Advertisement

Periostin: The bone and beyond

Published:December 06, 2016DOI:https://doi.org/10.1016/j.ejim.2016.11.015

      Highlights

      • PO is a multifunctional protein and its expression is enhanced by mechanical stress.
      • Its overexpression was observed in inflammation, fibrosis and tumorigenesis.
      • PO expression correlates with lung diseases.
      • PO seems to play an important role in the epidermal hyperplasia process.
      • Po is involved in various phases of bone repair and fracture healing.

      Abstract

      In recent years the relationship between bone, metabolism and many pathophysiologic mechanisms involving other organs and the immune system, was increasingly apparent. This observation concerns vitamin D, osteopontin and periostin (PO). PO is expressed in the periosteum of long bones but also in many other tissues and organs, including heart, kidney, skin and lungs, being enhanced by mechanical stress or injury. PO has a relevant physiological function in promoting injury repair in a large number of tissues. However, its overexpression was observed in different diseases characterized by inflammation, fibrosis and tumorigenesis. Here we review the current knowledge on the role of PO in physiologic and pathologic pathways of different diseases. A specific focus regards the correlation between the level of PO and lung diseases and the identification of PO also as an inflammatory key effector in asthma, strongly associated with airways eosinophilia. In fact PO seems to be a useful biomarker of “Th2-high” asthma compared to “Th2-low” asthma phenotype and a predictor of response to therapeutic agents. Currently, a growing number of studies suggests a possible role of PO as a new diagnostic marker and/or therapeutic target for different diseases and its usefulness in clinical practice should be supported and confirmed by further and larger studies.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to European Journal of Internal Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bonnet N.
        • Garnero P.
        • Ferrari S.
        Periostin action in bone.
        Mol Cell Endocrinol. 2016; 432: 75-82https://doi.org/10.1016/j.mce.2015.12.014
        • Coutu D.L.
        • Wu J.H.
        • Monette A.
        • Rivard G.-E.
        • Blostein M.D.
        • Galipeau J.
        Periostin, a member of a novel family of vitamin K-dependent proteins, is expressed by mesenchymal stromal cells.
        J Biol Chem. 2008; 283: 17991-18001https://doi.org/10.1074/jbc.M708029200
        • Annis D.S.
        • Ma H.
        • Balas D.M.
        • Kumfer K.T.
        • Sandbo N.
        • Potts G.K.
        • et al.
        Absence of vitamin K-dependent γ-carboxylation in human periostin extracted from fibrotic lung or secreted from a cell line engineered to optimize γ-carboxylation.
        PLoS One. 2015; 10e0135374https://doi.org/10.1371/journal.pone.0135374
        • Liu A.Y.
        • Zheng H.
        • Ouyang G.
        Periostin, a multifunctional matricellular protein in inflammatory and tumor microenvironments.
        Matrix Biol. 2014; 37: 150-156https://doi.org/10.1016/j.matbio.2014.04.007
        • Norris R.A.
        • Damon B.
        • Mironov V.
        • Kasyanov V.
        • Ramamurthi A.
        • Moreno-Rodriguez R.
        • et al.
        Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues.
        J Cell Biochem. 2007; 101: 695-711https://doi.org/10.1002/jcb.21224
        • Parfitt A.M.
        Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression.
        Bone. 2002; 30: 5-7
        • Ruan K.
        • Bao S.
        • Ouyang G.
        The multifaceted role of periostin in tumorigenesis.
        Cell Mol Life Sci. 2009; 66: 2219-2230https://doi.org/10.1007/s00018-009-0013-7
        • Bonewald L.F.
        The amazing osteocyte.
        J Bone Miner Res. 2011; 26: 229-238https://doi.org/10.1002/jbmr.320
        • Rossini M.
        • Gatti D.
        • Adami S.
        Involvement of WNT/β-catenin signaling in the treatment of osteoporosis.
        Calcif Tissue Int. 2013; 93: 121-132https://doi.org/10.1007/s00223-013-9749-z
        • Bonnet N.
        • Standley K.N.
        • Bianchi E.N.
        • Stadelmann V.
        • Foti M.
        • Conway S.J.
        • et al.
        The matricellular protein periostin is required for sost inhibition and the anabolic response to mechanical loading and physical activity.
        J Biol Chem. 2009; 284: 35939-35950https://doi.org/10.1074/jbc.M109.060335
        • Bonnet N.
        • Conway S.J.
        • Ferrari S.L.
        Regulation of beta catenin signaling and parathyroid hormone anabolic effects in bone by the matricellular protein periostin.
        Proc Natl Acad Sci U S A. 2012; 109: 15048-15053https://doi.org/10.1073/pnas.1203085109
        • Gerbaix M.
        • Vico L.
        • Ferrari S.L.
        • Bonnet N.
        Periostin expression contributes to cortical bone loss during unloading.
        Bone. 2015; 71: 94-100https://doi.org/10.1016/j.bone.2014.10.011
        • Kim B.-J.
        • Rhee Y.
        • Kim C.H.
        • Baek K.H.
        • Min Y.-K.
        • Kim D.-Y.
        • et al.
        Plasma periostin associates significantly with non-vertebral but not vertebral fractures in postmenopausal women: clinical evidence for the different effects of periostin depending on the skeletal site.
        Bone. 2015; 81: 435-441https://doi.org/10.1016/j.bone.2015.08.014
        • Conway S.J.
        • Izuhara K.
        • Kudo Y.
        • Litvin J.
        • Markwald R.
        • Ouyang G.
        • et al.
        The role of periostin in tissue remodeling across health and disease.
        Cell Mol Life Sci. 2014; 71: 1279-1288https://doi.org/10.1007/s00018-013-1494-y
        • Venning F.A.
        • Wullkopf L.
        • Erler J.T.
        Targeting ECM disrupts cancer progression.
        Front Oncol. 2015; 5: 224https://doi.org/10.3389/fonc.2015.00224
        • Morra L.
        • Moch H.
        Periostin expression and epithelial-mesenchymal transition in cancer: a review and an update.
        Virchows Arch Int J Pathol. 2011; 459: 465-475https://doi.org/10.1007/s00428-011-1151-5
        • Lindsley A.
        • Snider P.
        • Zhou H.
        • Rogers R.
        • Wang J.
        • Olaopa M.
        • et al.
        Identification and characterization of a novel Schwann and outflow tract endocardial cushion lineage-restricted periostin enhancer.
        Dev Biol. 2007; 307: 340-355https://doi.org/10.1016/j.ydbio.2007.04.041
        • Guarino M.
        Epithelial-mesenchymal transition and tumour invasion.
        Int J Biochem Cell Biol. 2007; 39: 2153-2160https://doi.org/10.1016/j.biocel.2007.07.011
        • Hu F.
        • Shang X.-F.
        • Wang W.
        • Jiang W.
        • Fang C.
        • Tan D.
        • et al.
        High-level expression of periostin is significantly correlated with tumour angiogenesis and poor prognosis in osteosarcoma.
        Int J Exp Pathol. 2016; 97: 86-92https://doi.org/10.1111/iep.12171
        • Kühn B.
        • del Monte F.
        • Hajjar R.J.
        • Chang Y.-S.
        • Lebeche D.
        • Arab S.
        • et al.
        Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair.
        Nat Med. 2007; 13: 962-969https://doi.org/10.1038/nm1619
        • Shimazaki M.
        • Nakamura K.
        • Kii I.
        • Kashima T.
        • Amizuka N.
        • Li M.
        • et al.
        Periostin is essential for cardiac healing after acute myocardial infarction.
        J Exp Med. 2008; 205: 295-303https://doi.org/10.1084/jem.20071297
        • Lindner V.
        • Wang Q.
        • Conley B.A.
        • Friesel R.E.
        • Vary C.P.H.
        Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration.
        Arterioscler Thromb Vasc Biol. 2005; 25: 77-83https://doi.org/10.1161/01.ATV.0000149141.81230.c6
        • Bagnato C.
        • Thumar J.
        • Mayya V.
        • Hwang S.-I.
        • Zebroski H.
        • Claffey K.P.
        • et al.
        Proteomics analysis of human coronary atherosclerotic plaque: a feasibility study of direct tissue proteomics by liquid chromatography and tandem mass spectrometry.
        Mol Cell Proteomics. 2007; 6: 1088-1102https://doi.org/10.1074/mcp.M600259-MCP200
        • Hakuno D.
        • Kimura N.
        • Yoshioka M.
        • Mukai M.
        • Kimura T.
        • Okada Y.
        • et al.
        Periostin advances atherosclerotic and rheumatic cardiac valve degeneration by inducing angiogenesis and MMP production in humans and rodents.
        J Clin Invest. 2010; 120: 2292-2306https://doi.org/10.1172/JCI40973
        • Zhao S.
        • Wu H.
        • Xia W.
        • Chen X.
        • Zhu S.
        • Zhang S.
        • et al.
        Periostin expression is upregulated and associated with myocardial fibrosis in human failing hearts.
        J Cardiol. 2014; 63: 373-378https://doi.org/10.1016/j.jjcc.2013.09.013
        • Mael-Ainin M.
        • Abed A.
        • Conway S.J.
        • Dussaule J.-C.
        • Chatziantoniou C.
        Inhibition of periostin expression protects against the development of renal inflammation and fibrosis.
        J Am Soc Nephrol. 2014; 25: 1724-1736https://doi.org/10.1681/ASN.2013060664
        • Bible E.
        Polycystic kidney disease: periostin is involved in cell proliferation and interstitial fibrosis in polycystic kidney disease.
        Nat Rev Nephrol. 2014; 10: 66https://doi.org/10.1038/nrneph.2013.270
        • Guerrot D.
        • Dussaule J.-C.
        • Mael-Ainin M.
        • Xu-Dubois Y.-C.
        • Rondeau E.
        • Chatziantoniou C.
        • et al.
        Identification of periostin as a critical marker of progression/reversal of hypertensive nephropathy.
        PLoS One. 2012; 7e31974https://doi.org/10.1371/journal.pone.0031974
        • Wantanasiri P.
        • Satirapoj B.
        • Charoenpitakchai M.
        • Aramwit P.
        Periostin: a novel tissue biomarker correlates with chronicity index and renal function in lupus nephritis patients.
        Lupus. 2015; 24: 835-845https://doi.org/10.1177/0961203314566634
        • Satirapoj B.
        • Tassanasorn S.
        • Charoenpitakchai M.
        • Supasyndh O.
        Periostin as a tissue and urinary biomarker of renal injury in type 2 diabetes mellitus.
        PLoS One. 2015; 10e0124055https://doi.org/10.1371/journal.pone.0124055
        • Walker J.T.
        • McLeod K.
        • Kim S.
        • Conway S.J.
        • Hamilton D.W.
        Periostin as a multifunctional modulator of the wound healing response.
        Cell Tissue Res. 2016; 365: 453-465https://doi.org/10.1007/s00441-016-2426-6
        • Yamaguchi Y.
        • Ono J.
        • Masuoka M.
        • Ohta S.
        • Izuhara K.
        • Ikezawa Z.
        • et al.
        Serum periostin levels are correlated with progressive skin sclerosis in patients with systemic sclerosis.
        Br J Dermatol. 2013; 168: 717-725https://doi.org/10.1111/bjd.12117
        • Yamaguchi Y.
        Periostin in skin tissue and skin-related diseases.
        Allergol Int. 2014; 63: 161-170https://doi.org/10.2332/allergolint.13-RAI-0685
        • Kou K.
        • Okawa T.
        • Yamaguchi Y.
        • Ono J.
        • Inoue Y.
        • Kohno M.
        • et al.
        Periostin levels correlate with disease severity and chronicity in patients with atopic dermatitis.
        Br J Dermatol. 2014; 171: 283-291https://doi.org/10.1111/bjd.12943
        • Guttman-Yassky E.
        • Nograles K.E.
        • Krueger J.G.
        Contrasting pathogenesis of atopic dermatitis and psoriasis–part I: clinical and pathologic concepts.
        J Allergy Clin Immunol. 2011; 127: 1110-1118https://doi.org/10.1016/j.jaci.2011.01.053
        • Arima K.
        • Ohta S.
        • Takagi A.
        • Shiraishi H.
        • Masuoka M.
        • Ontsuka K.
        • et al.
        Periostin contributes to epidermal hyperplasia in psoriasis common to atopic dermatitis.
        Allergol Int. 2015; 64: 41-48https://doi.org/10.1016/j.alit.2014.06.001
        • Izuhara K.
        • Conway S.J.
        • Moore B.B.
        • Matsumoto H.
        • Holweg C.T.J.
        • Matthews J.G.
        • et al.
        Roles of periostin in respiratory disorders.
        Am J Respir Crit Care Med. 2016; 193: 949-956https://doi.org/10.1164/rccm.201510-2032PP
        • Suzaki I.
        • Kawano S.
        • Komiya K.
        • Tanabe T.
        • Akaba T.
        • Asano K.
        • et al.
        Inhibition of IL-13-induced periostin in airway epithelium attenuates cellular protein expression of MUC5AC.
        Respirology (Carlton Vic). 2016; https://doi.org/10.1111/resp.12873
        • Wang M.
        • Wang X.
        • Zhang N.
        • Wang H.
        • Li Y.
        • Fan E.
        • et al.
        Association of periostin expression with eosinophilic inflammation in nasal polyps.
        J Allergy Clin Immunol. 2015; 136 ([1700-1703-9])https://doi.org/10.1016/j.jaci.2015.09.005
        • Uchida M.
        • Shiraishi H.
        • Ohta S.
        • Arima K.
        • Taniguchi K.
        • Suzuki S.
        • et al.
        Periostin, a matricellular protein, plays a role in the induction of chemokines in pulmonary fibrosis.
        Am J Respir Cell Mol Biol. 2012; 46: 677-686https://doi.org/10.1165/rcmb.2011-0115OC
        • Ashley S.L.
        • Wilke C.A.
        • Kim K.K.
        • Moore B.B.
        Periostin regulates fibrocyte function to promote myofibroblast differentiation and lung fibrosis.
        Mucosal Immunol. 2016; https://doi.org/10.1038/mi.2016.61
        • Jia G.
        • Erickson R.W.
        • Choy D.F.
        • Mosesova S.
        • Wu L.C.
        • Solberg O.D.
        • et al.
        Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients.
        J Allergy Clin Immunol. 2012; 130 ([647–654.e10])https://doi.org/10.1016/j.jaci.2012.06.025
        • Nair P.
        • Kraft M.
        Serum periostin as a marker of T(H)2-dependent eosinophilic airway inflammation.
        J Allergy Clin Immunol. 2012; 130: 655-656https://doi.org/10.1016/j.jaci.2012.07.021
        • Takayama G.
        • Arima K.
        • Kanaji T.
        • Toda S.
        • Tanaka H.
        • Shoji S.
        • et al.
        Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals.
        J Allergy Clin Immunol. 2006; 118: 98-104https://doi.org/10.1016/j.jaci.2006.02.046
        • Sidhu S.S.
        • Yuan S.
        • Innes A.L.
        • Kerr S.
        • Woodruff P.G.
        • Hou L.
        • et al.
        Roles of epithelial cell-derived periostin in TGF-beta activation, collagen production, and collagen gel elasticity in asthma.
        Proc Natl Acad Sci U S A. 2010; 107: 14170-14175https://doi.org/10.1073/pnas.1009426107
        • Blanchard C.
        • Mingler M.K.
        • McBride M.
        • Putnam P.E.
        • Collins M.H.
        • Chang G.
        • et al.
        Periostin facilitates eosinophil tissue infiltration in allergic lung and esophageal responses.
        Mucosal Immunol. 2008; 1: 289-296https://doi.org/10.1038/mi.2008.15
        • Chiappori A.
        • De Ferrari L.
        • Folli C.
        • Mauri P.
        • Riccio A.M.
        • Canonica G.W.
        Biomarkers and severe asthma: a critical appraisal.
        Clin Mol Allergy. 2015; 13: 20https://doi.org/10.1186/s12948-015-0027-7
        • Wagener A.H.
        • de Nijs S.B.
        • Lutter R.
        • Sousa A.R.
        • Weersink E.J.M.
        • Bel E.H.
        • et al.
        External validation of blood eosinophils, FE(NO) and serum periostin as surrogates for sputum eosinophils in asthma.
        Thorax. 2015; 70: 115-120https://doi.org/10.1136/thoraxjnl-2014-205634
        • Matsusaka M.
        • Kabata H.
        • Fukunaga K.
        • Suzuki Y.
        • Masaki K.
        • Mochimaru T.
        • et al.
        Phenotype of asthma related with high serum periostin levels.
        Allergol Int. 2015; 64: 175-180https://doi.org/10.1016/j.alit.2014.07.003
        • Kanemitsu Y.
        • Matsumoto H.
        • Izuhara K.
        • Tohda Y.
        • Kita H.
        • Horiguchi T.
        • et al.
        Increased periostin associates with greater airflow limitation in patients receiving inhaled corticosteroids.
        J Allergy Clin Immunol. 2013; 132 ([305–312.e3])https://doi.org/10.1016/j.jaci.2013.04.050
        • Kimura H.
        • Suzuki M.
        • Konno S.
        • Nishimura M.
        • Bobolea I.
        • Barranco P.
        • et al.
        Sputum periostin in patients with different severe asthma phenotypes.
        Allergy. 2015; 70: 884-885https://doi.org/10.1111/all.12639
        • Corren J.
        • Lemanske R.F.
        • Hanania N.A.
        • Korenblat P.E.
        • Parsey M.V.
        • Arron J.R.
        • et al.
        Lebrikizumab treatment in adults with asthma.
        N Engl J Med. 2011; 365: 1088-1098https://doi.org/10.1056/NEJMoa1106469
        • Hanania N.A.
        • Wenzel S.
        • Rosén K.
        • Hsieh H.-J.
        • Mosesova S.
        • Choy D.F.
        • et al.
        Exploring the effects of omalizumab in allergic asthma: an analysis of biomarkers in the EXTRA study.
        Am J Respir Crit Care Med. 2013; 187: 804-811https://doi.org/10.1164/rccm.201208-1414OC
        • Parulekar A.D.
        • Atik M.A.
        • Hanania N.A.
        Periostin, a novel biomarker of TH2-driven asthma.
        Curr Opin Pulm Med. 2014; 20: 60-65https://doi.org/10.1097/MCP.0000000000000005
        • Fingleton J.
        • Braithwaite I.
        • Travers J.
        • Bowles D.
        • Strik R.
        • Siebers R.
        • et al.
        Serum periostin in obstructive airways disease.
        Eur Respir J. 2016; 47: 1383-1391https://doi.org/10.1183/13993003.01384-2015
        • Daines S.M.
        • Wang Y.
        • Orlandi R.R.
        Periostin and osteopontin are overexpressed in chronically inflamed sinuses.
        Int Forum Allergy Rhinol. 2011; 1: 101-105https://doi.org/10.1002/alr.20031
        • Weitzmann M.N.
        • Ofotokun I.
        Physiological and pathophysiological bone turnover - role of the immune system.
        Nat Rev Endocrinol. 2016; 12: 518-532https://doi.org/10.1038/nrendo.2016.91
        • Mirzakhani H.
        • Al-Garawi A.
        • Weiss S.T.
        • Litonjua A.A.
        Vitamin D and the development of allergic disease: how important is it?.
        Clin Exp Allergy. 2015; 45: 114-125https://doi.org/10.1111/cea.12430
        • Vig M.
        • Kinet J.-P.
        Calcium signaling in immune cells.
        Nat Immunol. 2009; 10: 21-27https://doi.org/10.1038/ni.f.220
        • Wang K.X.
        • Denhardt D.T.
        Osteopontin: role in immune regulation and stress responses.
        Cytokine Growth Factor Rev. 2008; 19: 333-345https://doi.org/10.1016/j.cytogfr.2008.08.001
        • Konno S.
        • Kurokawa M.
        • Uede T.
        • Nishimura M.
        • Huang S.-K.
        Role of osteopontin, a multifunctional protein, in allergy and asthma.
        Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2011; 41: 1360-1366https://doi.org/10.1111/j.1365-2222.2011.03775.x
        • Kanemitsu Y.
        • Ito I.
        • Niimi A.
        • Izuhara K.
        • Ohta S.
        • Ono J.
        • et al.
        Osteopontin and periostin are associated with a 20-year decline of pulmonary function in patients with asthma.
        Am J Respir Crit Care Med. 2014; 190: 472-474https://doi.org/10.1164/rccm.201403-0562LE