROBLASTS; HYALURONIC ACID; MAMMALS;

ALLERGIC REACTIONS; BRONCHOALVEOLAR LAVAGE FLUID; EXTRACELLULAR MATRICES; INFLAMMATORY MEDIATORS; INFLAMMATORY RESPONSE; MONOCYTE ADHESION; PROINFLAMMATORY CYTOKINES; TOLL-LIKE RECEPTOR 3;

BIOLOGICAL ORGANS;

ALPHA INTERFERON; CXCL2 CHEMOKINE; GAMMA INTERFERON; HYALURONIC ACID; INTERLEUKIN 10; INTERLEUKIN 1BETA; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; VERSICAN; CHEMOKINE; CSPG2 PROTEIN, MOUSE; CYTOKINE; INTERFERON INDUCING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CONTROLLED STUDY; EXTRACELLULAR MATRIX; LEUKOCYTE ADHERENCE; LEUKOCYTE COUNT; LUNG FIBROBLAST; MONOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; RESPIRATORY TRACT INFLAMMATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FEMALE; FIBROBLAST; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PNEUMONIA;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; CHEMOKINES; CYTOKINES; FEMALE; FIBROBLASTS; INTERFERON INDUCERS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; PNEUMONIA; POLY I-C; VERSICANS;

EID: 85009388236     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: None     Document Type: Article

References (77)

1. Shibata, T., Habiel, D. M., Coelho, A. L., Kunkel, S. L., Lukacs, N. W., and Hogaboam, C. M. (2014) Axl receptor blockade ameliorates pulmonary pathology resulting from primary viral infection and viral exacerbation of asthma. J. Immunol. 192, 3569-3581
2. Tan, W. C. (2005) Viruses in asthma exacerbations. Curr. Opin. Pulm. Med. 11, 21-26
3. Saraya, T., Kurai, D., Ishii, H., Ito, A., Sasaki, Y., Niwa, S., Kiyota, N., Tsukagoshi, H., Kozawa, K., Goto, H., and Takizawa, H. (2014) Epidemiology of virus-induced asthma exacerbations: with special reference to the role of human rhinovirus. Front. Microbiol. 5, 226
4. Kurai, D., Saraya, T., Ishii, H., and Takizawa, H. (2013) Virus-induced exacerbations in asthma and COPD. Front. Microbiol. 4, 293
5. Papadopoulos, N. G., Christodoulou, I., Rohde, G., Agache, I., Almqvist, C., Bruno, A., Bonini, S., Bont, L., Bossios, A., Bousquet, J., Braido, F., Brusselle, G., Canonica, G. W., Carlsen, K. H., Chanez, P., et al. (2011) Viruses and bacteria in acute asthma exacerbations-a GA(2) LEN-DARE systematic review. Allergy 66, 458-468
6. Clarke, D. L., Davis, N. H., Majithiya, J. B., Piper, S. C., Lewis, A., Sleeman, M. A., Corkill, D. J., and May, R. D. (2014) Development of a mouse model mimicking key aspects of a viral asthma exacerbation. Clin. Sci. 126, 567-580
7. Shannon, J. M., McCormick-Shannon, K., Burhans, M. S., Shangguan, X., Srivastava, K., and Hyatt, B. A. (2003) Chondroitin sulfate proteoglycans are required for lung growth and morphogenesis in vitro. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L1323-L1336
8. Faggian, J., Fosang, A. J., Zieba, M., Wallace, M. J., and Hooper, S. B. (2007) Changes in versican and chondroitin sulphate proteoglycans during structural development of the lung. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R784-R792
9. Snyder, J. M., Washington, I. M., Birkland, T., Chang, M. Y., and Frevert, C. W. (2015) Correlation of versican expression, accumulation, and degradation during embryonic development by quantitative immunohistochemistry. J. Histochem. Cytochem. 63, 952-967
10. Johnson, P. R. (2001) Role of human airway smooth muscle in altered extracellular matrix production in asthma. Clin. Exp. Pharmacol. Physiol. 28, 233-236
11. Roberts, C. R. (1995) Is asthma a fibrotic disease? Chest 107, 111S-117S
12. Huang, J., Olivenstein, R., Taha, R., Hamid, Q., and Ludwig, M. (1999) Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am. J. Respir. Crit. Care Med. 160, 725-729
13. de Medeiros Matsushita, M., da Silva, L. F., dos Santos, M. A., Fernezlian, S., Schrumpf, J. A., Roughley, P., Hiemstra, P. S., Saldiva, P. H., Mauad, T., and Dolhnikoff, M. (2005) Airway proteoglycans are differentially altered in fatal asthma. J. Pathol. 207, 102-110
14. Westergren-Thorsson, G., Chakir, J., Lafrenière-Allard, M. J., Boulet, L. P., and Tremblay, G. M. (2002) Correlation between airway responsiveness and proteoglycan production by bronchial fibroblasts from normal and asthmatic subjects. Int. J. Biochem. Cell Biol. 34, 1256-1267
15. Weitoft, M., Andersson, C., Andersson-Sjöland, A., Tufvesson, E., Bjermer, L., Erjefält, J., and Westergren-Thorsson, G. (2014) Controlled and uncontrolled asthma display distinct alveolar tissue matrix compositions. Respir. Res. 15, 67
16. Andersson-Sjöland, A., Hallgren, O., Rolandsson, S., Weitoft, M., Tykesson, E., Larsson-Callerfelt, A. K., Rydell-Törmänen, K., Bjermer, L., Malmström, A., Karlsson, J. C., and Westergren-Thorsson, G. (2015) Versican in inflammation and tissue remodeling: the impact on lung disorders. Glycobiology 25, 243-251
17. Zhu, Z., Ma, B., Zheng, T., Homer, R. J., Lee, C. G., Charo, I. F., Noble, P., and Elias, J. A. (2002) IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 168, 2953-2962
18. Lowry, M. H., McAllister, B. P., Jean, J. C., Brown, L. A., Hughey, R. P., Cruikshank, W. W., Amar, S., Lucey, E. C., Braun, K., Johnson, P., Wight, T. N., and Joyce-Brady, M. (2008) Lung lining fluid glutathione attenuates IL-13-induced asthma. Am. J. Respir. Cell Mol. Biol. 38, 509-516
19. Chang, M. Y., Tanino, Y., Vidova, V., Kinsella, M. G., Chan, C. K., Johnson, P. Y., Wight, T. N., and Frevert, C. W. (2014) A rapid increase in macrophage-derived versican and hyaluronan in infectious lung disease. Matrix Biol. 34, 1-12
20. Malmström, J., Larsen, K., Hansson, L., Löfdahl, C. G., Nörregard-Jensen, O., Marko-Varga, G., and Westergren-Thorsson, G. (2002) Proteoglycan and proteome profiling of central human pulmonary fibrotic tissue utilizing miniaturized sample preparation: a feasibility study. Proteomics 2, 394-404
21. Ludwig, M. S., Ftouhi-Paquin, N., Huang, W., Pagé, N., Chakir, J., and Hamid, Q. (2004) Mechanical strain enhances proteoglycan message in fibroblasts from asthmatic subjects. Clin. Exp. Allergy 34, 926-930
22. Reeves, S. R., Kaber, G., Sheih, A., Cheng, G., Aronica, M. A., Merrilees, M. J., Debley, J. S., Frevert, C. W., Ziegler, S. F., and Wight, T. N. (2016) Subepithelial accumulation of versican in a cockroach antigen-induced murine model of allerigic asthma. J. Histochem. Cytochem. 64, 364-380
23. de la Motte, C., Hascall, V. C., Drazba, J. A., and Strong, S. A. (2002) Poly I:C induces mononuclear leukocyte-adhesive hyaluronan structures on colon smooth muscle cells: IaI and versican facilitate adhesion. in Hyaluronan: Chemical, Biochemical and Biological Aspects (Kennedy, J. F., Phillips, G. O., Williams, P. A., and Hascall, V. C., eds) pp. 381-388, Woodhead Publishing Ltd., Cambridge, UK
24. de la Motte, C. A., Hascall, V. C., Drazba, J., Bandyopadhyay, S. K., and Strong, S. A. (2003) Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid:polycytidylic acid: inter-trypsin inhibitor is crucial to structure and function. Am. J. Pathol. 163, 121-133
25. 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-inhibitor heavy chain attachment. J. Biol. Chem. 284, 5313-5323
26. Lauer, M. E., Mukhopadhyay, D., Fulop, C., de la Motte, C. A., Majors, A. K., and Hascall, V. C. (2009) Primary murine airway smooth muscle cells exposed to poly(I,C) or tunicamycin synthesize a leukocyte-adhesive hyaluronan matrix. J. Biol. Chem. 284, 5299-5312
27. Wang, A., and Hascall, V. C. (2004) Hyaluronan structures synthesized by rat mesangial cells in response to hyperglycemia induce monocyte adhesion. J. Biol. Chem. 279, 10279-10285
28. Torres, D., Dieudonné, A., Ryffel, B., Vilain, E., Si-Tahar, M., Pichavant, M., Lassalle, P., Trottein, F., and Gosset, P. (2010) Double-stranded RNA exacerbates pulmonary allergic reaction through TLR3: implication of airway epithelium and dendritic cells. J. Immunol. 185, 451-459
29. Stowell, N. C., Seideman, J., Raymond, H. A., Smalley, K. A., Lamb, R. J., Egenolf, D. D., Bugelski, P. J., Murray, L. A., Marsters, P. A., Bunting, R. A., Flavell, R. A., Alexopoulou, L., San Mateo, L. R., Griswold, D. E., Sarisky, R. T., et al. (2009) Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir. Res. 10, 43
30. Evanko, S. P., Potter-Perigo, S., Bollyky, P. L., Nepom, G. T., and Wight, T. N. (2012) Hyaluronan and versican in the control of human T-lymphocyte adhesion and migration. Matrix Biol. 31, 90-100
31. Evanko, S. P., Potter-Perigo, S., Johnson, P. Y., and Wight, T. N. (2009) Organization of hyaluronan and versican in the extracellular matrix of human fibroblasts treated with the viral mimetic poly I:C. J. Histochem. Cytochem. 57, 1041-1060
32. Potter-Perigo, S., Johnson, P. Y., Evanko, S. P., Chan, C. K., Braun, K. R., Wilkinson, T. S., Altman, L. C., and Wight, T. N. (2010) Polyinosinepolycytidylic acid stimulates versican accumulation in the extracellular matrix promoting monocyte adhesion. Am. J. Respir. Cell Mol. Biol. 43, 109-120
33. Wight, T. N., Kang, I., and Merrilees, M. J. (2014) Versican and the control of inflammation. Matrix Biol. 35, 152-161
34. Kang, I., Yoon, D. W., Braun, K. R., and Wight, T. N. (2014) Expression of versicanV3byarterialsmoothmusclecellsaltersTGF-,EGF-,andNF-B-dependent signaling pathways, creating a microenvironment that resists monocyte adhesion. J. Biol. Chem. 289, 15393-15404
35. Mjaatvedt, C. H., Yamamura, H., Capehart, A. A., Turner, D., and Markwald, R. R. (1998) The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 202, 56-66
36. Selbi, W., de la Motte, C. A., Hascall, V. C., Day, A. J., Bowen, T., and Phillips, A. O. (2006) Characterization of hyaluronan cable structure and function in renal proximal tubular epithelial cells. Kidney Int. 70, 1287-1295
37. Jokela, T. A., Lindgren, A., Rilla, K., Maytin, E., Hascall, V. C., Tammi, R. H., and Tammi, M. I. (2008) Induction of hyaluronan cables and monocyte adherence in epidermal keratinocytes. Connect. Tissue Res. 49, 115-119
38. 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
39. Hatano, S., Kimata, K., Hiraiwa, N., Kusakabe, M., Isogai, Z., Adachi, E., Shinomura, T., and Watanabe, H. (2012) Versican/PG-M is essential for ventricular septal formation subsequent to cardiac atrioventricular cushion development. Glycobiology 22, 1268-1277
40. Choocheep, K., Hatano, S., Takagi, H., Watanabe, H., Kimata, K., Kongtawelert, P., and Watanabe, H. (2010) Versican facilitates chondrocyte differentiation and regulates joint morphogenesis. J. Biol. Chem. 285, 21114-21125
41. Fanhchaksai, K., Okada, F., Nagai, N., Pothacharoen, P., Kongtawelert, P., Hatano, S., Makino, S., Nakamura, T., and Watanabe, H. (2016) Host stromal versican is essential for cancer-associated fibroblast function to inhibit cancer growth. Int. J. Cancer 138, 630-641
42. Merrilees, M. J., Ching, P. S. T., Beaumont, B., Hinek, A., Wight, T. N., and Black, P. N. (2008) Changes in elastin, elastin binding protein and versican in alveoli in chronic obstructive pulmonary disease. Respir. Res. 9, 41
43. Bensadoun, E. S., Burke, A. K., Hogg, J. C., and Roberts, C. R. (1996) Proteoglycan deposition in pulmonary fibrosis. Am. J. Respir Crit. Care Med. 154, 1819-1828
44. Merrilees, M. J., Hankin, E. J., Black, J. L., and Beaumont, B. (2004) Matrix proteoglycans and remodelling of interstitial lung tissue in lymphangioleiomyomatosis. J. Pathol. 203, 653-660
45. Morales, M. M., Pires-Neto, R. C., Inforsato, N., Lancas, T., da Silva, L. F., Saldiva, P. H., Mauad, T., Carvalho, C. R., Amato, M. B., and Dolhnikoff, M. (2011) Small airway remodeling in acute respiratory distress syndrome: a study in autopsy lung tissue. Crit. Care 15, R4
46. Araujo, B. B., Dolhnikoff, M., Silva, L. F., Elliot, J., Lindeman, J. H., Ferreira, D. S., Mulder, A., Gomes, H. A., Fernezlian, S. M., James, A., and Mauad, T. (2008) Extracellular matrix components and regulators in the airway smooth muscle in asthma. Eur. Respir. J. 32, 61-69
47. Ayars, A. G., Altman, L. C., Potter-Perigo, S., Radford, K., Wight, T. N., and Nair, P. (2013) Sputum hyaluronan and versican in severe eosinophilic asthma. Int. Arch. Allergy Immunol. 161, 65-73
48. Gordon, S. (2002) Pattern recognition receptors: doubling up for the innate immune response. Cell 111, 927-930
49. Alexopoulou, L., Holt, A. C., Medzhitov, R., and Flavell, R. A. (2001) Recognition of double-stranded RNA and activation of NF-B by Toll-like receptor 3. Nature 413, 732-738
50. Vigetti, D., Genasetti, A., Karousou, E., Viola, M., Moretto, P., Clerici, M., Deleonibus, S., De Luca, G., Hascall, V. C., and Passi, A. (2010) Proinflammatory cytokines induce hyaluronan synthesis and monocyte adhesion in human endothelial cells through hyaluronan synthase 2 (HAS2) and the nuclear factor-B (NF-B) pathway. J. Biol. Chem. 285, 24639-24645
51. Wilkinson, T. S., Potter-Perigo, S., Tsoi, C., Altman, L. C., and Wight, T. N. (2004) Pro-and anti-inflammatory factors cooperate to control hyaluronan synthesis in lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 31, 92-99
52. Mohamadzadeh, M., DeGrendele, H., Arizpe, H., Estess, P., and Siegelman, M. (1998) Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion. J. Clin. Invest. 101, 97-108
53. Bauernfeind, F. G., Horvath, G., Stutz, A., Alnemri, E. S., MacDonald, K., Speert, D., Fernandes-Alnemri, T., Wu, J., Monks, B. G., Fitzgerald, K. A., Hornung, V., and Latz, E. (2009) Cutting edge: NF-B activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183, 787-791
54. Babelova, A., Moreth, K., Tsalastra-Greul, W., Zeng-Brouwers, J., Eickelberg, O., Young, M. F., Bruckner, P., Pfeilschifter, J., Schaefer, R. M., Gröne, H. J., and Schaefer, L. (2009) Biglycan, a danger signal that activates the NLRP3 inflammasome via Toll-like and P2X receptors. J. Biol. Chem. 284, 24035-24048
55. Allen, I. C., Scull, M. A., Moore, C. B., Holl, E. K., McElvania-TeKippe, E., Taxman, D. J., Guthrie, E. H., Pickles, R. J., and Ting, J. P. (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556-565
56. Kim, S., Takahashi, H., Lin, W. W., Descargues, P., Grivennikov, S., Kim, Y., Luo, J. L., and Karin, M. (2009) Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457, 102-106
57. Wang, W., Xu, G. L., Jia, W. D., Ma, J. L., Li, J. S., Ge, Y. S., Ren, W. H., Yu, J. H., and Liu, W. B. (2009) Ligation of TLR2 by versican: a link between inflammation and metastasis. Arch. Med. Res. 40, 321-323
58. Bögels, M., Braster, R., Nijland, P. G., Gül, N., van de Luijtgaarden, W., Fijneman, R. J., Meijer, G. A., Jimenez, C. R., Beelen, R. H., and van Egmond, M. (2012) Carcinoma origin dictates differential skewing of monocyte function. Oncoimmunology 1, 798-809
59. Li, D., Wang, X., Wu, J. L., Quan, W. Q., Ma, L., Yang, F., Wu, K. Y., and Wan, H. Y. (2013) Tumor-produced versican V1 enhances hCAP18/ LL-37 expression in macrophages through activation of TLR2 and vitamin D3 signaling to promote ovarian cancer progression in vitro. PLoS One 8, e56616
60. Said, N., Sanchez-Carbayo, M., Smith, S. C., and Theodorescu, D. (2012) RhoGDI2 suppresses lung metastasis in mice by reducing tumor versican expression and macrophage infiltration. J. Clin. Invest. 122, 1503-1518
61. Said, N., and Theodorescu, D. (2012) RhoGDI2 suppresses bladder cancer metastasis via reduction of inflammation in the tumor microenvironment. Oncoimmunology 1, 1175-1177
62. Zhang, Z., Miao, L., and Wang, L. (2012) Inflammation amplification by versican: the first mediator. Int. J. Mol. Sci. 13, 6873-6882
63. Hope, C., Ollar, S. J., Heninger, E., Hebron, E., Jensen, J. L., Kim, J., Maroulakou, I., Miyamoto, S., Leith, C., Yang, D. T., Callander, N., Hematti, P., Chesi, M., Bergsagel, P. L., and Asimakopoulos, F. (2014) TPL2 kinase regulates the inflammatory milieu of the myeloma niche. Blood 123, 3305-3315
64. Tang, M., Diao, J., Gu, H., Khatri, I., Zhao, J., and Cattral, M. S. (2015) Toll-like receptor 2 activation promotes tumor dendritic cell dysfunction by regulating IL-6 and IL-10 receptor signaling. Cell Rep. 13, 2851-2864
65. Schaefer, L., Babelova, A., Kiss, E., Hausser, H. J., Baliova, M., Krzyzankova, M., Marsche, G., Young, M. F., Mihalik, D., Götte, M., Malle, E., Schaefer, R. M., and Gröne, H. J. (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J. Clin. Invest. 115, 2223-2233
66. Moreth, K., Frey, H., Hubo, M., Zeng-Brouwers, J., Nastase, M. V., Hsieh, L. T., Haceni, R., Pfeilschifter, J., Iozzo, R. V., and Schaefer, L. (2014) Biglycan-triggered TLR-2-and TLR-4-signaling exacerbates the pathophysiology of ischemic acute kidney injury. Matrix Biol. 35, 143-151
67. Kawashima, H., Hirose, M., Hirose, J., Nagakubo, D., Plaas, A. H., and Miyasaka, M. (2000) Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J. Biol. Chem. 275, 35448-35456
68. Misra, S., Toole, B. P., and Ghatak, S. (2006) Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells. J. Biol. Chem. 281, 34936-34941
69. Misra, S., Ghatak, S., and Toole, B. P. (2005) Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hyaluronan, phosphoinositide 3-kinase, and ErbB2. J. Biol. Chem. 280, 20310-20315
70. Ghatak, S., Misra, S., and Toole, B. P. (2005) Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J. Biol. Chem. 280, 8875-8883
71. Ghatak, S., Misra, S., and Toole, B. P. (2002) Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J. Biol. Chem. 277, 38013-38020
72. Bourguignon, L. Y., Gilad, E., and Peyrollier, K. (2007) Heregulin-mediated ErbB2-ERK signaling activates hyaluronan synthases leading to CD44-dependent ovarian tumor cell growth and migration. J. Biol. Chem. 282, 19426-19441
73. Ohkawa, T., Ueki, N., Taguchi, T., Shindo, Y., Adachi, M., Amuro, Y., Hada, T., and Higashino, K. (1999) Stimulation of hyaluronan synthesis by tumor necrosis factor-is mediated by the p50/p65 NF-B complex in MRC-5 myofibroblasts. Biochim. Biophys. Acta 1448, 416-424
74. Han, H., and Ziegler, S. F. (2013) Bronchoalveolar lavage and lung tissue digestion. Bio. Protoc. 3, e859
75. Shih, S. C., and Smith, L. E. (2005) Quantitative multi-gene transcriptional profiling using real-time PCR with a master template. Exp. Mol. Pathol. 79, 14-22
76. Schönherr, E., Kinsella, M. G., and Wight, T. N. (1997) Genistein selectively inhibits platelet-derived growth factor stimulated versican biosynthesis in monkey arterial smooth muscle cells. Arch. Biochem. Biophys. 339, 353-361
77. Masuda, A., Yasuoka, H., Satoh, T., Okazaki, Y., Yamaguchi, Y., and Kuwana, M. (2013) Versican is upregulated in circulating monocytes in patients with systemic sclerosis and amplifies a CCL2-mediated pathogenic loop. Arthritis Res. Ther. 15, R74