Skip to main content

Advertisement

SpringerLink
Log in

The role of periostin in lung fibrosis and airway remodeling

  • Multi-author review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Periostin is a protein that plays a key role in development and repair within the biological matrix of the lung. As a matricellular protein that does not contribute to extracellular matrix structure, periostin interacts with other extracellular matrix proteins to regulate the composition of the matrix in the lung and other organs. In this review, we discuss the studies exploring the role of periostin to date in chronic respiratory diseases, namely asthma and idiopathic pulmonary fibrosis. Asthma is a major health problem globally affecting millions of people worldwide with significant associated morbidity and mortality. Periostin is highly expressed in the lungs of asthmatic patients, contributes to mucus secretion, airway fibrosis and remodeling and is recognized as a biomarker of Th2 high inflammation. Idiopathic pulmonary fibrosis is a fatal interstitial lung disease characterized by progressive aberrant fibrosis of the lung matrix and respiratory failure. It predominantly affects adults over 50 years of age and its incidence is increasing worldwide. Periostin is also highly expressed in the lungs of idiopathic pulmonary fibrosis patients. Serum levels of periostin may predict clinical progression in this disease and periostin promotes myofibroblast differentiation and type 1 collagen production to contribute to aberrant lung fibrosis. Studies to date suggest that periostin is a key player in several pathogenic mechanisms within the lung and may provide us with a useful biomarker of clinical progression in both asthma and idiopathic pulmonary fibrosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bozyk PD, Bentley JK, Popova AP, Anyanwu AC, Linn MD, Goldsmith AM, Pryhuber GS, Moore BB, Hershenson MB (2012) Neonatal periostin knockout mice are protected from hyperoxia-induced alveolar simplication. PLoS One 7(2):e31336. doi:10.1371/journal.pone.0031336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Izuhara K, Conway SJ, Moore BB, Matsumoto H, Holweg CT, Matthews JG, Arron JR (2016) Roles of periostin in respiratory disorders. Am J Respir Crit Care Med 193(9):949–956. doi:10.1164/rccm.201510-2032PP

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68(19):3201–3207. doi:10.1007/s00018-011-0784-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Liu AY, Zheng H, Ouyang G (2014) Periostin, a multifunctional matricellular protein in inflammatory and tumor microenvironments. Matrix Biol 37:150–156. doi:10.1016/j.matbio.2014.04.007

    Article  PubMed  CAS  Google Scholar 

  5. Wilson MS, Wynn TA (2009) Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol 2(2):103–121. doi:10.1038/mi.2008.85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus (2002) Classification of the Idiopathic Interstitial Pneumonias. Am J Respir Crit Care Med 165(2):277–304. doi:10.1164/ajrccm.165.2.ats01

    Article  Google Scholar 

  7. King TE Jr, Pardo A, Selman M (2011) Idiopathic pulmonary fibrosis. Lancet 378(9807):1949–1961. doi:10.1016/S0140-6736(11)60052-4

    Article  PubMed  Google Scholar 

  8. Hutchinson JP, McKeever TM, Fogarty AW, Navaratnam V, Hubbard RB (2014) Increasing global mortality from idiopathic pulmonary fibrosis in the twenty-first century. Ann Am Thorac Soc 11(8):1176–1185. doi:10.1513/AnnalsATS.201404-145OC

    Article  PubMed  Google Scholar 

  9. Martinez FJ, Safrin S, Weycker D, Starko KM, Bradford WZ, King TE Jr, Flaherty KR, Schwartz DA, Noble PW, Raghu G, Brown KK (2005) The clinical course of patients with idiopathic pulmonary fibrosis. Ann Intern Med 142(12 Pt 1):963–967

    Article  PubMed  Google Scholar 

  10. Trejo Bittar HE, Yousem SA, Wenzel SE (2015) Pathobiology of severe asthma. Annu Rev Pathol 10:511–545. doi:10.1146/annurev-pathol-012414-040343

    Article  CAS  PubMed  Google Scholar 

  11. Kuehnel M, Maegel L, Vogel-Claussen J, Robertus JL, Jonigk D (2017) Airway remodelling in the transplanted lung. Cell Tissue Res 367(3):663–675. doi:10.1007/s00441-016-2529-0

    Article  PubMed  Google Scholar 

  12. White ES, Xia M, Murray S, Dyal R, Flaherty CM, Flaherty KR, Moore BB, Cheng L, Doyle TJ, Villalba J, Dellaripa PF, Rosas IO, Kurtis JD, Martinez FJ (2016) Plasma surfactant protein-D, matrix metalloproteinase-7, and osteopontin Index distinguishes idiopathic pulmonary fibrosis from other idiopathic interstitial pneumonias. Am J Respir Crit Care Med 194(10):1242–1251. doi:10.1164/rccm.201505-0862OC

    Article  PubMed  Google Scholar 

  13. Bhattacharyya S, Wang W, Morales-Nebreda L, Feng G, Wu M, Zhou X, Lafyatis R, Lee J, Hinchcliff M, Feghali-Bostwick C, Lakota K, Budinger GR, Raparia K, Tamaki Z, Varga J (2016) Tenascin-C drives persistence of organ fibrosis. Nat Commun 7:11703. doi:10.1038/ncomms11703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chang W, Wei K, Jacobs SS, Upadhyay D, Weill D, Rosen GD (2010) SPARC suppresses apoptosis of idiopathic pulmonary fibrosis fibroblasts through constitutive activation of beta-catenin. J Biol Chem 285(11):8196–8206. doi:10.1074/jbc.M109.025684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14(7):1239–1249. doi:10.1359/jbmr.1999.14.7.1239

    Article  CAS  PubMed  Google Scholar 

  16. Takayama G, Arima K, Kanaji T, Toda S, Tanaka H, Shoji S, McKenzie AN, Nagai H, Hotokebuchi T, Izuhara K (2006) Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 118(1):98–104. doi:10.1016/j.jaci.2006.02.046

    Article  CAS  PubMed  Google Scholar 

  17. Ashley SL, Wilke CA, Kim KK, Moore BB (2017) Periostin regulates fibrocyte function to promote myofibroblast differentiation and lung fibrosis. Mucosal Immunol 10(2):341–351. doi:10.1038/mi.2016.61

    Article  CAS  PubMed  Google Scholar 

  18. Morra L, Rechsteiner M, Casagrande S, von Teichman A, Schraml P, Moch H, Soltermann A (2012) Characterization of periostin isoform pattern in non-small cell lung cancer. Lung Cancer 76(2):183–190. doi:10.1016/j.lungcan.2011.10.013

    Article  PubMed  Google Scholar 

  19. Ruan K, Bao S, Ouyang G (2009) The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66(14):2219–2230. doi:10.1007/s00018-009-0013-7

    Article  CAS  PubMed  Google Scholar 

  20. Naik PK, Bozyk PD, Bentley JK, Popova AP, Birch CM, Wilke CA, Fry CD, White ES, Sisson TH, Tayob N, Carnemolla B, Orecchia P, Flaherty KR, Hershenson MB, Murray S, Martinez FJ, Moore BB (2012) Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 303(12):L1046–L1056. doi:10.1152/ajplung.00139.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Okamoto M, Hoshino T, Kitasato Y, Sakazaki Y, Kawayama T, Fujimoto K, Ohshima K, Shiraishi H, Uchida M, Ono J, Ohta S, Kato S, Izuhara K, Aizawa H (2011) Periostin, a matrix protein, is a novel biomarker for idiopathic interstitial pneumonias. Eur Respir J 37(5):1119–1127. doi:10.1183/09031936.00059810

    Article  CAS  PubMed  Google Scholar 

  22. Ohta S, Okamoto M, Fujimoto K, Sakamoto N, Takahashi K, Yamamoto H, Kushima H, Ishii H, Akasaka K, Ono J, Kamei A, Azuma Y, Matsumoto H, Yamaguchi Y, Aihara M, Johkoh T, Kawaguchi A, Ichiki M, Sagara H, Kadota JI, Hanaoka M, Hayashi SI, Kohno S, Hoshino T, Izuhara K (2017) The usefulness of monomeric periostin as a biomarker for idiopathic pulmonary fibrosis. PLoS One 12(3):e0174547. doi:10.1371/journal.pone.0174547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. James A, Janson C, Malinovschi A, Holweg C, Alving K, Ono J, Ohta S, Ek A, Middelveld R, Dahlen B, Forsberg B, Izuhara K, Dahlen SE (2017) Serum periostin relates to type-2 inflammation and lung function in asthma: data from the large population-based cohort Swedish GA(2)LEN. Allergy. doi:10.1111/all.13181 (in press)

    PubMed  Google Scholar 

  24. Sood A, Qualls C, Schuyler M, Arynchyn A, Alvarado JH, Smith LJ, Jacobs DR Jr (2013) Adult-onset asthma becomes the dominant phenotype among women by age 40 years. The longitudinal CARDIA study. Ann Am Thorac Soc 10(3):188–197. doi:10.1513/AnnalsATS.201212-115OC

    Article  PubMed  PubMed Central  Google Scholar 

  25. Woodruff PG, Boushey HA, Dolganov GM, Barker CS, Yang YH, Donnelly S, Ellwanger A, Sidhu SS, Dao-Pick TP, Pantoja C, Erle DJ, Yamamoto KR, Fahy JV (2007) Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Proc Natl Acad Sci USA 104(40):15858–15863. doi:10.1073/pnas.0707413104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lopez-Guisa JM, Powers C, File D, Cochrane E, Jimenez N, Debley JS (2012) Airway epithelial cells from asthmatic children differentially express proremodeling factors. J Allergy Clin Immunol 129(4):990.e6–997.e6. doi:10.1016/j.jaci.2011.11.035

    Article  CAS  Google Scholar 

  27. Stokes JR, Casale TB (2016) Characterization of asthma endotypes: implications for therapy. Ann Allergy Asthma Immunol 117(2):121–125. doi:10.1016/j.anai.2016.05.016

    Article  CAS  PubMed  Google Scholar 

  28. Woodruff PG, Modrek B, Choy DF, Jia G, Abbas AR, Ellwanger A, Koth LL, Arron JR, Fahy JV (2009) T-helper type 2-driven inflammation defines major subphenotypes of asthma. Am J Respir Crit Care Med 180(5):388–395. doi:10.1164/rccm.200903-0392OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Antoniu SA (2016) Lebrikizumab for the treatment of asthma. Expert Opin Investig Drugs 25(10):1239–1249. doi:10.1080/13543784.2016.1227319

    Article  CAS  PubMed  Google Scholar 

  30. Sidhu SS, Yuan S, Innes AL, Kerr S, Woodruff PG, Hou L, Muller SJ, Fahy JV (2010) Roles of epithelial cell-derived periostin in TGF-beta activation, collagen production, and collagen gel elasticity in asthma. Proc Natl Acad Sci USA 107(32):14170–14175. doi:10.1073/pnas.1009426107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Johansson MW, Annis DS, Mosher DF (2013) alpha(M)beta(2) integrin-mediated adhesion and motility of IL-5-stimulated eosinophils on periostin. Am J Respir Cell Mol Biol 48(4):503–510. doi:10.1165/rcmb.2012-0150OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Blanchard C, Mingler MK, McBride M, Putnam PE, Collins MH, Chang G, Stringer K, Abonia JP, Molkentin JD, Rothenberg ME (2008) Periostin facilitates eosinophil tissue infiltration in allergic lung and esophageal responses. Mucosal Immunol 1(4):289–296. doi:10.1038/mi.2008.15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Matsusaka M, Kabata H, Fukunaga K, Suzuki Y, Masaki K, Mochimaru T, Sakamaki F, Oyamada Y, Inoue T, Oguma T, Sayama K, Koh H, Nakamura M, Umeda A, Ono J, Ohta S, Izuhara K, Asano K, Betsuyaku T (2015) Phenotype of asthma related with high serum periostin levels. Allergol Int 64(2):175–180. doi:10.1016/j.alit.2014.07.003

    Article  CAS  PubMed  Google Scholar 

  34. Jia G, Erickson RW, Choy DF, Mosesova S, Wu LC, Solberg OD, Shikotra A, Carter R, Audusseau S, Hamid Q, Bradding P, Fahy JV, Woodruff PG, Harris JM, Arron JR (2012) Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients. J Allergy Clin Immunol 130(3):647.e610–654.e610. doi:10.1016/j.jaci.2012.06.025

    Article  CAS  Google Scholar 

  35. Wang M, Wang X, Zhang N, Wang H, Li Y, Fan E, Zhang L, Zhang L, Bachert C (2015) Association of periostin expression with eosinophilic inflammation in nasal polyps. J Allergy Clin Immunol 136(6):1700.e1701–1703.e1709. doi:10.1016/j.jaci.2015.09.005

    Article  CAS  Google Scholar 

  36. Kim MA, Izuhara K, Ohta S, Ono J, Yoon MK, Ban GY, Yoo HS, Shin YS, Ye YM, Nahm DH, Park HS (2014) Association of serum periostin with aspirin-exacerbated respiratory disease. Ann Allergy Asthma Immunol 113(3):314–320. doi:10.1016/j.anai.2014.06.014

    Article  CAS  PubMed  Google Scholar 

  37. Hanania NA, Wenzel S, Rosen K, Hsieh HJ, Mosesova S, Choy DF, Lal P, Arron JR, Harris JM, Busse W (2013) Exploring the effects of omalizumab in allergic asthma: an analysis of biomarkers in the EXTRA study. Am J Respir Crit Care Med 187(8):804–811. doi:10.1164/rccm.201208-1414OC

    Article  CAS  PubMed  Google Scholar 

  38. Gordon ED, Sidhu SS, Wang ZE, Woodruff PG, Yuan S, Solon MC, Conway SJ, Huang X, Locksley RM, Fahy JV (2012) A protective role for periostin and TGF-beta in IgE-mediated allergy and airway hyperresponsiveness. Clin Exp Allergy 42(1):144–155. doi:10.1111/j.1365-2222.2011.03840.x

    Article  CAS  PubMed  Google Scholar 

  39. Sehra S, Yao W, Nguyen ET, Ahyi AN, Tuana FM, Ahlfeld SK, Snider P, Tepper RS, Petrache I, Conway SJ, Kaplan MH (2011) Periostin regulates goblet cell metaplasia in a model of allergic airway inflammation. J Immunol 186(8):4959–4966. doi:10.4049/jimmunol.1002359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Bentley JK, Chen Q, Hong JY, Popova AP, Lei J, Moore BB, Hershenson MB (2014) Periostin is required for maximal airways inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 134(6):1433–1442. doi:10.1016/j.jaci.2014.05.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Scheerens H, Arron JR, Zheng Y, Putnam WS, Erickson RW, Choy DF, Harris JM, Lee J, Jarjour NN, Matthews JG (2014) The effects of lebrikizumab in patients with mild asthma following whole lung allergen challenge. Clin Exp Allergy 44(1):38–46. doi:10.1111/cea.12220

    Article  CAS  PubMed  Google Scholar 

  42. Goodwin AT, Jenkins G (2016) Molecular endotyping of pulmonary fibrosis. Chest 149(1):228–237. doi:10.1378/chest.15-1511

    Article  PubMed  Google Scholar 

  43. Lama V, Moore BB, Christensen P, Toews GB, Peters-Golden M (2002) Prostaglandin E2 synthesis and suppression of fibroblast proliferation by alveolar epithelial cells is cyclooxygenase-2-dependent. Am J Respir Cell Mol Biol 27(6):752–758. doi:10.1165/rcmb.4857

    Article  CAS  PubMed  Google Scholar 

  44. Kolodsick JE, Peters-Golden M, Larios J, Toews GB, Thannickal VJ, Moore BB (2003) Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E. prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am J Respir Cell Mol Biol 29(5):537–544. doi:10.1165/rcmb.2002-0243OC

    Article  CAS  PubMed  Google Scholar 

  45. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmouliere A, Varga J, De Wever O, Mareel M, Gabbiani G (2012) Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 180(4):1340–1355. doi:10.1016/j.ajpath.2012.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Aschner Y, Downey GP (2016) Transforming growth factor-beta: master regulator of the respiratory system in health and disease. Am J Respir Cell Mol Biol 54(5):647–655. doi:10.1165/rcmb.2015-0391TR

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Thannickal VJ, Horowitz JC (2006) Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 3(4):350–356. doi:10.1513/pats.200601-001TK

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Loomis-King H, Moore BB (2013) Fibrocytes in the pathogenesis of chronic fibrotic lung disease. Curr Respir Med Rev 9(1):34–41

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lawson WE, Grant SW, Ambrosini V, Womble KE, Dawson EP, Lane KB, Markin C, Renzoni E, Lympany P, Thomas AQ, Roldan J, Scott TA, Blackwell TS, Phillips JA 3rd, Loyd JE, du Bois RM (2004) Genetic mutations in surfactant protein C are a rare cause of sporadic cases of IPF. Thorax 59(11):977–980. doi:10.1136/thx.2004.026336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, Markin C, Lawson WE, Xie M, Vulto I, Phillips JA 3rd, Lansdorp PM, Greider CW, Loyd JE (2007) Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med 356(13):1317–1326. doi:10.1056/NEJMoa066157

    Article  CAS  PubMed  Google Scholar 

  51. Naikawadi RP, Disayabutr S, Mallavia B, Donne ML, Green G, La JL, Rock JR, Looney MR, Wolters PJ (2016) Telomere dysfunction in alveolar epithelial cells causes lung remodeling and fibrosis. JCI Insight 1(14):e86704. doi:10.1172/jci.insight.86704

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bridges JP, Wert SE, Nogee LM, Weaver TE (2003) Expression of a human surfactant protein C mutation associated with interstitial lung disease disrupts lung development in transgenic mice. J Biol Chem 278(52):52739–52746. doi:10.1074/jbc.M309599200

    Article  CAS  PubMed  Google Scholar 

  53. Lawson WE, Cheng DS, Degryse AL, Tanjore H, Polosukhin VV, Xu XC, Newcomb DC, Jones BR, Roldan J, Lane KB, Morrisey EE, Beers MF, Yull FE, Blackwell TS (2011) Endoplasmic reticulum stress enhances fibrotic remodeling in the lungs. Proc Natl Acad Sci USA 108(26):10562–10567. doi:10.1073/pnas.1107559108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. O’Dwyer DN, Armstrong ME, Trujillo G, Cooke G, Keane MP, Fallon PG, Simpson AJ, Millar AB, McGrath EE, Whyte MK, Hirani N, Hogaboam CM, Donnelly SC (2013) The Toll-like receptor 3 L412F polymorphism and disease progression in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 188(12):1442–1450. doi:10.1164/rccm.201304-0760OC

    Article  PubMed  CAS  Google Scholar 

  55. Seibold MA, Wise AL, Speer MC, Steele MP, Brown KK, Loyd JE, Fingerlin TE, Zhang W, Gudmundsson G, Groshong SD, Evans CM, Garantziotis S, Adler KB, Dickey BF, du Bois RM, Yang IV, Herron A, Kervitsky D, Talbert JL, Markin C, Park J, Crews AL, Slifer SH, Auerbach S, Roy MG, Lin J, Hennessy CE, Schwarz MI, Schwartz DA (2011) A common MUC5B promoter polymorphism and pulmonary fibrosis. N Engl J Med 364(16):1503–1512. doi:10.1056/NEJMoa1013660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Noth I, Zhang Y, Ma SF, Flores C, Barber M, Huang Y, Broderick SM, Wade MS, Hysi P, Scuirba J, Richards TJ, Juan-Guardela BM, Vij R, Han MK, Martinez FJ, Kossen K, Seiwert SD, Christie JD, Nicolae D, Kaminski N, Garcia JG (2013) Genetic variants associated with idiopathic pulmonary fibrosis susceptibility and mortality: a genome-wide association study. Lancet Respir Med 1(4):309–317. doi:10.1016/S2213-2600(13)70045-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. O’Dwyer DN, Norman KC, Xia M, Huang Y, Gurczynski SJ, Ashley SL, White ES, Flaherty KR, Martinez FJ, Murray S, Noth I, Arnold KB, Moore BB (2017) The peripheral blood proteome signature of idiopathic pulmonary fibrosis is distinct from normal and is associated with novel immunological processes. Sci Rep 7:46560. doi:10.1038/srep46560

    Article  PubMed  PubMed Central  Google Scholar 

  58. Molyneaux PL, Cox MJ, Willis-Owen SA, Mallia P, Russell KE, Russell AM, Murphy E, Johnston SL, Schwartz DA, Wells AU, Cookson WO, Maher TM, Moffatt MF (2014) The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 190(8):906–913. doi:10.1164/rccm.201403-0541OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Han MK, Zhou Y, Murray S, Tayob N, Noth I, Lama VN, Moore BB, White ES, Flaherty KR, Huffnagle GB, Martinez FJ, Investigators C (2014) Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med 2(7):548–556. doi:10.1016/S2213-2600(14)70069-4

    Article  PubMed  PubMed Central  Google Scholar 

  60. Huang Y, Ma SF, Espindola MS, Vij R, Oldham JM, Huffnagle GB, Erb-Downward JR, Flaherty KR, Moore BB, White ES, Zhou T, Li J, Lussier YA, Han MK, Kaminski N, Garcia JG, Hogaboam CM, Martinez FJ, Noth I, Investigators C (2017) Microbes Associate with Host Innate Immune Response in Idiopathic Pulmonary Fibrosis. Am J Respir Crit Care Med. doi:10.1164/rccm.201607-1525OC (in press)

    Google Scholar 

  61. Raghu G, Freudenberger TD, Yang S, Curtis JR, Spada C, Hayes J, Sillery JK, Pope CE 2nd, Pellegrini CA (2006) High prevalence of abnormal acid gastro-oesophageal reflux in idiopathic pulmonary fibrosis. Eur Respir J 27(1):136–142. doi:10.1183/09031936.06.00037005

    Article  CAS  PubMed  Google Scholar 

  62. Moore BB, Moore TA (2015) Viruses in idiopathic pulmonary fibrosis. Etiology and exacerbation. Ann Am Thorac Soc 12(Suppl 2):S186–192. doi:10.1513/AnnalsATS.201502-088AW

    PubMed  PubMed Central  Google Scholar 

  63. Collard HR, Moore BB, Flaherty KR, Brown KK, Kaner RJ, King TE Jr, Lasky JA, Loyd JE, Noth I, Olman MA, Raghu G, Roman J, Ryu JH, Zisman DA, Hunninghake GW, Colby TV, Egan JJ, Hansell DM, Johkoh T, Kaminski N, Kim DS, Kondoh Y, Lynch DA, Muller-Quernheim J, Myers JL, Nicholson AG, Selman M, Toews GB, Wells AU, Martinez FJ (2007) Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 176(7):636–643. doi:10.1164/rccm.200703-463PP

    Article  PubMed  PubMed Central  Google Scholar 

  64. Moeller A, Gilpin SE, Ask K, Cox G, Cook D, Gauldie J, Margetts PJ, Farkas L, Dobranowski J, Boylan C, O’Byrne PM, Strieter RM, Kolb M (2009) Circulating fibrocytes are an indicator of poor prognosis in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 179(7):588–594. doi:10.1164/rccm.200810-1534OC

    Article  PubMed  Google Scholar 

  65. McDonald LT, Mehrotra M, LaRue AC (2015) Hematopoietic origin of murine lung fibroblasts. Stem Cells Int 2015:159713. doi:10.1155/2015/159713

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Kleaveland KR, Moore BB, Kim KK (2014) Paracrine functions of fibrocytes to promote lung fibrosis. Expert Rev Respir Med 8(2):163–172. doi:10.1586/17476348.2014.862154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A (1994) Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med 1(1):71–81

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Chesney J, Bacher M, Bender A, Bucala R (1997) The peripheral blood fibrocyte is a potent antigen-presenting cell capable of priming naive T cells in situ. Proc Natl Acad Sci USA 94(12):6307–6312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Chesney J, Metz C, Stavitsky AB, Bacher M, Bucala R (1998) Regulated production of type I collagen and inflammatory cytokines by peripheral blood fibrocytes. J Immunol 160(1):419–425

    CAS  PubMed  Google Scholar 

  70. Moore BB, Kolodsick JE, Thannickal VJ, Cooke K, Moore TA, Hogaboam C, Wilke CA, Toews GB (2005) CCR2-mediated recruitment of fibrocytes to the alveolar space after fibrotic injury. Am J Pathol 166(3):675–684. doi:10.1016/S0002-9440(10)62289-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Moore BB, Murray L, Das A, Wilke CA, Herrygers AB, Toews GB (2006) The role of CCL12 in the recruitment of fibrocytes and lung fibrosis. Am J Respir Cell Mol Biol 35(2):175–181. doi:10.1165/rcmb.2005-0239OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY, Belperio JA, Keane MP, Strieter RM (2004) Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest 114(3):438–446. doi:10.1172/JCI20997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Madsen DH, Ingvarsen S, Jurgensen HJ, Melander MC, Kjoller L, Moyer A, Honore C, Madsen CA, Garred P, Burgdorf S, Bugge TH, Behrendt N, Engelholm LH (2011) The non-phagocytic route of collagen uptake: a distinct degradation pathway. J Biol Chem 286(30):26996–27010. doi:10.1074/jbc.M110.208033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bianchetti L, Barczyk M, Cardoso J, Schmidt M, Bellini A, Mattoli S (2012) Extracellular matrix remodelling properties of human fibrocytes. J Cell Mol Med 16(3):483–495. doi:10.1111/j.1582-4934.2011.01344.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kleaveland KR, Velikoff M, Yang J, Agarwal M, Rippe RA, Moore BB, Kim KK (2014) Fibrocytes are not an essential source of type I collagen during lung fibrosis. J Immunol 193(10):5229–5239. doi:10.4049/jimmunol.1400753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN (2001) Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 166(12):7556–7562

    Article  CAS  PubMed  Google Scholar 

  77. Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S (2003) Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J Immunol 171(1):380–389

    Article  CAS  PubMed  Google Scholar 

  78. Hashimoto N, Jin H, Liu T, Chensue SW, Phan SH (2004) Bone marrow-derived progenitor cells in pulmonary fibrosis. J Clin Invest 113(2):243–252. doi:10.1172/jci18847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Tanjore H, Xu XC, Polosukhin VV, Degryse AL, Li B, Han W, Sherrill TP, Plieth D, Neilson EG, Blackwell TS, Lawson WE (2009) Contribution of epithelial-derived fibroblasts to bleomycin-induced lung fibrosis. Am J Respir Crit Care Med 180(7):657–665. doi:10.1164/rccm.200903-0322OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Xu J, Kisseleva T (2015) Bone marrow-derived fibrocytes contribute to liver fibrosis. Exp Biol Med (Maywood) 240(6):691–700. doi:10.1177/1535370215584933

    Article  CAS  Google Scholar 

  81. Xu J, Cong M, Park TJ, Scholten D, Brenner DA, Kisseleva T (2015) Contribution of bone marrow-derived fibrocytes to liver fibrosis. Hepatobiliary Surg Nutr 4(1):34–47. doi:10.3978/j.issn.2304-3881.2015.01.01

    PubMed  PubMed Central  Google Scholar 

  82. Garcia de Alba C, Buendia-Roldan I, Salgado A, Becerril C, Ramirez R, Gonzalez Y, Checa M, Navarro C, Ruiz V, Pardo A, Selman M (2015) Fibrocytes contribute to inflammation and fibrosis in chronic hypersensitivity pneumonitis through paracrine effects. Am J Respir Crit Care Med 191(4):427–436. doi:10.1164/rccm.201407-1334OC

    Article  CAS  PubMed  Google Scholar 

  83. Moore BB, Kolb M (2014) Fibrocytes and progression of fibrotic lung disease. Ready for showtime? Am J Respir Crit Care Med 190(12):1338–1339. doi:10.1164/rccm.201411-2013ED

    Article  PubMed  Google Scholar 

  84. Madala SK, Edukulla R, Schmidt S, Davidson C, Ikegami M, Hardie WD (2014) Bone marrow-derived stromal cells are invasive and hyperproliferative and alter transforming growth factor-alpha-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 50(4):777–786. doi:10.1165/rcmb.2013-0042OC

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Nance T, Smith KS, Anaya V, Richardson R, Ho L, Pala M, Mostafavi S, Battle A, Feghali-Bostwick C, Rosen G, Montgomery SB (2014) Transcriptome analysis reveals differential splicing events in IPF lung tissue. PLoS One 9(3):e92111. doi:10.1371/journal.pone.0092111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Walsh JS, Gossiel F, Scott JR, Paggiosi MA, Eastell R (2017) Effect of age and gender on serum periostin: relationship to cortical measures, bone turnover and hormones. Bone 99:8–13. doi:10.1016/j.bone.2017.03.041

    Article  CAS  PubMed  Google Scholar 

  87. Khalil N, O’Connor R, Unruh H, Warren P, Kemp A, Greenberg A (1991) Enhanced expression and immunohistochemical distribution of transforming growth factor-beta in idiopathic pulmonary fibrosis. Chest 99(3 Suppl):65S–66S

    Article  CAS  PubMed  Google Scholar 

  88. Khalil N, O’Connor RN, Unruh HW, Warren PW, Flanders KC, Kemp A, Bereznay OH, Greenberg AH (1991) Increased production and immunohistochemical localization of transforming growth factor-beta in idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 5(2):155–162

    Article  CAS  PubMed  Google Scholar 

  89. Passalacqua G, Mincarini M, Colombo D, Troisi G, Ferrari M, Bagnasco D, Balbi F, Riccio A, Canonica GW (2017) IL-13 and idiopathic pulmonary fibrosis: possible links and new therapeutic strategies. Pulm Pharmacol Ther. doi:10.1016/j.pupt.2017.05.007

    PubMed  Google Scholar 

  90. Maruhashi T, Kii I, Saito M, Kudo A (2010) Interaction between periostin and BMP-1 promotes proteolytic activation of lysyl oxidase. J Biol Chem 285(17):13294–13303. doi:10.1074/jbc.M109.088864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Tschumperlin DJ, Jones JC, Senior RM (2012) The fibrotic matrix in control: does the extracellular matrix drive progression of idiopathic pulmonary fibrosis? Am J Respir Crit Care Med 186(9):814–816. doi:10.1164/rccm.201208-1561ED

    Article  CAS  PubMed  Google Scholar 

  92. Shulgina L, Cahn AP, Chilvers ER, Parfrey H, Clark AB, Wilson EC, Twentyman OP, Davison AG, Curtin JJ, Crawford MB, Wilson AM (2013) Treating idiopathic pulmonary fibrosis with the addition of co-trimoxazole: a randomised controlled trial. Thorax 68(2):155–162. doi:10.1136/thoraxjnl-2012-202403

    Article  PubMed  Google Scholar 

  93. Komiya K, Ohta S, Arima K, Ogawa M, Suzuki S, Mitamura Y, Nunomura S, Nanri Y, Yoshihara T, Kawaguchi A, Kadota JI, Rubin BK, Izuhara K (2017) Clarithromycin attenuates IL-13-induced periostin production in human lung fibroblasts. Respir Res 18(1):37. doi:10.1186/s12931-017-0519-8

    Article  PubMed  PubMed Central  Google Scholar 

  94. Moore B, Lawson WE, Oury TD, Sisson TH, Raghavendran K, Hogaboam CM (2013) Animal models of fibrotic lung disease. Am J Respir Cell Mol Biol 49(2):167–179. doi:10.1165/rcmb.2013-0094TR

    Article  CAS  Google Scholar 

  95. Jenkins RG, Moore BB, Chambers RC, Eickelberg O, Konigshoff M, Kolb M, Laurent GJ, Nanthakumar CB, Olman MA, Pardo A, Selman M, Sheppard D, Sime PJ, Tager AM, Tatler AL, Thannickal VJ, White ES (2017) An official American Thoracic Society Workshop Report: use of animal models for the preclinical assessment of potential therapies for pulmonary fibrosis. Am J Respir Cell Mol Biol 56(5):667–679. doi:10.1165/rcmb.2017-0096ST

    Article  PubMed  Google Scholar 

  96. Uchida M, Shiraishi H, Ohta S, Arima K, Taniguchi K, Suzuki S, Okamoto M, Ahlfeld SK, Ohshima K, Kato S, Toda S, Sagara H, Aizawa H, Hoshino T, Conway SJ, Hayashi S, Izuhara K (2012) Periostin, a matricellular protein, plays a role in the induction of chemokines in pulmonary fibrosis. Am J Respir Cell Mol Biol 46(5):677–686. doi:10.1165/rcmb.2011-0115OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Chen B, You WJ, Liu XQ, Xue S, Qin H, Jiang HD (2017) Chronic microaspiration of bile acids induces lung fibrosis through multiple mechanisms in rats. Clin Sci (Lond) 131(10):951–963. doi:10.1042/cs20160926

    Article  CAS  Google Scholar 

  98. Akram KM, Samad S, Spiteri MA, Forsyth NR (2013) Mesenchymal stem cells promote alveolar epithelial cell wound repair in vitro through distinct migratory and paracrine mechanisms. Respir Res 14:9. doi:10.1186/1465-9921-14-9

    Article  PubMed  PubMed Central  Google Scholar 

  99. Hong L, Sun H, Lv X, Yang D, Zhang J, Shi Y (2010) Expression of periostin in the serum of NSCLC and its function on proliferation and migration of human lung adenocarcinoma cell line (A549) in vitro. Mol Biol Rep 37(5):2285–2293. doi:10.1007/s11033-009-9721-1

    Article  CAS  PubMed  Google Scholar 

  100. Chetta A, Zanini A, Foresi A, D’Ippolito R, Tipa A, Castagnaro A, Baraldo S, Neri M, Saetta M, Olivieri D (2005) Vascular endothelial growth factor up-regulation and bronchial wall remodelling in asthma. Clin Exp Allergy 35(11):1437–1442. doi:10.1111/j.1365-2222.2005.02360.x

    Article  CAS  PubMed  Google Scholar 

  101. Suzaki I, Kawano S, Komiya K, Tanabe T, Akaba T, Asano K, Suzaki H, Izuhara K, Rubin BK (2017) Inhibition of IL-13-induced periostin in airway epithelium attenuates cellular protein expression of MUC5AC. Respirology 22(1):93–100. doi:10.1111/resp.12873

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Funded by NIH HL115618 (Moore, B.).

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, University of Michigan, 4053 BSRB, 109 Zina Pitcher Place, Ann Arbor, MI, 48109-2200, USA

    David N. O’Dwyer & Bethany B. Moore

  2. Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI, USA

    Bethany B. Moore

Authors
  1. David N. O’Dwyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bethany B. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bethany B. Moore.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

O’Dwyer, D.N., Moore, B.B. The role of periostin in lung fibrosis and airway remodeling. Cell. Mol. Life Sci. 74, 4305–4314 (2017). https://doi.org/10.1007/s00018-017-2649-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-017-2649-z

Keywords

Search

Navigation