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Mini-Reviews in Medicinal Chemistry

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ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

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Review Article

Hyaluronan Fragmentation During Inflammatory Pathologies: A Signal that Empowers Tissue Damage

Author(s): Angela Avenoso, Giuseppe Bruschetta, Angela D`Ascola, Michele Scuruchi, Giuseppe Mandraffino, Antonino Saitta, Salvatore Campo and Giuseppe M. Campo*

Volume 20, Issue 1, 2020

Page: [54 - 65] Pages: 12

DOI: 10.2174/1389557519666190906115619

Price: $65

Abstract

The mechanisms that modulate the response to tissue injury are not fully understood. Abnormalities in the repair response are associated with a variety of chronic disease states characterized by inflammation, followed subsequently by excessive ECM deposition. As cell-matrix interactions are able to regulate cellular homeostasis, modification of ECM integrity appears to be an unspecific factor in promoting the onset and progression of inflammatory diseases. Evidence is emerging to show that endogenous ECM molecules supply signals to damage tissues and cells in order to promote further ECM degradation and inflammation progression. Several investigations have been confirmed that HA fragments of different molecular sizes exhibit different biological effects and responses. In fact, the increased deposition of HA into the ECM is a strong hallmark of inflammation processes. In the context of inflammatory pathologies, highly polymerized HA is broken down into small components, which are able to exacerbate the inflammatory response by inducing the release of various detrimental mediators such as reactive oxygen species, cytokines, chemokines and destructive enzymes and by facilitating the recruitment of leukocytes. However, strategies involving the modulation of the HA fragment with specific receptors on cell surface could represent different promising effects for therapeutic scope.

This review will focus on the inflammation action of small HA fragments in recent years obtained by in vivo reports.

Keywords: Hyaluronan fragments, inflammation, transcription factors, extracellular matrix, cytokines, toll-like receptors.

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[1]
Bonnans, C.; Chou, J.; Werb, Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol., 2014, 15(12), 786-801.
[http://dx.doi.org/10.1038/nrm3904] [PMID: 25415508]
[2]
Fraser, J.R.; Laurent, T.C.; Laurent, U.B. Hyaluronan: Its nature, distribution, functions and turnover. J. Intern. Med., 1997, 242(1), 27-33.
[http://dx.doi.org/10.1046/j.1365-2796.1997.00170.x] [PMID: 9260563]
[3]
Jiang, D.; Liang, J.; Noble, P.W. Hyaluronan as an immune regulator in human diseases. Physiol. Rev., 2011, 91(1), 221-264.
[http://dx.doi.org/10.1152/physrev.00052.2009] [PMID: 21248167]
[4]
Avenoso, A.; Bruschetta, G.; D’Ascola, A.; Scuruchi, M.; Mandraffino, G.; Gullace, R.; Saitta, A.; Campo, S.; Campo, G.M. Hyaluronan fragments produced during tissue injury: A signal amplifying the inflammatory response. Arch. Biochem. Biophys., 2019, 663, 228-238.
[http://dx.doi.org/10.1016/j.abb.2019.01.015] [PMID: 30668938]
[5]
Garantziotis, S.; Savani, R.C. Hyaluronan biology: A complex balancing act of structure, function, location and context. Matrix Biol., 2019, 78-79, 1-10.
[http://dx.doi.org/10.1016/j.matbio.2019.02.002] [PMID: 30802498]
[6]
Tavianatou, A.G.; Caon, I.; Franchi, M.; Piperigkou, Z.; Galesso, D.; Karamanos, N.K. Hyaluronan: molecular size-dependent signaling and biological functions in inflammation and cancer. FEBS J. Available from, 2019 In press
[7]
Petrey, A.C.; de la Motte, C.A. Hyaluronan, a crucial regulator of inflammation. Front. Immunol., 2014, 5, 101.
[http://dx.doi.org/10.3389/fimmu.2014.00101] [PMID: 24653726]
[8]
Yang, C.; Cao, M.; Liu, H.; He, Y.; Xu, J.; Du, Y.; Liu, Y.; Wang, W.; Cui, L.; Hu, J.; Gao, F. The high and low molecular weight forms of hyaluronan have distinct effects on CD44 clustering. J. Biol. Chem., 2012, 287(51), 43094-43107.
[http://dx.doi.org/10.1074/jbc.M112.349209] [PMID: 23118219]
[9]
Hauser-Kawaguchi, A.; Luyt, L.G.; Turley, E. Design of peptide mimetics to block pro-inflammatory functions of HA fragments. Matrix Biol., 2019, 78-79, 346-356.
[http://dx.doi.org/10.1016/j.matbio.2018.01.021] [PMID: 29408009]
[10]
Avenoso, A.; D’Ascola, A.; Scuruchi, M.; Mandraffino, G.; Calatroni, A.; Saitta, A.; Campo, S.; Campo, G.M. Hyaluronan in experimental injured/inflamed cartilage: In vivo studies. Life Sci., 2018, 193, 132-140.
[http://dx.doi.org/10.1016/j.lfs.2017.11.006] [PMID: 29126884]
[11]
Webb, D.R. Animal models of human disease: Inflammation. Biochem. Pharmacol., 2014, 87(1), 121-130.
[http://dx.doi.org/10.1016/j.bcp.2013.06.014] [PMID: 23811309]
[12]
El-Aarag, B.; Magdy, M.; AlAjmi, M.F.; Khalifa, S.A.; El-Seedi, H.R. Melittin exerts beneficial effects on paraquat-induced lung injuries in mice by modifying oxidative stress and apoptosis. Molecules, 2019, 24(8) E1498
[http://dx.doi.org/10.3390/molecules24081498]
[13]
Pedicino, D.; Vinci, R.; Giglio, A.F.; Pisano, E.; Porto, I.; Vergallo, R.; Russo, G.; Ruggio, A.; D’Aiello, A.; Flego, D.; Annibali, G.; Trotta, F.; Piacentini, R.; Niccoli, G.; Liuzzo, G.; Crea, F. Alterations of hyaluronan metabolism in acute coronary syndrome: Implications for plaque erosion. J. Am. Coll. Cardiol., 2018, 72(13), 1490-1503.
[http://dx.doi.org/10.1016/j.jacc.2018.06.072] [PMID: 30236312]
[14]
Garantziotis, S.; Li, Z.; Potts, E.N.; Lindsey, J.Y.; Stober, V.P.; Polosukhin, V.V.; Blackwell, T.S.; Schwartz, D.A.; Foster, W.M.; Hollingsworth, J.W. TLR4 is necessary for hyaluronan-mediated airway hyperresponsiveness after ozone inhalation. Am. J. Respir. Crit. Care Med., 2010, 181(7), 666-675.
[http://dx.doi.org/10.1164/rccm.200903-0381OC] [PMID: 20007931]
[15]
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, 2011, 6(11) e27137
[http://dx.doi.org/10.1371/journal.pone.0027137] [PMID: 22073274]
[16]
Cheng, G.; Swaidani, S.; Sharma, M.; Lauer, M.E.; Hascall, V.C.; Aronica, M.A. Hyaluronan deposition and correlation with inflammation in a murine ovalbumin model of asthma. Matrix Biol., 2011, 30(2), 126-134.
[http://dx.doi.org/10.1016/j.matbio.2010.12.003] [PMID: 21251977]
[17]
Ghosh, S.; Hoselton, S.A.; Wanjara, S.B.; Carlson, J.; McCarthy, J.B.; Dorsam, G.P.; Schuh, J.M. Hyaluronan stimulates ex vivo B lymphocyte chemotaxis and cytokine production in a murine model of fungal allergic asthma. Immunobiology, 2015, 220(7), 899-909.
[http://dx.doi.org/10.1016/j.imbio.2015.01.011] [PMID: 25698348]
[18]
Papakonstantinou, E.; Roth, M.; Klagas, I.; Karakiulakis, G.; Tamm, M.; Stolz, D. COPD exacerbations are associated with proinflammatory degradation of hyaluronic acid. Chest, 2015, 148(6), 1497-1507.
[http://dx.doi.org/10.1378/chest.15-0153] [PMID: 26226411]
[19]
Soroosh, A.; Albeiroti, S.; West, G.A.; Willard, B.; Fiocchi, C.; de la Motte, C.A. Crohn’s disease fibroblasts overproduce the novel protein KIAA1199 to create proinflammatory hyaluronan fragments. Cell. Mol. Gastroenterol. Hepatol., 2016, 2, 358-368.
[http://dx.doi.org/10.1016/j.jcmgh.2015.12.007]
[20]
Bracke, K.R.; Dentener, M.A.; Papakonstantinou, E.; Vernooy, J.H.; Demoor, T.; Pauwels, N.S.; Cleutjens, J.; van Suylen, R.J.; Joos, G.F.; Brusselle, G.G.; Wouters, E.F. Enhanced deposition of low-molecular-weight hyaluronan in lungs of cigarette smoke-exposed mice. Am. J. Respir. Cell Mol. Biol., 2010, 42(6), 753-761.
[http://dx.doi.org/10.1165/rcmb.2008-0424OC] [PMID: 19675307]
[21]
Monzon, M.E.; Fregien, N.; Schmid, N.; Falcon, N.S.; Campos, M.; Casalino-Matsuda, S.M.; Forteza, R.M. Reactive oxygen species and hyaluronidase 2 regulate airway epithelial hyaluronan fragmentation. J. Biol. Chem., 2010, 285(34), 26126-26134.
[http://dx.doi.org/10.1074/jbc.M110.135194] [PMID: 20554532]
[22]
Matuska, B.; Comhair, S.; Farver, C.; Chmiel, J.; Midura, R.J.; Bonfield, T.; Lauer, M.E. Pathological hyaluronan matrices in cystic fibrosis airways and secretions. Am. J. Respir. Cell Mol. Biol., 2016, 55(4), 576-585.
[http://dx.doi.org/10.1165/rcmb.2015-0358OC] [PMID: 27243106]
[23]
Bauer, J.; Rothley, M.; Schmaus, A.; Quagliata, L.; Ehret, M.; Biskup, M.; Orian-Rousseau, V.; Jackson, D.G.; Pettis, R.J.; Harvey, A.; Bräse, S.; Thiele, W.; Sleeman, J.P. TGFβ counteracts LYVE-1-mediated induction of lymphangiogenesis by small hyaluronan oligosaccharides. J. Mol. Med. (Berl.), 2018, 96(2), 199-209.
[http://dx.doi.org/10.1007/s00109-017-1615-4] [PMID: 29282520]
[24]
Zhang, G.; Lu, R.; Wu, M.; Liu, Y.; He, Y.; Xu, J.; Yang, C.; Du, Y.; Gao, F. Colorectal cancer-associated ~ 6 kDa hyaluronan serves as a novel biomarker for cancer progression and metastasis. FEBS J., 2019, 286(16), 3148-3163.
[http://dx.doi.org/10.1111/febs.14859] [PMID: 31004406]
[25]
Lorén, C.E.; Dahl, C.P.; Do, L.; Almaas, V.M.; Geiran, O.R.; Mörner, S.; Hellman, U. Low Molecular mass myocardial hyaluronan in human hypertrophic cardiomyopathy. Cells, 2019, 8(2), 97.
[http://dx.doi.org/10.3390/cells8020097]
[26]
Todd, J.L.; Wang, X.; Sugimoto, S.; Kennedy, V.E.; Zhang, H.L.; Pavlisko, E.N.; Kelly, F.L.; Huang, H.; Kreisel, D.; Palmer, S.M.; Gelman, A.E. Hyaluronan contributes to bronchiolitis obliterans syndrome and stimulates lung allograft rejection through activation of innate immunity. Am. J. Respir. Crit. Care Med., 2014, 189(5), 556-566.
[http://dx.doi.org/10.1164/rccm.201308-1481OC]
[27]
Ferrari, L.F.; Araldi, D.; Bogen, O.; Levine, J.D. Extracellular matrix hyaluronan signals via its CD44 receptor in the increased responsiveness to mechanical stimulation. Neuroscience, 2016, 324, 390-398.
[http://dx.doi.org/10.1016/j.neuroscience.2016.03.032] [PMID: 26996509]
[28]
Panogeorgou, T.; Tserbini, E.; Filou, S.; Vynios, D.H.; Naxakis, S.S.; Papadas, T.A.; Goumas, P.D.; Mastronikolis, N.S. Hyaluronan synthases and hyaluronidases in nasal polyps. Eur. Arch. Otorhinolaryngol., 2016, 273(7), 1801-1808.
[http://dx.doi.org/10.1007/s00405-015-3848-6] [PMID: 26661071]
[29]
Ormiston, M.L.; Slaughter, G.R.; Deng, Y.; Stewart, D.J.; Courtman, D.W. The enzymatic degradation of hyaluronan is associated with disease progression in experimental pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol., 2010, 298(2), L148-L157.
[http://dx.doi.org/10.1152/ajplung.00097.2009] [PMID: 19915162]
[30]
Eldridge, L.; Moldobaeva, A.; Wagner, E.M. Increased hyaluronan fragmentation during pulmonary ischemia. Am. J. Physiol. Lung Cell. Mol. Physiol., 2011, 301(5), L782-L788.
[http://dx.doi.org/10.1152/ajplung.00079.2011] [PMID: 21821727]
[31]
Lindqvist, U.; Phil-Lundin, I.; Engström-Laurent, A. Dermal distribution of hyaluronan in psoriatic arthritis; coexistence of CD44, MMP3 and MMP9. Acta Derm. Venereol., 2012, 92(4), 372-377.
[http://dx.doi.org/10.2340/00015555-1286] [PMID: 22278305]
[32]
Ruscheinsky, M.; De la Motte, C.; Mahendroo, M. Hyaluronan and its binding proteins during cervical ripening and parturition: Dynamic changes in size, distribution and temporal sequence. Matrix Biol., 2008, 27(5), 487-497.
[http://dx.doi.org/10.1016/j.matbio.2008.01.010] [PMID: 18353623]
[33]
Østerholt, H.C.; Dannevig, I.; Wyckoff, M.H.; Liao, J.; Akgul, Y.; Ramgopal, M.; Mija, D.S.; Cheong, N.; Longoria, C.; Mahendroo, M.; Nakstad, B.; Saugstad, O.D.; Savani, R.C. Antioxidant protects against increases in low molecular weight hyaluronan and inflammation in asphyxiated newborn pigs resuscitated with 100% oxygen. PLoS One, 2012, 7(6) e38839
[http://dx.doi.org/10.1371/journal.pone.0038839] [PMID: 22701723]
[34]
van der Windt, G.J.; Florquin, S.; de Vos, A.F.; van’t Veer, C.; Queiroz, K.C.; Liang, J.; Jiang, D.; Noble, P.W.; van der Poll, T. CD44 deficiency is associated with increased bacterial clearance but enhanced lung inflammation during Gram-negative pneumonia. Am. J. Pathol., 2010, 177(5), 2483-2494.
[http://dx.doi.org/10.2353/ajpath.2010.100562] [PMID: 20864681]
[35]
Lazrak, A.; Creighton, J.; Yu, Z.; Komarova, S.; Doran, S.F.; Aggarwal, S.; Emala, C.W., Sr; Stober, V.P.; Trempus, C.S.; Garantziotis, S.; Matalon, S. Hyaluronan mediates airway hyperresponsiveness in oxidative lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol., 2015, 308(9), L891-L903.
[http://dx.doi.org/10.1152/ajplung.00377.2014] [PMID: 25747964]
[36]
Ni, K.; Gill, A.; Tseng, V.; Mikosz, A.M.; Koike, K.; Beatman, E.L.; Xu, C.Y.; Cao, D.; Gally, F.; Mould, K.J.; Serban, K.A.; Schweitzer, K.S.; March, K.L.; Janssen, W.J.; Nozik-Grayck, E.; Garantziotis, S.; Petrache, I. Rapid clearance of heavy chain-modified hyaluronan during resolving acute lung injury. Respir. Res., 2018, 19(1), 107.
[http://dx.doi.org/10.1186/s12931-018-0812-1] [PMID: 29855321]
[37]
Day, A.J.; Milner, C.M. TSG-6: A multifunctional protein with anti-inflammatory and tissue-protective properties. Matrix Biol., 2019, 78-79, 60-83.
[http://dx.doi.org/10.1016/j.matbio.2018.01.011] [PMID: 29362135]
[38]
Lauer, M.E.; Glant, T.T.; Mikecz, K.; DeAngelis, P.L.; Haller, F.M.; Husni, M.E.; Hascall, V.C.; Calabro, A. Irreversible heavy chain transfer to hyaluronan oligosaccharides by tumor necrosis factor-stimulated gene-6. J. Biol. Chem., 2013, 288(1), 205-214.
[http://dx.doi.org/10.1074/jbc.M112.403998] [PMID: 23166324]
[39]
Campo, G.M.; Avenoso, A.; D’Ascola, A.; Nastasi, G.; Micali, A.; Puzzolo, D.; Pisani, A.; Prestipino, V.; Scuruchi, M.; Calatroni, A.; Campo, S. Combined treatment with hyaluronan inhibitor Pep-1 and a selective adenosine A2 receptor agonist reduces inflammation in experimental arthritis. Innate Immun., 2013, 19(5), 462-478.
[http://dx.doi.org/10.1177/1753425912470391] [PMID: 23283732]
[40]
Campo, G.M.; Micali, A.; Avenoso, A.; D’Ascola, A.; Scuruchi, M.; Pisani, A.; Bruschetta, A.; Calatroni, A.; Puzzolo, D.; Campo, S. Inhibition of small HA fragment activity and stimulation of A2A adenosine receptor pathway limit apoptosis and reduce cartilage damage in experimental arthritis. Histochem. Cell Biol., 2015, 143(5), 531-543.
[http://dx.doi.org/10.1007/s00418-014-1298-7] [PMID: 25511416]
[41]
Morioka, Y.; Yamasaki, K.; Leung, D.; Gallo, R.L. Cathelicidin antimicrobial peptides inhibit hyaluronan-induced cytokine release and modulate chronic allergic dermatitis. J. Immunol., 2008, 181(6), 3915-3922.
[http://dx.doi.org/10.4049/jimmunol.181.6.3915] [PMID: 18768846]
[42]
King, T.P.; Wittkowski, K.M. Hyaluronidase and hyaluronan in insect venom allergy. Int. Arch. Allergy Immunol., 2011, 156(2), 205-211.
[http://dx.doi.org/10.1159/000322847] [PMID: 21597301]
[43]
Kwon, M.J.; Han, J.; Kim, B.H.; Lee, Y.S.; Kim, T.Y. Superoxide dismutase 3 suppresses hyaluronic acid fragments mediated skin inflammation by inhibition of toll-like receptor 4 signaling pathway: superoxide dismutase 3 inhibits reactive oxygen species-induced trafficking of toll-like receptor 4 to lipid rafts. Antioxid. Redox Signal., 2012, 16(4), 297-313.
[http://dx.doi.org/10.1089/ars.2011.4066] [PMID: 21957979]
[44]
Esser, P.R.; Wölfle, U.; Dürr, C.; von Loewenich, F.D.; Schempp, C.M.; Freudenberg, M.A.; Jakob, T.; Martin, S.F. Contact sensitizers induce skin inflammation via ROS production and hyaluronic acid degradation. PLoS One, 2012, 7(7) e41340
[http://dx.doi.org/10.1371/journal.pone.0041340] [PMID: 22848468]
[45]
Tolg, C.; Hamilton, S.R.; Zalinska, E.; McCulloch, L.; Amin, R.; Akentieva, N.; Winnik, F.; Savani, R.; Bagli, D.J.; Luyt, L.G.; Cowman, M.K.; McCarthy, J.B.; Turley, E.A. A RHAMM mimetic peptide blocks hyaluronan signaling and reduces inflammation and fibrogenesis in excisional skin wounds. Am. J. Pathol., 2012, 181(4), 1250-1270.
[http://dx.doi.org/10.1016/j.ajpath.2012.06.036] [PMID: 22889846]
[46]
Muto, J.; Morioka, Y.; Yamasaki, K.; Kim, M.; Garcia, A.; Carlin, A.F.; Varki, A.; Gallo, R.L. Hyaluronan digestion controls DC migration from the skin. J. Clin. Invest., 2014, 124(3), 1309-1319.
[http://dx.doi.org/10.1172/JCI67947] [PMID: 24487587]
[47]
Wang, Y.; Han, G.; Guo, B.; Huang, J. Hyaluronan oligosaccharides promote diabetic wound healing by increasing angiogenesis. Pharmacol. Rep., 2016, 68(6), 1126-1132.
[http://dx.doi.org/10.1016/j.pharep.2016.07.001] [PMID: 27588388]

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