Endotoxin free hyaluronan and hyaluronan fragments do not stimulate TNF-α, interleukin-12 or upregulate co-stimulatory molecules in dendritic cells or macrophages

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Dong, Yifei ^a   Arif, Arif ^a   Olsson, Mia ^a,b   Cali, Valbona ^c   Hardman, Blair ^a   Dosanjh, Manisha ^a   Lauer, Mark ^c   Midura, Ronald J ^c   Hascall, Vincent C ^c   Brown, Kelly L ^b   Johnson, Pauline ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; INTERLEUKIN 12; TUMOR NECROSIS FACTOR;

ANIMAL; BIOSYNTHESIS; CELL CULTURE; DENDRITIC CELL; DRUG EFFECT; IMMUNOLOGY; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLISM; MOUSE;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; HYALURONIC ACID; INTERLEUKIN-12; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84995938229     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36928     Document Type: Article

References (54)

1. Lee-Sayer, S. S. M. et al. The where, when, how, and why of hyaluronan binding by immune cells. Front. Immunol. 6, 150, 10.3389/fimmu.2015.00150 (2015).
2. Monslow, J., Govindaraju, P. & Pure, E. Hyaluronan - a functional and structural sweet spot in the tissue microenvironment. Front. Immunol. 6, 231, 10.3389/fimmu.2015.00231 (2015).
3. Jiang, D., Liang, J. & Noble, P. W. Hyaluronan in tissue injury and repair. Annu. Rev. Cell Dev. Biol. 23, 435-461 (2007).
4. Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C. B. & Seed, B. CD44 is the principal cell-surface receptor for hyaluronate. Cell 61, 1303-1313 (1990).
5. Culty, M., Omara, T. E., Underhill, C. B., Yeager, H. & Swartz, R. P. Hyaluronan receptor (CD44) expression and function in human peripheral-blood monocytes and alveolar macrophages. J. Leukoc. Biol. 56, 605-611 (1994).
6. Underhill, C. B., Nguyen, H. A., Shizari, M. & Culty, M. CD44 positive macrophages take up hyaluronan during lung development. Dev. Biol. 155, 324-336 (1993).
7. Jadin, L., Bookbinder, L. H. & Frost, G. I. A comprehensive model of hyaluronan turnover in the mouse. Matrix Biol. 31, 81-89 (2012).
8. Yasuda, T. Hyaluronan inhibits cytokine production by lipopolysaccharide-stimulated U937 macrophages through down-regulation of NF-kB. Ann. Rheum. Dis. 66, 155-155 (2007).
9. Gavina, M. et al. Nebulized hyaluronan ameliorates lung inflammation in cystic fibrosis mice. Pediatr. Pulmonol. 48, 761-771 (2013).
10. Teder, P. et al. Resolution of lung inflammation by CD44. Science 296, 155-158 (2002).
11. Bracke, K. R. et al. Enhanced deposition of low-molecular-weight hyaluronan in lungs of cigarette smoke-exposed mice. Am. J. Respir. Cell Mol. Biol. 42, 753-761 (2010).
12. Cheng, G. et al. Hyaluronan deposition and correlation with inflammation in a murine ovalbumin model of asthma. Matrix Biol. 30, 126-134 (2011).
13. Monzon, M. E. et al. Reactive oxygen species and hyaluronidase 2 regulate airway epithelial hyaluronan fragmentation. J. Biol. Chem. 285, 26126-26134 (2010).
14. Muto, J. et al. Hyaluronan digestion controls DC migration from the skin. J. Clin. Invest. 124, 1309-1319 (2014).
15. Esser, P. R. et al. Contact sensitizers induce skin inflammation via ROS production and hyaluronic acid degradation. PLoS One 7, e41340, 10.1371/journal.pone.0041340 (2012).
16. Cyphert, J. M., Trempus, C. S. & Garantziotis, S. Size matters: molecular weight specificity of hyaluronan effects in cell biology. Int. J. Cell. Biol. 2015, 563818, 10.1155/2015/563818 (2015).
17. de la Motte, C. A., Hascall, V. C., Drazba, J., Bandyopadhyay, S. K. & Strong, S. A. Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid: polycytidylic acid-inter-alpha-trypsin inhibitor is crucial to structure and function. Am. J. Pathol. 163, 121-133 (2003).
18. Rugg, M. S. et al. Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 280, 25674-25686 (2005).
19. Lauer, M. E. et al. Irreversible heavy chain transfer to hyaluronan oligosaccharides by tumor necrosis factor-stimulated gene-6. J. Biol. Chem. 288, 205-214 (2013).
20. Swaidani, S. et al. TSG-6 protein is crucial for the development of pulmonary hyaluronan deposition, eosinophilia, and airway hyperresponsiveness in a murine model of asthma. J. Biol. Chem. 288, 412-422 (2013).
21. Krejcova, D., Pekarova, M., Safrankova, B. & Kubala, L. The effect of different molecular weight hyaluronan on macrophage physiology. Neuro. Endocrinol. Lett. 30 Suppl 1, 106-111 (2009).
22. Ebid, R., Lichtnekert, J. & Anders, H. J. Hyaluronan is not a ligand but a regulator of Toll-like receptor signaling in mesangial cells: role of extracellular matrix in innate immunity. ISRN Nephrol. 2014, 714081, 10.1155/2014/714081 (2014).
23. Huang, Z. et al. Recombinant human hyaluronidase PH20 does not stimulate an acute inflammatory response and inhibits lipopolysaccharide-induced neutrophil recruitment in the air pouch model of inflammation. J. Immunol. 192, 5285-5295 (2014).
24. Shiedlin, A. et al. Evaluation of hyaluronan from different sources: Streptococcus zooepidemicus, rooster comb, bovine vitreous, and human umbilical cord. Biomacromolecules 5, 2122-2127 (2004).
25. Filion, M. C. & Phillips, N. C. Pro-inflammatory activity of contaminating DNA in hyaluronic acid preparations. J. Pharm. Pharmacol. 53, 555-561 (2001).
26. Tynan, G. A., McNaughton, A., Jarnicki, A., Tsuji, T. & Lavelle, E. C. Polymyxin B inadequately quenches the effects of contaminating lipopolysaccharide on murine dendritic cells. PLoS One 7, e37261, 10.1371/journal.pone.0037261 (2012).
27. Ruffell, B. et al. Differential use of chondroitin sulfate to regulate hyaluronan binding by receptor CD44 in inflammatory and interleukin 4-activated macrophages. J. Biol. Chem. 286, 19179-19190 (2011).
28. Poon, G. F. et al. Hyaluronan binding identifies a functionally distinct alveolar macrophage-like population in bone marrow-derived dendritic cell cultures. J. Immunol. 195, 632-642 (2015).
29. Lazrak, A. et al. Hyaluronan mediates airway hyperresponsiveness in oxidative lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 308, L891-L903 (2015).
30. McKee, C. M. et al. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J. Clin. Invest. 98, 2403-2413 (1996).
31. Andonegui, G. et al. Endothelium-derived toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J. Clin. Invest. 112, 1011-1020 (2003).
32. Agren, U. M., Tammi, R. H. & Tammi, M. I. Reactive oxygen species contribute to epidermal hyaluronan catabolism in human skin organ culture. Free Radic. Biol. Med. 23, 996-1001 (1997).
33. Duner, K. I. A New kinetic single-stage limulus amebocyte lysate method for the detection of endotoxin in water and plasma. J. Biochem. Bioph. Meth. 26, 131-142 (1993).
34. Cooperstock, M. S. Inactivation of endotoxin by polymyxin B. Antimicrob. Agents Chemother. 6, 422-425 (1974).
35. Sokolowska, M. et al. Low molecular weight hyaluronan activates cytosolic phospholipase A2alpha and eicosanoid production in monocytes and macrophages. J. Biol. Chem. 289, 4470-4488 (2014).
36. Oertli, B., Beck-Schimmer, B., Fan, X. & Wuthrich, R. P. Mechanisms of hyaluronan-induced up-regulation of ICAM-1 and VCAM-1 expression by murine kidney tubular epithelial cells: hyaluronan triggers cell adhesion molecule expression through a mechanism involving activation of nuclear factor-kappa B and activating protein-1. J. Immunol. 161, 3431-3437 (1998).
37. Wallet, M. A., Wallet, S. M., Guiulfo, G., Sleasman, J. W. & Goodenow, M. M. IFNgamma primes macrophages for inflammatory activation by high molecular weight hyaluronan. Cell. Immunol. 262, 84-88 (2010).
38. Liu, S. et al. Removal of endotoxin from recombinant protein preparations. Clin. Biochem. 30, 455-463 (1997).
39. Thalberg, K. & Lindman, B. Interaction between hyaluronan and cationic surfactants. J. Phys. Chem. 93, 1478-1483 (1989).
40. Schromm, A. B. et al. The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity. J. Immunol. 161, 5464-5471 (1998).
41. Mares, J., Kumaran, S., Gobbo, M. & Zerbe, O. Interactions of lipopolysaccharide and polymyxin studied by NMR spectroscopy. J. Biol. Chem. 284, 11498-11506, (2009).
42. Termeer, C. C. et al. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J. Immunol. 165, 1863-1870 (2000).
43. Scheibner, K. A. et al. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J. Immunol. 177, 1272-1281 (2006).
44. Chong, B. F., Blank, L. M., McLaughlin, R. & Nielsen, L. K. Microbial hyaluronic acid production. Appl. Microbiol. Biotechnol. 66, 341-351 (2005).
45. Li, Z., Potts-Kant, E. N., Garantziotis, S., Foster, W. M. & Hollingsworth, J. W. Hyaluronan signaling during ozone-induced lung injury requires TLR4, MyD88, and TIRAP. PLoS One 6, e27137, 10.1371/journal.pone.0027137 (2011).
46. Vistejnova, L. et al. Low molecular weight hyaluronan mediated CD44 dependent induction of IL-6 and chemokines in human dermal fibroblasts potentiates innate immune response. Cytokine 70, 97-103 (2014).
47. Noble, P. W., McKee, C. M., Cowman, M. & Shin, H. S. Hyaluronan fragments activate an NF-kappa B/I-kappa B alpha autoregulatory loop in murine macrophages. J. Exp. Med. 183, 2373-2378 (1996).
48. Martin, S. F. et al. Toll-like receptor and IL-12 signaling control susceptibility to contact hypersensitivity. J. Exp. Med. 205, 2151-2162, (2008).
49. Sasaki, E. et al. Serum hyaluronic acid concentration predicts the progression of joint space narrowing in normal knees and established knee osteoarthritis - a five-year prospective cohort study. Arthritis Res. Ther. 17, 283, 10.1186/s13075-015-0793-0 (2015).
50. Peng, C. et al. Plasma hyaluronic acid level as a prognostic and monitoring marker of metastatic breast cancer. Int J Cancer, 138, 2499-2509 (2016).
51. Neuman, M. G., Cohen, L. B. & Nanau, R. M. Hyaluronic acid as a non-invasive biomarker of liver fibrosis. Clin. Biochem. 49, 302-315, (2016).
52. Schmits, R. et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood 90, 2217-2233 (1997).
53. de Belder, A. N. & Wik, K. O. Preparation and properties of fluorescein-labelled hyaluronate. Carbohydr. Res. 44, 251-257 (1975).
54. Stockinger, B., Zal, T., Zal, A. & Gray, D. B cells solicit their own help from T cells. J. Exp. Med. 183, 891-899 (1996).