Today: Dec 27, 2024
RU / EN
Last update: Dec 27, 2024
Home page → All issues → Volume 10, Issue 4 (2018) → Article details
Metabolism of the Extracellular Matrix in Bronchial Asthma (Review)

Metabolism of the Extracellular Matrix in Bronchial Asthma (Review)

Eliseeva Т.I., Tush Е.V., Krasilnikova S.V., Kuznetsova S.V., Larin R.A., Kubysheva N.I., Khaletskaya О.V., Potemina T.E., Ryazantsev S.V., Ignatov S.K.
Key words: bronchial asthma; allergic rhinitis; chronic rhinosinusitis; extracellular matrix; remodeling.
2018, volume 10, issue 4, page 220.
DOI: https://doi.org/10.17691/stm2018.10.4.25

Full text

html pdf
4097
2481

Bronchial asthma is associated with upper airway (UA) disorders, primarily with allergic rhinitis, which, in turn, occurs in combination with other UA conditions, including hyperplasia of the nasal mucosa. Chronic rhinosinusitis, if confirmed, is a predictor of asthma severity.

The pathogenesis of these diseases includes the remodeling (restructuring) of the extracellular matrix and the adjacent UA structures, which is associated with further worsening of the diseases and their resistance to therapy. It is known that remodeling of the lower respiratory tract in bronchial asthma is characterized by epithelial desquamation, hyperplasia of goblet cells, thickening of the basement membrane, fibrosis of the subepithelium, hyperplasia of smooth muscles of the respiratory tract, and increased angiogenesis. At the same time, the UA remodeling in patients with asthma is still poorly understood; the data are still limited and often contradict each other. With isolated allergic rhinitis, the remodeling process is not very much pronounced and is limited, apparently, to a basement membrane thickening. In chronic rhinosinusitis, the UA remodeling manifests by epithelial hyperplasia and an increased sedimentation and degradation of the matrix along with the accumulation of plasma proteins.

Despite recent extensive studies, the cellular and molecular mechanisms involved in the respiratory tract remodeling remain largely undetermined, which necessitates further research into these processes. The review addresses several aspects of neuro-humoral control of the extracellular matrix metabolism and the associated remodeling of the upper and lower airway in patients with asthma.

  1. Theocharis A.D., Skandalis S.S., Gialeli C., Karamanos N.K. Extracellular matrix structure. Adv Drug Deliv Rev 2016; 97: 4–27, https://doi.org/10.1016/j.addr.2015.11.001.
  2. LeMessurier K.S., Palipane M., Tiwary M., Gavin B., Samarasinghe A.E. Chronic features of allergic asthma are enhanced in the absence of resistin-like molecule-beta. Sci Rep 2018; 8(1): 7061, https://doi.org/10.1038/s41598-018-25321-y.
  3. Gu B.H., Madison M.C., Corry D., Kheradmand F. Matrix remodeling in chronic lung diseases. Matrix Biol 2018, 73: 52–63, https://doi.org/10.1016/j.matbio.2018.03.012.
  4. Annoni R., Lancas T., Yukimatsu Tanigawa R., de Medeiros Matsushita M., de Morais Fernezlian S., Bruno A., Fernando Ferraz da Silva L., Roughley P.J., Battaglia S., Dolhnikoff M., Hiemstra P.S., Sterk P.J., Rabe K.F., Mauad T. Extracellular matrix composition in COPD. Eur Respir J 2012; 40(6): 1362–1373, https://doi.org/10.1183/09031936.00192611.
  5. Samitas K., Carter A., Kariyawasam H.H., Xanthou G. Upper and lower airway remodelling mechanisms in asthma, allergic rhinitis and chronic rhinosinusitis: the one airway concept revisited. Allergy 2018; 73(5): 993–1002, https://doi.org/10.1111/all.13373.
  6. Weitoft M., Andersson C., Andersson-Sjoland A., Tufvesson E., Bjermer L., Erjefalt J., Westergren-Thorsson G. Controlled and uncontrolled asthma display distinct alveolar tissue matrix compositions. Respir Res 2014; 15: 67, https://doi.org/10.1186/1465-9921-15-67.
  7. Wight T.N., Frevert C.W., Debley J.S., Reeves S.R., Parks W.C., Ziegler S.F. Interplay of extracellular matrix and leukocytes in lung inflammation. Cell Immunol 2017; 312: 1–14, https://doi.org/10.1016/j.cellimm.2016.12.003.
  8. Grzela K., Zagorska W., Krejner A., Litwiniuk M., Zawadzka-Krajewska A., Banaszkiewicz A., Kulus M., Grzela T. Prolonged treatment with inhaled corticosteroids does not normalize high activity of matrix metalloproteinase-9 in exhaled breath condensates of children with asthma. Arch Immunol Ther Exp (Warsz) 2015; 63(3): 231–237, https://doi.org/10.1007/s00005-015-0328-z.
  9. Mouw J.K., Ou G., Weaver V.M. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 2014; 15(12): 771–785, https://doi.org/10.1038/nrm3902.
  10. Pozzi A., Yurchenco P.D., Iozzo R.V. The nature and biology of basement membranes. Matrix Biol 2017; 57–58: 1–11, https://doi.org/10.1016/j.matbio.2016.12.009.
  11. Hohenester E., Yurchenco P.D. Laminins in basement membrane assembly. Cell Adh Migr 2013; 7(1): 56–63, https://doi.org/10.4161/cam.21831.
  12. Timpl R., Brown J.C. Supramolecular assembly of basement membranes. Bioessays 1996; 18(2): 123–132, https://doi.org/10.1002/bies.950180208.
  13. Dziadek M. Role of laminin-nidogen complexes in basement membrane formation during embryonic development. Experientia 1995; 51(9–10): 901–913, https://doi.org/10.1007/bf01921740.
  14. Sonbol H.S. Extracellular matrix remodeling in human disease. J Microsc Ultrastruct 2018; 6(3): 123–128, https://doi.org/10.4103/jmau.jmau_4_18.
  15. LeBleu V.S., Macdonald B., Kalluri R. Structure and function of basement membranes. Exp Biol Med (Maywood) 2007; 232(9): 1121–1129, https://doi.org/10.3181/0703-mr-72.
  16. Halfter W., Oertle P., Monnier C.A., Camenzind L., Reyes-Lua M., Hu H., Candiello J., Labilloy A., Balasubramani M., Henrich P.B., Plodinec M. New concepts in basement membrane biology. FEBS J 2015; 282(23): 4466–4479, https://doi.org/10.1111/febs.13495.
  17. Behrens D.T., Villone D., Koch M., Brunner G., Sorokin L., Robenek H., Bruckner-Tuderman L., Bruckner P., Hansen U. The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 2012; 287(22): 18700–18709, https://doi.org/10.1074/jbc.M111.336073.
  18. Fernandes D.J., Bonacci J.V., Stewart A.G. Extracellular matrix, integrins, and mesenchymal cell function in the airways. Curr Drug Targets 2006; 7(5): 567–577.
  19. Hansen S.W., Ohtani K., Roy N., Wakamiya N. The collectins CL-L1, CL-K1 and CL-P1, and their roles in complement and innate immunity. Immunobiology 2016; 221(10): 1058–1067, https://doi.org/10.1016/j.imbio.2016.05.012.
  20. Kubysheva N., Soodaeva S., Novikov V., Eliseeva T., Li T., Klimanov I., Kuzmina E., Baez-Medina H., Solovyev V., Ovsyannikov D.Y., Batyrshin I. Soluble HLA-I and HLA-II molecules are potential prognostic markers of progression of systemic and local inflammation in patients with COPD. Disease Markers 2018; 2018: 1–7, https:/doi.org/10.1155/2018/3614341.
  21. Barnes P.J. Cellular and molecular mechanisms of asthma and COPD. Clin Sci (Lond) 2017; 131(13): 1541–1558, https://doi.org/10.1042/CS20160487.
  22. Burgess J.K., Ceresa C., Johnson S.R., Kanabar V., Moir L.M., Nguyen T.T., Oliver B.G., Schuliga M., Ward J. Tissue and matrix influences on airway smooth muscle function. Pulm Pharmacol Ther 2009; 22(5): 379–387, https://doi.org/10.1016/j.pupt.2008.12.007.
  23. Sapir L., Tzlil S. Talking over the extracellular matrix: how do cells communicate mechanically? Semin Cell Dev Biol 2017; 71: 99–105, https://doi.org/10.1016/j.semcdb.2017.06.010.
  24. Wells J.M., Gaggar A., Blalock J.E. MMP generated matrikines. Matrix Biol 2015; 44–46: 122–129, https://doi.org/10.1016/j.matbio.2015.01.016.
  25. Ricard-Blum S., Salza R. Matricryptins and matrikines: biologically active fragments of the extracellular matrix. Exp Dermatol 2014; 23(7): 457–463, https://doi.org/10.1111/exd.12435.
  26. Jarvelainen H., Sainio A., Koulu M., Wight T.N., Penttinen R. Extracellular matrix molecules: potential targets in pharmacotherapy. Pharmacol Rev 2009; 61(2): 198–223, https://doi.org/10.1124/pr.109.001289.
  27. Burgess J.K., Mauad T., Tjin G., Karlsson J.C., Westergren-Thorsson G. The extracellular matrix — the under-recognized element in lung disease? J Pathol 2016; 240(4): 397–409, https://doi.org/10.1002/path.4808.
  28. Liu G., Cooley M.A., Nair P.M., Donovan C., Hsu A.C., Jarnicki A.G., Haw T.J., Hansbro N.G., Ge Q., Brown A.C., Tay H., Foster P.S., Wark P.A., Horvat J.C., Bourke J.E., Grainge C.L., Argraves W.S., Oliver B.G., Knight D.A., Burgess J.K., Hansbro P.M. Airway remodelling and inflammation in asthma are dependent on the extracellular matrix protein fibulin-1c. J Pathol 2017; 243(4): 510–523, https://doi.org/10.1002/path.4979.
  29. White E.S. Lung extracellular matrix and fibroblast function. Ann Am Thorac Soc 2015; 12(Suppl 1): S30–S33, https://doi.org/10.1513/annalsats.201406-240mg.
  30. Pawankar R., Nonaka M. Inflammatory mechanisms and remodeling in chronic rhinosinusitis and nasal polyps. Curr Allergy Asthma Rep 2007; 7(3): 202–208.
  31. Watelet J.B., Dogne J.M., Mullier F. Remodeling and repair in rhinosinusitis. Curr Allergy Asthma Rep 2015; 15(6): 34, https://doi.org/10.1007/s11882-015-0531-3.
  32. Boulet L.P. Airway remodeling in asthma: update on mechanisms and therapeutic approaches. Curr Opin Pulm Med 2018; 24(1): 56–62, https://doi.org/10.1097/MCP.0000000000000441.
  33. Bonnans C., Chou J., Werb Z. Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 2014; 15(12): 786–801, https://doi.org/10.1038/nrm3904.
  34. Cox T.R., Erler J.T. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 2011; 4(2): 165–178, https://doi.org/10.1242/dmm.004077.
  35. Smith H.W., Marshall C.J. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 2010; 11(1): 23–36, https://doi.org/10.1038/nrm2821.
  36. Giuffrida P., Biancheri P., MacDonald T.T. Proteases and small intestinal barrier function in health and disease. Curr Opin Gastroenterol 2014; 30(2): 147–153, https://doi.org/10.1097/MOG.0000000000000042.
  37. Rawlings N.D., Waller M., Barrett A.J., Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2014; 42(D1): D503–D509, https://doi.org/10.1093/nar/gkt953.
  38. Murphy G. Riding the metalloproteinase roller coaster. J Biol Chem 2017; 292(19): 7708–7718, https://doi.org/10.1074/jbc.x117.785295.
  39. Jones G.C., Riley G.P. ADAMTS proteinases: a multi-domain, multi-functional family with roles in extracellular matrix turnover and arthritis. Arthritis Res Ther 2005; 7(4): 160–169, https://doi.org/10.1186/ar1783.
  40. Krouse J.H. Asthma management for the otolaryngologist. Otolaryngol Clin North Am 2017; 50(6): 1065–1076, https://doi.org/10.1016/j.otc.2017.08.006.
  41. Broder C., Arnold P., Vadon-Le Goff S., Konerding M.A., Bahr K., Muller S., Overall C.M., Bond J.S., Koudelka T., Tholey A., Hulmes D.J., Moali C., Becker-Pauly C. Metalloproteases meprin alpha and meprin beta are C- and N-procollagen proteinases important for collagen assembly and tensile strength. Proc Natl Acad Sci USA 2013; 110(35): 14219–14224, https://doi.org/10.1073/pnas.1305464110.
  42. Prakash Y.S. Airway smooth muscle in airway reactivity and remodeling: what have we learned? Am J Physiol Lung Cell Mol Physiol 2013; 305(12): L912–L933, https://doi.org/10.1152/ajplung.00259.2013.
  43. Al-Muhsen S., Johnson J.R., Hamid Q. Remodeling in asthma. J Allergy Clin Immunol 2011; 128(3): 451–462, https://doi.org/10.1016/j.jaci.2011.04.047.
  44. Tschumperlin D.J. Physical forces and airway remodeling in asthma. N Engl J Med 2011; 364(21): 2058–2059, https://doi.org/10.1056/NEJMe1103121.
  45. Fehrenbach H., Wagner C., Wegmann M. Airway remodeling in asthma: what really matters. Cell Tissue Res 2017; 367(3): 551–569, https://doi.org/10.1007/s00441-016-2566-8.
  46. Payne D.N., Rogers A.V., Adelroth E., Bandi V., Guntupalli K.K., Bush A., Jeffery P.K. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med 2003; 167(1): 78–82, https://doi.org/10.1164/rccm.200205-414oc.
  47. Pohunek P., Warner J.O., Turzikova J., Kudrmann J., Roche W.R. Markers of eosinophilic inflammation and tissue re-modelling in children before clinically diagnosed bronchial asthma. Pediatr Allergy Immunol 2005; 16(1): 43–51, https://doi.org/10.1111/j.1399-3038.2005.00239.x.
  48. Elliot J.G., Noble P.B., Mauad T., Bai T.R., Abramson M.J., McKay K.O., Green F.H.Y., James A.L. Inflammation-dependent and independent airway remodelling in asthma. Respirology 2018; 23(12): 1138–1145, https://doi.org/10.1111/resp.13360.
  49. Kicic A., Sutanto E.N., Stevens P.T., Knight D.A., Stick S.M. Intrinsic biochemical and functional differences in bronchial epithelial cells of children with asthma. Am J Respir Crit Care Med 2006; 174(10): 1110–1118, https://doi.org/10.1164/rccm.200603-392oc.
  50. James A.L., Bai T.R., Mauad T., Abramson M.J., Dolhnikoff M., McKay K.O., Maxwell P.S., Elliot J.G., Green F.H. Airway smooth muscle thickness in asthma is related to severity but not duration of asthma. Eur Respir J 2009; 34(5): 1040–1045, https://doi.org/10.1183/09031936.00181608.
  51. Prakash Y.S., Halayko A.J., Gosens R., Panettieri R.A. Jr., Camoretti-Mercado B., Penn R.B. An official American Thoracic Society research statement: current challenges facing research and therapeutic advances in airway remodeling. Am J Respir Crit Care Med 2017; 195(2): e4–e19, https://doi.org/10.1164/rccm.201611-2248st.
  52. Huber H.L., Koessler K.K. The pathology of bronchial asthma. Arch Intern Med 1922; 30(6): 689–760, https://doi.org/10.1001/archinte.1922.00110120002001.
  53. Pascoe C.D., Seow C.Y., Hackett T.L., Pare P.D., Donovan G.M. Heterogeneity of airway wall dimensions in humans: a critical determinant of lung function in asthmatics and nonasthmatics. Am J Physiol Lung Cell Mol Physiol 2017; 312(3): L425–L431, https://doi.org/10.1152/ajplung.00421.2016.
  54. Poon A.H., Hamid Q. Severe asthma: have we made progress? Ann Am Thorac Soc 2016; 13(Suppl 1): S68–S77.
  55. Huang J., Olivenstein R., Taha R., Hamid Q., Ludwig M. Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am J Respir Crit Care Med 1999; 160(2): 725–729, https://doi.org/10.1164/ajrccm.160.2.9809040.
  56. Ward C., Reid D.W., Orsida B.E., Feltis B., Ryan V.A., Johns D.P., Walters E.H. Inter-relationships between airway inflammation, reticular basement membrane thickening and bronchial hyper-reactivity to methacholine in asthma; a systematic bronchoalveolar lavage and airway biopsy analysis. Clin Exp Allergy 2005; 35(12): 1565–1571, https://doi.org/10.1111/j.1365-2222.2005.02365.x.
  57. Davies D.E. The role of the epithelium in airway remodeling in asthma. Proc Am Thorac Soc 2009; 6(8): 678–682, https://doi.org/10.1513/pats.200907-067dp.
  58. Holgate S.T., Wenzel S., Postma D.S., Weiss S.T., Renz H., Sly P.D. Asthma. Nat Rev Dis Primers 2015; 1: 15025, https://doi.org/10.1038/nrdp.2015.25.
  59. Holgate S.T. Mechanisms of asthma and implications for its prevention and treatment: a personal journey. Allergy Asthma Immunol Res 2013; 5(6): 343–347, https://doi.org/10.4168/aair.2013.5.6.343.
  60. Nayak A.P., Deshpande D.A., Penn R.B. New targets for resolution of airway remodeling in obstructive lung diseases. F1000Res 2018; 7: 680, https://doi.org/10.12688/f1000research.14581.1.
  61. Chan V., Burgess J.K., Ratoff J.C., O’Connor B.J., Greenough A., Lee T.H., Hirst S.J. Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006; 174(4): 379–385, https://doi.org/10.1164/rccm.200509-1420oc.
  62. Lauzon A.M., Martin J.G. Airway hyperresponsiveness; smooth muscle as the principal actor. F1000Res 2016; 5: 306, https://doi.org/10.12688/f1000research.7422.1.
  63. Grainge C.L., Lau L.C., Ward J.A., Dulay V., Lahiff G., Wilson S., Holgate S., Davies D.E., Howarth P.H. Effect of bronchoconstriction on airway remodeling in asthma. N Engl J Med 2011; 364(21): 2006–2015, https://doi.org/10.1056/nejmoa1014350.
  64. Gosens R., Grainge C. Bronchoconstriction and airway biology: potential impact and therapeutic opportunities. Chest 2015; 147(3): 798–803, https://doi.org/10.1378/chest.14-1142.
  65. Dogan M., Han Y.S., Delmotte P., Sieck G.C. TNFalpha enhances force generation in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2017; 312(6): L994–L1002, https://doi.org/10.1152/ajplung.00550.2016.
  66. Burgess J.K., Ge Q., Boustany S., Black J.L., Johnson P.R. Increased sensitivity of asthmatic airway smooth muscle cells to prostaglandin E2 might be mediated by increased numbers of E-prostanoid receptors. J Allergy Clin Immunol 2004; 113(5): 876–881, https://doi.org/10.1016/j.jaci.2004.02.029.
  67. Brightling C.E., Bradding P. The re-emergence of the mast cell as a pivotal cell in asthma pathogenesis. Curr Allergy Asthma Rep 2005; 5(2): 130–135, https://doi.org/10.1007/s11882-005-0086-9.
  68. Niimi A., Matsumoto H., Amitani R., Nakano Y., Sakai H., Takemura M., Ueda T., Chin K., Itoh H., Ingenito E.P., Mishima M. Effect of short-term treatment with inhaled corticosteroid on airway wall thickening in asthma. Am J Med 2004; 116(11): 725–731, https://doi.org/10.1016/j.amjmed.2003.11.026.
  69. Walker J.K.L., Theriot B.S., Ghio M., Trempus C.S., Wong J.E., McQuade V.L., Liang J., Jiang D., Noble P.W., Garantziotis S., Kraft M., Ingram J.L. Targeted HAS2 expression lessens airway responsiveness in chronic murine allergic airway disease. Am J Respir Cell Mol Biol 2017; 57(6): 702–710, https://doi.org/10.1165/rcmb.2017-0095oc.
  70. Kruse M.N., Becker C., Lottaz D., Köhler D., Yiallouros I., Krell H.W., Sterchi E.E., Stöcker W. Human meprin alpha and beta homo-oligomers: cleavage of basement membrane proteins and sensitivity to metalloprotease inhibitors. Biochem J 2004; 378(Pt 2): 383–389, https://doi.org/10.1042/bj20031163.
  71. Bougault V., Loubaki L., Joubert P., Turmel J., Couture C., Laviolette M., Chakir J., Boulet L.P. Airway remodeling and inflammation in competitive swimmers training in indoor chlorinated swimming pools. J Allergy Clin Immunol 2012; 129(2): 351–358.e1, https://doi.org/10.1016/j.jaci.2011.11.010.
  72. ten Brinke A. Risk factors associated with irreversible airflow limitation in asthma. Curr Opin Allergy Clin Immunol 2008; 8(1): 63–69, https://doi.org/10.1097/aci.0b013e3282f3b5b5.
  73. Lange P., Parner J., Vestbo J., Schnohr P., Jensen G. A 15-year follow-up study of ventilatory function in adults with asthma. N Engl J Med 1998; 339(17): 1194–1200, https://doi.org/10.1056/nejm199810223391703.
  74. Niimi A., Matsumoto H., Takemura M., Ueda T., Chin K., Mishima M. Relationship of airway wall thickness to airway sensitivity and airway reactivity in asthma. Am J Respir Crit Care Med 2003; 168(8): 983–988, https://doi.org/10.1164/rccm.200211-1268oc.
  75. McParland B.E., Macklem P.T., Pare P.D. Airway wall remodeling: friend or foe? J Appl Physiol 2003; 95(1): 426–434, https://doi.org/10.1152/japplphysiol.00159.2003.
  76. Lezmi G., Gosset P., Deschildre A., Abou-Taam R., Mahut B., Beydon N., de Blic J. Airway Remodeling in preschool children with severe recurrent wheeze. Am J Respir Crit Care Med 2015; 192(2): 164–171, https://doi.org/10.1164/rccm.201411-1958oc.
  77. Chakir J., Laviolette M., Boutet M., Laliberté R., Dubé J., Boulet L.P. Lower airways remodeling in nonasthmatic subjects with allergic rhinitis. Lab Invest 1996; 75(5): 735–744.
  78. Tillie-Leblond I., de Blic J., Jaubert F., Wallaert B., Scheinmann P., Gosset P. Airway remodeling is correlated with obstruction in children with severe asthma. Allergy 2008; 63(5): 533–541, https://doi.org/10.1111/j.1398-9995.2008.01656.x.
  79. O’Reilly R., Ullmann N., Irving S., Bossley C.J., Sonnappa S., Zhu J., Oates T., Banya W., Jeffery P.K., Bush A., Saglani S. Increased airway smooth muscle in preschool wheezers who have asthma at school age. J Allergy Clin Immunol 2013; 131(4): 1024–1032.e16, https://doi.org/10.1016/j.jaci.2012.08.044.
  80. Owens L., Laing I.A., Zhang G., Le Souef P.N. Infant lung function predicts asthma persistence and remission in young adults. Respirology 2017; 22(2): 289–294, https://doi.org/10.1111/resp.12901.
  81. Williams R.C., Skelton A.J., Todryk S.M., Rowan A.D., Preshaw P.M., Taylor J.J. Leptin and pro-inflammatory stimuli synergistically upregulate MMP-1 and MMP-3 secretion in human gingival fibroblasts. PLoS One 2016; 11(2): e0148024, https://doi.org/10.1371/journal.pone.0148024.
  82. Sicard D., Haak A.J., Choi K.M., Craig A.R., Fredenburgh L.E., Tschumperlin D.J. Aging and anatomical variations in lung tissue stiffness. Am J Physiol Lung Cell Mol Physiol 2018; 314(6): L946–L955, https://doi.org/10.1152/ajplung.00415.2017.
  83. Russell R.E., Culpitt S.V., DeMatos C., Donnelly L., Smith M., Wiggins J., Barnes P.J. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2002; 26(5): 602–609, https://doi.org/10.1165/ajrcmb.26.5.4685.
  84. Todorova L., Gurcan E., Miller-Larsson A., Westergren-Thorsson G. Lung fibroblast proteoglycan production induced by serum is inhibited by budesonide and formoterol. Am J Respir Cell Mol Biol 2006; 34(1): 92–100, https://doi.org/10.1165/rcmb.2005-0048oc.
  85. Eliseeva T.I., Geppe N.A., Tush E.V., Khaletskaya O.V., Balabolkin I.I., Bulgakova V.A., Kubysheva N.I., Ignatov S.K. Body height of children with bronchial asthma of various severities. Can Respir J 2017; 2017: 8761404, https://doi.org/10.1155/2017/8761404.
  86. Eliseeva Т.I., Geppe N.A., Ignatov S.K., Soodaeva S.K., Tush Е.V., Khaletskaya O.V., Potemina T.E., Malakhov A.B., Kubysheva N.I., Solovyov V.A. Relative body mass index as a new tool for nutritional status assessment in children and adolescents with bronchial asthma. Sovremennye tehnologii v medicine 2017; 9(1): 135–148, https://doi.org/10.17691/stm2017.9.1.18.
  87. Tushch E.V., Eliseeva T.I., Balabolkin I.I., Bulgakova V.A., Khaletskaya O.V., Shchukina D.A., Romanova N.V., Malyshev I.S., Kuzmichev K.V., Potemina T.E., Novikova N.A., Prakhov A.V. Peculiarities of physical development of children and adolescents having bronchial asthma. Medicinskij al’manah 2017; (2): 52–56, https://doi.org/10.21145/2499-9954-2017-2-52-56.
  88. Zhang Z., Wang F., Wang B.J., Chu G., Cao Q., Sun B.G., Dai Q.Y. Inhibition of leptin-induced vascular extracellular matrix remodelling by adiponectin. J Mol Endocrinol 2014; 53(2): 145–154, https://doi.org/10.1530/jme-14-0027.
  89. Arteaga-Solis E., Zee T., Emala C.W., Vinson C., Wess J., Karsenty G. Inhibition of leptin regulation of parasympathetic signaling as a cause of extreme body weight-associated asthma. Cell Metab 2013; 17(1): 35–48, https://doi.org/10.1016/j.cmet.2012.12.004.
  90. Deshpande M., Papp S., Schaffer L., Pouyani T. Hydrocortisone and triiodothyronine regulate hyaluronate synthesis in a tissue-engineered human dermal equivalent through independent pathways. J Biosci Bioeng 2015; 119(2): 226–236, https://doi.org/10.1016/j.jbiosc.2014.08.001.
  91. Cayrol F., Diaz Flaque M.C., Fernando T., Yang S.N., Sterle H.A., Bolontrade M., Amoros M., Isse B., Farias R.N., Ahn H., Tian Y.F., Tabbo F., Singh A., Inghirami G., Cerchietti L., Cremaschi G.A. Integrin alphavbeta3 acting as membrane receptor for thyroid hormones mediates angiogenesis in malignant T cells. Blood 2015; 125(5): 841–851, https://doi.org/10.1182/blood-2014-07-587337.
  92. Wenzel S.E., Robinson C.B., Leonard J.M., Panettieri R.A. Jr. Nebulized dehydroepiandrosterone-3-sulfate improves asthma control in the moderate-to-severe asthma results of a 6-week, randomized, double-blind, placebo-controlled study. Allergy Asthma Proc 2010; 31(6): 461–471, https://doi.org/10.2500/aap.2010.31.3384.
  93. Nair P., Radford K., Fanat A., Janssen L.J., Peters-Golden M., Cox P.G. The effects of leptin on airway smooth muscle responses. Am J Respir Cell Mol Biol 2008; 39(4): 475–481, https://doi.org/10.1165/rcmb.2007-0091oc.
  94. Gupta A., Sjoukes A., Richards D., Banya W., Hawrylowicz C., Bush A., Saglani S. Relationship between serum vitamin D, disease severity, and airway remodeling in children with asthma. Am J Respir Crit Care Med 2011; 184(12): 1342–1349, https://doi.org/10.1164/rccm.201107-1239oc.
  95. Gosens R., Nelemans S.A., Hiemstra M., Grootte Bromhaar M.M., Meurs H., Zaagsma J. Insulin induces a hypercontractile airway smooth muscle phenotype. Eur J Pharmacol 2003; 481(1): 125–131, https://doi.org/10.1016/j.ejphar.2003.08.081.
  96. Degano B., Mourlanette P., Valmary S., Pontier S., Prevost M.C., Escamilla R. Differential effects of low and high-dose estradiol on airway reactivity in ovariectomized rats. Respir Physiol Neurobiol 2003; 138(2–3): 265–274, https://doi.org/10.1016/j.resp.2003.08.007.
  97. Carlson C.L., Cushman M., Enright P.L., Cauley J.A., Newman A.B. Hormone replacement therapy is associated with higher FEV1 in elderly women. Am J Respir Crit Care Med 2001; 163(2): 423–428, https://doi.org/10.1164/ajrccm.163.2.2003040.
  98. Montaño L.M., Espinoza J., Flores-Soto E., Chávez J., Perusquía M. Androgens are bronchoactive drugs that act by relaxing airway smooth muscle and preventing bronchospasm. J Endocrinol 2014; 222(1): 1–13, https://doi.org/10.1530/joe-14-0074.
  99. Bordallo J., de Boto M.J., Meana C., Velasco L., Bordallo C., Suárez L., Cantabrana B., Sánchez M. Modulatory role of endogenous androgens on airway smooth muscle tone in isolated guinea-pig and bovine trachea; involvement of beta2-adrenoceptors, the polyamine system and external calcium. Eur J Pharmacol 2008; 601(1-3): 154–162, https://doi.org/10.1016/j.ejphar.2008.10.039.
  100. Ishida-Takahashi R., Uotani S., Abe T., Degawa-Yamauchi M., Fukushima T., Fujita N., Sakamaki H., Yamasaki H., Yamaguchi Y., Eguchi K. Rapid inhibition of leptin signaling by glucocorticoids in vitro and in vivo. J Biol Chem 2004; 279(19): 19658–19664, https://doi.org/10.1074/jbc.m310864200.
  101. Kistemaker L.E., Oenema T.A., Meurs H., Gosens R. Regulation of airway inflammation and remodeling by muscarinic receptors: perspectives on anticholinergic therapy in asthma and COPD. Life Sci 2012; 91(21–22): 1126–1133, https://doi.org/10.1016/j.lfs.2012.02.021.
  102. Matthiesen S., Bahulayan A., Kempkens S., Haag S., Fuhrmann M., Stichnote C., Juergens U.R., Racke K. Muscarinic receptors mediate stimulation of human lung fibroblast proliferation. Am J Respir Cell Mol Biol 2006; 35(6): 621–627, https://doi.org/10.1165/rcmb.2005-0343rc.
  103. Haag S., Matthiesen S., Juergens U.R., Racke K. Muscarinic receptors mediate stimulation of collagen synthesis in human lung fibroblasts. Eur Respir J 2008; 32(3): 555–562, https://doi.org/10.1183/09031936.00129307.
  104. Jia Y., Yue Y., Hu D.N., Chen J.L., Zhou J.B. Human aqueous humor levels of transforming growth factor-beta2: association with matrix metalloproteinases/tissue inhibitors of matrix metalloproteinases. Biomed Rep 2017; 7(6): 573–578, https://doi.org/10.3892/br.2017.1004.
  105. Eliseeva T.I., Balabolkin I.I. Modern technologies of bronchial asthma control in children (review). Sovremennye tehnologii v medicine 2015; 7(2): 168–184, https:// doi.org/10.17691/stm2015.7.2.21.
  106. Buels K.S., Jacoby D.B., Fryer A.D. Non-bronchodilating mechanisms of tiotropium prevent airway hyperreactivity in a guinea-pig model of allergic asthma. Br J Pharmacol 2012; 165(5): 1501–1514, https://doi.org/10.1111/j.1476-5381.2011.01632.x.
  107. Asano K., Shikama Y., Shoji N., Hirano K., Suzaki H., Nakajima H. Tiotropium bromide inhibits TGF-beta-induced MMP production from lung fibroblasts by interfering with Smad and MAPK pathways in vitro. Int J Chron Obstruct Pulmon Dis 2010; 5: 277–286, https://doi.org/10.2147/copd.s11737.
  108. Pera T., Zuidhof A., Valadas J., Smit M., Schoemaker R.G., Gosens R., Maarsingh H., Zaagsma J., Meurs H. Tiotropium inhibits pulmonary inflammation and remodelling in a guinea pig model of COPD. Eur Respir J 2011; 38(4): 789–796, https://doi.org/10.1183/09031936.00146610.
  109. Bousquet J., Arnavielhe S., Bedbrook A., Fonseca J., Morais Almeida M., Todo Bom A., Annesi-Maesano I., Caimmi D., Demoly P., Devillier P., Siroux V., Menditto E., Passalacqua G., Stellato C., Ventura M.T., Cruz A.A., Sarquis Serpa F., da Silva J., Larenas-Linnemann D., Rodriguez Gonzalez M., Burguete Cabanas M.T., Bergmann K.C., Keil T., Klimek L., Mosges R., Shamai S., Zuberbier T., Bewick M., Price D., Ryan D., Sheikh A., Anto J.M., Mullol J., Valero A., Haahtela T., Valovirta E., Fokkens W.J., Kuna P., Samolinski B., Bindslev-Jensen C., Eller E., Bosnic-Anticevich S., O’Hehir R.E., Tomazic P.V., Yorgancioglu A., Gemicioglu B., Bachert C., Hellings P.W., Kull I., Melen E., Wickman M., van Eerd M., De Vries G. The Allergic Rhinitis and its Impact on Asthma (ARIA) score of allergic rhinitis using mobile technology correlates with quality of life: the MASK study. Allergy 2018; 73(2): 505–510, https://doi.org/10.1111/all.13307.
  110. Krasilnikova S.V., Eliseeva T.I., Popov K.S., Tush E.V., Khaletskaya O.V., Ovsyannikov D.Y., Balabolkin I.I., Shakhov A.V., Prahov A.V. Multimorbidity of upper respiratory tract pathology in children with bronchial asthma. Pediatria 2018; 97(2): 19–26, https://doi.org/10.24110/0031-403X-2018-97-2-19-26.
  111. Krasilnikova S.V., Eliseeva Т.I., Shakhov А.V., Geppe N.A. Capabilities of nasal videoendoscopy in diagnostics of pharyngeal tonsil condition in children with bronchial asthma. Sovremennye tehnologii v medicine 2016; 8(3): 126–136, https://doi.org/10.17691/stm2016.8.3.15.
  112. Eliseeva Т.I., Krasilnikova S.V., Babaev S.Y., Novozhilov A.A., Ovsyannikov D.Y., Ignatov S.K., Kubysheva N.I., Shakhov A.V. Dependence of anterior active rhinomanometry indices on nasal obstructive disorders in children with atopic bronchial asthma complicated by nasal symptoms. BioMed Research International 2018; 2018: 1–10, https://doi.org/10.1155/2018/1869613.
  113. Eliseeva T.I., Krasilnikova S.V., Geppe N.A., Babaev S.Y., Tush E.V., Khaletskaya O.V., Ovsyannikov D.Y., Balabolkin I.I., Ignatov S.K., Kubysheva N.I. Effect of nasal obstructive disorders on sinonasal symptoms in children with different levels of bronchial asthma control. Canadian Respiratory Journal 2018; 2018, https://doi.org/10.1155/2018/4835823.
  114. Krasilnikova S.V., Tush Е.V., Babaev S.Y., Khaletskaya A.I., Popov K.S., Novozhilov A.A., Abubakirov T.E., Eliseeva Т.I., Ignatov S.K., Shakhov A.V., Kubysheva N.I., Solovyev V.D. Endonasal infrared thermometry for the diagnosis of allergic inflammation of the nasal mucosa in patients with bronchial asthma. Sovremennye tehnologii v medicine 2017; 9(4): 201, https://doi.org/10.17691/stm2017.9.4.25.
  115. Bhimrao S.K., Wilson S.J., Howarth P.H. Airway inflammation in atopic patients: a comparison of the upper and lower airways. Otolaryngol Head Neck Surg 2011; 145(3): 396–400, https://doi.org/10.1177/0194599811410531.
  116. Lim M.C., Taylor R.M., Naclerio R.M. The histology of allergic rhinitis and its comparison to cellular changes in nasal lavage. Am J Respir Crit Care Med 1995; 151(1): 136–144, https://doi.org/10.1164/ajrccm.151.1.7812543.
  117. Eifan A.O., Orban N.T., Jacobson M.R., Durham S.R. Severe persistent allergic rhinitis. inflammation but no histologic features of structural upper airway remodeling. Am J Respir Crit Care Med 2015; 192(12): 1431–1439, https://doi.org/10.1164/rccm.201502-0339oc.
  118. Krasilnikova S.V., Eliseeva Т.I., Shakhov А.V., Prakhov А.V., Balabolkin I.I. Video endoscopic method of estimation state of nasal and pharyngonasal cavity in children with bronchial asthma. Sovremennye tehnologii v medicine 2012; 3: 41–45.
  119. Licari A., Caimmi S., Bosa L., Marseglia A., Marseglia G.L., Caimmi D. Rhinosinusitis and asthma: a very long engagement. Int J Immunopathol Pharmacol 2014; 27(4): 499–508, https://doi.org/10.1177/039463201402700405.
  120. Licari A., Brambilla I., De Filippo M., Poddighe D., Castagnoli R., Marseglia G.L. The role of upper airway pathology as a co-morbidity in severe asthma. Expert Rev Respir Med 2017; 11(11): 855–865, https://doi.org/10.1080/17476348.2017.1381564.
  121. Fokkens W.J., Lund V.J., Mullol J., Bachert C., Alobid I., Baroody F., Cohen N., Cervin A., Douglas R., Gevaert P., Georgalas C., Goossens H., Harvey R., Hellings P., Hopkins C., Jones N., Joos G., Kalogjera L., Kern B., Kowalski M., Price D., Riechelmann H., Schlosser R., Senior B., Thomas M., Toskala E., Voegels R., Wang de Y., Wormald P.J. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 2012; 50(1): 1–12, https://doi.org/10.4193/rhino50e2.
  122. Rajan J.P., Wineinger N.E., Stevenson D.D., White A.A. Prevalence of aspirin-exacerbated respiratory disease among asthmatic patients: a meta-analysis of the literature. J Allergy Clin Immunol 2015; 135(3): 676–681.e1, https://doi.org/10.1016/j.jaci.2014.08.020.
  123. Meng J., Zhou P., Liu Y., Liu F., Yi X., Liu S., Holtappels G., Bachert C., Zhang N. The development of nasal polyp disease involves early nasal mucosal inflammation and remodelling. PLoS One 2013; 8(12): e82373, https://doi.org/10.1371/journal.pone.0082373.
  124. Martinez-Anton A., Debolos C., Garrido M., Roca-Ferrer J., Barranco C., Alobid I., Xaubet A., Picado C., Mullol J. Mucin genes have different expression patterns in healthy and diseased upper airway mucosa. Clin Exp Allergy 2006; 36(4): 448–457, https://doi.org/10.1111/j.1365-2222.2006.02451.x.
  125. Rehl R.M., Balla A.A., Cabay R.J., Hearp M.L., Pytynia K.B., Joe S.A. Mucosal remodeling in chronic rhinosinusitis. Am J Rhinol 2007; 21(6): 651–657, https://doi.org/10.2500/ajr.2007.21.3096.
  126. Barham H.P., Osborn J.L., Snidvongs K., Mrad N., Sacks R., Harvey R.J. Remodeling changes of the upper airway with chronic rhinosinusitis. Int Forum Allergy Rhinol 2015; 5(7): 565–572, https://doi.org/10.1002/alr.21546.
Eliseeva Т.I., Tush Е.V., Krasilnikova S.V., Kuznetsova S.V., Larin R.A., Kubysheva N.I., Khaletskaya О.V., Potemina T.E., Ryazantsev S.V., Ignatov S.K. Metabolism of the Extracellular Matrix in Bronchial Asthma (Review). Sovremennye tehnologii v medicine 2018; 10(4): 220, https://doi.org/10.17691/stm2018.10.4.25


Journal in Databases

pubmed_logo.jpg

web_of_science.jpg

scopus.jpg

crossref.jpg

ebsco.jpg

embase.jpg

ulrich.jpg

cyberleninka.jpg

e-library.jpg

lan.jpg

ajd.jpg

SCImago Journal & Country Rank

Publication is registered by Federal Service for Supervision in the Sphere of Telecom, Information Technologies and Mass Communications.
Mass Media Registration Certificate PE № FS 77-79187 dated October 16, 2020.

If reproducing any part of the publication a reference to the Journal is obligatory.