Biomolecules & Therapeutics

  • 제28권3호
  • /
  • Pages.272-281
  • /
  • 2020
  • /
  • 1976-9148(pISSN)
  • /
  • 2005-4483(eISSN)
한국응용약물학회 (The Korean Society of Applied Pharmacology)
권호 표지
DOI QR코드

DOI QR Code

A 3D "In Vitro" Model to Study Hyaluronan Effect in Nasal Epithelial Cell Line Exposed to Double-Stranded RNA Poly(I:C)

  • Albano, Giusy Daniela (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Bonanno, Anna (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Giacomazza, Daniela (Institute of Biophysic, CNR) ;
  • Cavalieri, Luca (Chiesi Farmaceutici SpA) ;
  • Sammarco, Martina (Chiesi Farmaceutici SpA) ;
  • Ingrassia, Eleonora (Chiesi Farmaceutici SpA) ;
  • Gagliardo, Rosalia (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Riccobono, Loredana (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Moscato, Monica (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Anzalone, Giulia (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Montalbano, Angela Marina (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR)) ;
  • Profita, Mirella (Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR))
  • 투고 : 2019.07.23
  • 심사 : 2019.09.16
  • 발행 : 2020.05.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Environmental agents, including viral and bacterial infectious agents, are involved in the alteration of physicochemical and biological parameters in the nasal epithelium. Hyaluronan (HA) has an important role in the regulation of tissue healing properties. High molecular weight HA (HMW-HA) shows greater anti-inflammatory responses than medium molecular weight HA (MMW-HA) and low molecular weight HA (LMW-HA). We investigated the effect of HMW-HA, MMW-HA and LMW-HA on the regulation of physicochemical and biological parameters in an "in vitro" model that might mimic viral infections of the nasal epithelium. Human nasal epithelial cell line RPMI2650 was stimulated with double-stranded RNA (dsRNA) Poly(I:C) for 5 days in air-liquid-interface (ALI) culture (3D model of airway tissue). dsRNA Poly(I:C) treatment significantly decreased transepithelial electrical resistance (TEER) in the stratified nasal epithelium of RPMI2650 and increased pH values, rheological parameters (elastic G' and viscous G''), and Muc5AC and Muc5B production in the apical wash of ALI culture of RPMI2650 in comparison to untreated cells. RPMI2650 treated with dsRNA Poly(I:C) in the presence of HMW-HA showed lower pH values, Muc5AC and Muc5B production, and rheological parameters, as well as increased TEER values in ALI culture, compared to cells treated with Poly(I:C) alone or pretreated with LMW-HA and MMW-HA. Our 3D "in vitro" model of epithelium suggests that HMW-HA might be a coadjuvant in the pharmacological treatment of viral infections, allowing for the control of some physicochemical and biological properties affecting the epithelial barrier of the nose during infection.

키워드

참고문헌

  1. Albano, G. D., Bonanno, A., Cavalieri, L., Ingrassia, E., Di Sano, C., Siena, L., Riccobono, L., Gagliardo, R. and Profita, M. (2016) effect of high, medium, and low molecular weight hyaluronan on inflammation and oxidative stress in an in vitro model of human nasal epithelial cells. Mediators Inflamm. 2016, 8727289.
  2. Ambort, D., Johansson, M. E., Gustafsson, J. K., Ermund, A. and Hansson, G. C. (2012) Perspectives on mucus properties and formation-lessons from the biochemical world. Cold Spring Harb. Perspect. Med. 2, a014159. https://doi.org/10.1101/cshperspect.a014159
  3. Ambrus, J. L., Sr., Chadha, K. C., Islam, A., Akhter, S. and Ambrus, J. L., Jr. (2006) Treatment of viral and neoplastic diseases with double-stranded RNA derivatives and other new agents. Exp. Biol. Med. (Maywood) 231, 1283-1286. https://doi.org/10.1177/153537020623100801
  4. Alexopulou, A., Holt, A. C., Medzhitov, R. and Flavell, R. A. (2001) Recognition of double-stranded RNA and activation of NF-kB by Toll-like receptor 3. Nature 413, 732-738. https://doi.org/10.1038/35099560
  5. Bai, S., Yang, T., Abbruscato, T. J. and Ahsan, F. (2008) Evaluation of human nasal RPMI 2650 cells grown at an air-liquid interface as a model for nasal drug transport studies. J. Pharm. Sci. 97, 1165-1178. https://doi.org/10.1002/jps.21031
  6. Balda, M. S. and Matter, K. (2009) Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta 1788, 761-777. https://doi.org/10.1016/j.bbamem.2008.11.024
  7. Ball, S. L., Suwara, M. I., Borthwick, L. A., Wilson, J. A., Mann, D. A. and Fisher, A.J. (2015) How reliable are sino-nasal cell lines for studying the pathophysiology of chronic rhinosinusitis? Ann. Otol. Rhinol. Laryngol. 124, 437-442. https://doi.org/10.1177/0003489414565003
  8. Bansil, R. and Turner, B. S. (2006) Mucin structure, aggregation, physiological functions and biomedical applications. Curr. Opin. Colloid Interface Sci. 11, 164-170. https://doi.org/10.1016/j.cocis.2005.11.001
  9. Burgel, P. R., Lazarus, S. C., Tam, D. C., Ueki, I. F., Atabai, K., Birch, M. and Nadel, J. A. (2001) Human eosinophils induce mucin production in airway epithelial cells via epidermal growth factor receptor activation. J. Immunol. 15, 5948-5954.
  10. Dahiya, P. and Kamal, R. (2013) Hyaluronic acid: a boon in periodontal therapy. N. Am. J. Med. Sci. 5, 309-315. https://doi.org/10.4103/1947-2714.112473
  11. Ducheyne, P., Healy, K., Hutmacher, D. W., Grainger, D. W. and Kirkpatrick, C. J. (2011) Comprehensive Biomaterials. Elsevier.
  12. England, R. J., Homer. J. J., Knight, L. C. and Ell, S. R. (1999) Nasal pH measurement: a reliable and repeatable parameter. Clin. Otolaryngol. Allied Sci. 24, 67-68. https://doi.org/10.1046/j.1365-2273.1999.00223.x
  13. Fahy, J. V. and Dickey, B. F. (2010) Airway mucus function and dysfunction. N. Engl. J. Med. 2, 2233-2247. https://doi.org/10.1056/NEJMra0910061
  14. Fischer, H. and Widdicombe, J. H. (2006) Mechanisms of acid and base secretion by the airway epithelium. J. Membr. Biol. 211, 139-150. https://doi.org/10.1007/s00232-006-0861-0
  15. Ganesan, S., Comstock, A. T. and Sajjan, U. S. (2013) Barrier function of airway tract epithelium. Tissue Barriers 1, e24997. https://doi.org/10.4161/tisb.24997
  16. Gelardi, M., Guglielmi, A. V., De Candia, N., Maffezzoni, E., Berardi, P. and Quaranta, N. (2013) Effect of sodium hyaluronate on mucociliary clearance after functional endoscopic sinus surgery. Eur. Ann. Allergy Clin. Immunol. 45, 103-108.
  17. Heijink, I. H., Jonker, M. R., de Vries, M., van Oosterhout, A. J., Telenga, E., Ten Hacken, N. H., Postma, D. S. and van den Berge, M. (2016) Budesonide and fluticasone propionate differentially affect the airway epithelial barrier. Respir. Res. 17, 2. https://doi.org/10.1186/s12931-015-0318-z
  18. Holgate, S. T. (2000) Epithelial damage and response. Clin. Exp. Allergy 30 Suppl 1, 37-41. https://doi.org/10.1046/j.1365-2222.2000.00095.x
  19. Hovenberg, H. W., Davies, J. R. and Carlstedt, I.(1996) Different mucins are produced by the surface epithelium and the submucosa in human trachea: identification of MUC5AC as a major mucin from the goblet cells. Biochem. J. 15, 319-324. https://doi.org/10.1042/bj0150319
  20. Ieki, K., Matsukura, S., Kokubu, F., Kimura, T., Kuga, H., Kawaguchi, M., Odaka, M., Suzuki, S., Watanabe, S., Takeuchi, H., Schleimer, R. P. and Adachi, M. (2004) Double-stranded RNA activates RANTES gene transcription through co-operation of nuclear factor-kB and interferon regulatory factors in human airway epithelial cells. Clin. Exp. Allergy 34, 745-752. https://doi.org/10.1111/j.1365-2222.2004.1941.x
  21. Karp, P. H., Moninger, T. O., Weber, S. P., Nesselhauf, T. S., Launspach, J. L., Zabner, J. and Welsh, M. J. (2002) An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol. Biol. 188, 115-137.
  22. Kreft, M. E., Jerman, U. D., Lasic, E., Lanisnik Rizner, T., Hevir-Kene, N., Peternel, L. and Kristan, K. (2015) The characterization of the human nasal epithelial cell line RPMI 2650 under different culture conditions and their optimization for an appropriate in vitro nasal model. Pharm. Res. 32, 665-679. https://doi.org/10.1007/s11095-014-1494-0
  23. Kurti, L., Veszelka, S., Bocsik, A., Ozsvari, B., Puskas, L. G., Kittel, A., Szabo-Revesz, P. and Deli, M. A. (2013) Retinoic acid and hydrocortisone strengthen the barrier function of human RPMI 2650 cells, a model for nasal epithelial permeability. Cytotechnology 65, 395-406. https://doi.org/10.1007/s10616-012-9493-7
  24. Lafforgue, O., Seyssiecq, I., Poncet, S. and Favier, J. (2018) Rheological properties of synthetic mucus for airway clearance. J. Biomed. Mater. Res. A 106, 386-396.
  25. Lai, S. K., Wang, Y. Y., Wirtz, D. and Hanes, J. (2009) Micro- and macrorheology of mucus. Adv. Drug Deliv. Rev. 61, 86-100. https://doi.org/10.1016/j.addr.2008.09.012
  26. Laurent, T. C., Fraser, J. R., Laurent, U. B. and Engstrom-Laurent, A. (1995) Hyaluronan in inflammatory joint disease. Acta Orthop. Scand. Suppl. 266, 116-120.
  27. Lee, M. K., Yoo, J. W., Lin, H., Kim, Y. S., Kim, D. D., Choi, Y. M., Park, S. K., Lee, C. H. and Roh H. J. (2005) Air-liquid interface culture of serially passaged human nasal epithelial cell monolayer for in vitro drug transport studies. Drug Deliv. 12, 305-311. https://doi.org/10.1080/10717540500177009
  28. Liu, Y. Y., Lee, C. H., Dedaj, R., Zhao, H., Mrabat, H., Sheidlin, A., Syrkina, O., Huang, P. M., Garg, H. G., Hales, C. A. and Quinn, D. A. (2008) High-molecular-weight hyaluronan--a possible new treatment for sepsis-induced lung injury: a preclinical study in mechanically ventilated rats. Crit. Care 12, R102. https://doi.org/10.1186/cc6982
  29. Lennon, F. E. and Singleton, P. A. (2011) Role of hyaluronan and hyaluronan-binding proteins in lung pathobiology. Am. J. Physiol. Lung Cell Mol. Physiol. 301, L137-L147. https://doi.org/10.1152/ajplung.00071.2010
  30. Marsh, D. G., Berlin, L., Bruce, C. A., Lichtenstein, L. M. and Hussain, R. (1981) Rapidly released allergens from short ragweed pollen. I. Kinetics of release of known allergens in relation to biologic activity. J. Allergy Clin. Immunol. 67, 206-216. https://doi.org/10.1016/0091-6749(81)90063-4
  31. Noble, P. W. (2002) Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol. 21, 25-29. https://doi.org/10.1016/S0945-053X(01)00184-6
  32. Pawankar, R., Bunnag, C., Khaltaev, N. and Bousquet, J. (2012) Allergic rhinitis and its impact on asthma in Asia Pacific and the ARIA update 2008. World Allergy Organ. J. 5, S212- S217. https://doi.org/10.1097/1939-4551-5-s3-s212
  33. Petrey, A. C. and de la Motte, C. A. (2014) Hyaluronan, a crucial regulator of inflammation. Front. Immunol. 5, 101. https://doi.org/10.3389/fimmu.2014.00101
  34. Pozzoli, M., Ong, H. X., Morgan., L., Sukkar, M., Traini, D., Young, P. M. and Sonvico, F. (2016) Application of RPMI 2650 nasal cell model to a 3D printed apparatus for the testing of drug deposition and permeation of nasal products. Eur. J. Pharm. Biopharm. 107, 223-233. https://doi.org/10.1016/j.ejpb.2016.07.010
  35. Rayner, R. E., Makena, P., Prasad, G. L. and Cormet-Boyaka, E. (2019) Optimization of normal human bronchial epithelial (NHBE) cell 3D cultures for in vitro lung model studies. Sci Rep. 9, 500. https://doi.org/10.1038/s41598-018-36735-z
  36. Reichl, S. and Becker, K. (2012) Cultivation of RPMI 2650 cells as an in-vitro model for human transmucosal nasal drug absorption studies: optimization of selected culture conditions. J. Pharm. Pharmacol. 64, 1621-1630. https://doi.org/10.1111/j.2042-7158.2012.01540.x
  37. Rogers, D. F. (2007) Mucoactive agents for airway mucus hypersecretory diseases. Respir. Care 52, 1176-1193; discussion 1193-1197.
  38. Salib, R. J., Lau, L. C. and Howarth, P. H. (2005) The novel use of the human nasal epithelial cell line RPMI 2650 as an in vitro model to study the influence of allergens and cytokines on transforming growth factor-beta gene expression and protein release. Clin. Exp. Allergy 35, 811-819. https://doi.org/10.1111/j.1365-2222.2005.02258.x
  39. Seagrave, J., Albrecht, H. H., Hill, D. B., Rogers, D. F. and Solomon, G. (2012) Effects of guaifenesin, N-acetylcysteine, and ambroxol on MUC5AC and mucociliary transport in primary differentiated human tracheal-bronchial cells. Respir. Res. 13, 98. https://doi.org/10.1186/1465-9921-13-98
  40. Srinivasan, B., Kolli, A. R., Esch, M. B., Abaci, H. E., Shuler, M. L. and Hickman, J. J. (2015) TEER measurement techniques for in vitro barrier model systems. J. Lab. Autom. 20, 107-126. https://doi.org/10.1177/2211068214561025
  41. Stowell, N. C. (2009) Long-term activation of TLR3 by poly (I:C) induces inflammation and impairs lung function in mice. Respir. Res. 10, 43. https://doi.org/10.1186/1465-9921-10-43
  42. Tang, X. X., Ostedgaard, L. S., Hoegger, M. J., Moninger, T. O., Karp, P. H., McMenimen, J. D., Choudhury, B., Varki, A., Stoltz, D. A. and Welsh, M. J. (2016) Acidic pH increases airway surface liquid viscosity in cystic fibrosis. J. Clin. Invest. 126, 879-891. https://doi.org/10.1172/JCI83922
  43. Tantilipikorn, P. (2014) The relationship between allergic rhinitis and viral infections. Curr. Opin. Otolaryngol. Head Neck Surg. 22, 249-252. https://doi.org/10.1097/MOO.0000000000000049
  44. Thornton, D. J., Rousseau, K. and McGuckin, M. A. (2008) Structure and function of the polymeric mucins in airways mucus. Annu. Rev. Physiol. 70, 459-486. https://doi.org/10.1146/annurev.physiol.70.113006.100702
  45. Vareille, M., Kieninger, E., Edwards, M. R. and Regamey, N. (2011) The airway epithelium: soldier in the fight against respiratory viruses. Clin. Microbiol. Rev. 24, 210-229. https://doi.org/10.1128/CMR.00014-10
  46. Vercammen, E., Staal, J. and Beyaert, R. (2008) Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin. Microbiol. Rev. 21, 13-25. https://doi.org/10.1128/CMR.00022-07
  47. Wengst, A. and Reichl, S. (2010) RPMI 2650 epithelial model and three-dimensional reconstructed human nasal mucosa as in vitro models for nasal permeation studies. Eur. J. Pharm.Biopharm. 74, 290-297. https://doi.org/10.1016/j.ejpb.2009.08.008
  48. Wickstrom, C., Davies, J. R., Eriksen, G. V., Veerman, E. C. and Carlstedt, I. (1998) MUC5B is a major gel-forming, oligomeric mucin from human salivary gland, respiratory tract and endocervix: identification of glycoforms and C-terminal cleavage. Biochem. J. 334, 685-693. https://doi.org/10.1042/bj3340685
  49. Wu, J., Wang, Y., Liu, G., Jia, Y., Yang, J., Shi, J., Dong, J., Wei, J. and Liu, X. (2017) Characterization of air-liquid interface culture of A549 alveolar epithelial cells. Braz. J. Med. Biol. Res. 51, e6950. https://doi.org/10.1590/1414-431x20176950
  50. Xiao, C., Puddicombe, S. M., Field, S., Haywood, J., Broughton-Head, V., Puxeddu, I.,Haitchi, H. M., Vernon-Wilson, E., Sammut, D., Bedke, N., Cremin, C., Sones, J., Djukanovic, R., Howarth, P. H., Collins, J. E., Holgate, S. T., Monk, P. and Davies, D. E. (2011) Defective epithelialbarrier function in asthma. J. Allergy Clin. Immunol. 128, 549-556. https://doi.org/10.1016/j.jaci.2011.05.038
  51. Zhao, R., Guo, Z., Zhang, R., Deng, C., Xu, J., Dong, W., Hong, Z., Yu, H., Situ, H., Liu, C. and Zhuang, G. (2018) Nasal epithelial barrier disruption by particulate matter $\leq$2.5 ${\mu}m$ viatight junction protein degradation. J. Appl.Toxicol. 38, 678-687. https://doi.org/10.1002/jat.3573