Abstract/References

Extracellular matrix (ECM) is a non-cellular constituent found in all tissues and organs. Although ECM was previously recognized as a mere “molecular glue” that supports the tissue structure of organs such as the lungs, it has recently been reported that ECM has important biological activities for tissue morphogenesis, inflammation, wound healing, and tumor progression. Proteoglycans are the main constituent of ECM, with growing evidence that proteoglycans and their associated glycosaminoglycans play important roles in the pathogenesis of several diseases. However, their roles in the lungs are incompletely understood.

Leukocyte migration into the lung is one of the main aspects involved in the pathogenesis of several lung diseases. Glycosaminoglycans bind to chemokines and their interaction fine-tunes leukocyte migration into the affected organs. This review focuses on the role chemokine and glycosaminoglycan interactions in neutrophil migration into the lung. Furthermore, this review presents the role of proteoglycans such as syndecan, versican, and hyaluronan in inflammatory and fibrotic lung diseases.

1. Kyriakopoulou K, Piperigkou Z, Tzaferi K, Karamanos NK. Trends in extracellular matrix biology. Mol Biol Rep, 50:853-863, 2023.

2. Sainio A, Järveläinen H. Extracellular matrix-cell interactions:Focus on therapeutic applications. Cell Signal, 66:109487, 2020.

3. Theocharis AD, Manou D, Karamanos NK. The extracellular matrix as a multitasking player in disease. FEBS J, 286:2830-2869, 2019.

4. Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Bopl, 15:786-801, 2014.

5. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci, 123:4195-4200, 2010.

6. Gill S, Wight TN, Frevert CW. Proteoglycans: key regulators of pulmonary inflammation and the innate immune response to lung infection. Anat Rec (Hoboken), 293(6):968-981, 2010.

7. Alexopoulou AN, Multhaupt HA, Couchman JR. Syndecans in wound healing, inflammation and vascular biology. Int J Biochem Cell Biol, 39:505-528, 2007.

8. Bartlett AH, Hayashida K, Park PW. Molecular and cellular mechanisms of syndecans in tissue injury and inflammation. Mol and Cells, 24:153-166, 2007.

9. Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature, 446:1030-1037, 2007.

10. Celie JW, Beelen RH, van den Born J. Heparan sulfate proteoglycans in extravasation:assisting leukocyte guidance. Front Biosci (Landmark Ed), 14:4932-4949, 2009.

11. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. Journal Clin Invest, 108:169-173, 2001.

12. Parish CR. The role of heparan sulphate in inflammation. Nat Rev Immunol, 6:633-643, 2006.

13. Sampson PM, Boyd RB, Pietra GG, Fishman AP. Glycosaminoglycan biosynthesis in the isolated perfused rat lung. J Appl Physiol Respir Environ Exerc Physiol, 57:1648-1654, 1984.

14. Scott JE. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J, 6:2639-2645, 1992.

15. Alexander CM, Reichsman F, Hinkes MT, Lincecum J, Becker KA, Cumberledge S, et al. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat Genet, 25:329-332, 2000.

16. Colin-Pierre C, El Baraka O, Danoux L, Bardey V, André V, Ramont L, et al. Regulation of stem cell fate by HSPGs:implication in hair follicle cycling. NPJ Regen Med, 7:77, 2022.

17. Merida-de-Barros DA, Chaves SP, Belmiro CLR, Wanderley JLM. Leishmaniasis and glycosaminoglycans: a future therapeutic strategy? Parasit Vectors, 11:536, 2018.

18. Kuschert GS, Coulin F, Power CA, Proudfoot AE, Hubbard RE, Hoogewerf AJ, et al. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry, 38:12959-12968, 1999.

19. Muramatsu T, Muramatsu H, Kojima T. Identification of proteoglycan-binding proteins. Methods Enzymol, 416:263-278, 2006.

20. Frevert CW, Kinsella MG, Vathanaprida C, Goodman RB, Baskin DG, Proudfoot A, et al. Binding of interleukin-8 to heparan sulfate and chondroitin sulfate in lung tissue. Am J Respir Cell Mol Biol, 28:464-472, 2003.

21. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol, 200:423-428, 2003.

22. Kinsella MG, Bressler SL, Wight TN. The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Eukaryot Gene Expr, 14:203-234, 2004.

23. Iozzo RV, Schaefer L. Proteoglycan form and function:A comprehensive nomenclature of proteoglycans. Matrix Biol, 42:11-55, 2015.

24. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem, 71:435-471, 2002.

25. Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE. Regulation of protein function by glycosaminoglycans — as exemplified by chemokines. Annu Rev Biochem, 74:385-410, 2005.

26. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans:host-associated molecular patterns for initiation and modulation of inflammation. FASEB J, 20:9-22, 2006.

27. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Iwase M, Yoshikai Y, et al. Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J Biol Chem, 276:47483-47488, 2001.

28. Minamiya Y, Saito S, Kalina U, Saito H, Terada K, Ogawa J. Antithrombin III diminishes production of oxygen radical in endotoxin-infused rat lung. Shock, 21:139-143, 2004.

29. Rehberg S, Yamamoto Y, Sousse LE, Jonkam C, Zhu Y, Traber LD, et al. Antithrombin attenuates vascular leakage via inhibiting neutrophil activation in acute lung injury. Crit Care Med, 41:e439-446, 2013.

30. Thompson BT, Chambers RC, Liu KD. Acute Respiratory Distress Syndrome. New Engl J Med, 377:562-572, 2017.

31. Matthay MA, Zemans RL, Zimmerman GA, Arabi YM, Beitler JR, Mercat A, et al. Acute respiratory distress syndrome. Nat Rev Dis Primers, 5:18, 2019.

32. Standiford TJ, Kunkel SL, Greenberger MJ, Laichalk LL, Strieter RM. Expression and regulation of chemokines in bacterial pneumonia. J Leukoc Biol, 59:24-28, 1996.

33. Lortat-Jacob H, Grosdidier A, Imberty A. Structural diversity of heparan sulfate binding domains in chemokines. Proc Natl Acad Sci USA, 99:1229-1234, 2002.

34. Bao X, Moseman EA, Saito H, Petryniak B, Thiriot A, Hatakeyama S, et al. Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity, 33:817-829, 2010.

35. Kuschert GS, Hoogewerf AJ, Proudfoot AE, Chung CW, Cooke RM, Hubbard RE, et al. Identification of a glycosaminoglycan binding surface on human interleukin-8. Biochemistry, 37:11193-11201, 1998.

36. Rot A. Binding of neutrophil attractant/activation protein-1 (interleukin 8) to resident dermal cells. Cytokine, 347:347-352, 1992.

37. Rot A. Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur J Immunol, 23:303-306, 1993.

38. Tanaka Y, Adams DH, Hubscher S, Hirano H, Siebenlist U, Shaw S. Nature, 361:79-82, 1993.

39. Tanino Y, Coombe DR, Gill SE, Kett WC, Kajikawa O, Proudfoot AE, et al. Kinetics of chemokine-glycosaminoglycan interactions control neutrophil migration into the airspaces of the lungs. J Immunol, 184:2677-2685, 2010.

40. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol, 8:365-393, 1992.

41. Götte M. Syndecans in inflammation. FASEB J, 17:575-591, 2003.

42. Okuyama E, Suzuki A, Murata M, Ando Y, Kato I, Takagi Y, et al. Molecular mechanisms of syndecan-4 upregulation by TNF-α in the endothelium-like EAhy926 cells. J Biochem, 154:41-50, 2013.

43. Saphire AC, Bobardt MD, Zhang Z, David G, Gallay PA. Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J Virol, 75:9187-9200, 2001.

44. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem, 68:729-777, 1999.

45. Fears CY, Woods A. The role of syndecans in disease and wound healing. Matrix Biol, 25:443-456, 2006.

46. Tanino Y, Chang MY, Wang X, Gill SE, Skerrett S, McGuire JK, et al. Syndecan-4 regulates early neutrophil migration and pulmonary inflammation in response to lipopolysaccharide. Am J Respir Cell Mol Biol, 47:196-202, 2012.

47. Nikaido T, Tanino Y, Wang X, Sato S, Misa K, Fukuhara N, et al. Serum Syndecan-4 as a Possible Biomarker in Patients With Acute Pneumonia. J Infect Dis, 212:1500-1508, 2015.

48. Tanino Y, Wang X, Nikaido T, Misa K, Sato Y, Togawa R, et al. Syndecan-4 Inhibits the Development of Pulmonary Fibrosis by Attenuating TGF-beta Signaling. Int J Mol Sci, 20:4989, 2019.

49. Sato Y, Tanino Y, Wang X, Nikaido T, Sato S, Misa K, et al. Baseline serum syndecan-4 predicts prognosis after the onset of acute exacerbation of idiopathic interstitial pneumonia. PLoS One, 12:e0176789, 2017.

50. Brule S, Charnaux N, Sutton A, Ledoux D, Chaigneau T, Saffar L, et al. The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9. Glycobiology, 16:488-501, 2006.

51. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell, 111:635-646, 2002.

52. Pruessmeyer J, Martin C, Hess FM, Schwarz N, Schmidt S, Kogel T, et al. A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and -4 by lung epithelial cells. J Biol Chem, 285:555-564, 2010.

53. Ramnath R, Foster RR, Qiu Y, Cope G, Butler MJ, Salmon AH, et al. Matrix metalloproteinase 9-mediated shedding of syndecan 4 in response to tumor necrosis factor α:a contributor to endothelial cell glycocalyx dysfunction. FASEB J, 28:4686-4699, 2014.

54. Hayashida K, Parks WC, Park PW. Syndecan-1 shedding facilitates the resolution of neutrophilic inflammation by removing sequestered CXC chemokines. Blood, 114:3033-3043, 2009.

55. Lederer DJ, Martinez FJ. Idiopathic Pulmonary Fibrosis. New Engl J Med, 378:1811-1823, 2018.

56. Richeldi L, Collard HR, Jones MG. Idiopathic pulmonary fibrosis. Lancet, 389:1941-1952, 2017.

57. Wijsenbeek M, Cottin V. Spectrum of Fibrotic Lung Diseases. New Engl J Med, 383:958-968, 2020.

58. Natsuizaka M, Chiba H, Kuronuma K, Otsuka M, Kudo K, Mori M, et al. Epidemiologic survey of Japanese patients with idiopathic pulmonary fibrosis and investigation of ethnic differences. Am J Respir Crit Care Med, 190:773-779, 2014.

59. Matsuzaki Y, Wang X, Tanino Y, Ikeda K. Insufficient Syndecan-4 is associated with CLD Development in Preterm Infants. Pediatr Int, 65(1): e15413, 2022.

60. Tang F, Brune JE, Chang MY, Reeves SR, Altemeier WA, Frevert CW. Defining the versican interactome in lung health and disease. Am J Physiol Cell physiol, 323:C249-c76, 2022.

61. Andersson-Sjöland A, Hallgren O, Rolandsson S, Weitoft M, Tykesson E, Larsson-Callerfelt AK, et al. Versican in inflammation and tissue remodeling:the impact on lung disorders. Glycobiology, 25:243-251, 2015.

62. Sotoodehnejadnematalahi F, Burke B. Structure, function and regulation of versican:the most abundant type of proteoglycan in the extracellular matrix. Acta Med Iran, 51:740-750, 2013.

63. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med, 11:1173-1179, 2005.

64. Hoarau A, Polette M, Coraux C. Lung Hyaluronasome:Involvement of Low Molecular Weight Ha (Lmw-Ha) in Innate Immunity. Biomolecules, 12:658, 2022.

65. Chang MY, Tanino Y, Vidova V, Kinsella MG, Chan CK, Johnson PY, et al. Reprint of:A rapid increase in macrophage-derived versican and hyaluronan in infectious lung disease. Matrix Biol, 35:162-173, 2014.

66. Inokoshi Y, Tanino Y, Wang X, Sato S, Fukuhara N, Nikaido T, et al. Clinical significance of serum hyaluronan in chronic fibrotic interstitial pneumonia. Respirology, 18:1236-1243, 2013.

67. Khan FA, Stewart I, Saini G, Robinson KA, Jenkins RG. A systematic review of blood biomarkers with individual participant data meta-analysis of matrix metalloproteinase-7 in idiopathic pulmonary fibrosis. Eur Respir J, 59:2101612, 2022.

68. Guiot J, Moermans C, Henket M, Corhay JL, Louis R. Blood Biomarkers in Idiopathic Pulmonary Fibrosis. Lung, 195:273-280, 2017.

69. Leeming DJ, Sand JM, Nielsen MJ, Genovese F, Martinez FJ, Hogaboam CM, et al. Serological investigation of the collagen degradation profile of patients with chronic obstructive pulmonary disease or idiopathic pulmonary fibrosis. Biomark Insights, 7:119-126, 2012.

70. Jenkins RG, Simpson JK, Saini G, Bentley JH, Russell AM, Braybrooke R, et al. Longitudinal change in collagen degradation biomarkers in idiopathic pulmonary fibrosis:an analysis from the prospective, multicentre PROFILE study. Lancet Respir Med, 3:462-472, 2015.

71. Sand JMB, Tanino Y, Karsdal MA, Nikaido T, Misa K, Sato Y, et al. A Serological Biomarker of Versican Degradation is Associated with Mortality Following Acute Exacerbations of Idiopathic Interstitial Pneumonia. Respir Res, 19:82, 2018.

72. Weber IT, Harrison RW, Iozzo RV. Model structure of decorin and implications for collagen fibrillogenesis. J Biol Chem, 271:31767-31770, 1996.

73. Gubbiotti MA, Vallet SD, Ricard-Blum S, Iozzo RV. Decorin interacting network:A comprehensive analysis of decorin-binding partners and their versatile functions. Matrix Biol, 55:7-21, 2016.

74. Neill T, Schaefer L, Iozzo RV. Decorin:a guardian from the matrix. Am J Pathol, 181:380-387, 2012.

75. Yamaguchi Y, Mann DM, Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature, 346:281-284, 1990.

76. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol, 136:729-743, 1997.

77. Järveläinen H, Sainio A, Wight TN. Pivotal role for decorin in angiogenesis. Matrix Biol, 43:15-26, 2015.

78. Dong Y, Zhong J, Dong L. The Role of Decorin in Autoimmune and Inflammatory Diseases. J Immunol Res, 2022:1283383, 2022.

79. Bensadoun ES, Burke AK, Hogg JC, Roberts CR. Proteoglycan deposition in pulmonary fibrosis. Am J Respir Crit Care Med, 154:1819-1828, 1996.

80. Nikaido T, Tanino Y, Wang X, Sato Y, Togawa R, Kikuchi M, et al. Serum decorin is a potential prognostic biomarker in patients with acute exacerbation of idiopathic pulmonary fibrosis. J Thorac Dis, 10:5346-5358, 2018