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Periostin and its interacting proteins in the construction of extracellular architectures

  • Multi-author review
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Abstract

Periostin is a matricellular protein that is composed of a multi-domain structure with an amino-terminal EMI domain, a tandem repeat of four FAS 1 domains, and a carboxyl-terminal domain. These distinct domains have been demonstrated to bind to many proteins including extracellular matrix proteins (Collagen type I and V, fibronectin, tenascin, and laminin), matricellular proteins (CCN3 and βig-h3), and enzymes that catalyze covalent crosslinking between extracellular matrix proteins (lysyl oxidase and BMP-1). Adjacent binding sites on periostin have been suggested to put the interacting proteins in close proximity, promoting intermolecular interactions between each protein, and leading to their assembly into extracellular architectures. These extracellular architectures determine the mechanochemical properties of connective tissues, in which periostin plays an important role in physiological homeostasis and disease progression. In this review, we introduce the proteins that interact with periostin, and discuss how the multi-domain structure of periostin functions as a scaffold for the assembly of interacting proteins, and how it underlies construction of highly sophisticated extracellular architectures.

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References

  1. 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 

  2. 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 

  3. Sugiura T, Takamatsu H, Kudo A, Amann E (1995) Expression and characterization of murine osteoblast-specific factor 2 (OSF-2) in a baculovirus expression system. Protein Expr Purif 6(3):305–311. doi:10.1006/prep.1995.1040

    Article  CAS  PubMed  Google Scholar 

  4. Hoersch S, Andrade-Navarro MA (2010) Periostin shows increased evolutionary plasticity in its alternatively spliced region. BMC Evol Biol 10:30. doi:10.1186/1471-2148-10-30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Elliott CG, Hamilton DW (2011) Deconstructing fibrosis research: do pro-fibrotic signals point the way for chronic dermal wound regeneration? J Cell Commun Signal 5(4):301–315. doi:10.1007/s12079-011-0131-5

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kii I, Nishiyama T, Li M, Matsumoto K, Saito M, Amizuka N, Kudo A (2010) Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J Biol Chem 285(3):2028–2039. doi:10.1074/jbc.M109.051961

    Article  CAS  PubMed  Google Scholar 

  7. 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 

  8. Snider P, Hinton RB, Moreno-Rodriguez RA, Wang J, Rogers R, Lindsley A, Li F, Ingram DA, Menick D, Field L, Firulli AB, Molkentin JD, Markwald R, Conway SJ (2008) Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ Res 102(7):752–760. doi:10.1161/CIRCRESAHA.107.159517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Shimazaki M, Nakamura K, Kii I, Kashima T, Amizuka N, Li M, Saito M, Fukuda K, Nishiyama T, Kitajima S, Saga Y, Fukayama M, Sata M, Kudo A (2008) Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 205(2):295–303. doi:10.1084/jem.20071297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kii I, Amizuka N, Minqi L, Kitajima S, Saga Y, Kudo A (2006) Periostin is an extracellular matrix protein required for eruption of incisors in mice. Biochem Biophys Res Commun 342(3):766–772. doi:10.1016/j.bbrc.2006.02.016

    Article  CAS  PubMed  Google Scholar 

  11. Rios H, Koushik SV, Wang H, Wang J, Zhou HM, Lindsley A, Rogers R, Chen Z, Maeda M, Kruzynska-Frejtag A, Feng JQ, Conway SJ (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25(24):11131–11144. doi:10.1128/MCB.25.24.11131-11144.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Suzuki H, Amizuka N, Kii I, Kawano Y, Nozawa-Inoue K, Suzuki A, Yoshie H, Kudo A, Maeda T (2004) Immunohistochemical localization of periostin in tooth and its surrounding tissues in mouse mandibles during development. Anat Rec A Discov Mol Cell Evol Biol 281(2):1264–1275. doi:10.1002/ar.a.20080

    Article  PubMed  CAS  Google Scholar 

  13. Hakuno D, Kimura N, Yoshioka M, Mukai M, Kimura T, Okada Y, Yozu R, Shukunami C, Hiraki Y, Kudo A, Ogawa S, Fukuda K (2010) Periostin advances atherosclerotic and rheumatic cardiac valve degeneration by inducing angiogenesis and MMP production in humans and rodents. J Clin Investig 120(7):2292–2306. doi:10.1172/JCI40973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Norris RA, Moreno-Rodriguez R, Hoffman S, Markwald RR (2009) The many facets of the matricellular protein periostin during cardiac development, remodeling, and pathophysiology. J Cell Commun Signal 3(3–4):275–286. doi:10.1007/s12079-009-0063-5

    Article  PubMed  PubMed Central  Google Scholar 

  15. Norris RA, Potts JD, Yost MJ, Junor L, Brooks T, Tan H, Hoffman S, Hart MM, Kern MJ, Damon B, Markwald RR, Goodwin RL (2009) Periostin promotes a fibroblastic lineage pathway in atrioventricular valve progenitor cells. Dev Dyn 238(5):1052–1063. doi:10.1002/dvdy.21933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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 

  17. Kondoh H, Nishiyama T, Kikuchi Y, Fukayama M, Saito M, Kii I, Kudo A (2016) Periostin deficiency causes severe and lethal lung injury in mice with bleomycin administration. J Histochem Cytochem 64(7):441–453. doi:10.1369/0022155416652611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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 

  19. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW 2nd, Conway SJ, Aronow BJ, Robbins J, Molkentin JD (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 101(3):313–321. doi:10.1161/CIRCRESAHA.107.149047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ishikawa K, Yoshida S, Nakao S, Nakama T, Kita T, Asato R, Sassa Y, Arita R, Miyazaki M, Enaida H, Oshima Y, Murakami N, Niiro H, Ono J, Matsuda A, Goto Y, Akashi K, Izuhara K, Kudo A, Kono T, Hafezi-Moghadam A, Ishibashi T (2014) Periostin promotes the generation of fibrous membranes in proliferative vitreoretinopathy. FASEB J 28(1):131–142. doi:10.1096/fj.13-229740

    Article  CAS  PubMed  Google Scholar 

  21. 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, Investigators Consortium (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 

  22. 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 

  23. 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 

  24. Nishiyama T, Kii I, Kashima TG, Kikuchi Y, Ohazama A, Shimazaki M, Fukayama M, Kudo A (2011) Delayed re-epithelialization in periostin-deficient mice during cutaneous wound healing. PLoS One 6(4):e18410. doi:10.1371/journal.pone.0018410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Norris RA, Damon B, Mironov V, Kasyanov V, Ramamurthi A, Moreno-Rodriguez R, Trusk T, Potts JD, Goodwin RL, Davis J, Hoffman S, Wen X, Sugi Y, Kern CB, Mjaatvedt CH, Turner DK, Oka T, Conway SJ, Molkentin JD, Forgacs G, Markwald RR (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 101(3):695–711. doi:10.1002/jcb.21224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ontsuka K, Kotobuki Y, Shiraishi H, Serada S, Ohta S, Tanemura A, Yang L, Fujimoto M, Arima K, Suzuki S, Murota H, Toda S, Kudo A, Conway SJ, Narisawa Y, Katayama I, Izuhara K, Naka T (2012) Periostin, a matricellular protein, accelerates cutaneous wound repair by activating dermal fibroblasts. Exp Dermatol 21(5):331–336. doi:10.1111/j.1600-0625.2012.01454.x

    Article  CAS  PubMed  Google Scholar 

  27. Zhou HM, Wang J, Elliott C, Wen W, Hamilton DW, Conway SJ (2010) Spatiotemporal expression of periostin during skin development and incisional wound healing: lessons for human fibrotic scar formation. J Cell Commun Signal 4(2):99–107. doi:10.1007/s12079-010-0090-2

    Article  PubMed  PubMed Central  Google Scholar 

  28. Fukushima N, Kikuchi Y, Nishiyama T, Kudo A, Fukayama M (2008) Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas. Mod Pathol 21(8):1044–1053. doi:10.1038/modpathol.2008.77

    Article  CAS  PubMed  Google Scholar 

  29. Kashima TG, Nishiyama T, Shimazu K, Shimazaki M, Kii I, Grigoriadis AE, Fukayama M, Kudo A (2009) Periostin, a novel marker of intramembranous ossification, is expressed in fibrous dysplasia and in c-Fos-overexpressing bone lesions. Hum Pathol 40(2):226–237. doi:10.1016/j.humpath.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  30. Kikuchi Y, Kashima TG, Nishiyama T, Shimazu K, Morishita Y, Shimazaki M, Kii I, Horie H, Nagai H, Kudo A, Fukayama M (2008) Periostin is expressed in pericryptal fibroblasts and cancer-associated fibroblasts in the colon. J Histochem Cytochem 56(8):753–764. doi:10.1369/jhc.2008.951061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kikuchi Y, Kunita A, Iwata C, Komura D, Nishiyama T, Shimazu K, Takeshita K, Shibahara J, Kii I, Morishita Y, Yashiro M, Hirakawa K, Miyazono K, Kudo A, Fukayama M, Kashima TG (2014) The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am J Pathol 184(3):859–870. doi:10.1016/j.ajpath.2013.11.012

    Article  CAS  PubMed  Google Scholar 

  32. 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 

  33. Nitsche U, Stangel D, Pan Z, Schlitter AM, Esposito I, Regel I, Raulefs S, Friess H, Kleeff J, Erkan M (2016) Periostin and tumor–stroma interactions in non-small cell lung cancer. Oncol Lett 12(5):3804–3810. doi:10.3892/ol.2016.5132

    PubMed  PubMed Central  Google Scholar 

  34. Oskarsson T, Massague J (2012) Extracellular matrix players in metastatic niches. EMBO J 31(2):254–256. doi:10.1038/emboj.2011.469

    Article  CAS  PubMed  Google Scholar 

  35. Qin X, Yan M, Zhang J, Wang X, Shen Z, Lv Z, Li Z, Wei W, Chen W (2016) TGFbeta3-mediated induction of Periostin facilitates head and neck cancer growth and is associated with metastasis. Sci Rep 6:20587. doi:10.1038/srep20587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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 

  37. Sung PL, Jan YH, Lin SC, Huang CC, Lin H, Wen KC, Chao KC, Lai CR, Wang PH, Chuang CM, Wu HH, Twu NF, Yen MS, Hsiao M, Huang CY (2016) Periostin in tumor microenvironment is associated with poor prognosis and platinum resistance in epithelial ovarian carcinoma. Oncotarget 7(4):4036–4047. doi:10.18632/oncotarget.6700

    Article  PubMed  Google Scholar 

  38. Tian Y, Choi CH, Li QK, Rahmatpanah FB, Chen X, Kim SR, Veltri R, Chia D, Zhang Z, Mercola D, Zhang H (2015) Overexpression of periostin in stroma positively associated with aggressive prostate cancer. PLoS One 10(3):e0121502. doi:10.1371/journal.pone.0121502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Underwood TJ, Hayden AL, Derouet M, Garcia E, Noble F, White MJ, Thirdborough S, Mead A, Clemons N, Mellone M, Uzoho C, Primrose JN, Blaydes JP, Thomas GJ (2015) Cancer-associated fibroblasts predict poor outcome and promote periostin-dependent invasion in oesophageal adenocarcinoma. J Pathol 235(3):466–477. doi:10.1002/path.4467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wang Z, Ouyang G (2012) Periostin: a bridge between cancer stem cells and their metastatic niche. Cell Stem Cell 10(2):111–112. doi:10.1016/j.stem.2012.01.002

    Article  CAS  PubMed  Google Scholar 

  41. Conway SJ, Izuhara K, Kudo Y, Litvin J, Markwald R, Ouyang G, Arron JR, Holweg CT, Kudo A (2014) The role of periostin in tissue remodeling across health and disease. Cell Mol Life Sci 71(7):1279–1288. doi:10.1007/s00018-013-1494-y

    Article  CAS  PubMed  Google Scholar 

  42. Doliana R, Bot S, Bonaldo P, Colombatti A (2000) EMI, a novel cysteine-rich domain of EMILINs and other extracellular proteins, interacts with the gC1q domains and participates in multimerization. FEBS Lett 484(2):164–168

    Article  CAS  PubMed  Google Scholar 

  43. Callebaut I, Mignotte V, Souchet M, Mornon JP (2003) EMI domains are widespread and reveal the probable orthologs of the Caenorhabditis elegans CED-1 protein. Biochem Biophys Res Commun 300(3):619–623

    Article  CAS  PubMed  Google Scholar 

  44. Zanetti M, Braghetta P, Sabatelli P, Mura I, Doliana R, Colombatti A, Volpin D, Bonaldo P, Bressan GM (2004) EMILIN-1 deficiency induces elastogenesis and vascular cell defects. Mol Cell Biol 24(2):638–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Bot S, Andreuzzi E, Capuano A, Schiavinato A, Colombatti A, Doliana R (2015) Multiple-interactions among EMILIN1 and EMILIN2N- and C-terminal domains. Matrix Biol 41:44–55. doi:10.1016/j.matbio.2014.10.001

    Article  CAS  PubMed  Google Scholar 

  46. Doliana R, Canton A, Bucciotti F, Mongiat M, Bonaldo P, Colombatti A (2000) Structure, chromosomal localization, and promoter analysis of the human elastin microfibril interfase located proteIN (EMILIN) gene. J Biol Chem 275(2):785–792

    Article  CAS  PubMed  Google Scholar 

  47. Schiavinato A, Becker AK, Zanetti M, Corallo D, Milanetto M, Bizzotto D, Bressan G, Guljelmovic M, Paulsson M, Wagener R, Braghetta P, Bonaldo P (2012) EMILIN-3, peculiar member of elastin microfibril interface-located protein (EMILIN) family, has distinct expression pattern, forms oligomeric assemblies, and serves as transforming growth factor beta (TGF-beta) antagonist. J Biol Chem 287(14):11498–11515. doi:10.1074/jbc.M111.303578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zacchigna L, Vecchione C, Notte A, Cordenonsi M, Dupont S, Maretto S, Cifelli G, Ferrari A, Maffei A, Fabbro C, Braghetta P, Marino G, Selvetella G, Aretini A, Colonnese C, Bettarini U, Russo G, Soligo S, Adorno M, Bonaldo P, Volpin D, Piccolo S, Lembo G, Bressan GM (2006) Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell 124(5):929–942. doi:10.1016/j.cell.2005.12.035

    Article  CAS  PubMed  Google Scholar 

  49. Kii I, Nishiyama T, Kudo A (2016) Periostin promotes secretion of fibronectin from the endoplasmic reticulum. Biochem Biophys Res Commun 470(4):888–893. doi:10.1016/j.bbrc.2016.01.139

    Article  CAS  PubMed  Google Scholar 

  50. Kim BY, Olzmann JA, Choi SI, Ahn SY, Kim TI, Cho HS, Suh H, Kim EK (2009) Corneal dystrophy-associated R124H mutation disrupts TGFBI interaction with Periostin and causes mislocalization to the lysosome. J Biol Chem 284(29):19580–19591. doi:10.1074/jbc.M109.013607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kadler KE, Hill A, Canty-Laird EG (2008) Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20(5):495–501. doi:10.1016/j.ceb.2008.06.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118(Pt 7):1341–1353. doi:10.1242/jcs.01731

    Article  CAS  PubMed  Google Scholar 

  53. Mosher DF, Johansson MW, Gillis ME, Annis DS (2015) Periostin and TGF-beta-induced protein: two peas in a pod? Crit Rev Biochem Mol Biol 50(5):427–439. doi:10.3109/10409238.2015.1069791

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kannabiran C, Klintworth GK (2006) TGFBI gene mutations in corneal dystrophies. Hum Mutat 27(7):615–625. doi:10.1002/humu.20334

    Article  CAS  PubMed  Google Scholar 

  55. Hashimoto K, Noshiro M, Ohno S, Kawamoto T, Satakeda H, Akagawa Y, Nakashima K, Okimura A, Ishida H, Okamoto T, Pan H, Shen M, Yan W, Kato Y (1997) Characterization of a cartilage-derived 66-kDa protein (RGD-CAP/beta ig-h3) that binds to collagen. Biochim Biophys Acta 1355(3):303–314

    Article  CAS  PubMed  Google Scholar 

  56. Clout NJ, Hohenester E (2003) A model of FAS1 domain 4 of the corneal protein beta(ig)-h3 gives a clearer view on corneal dystrophies. Mol Vis 9:440–448

    CAS  PubMed  Google Scholar 

  57. Clout NJ, Tisi D, Hohenester E (2003) Novel fold revealed by the structure of a FAS1 domain pair from the insect cell adhesion molecule fasciclin I. Structure 11(2):197–203

    Article  CAS  PubMed  Google Scholar 

  58. Carr MD, Bloemink MJ, Dentten E, Whelan AO, Gordon SV, Kelly G, Frenkiel TA, Hewinson RG, Williamson RA (2003) Solution structure of the Mycobacterium tuberculosis complex protein MPB70: from tuberculosis pathogenesis to inherited human corneal desease. J Biol Chem 278(44):43736–43743. doi:10.1074/jbc.M307235200

    Article  CAS  PubMed  Google Scholar 

  59. Midwood KS, Chiquet M, Tucker RP, Orend G (2016) Tenascin-C at a glance. J Cell Sci 129(23):4321–4327. doi:10.1242/jcs.190546

    Article  CAS  PubMed  Google Scholar 

  60. Takayama I, Kii I, Kudo A (2009) Expression, purification and characterization of soluble recombinant periostin protein produced by Escherichia coli. J Biochem 146(5):713–723. doi:10.1093/jb/mvp117

    Article  CAS  PubMed  Google Scholar 

  61. Vadon-Le Goff S, Hulmes DJ, Moali C (2015) BMP-1/tolloid-like proteinases synchronize matrix assembly with growth factor activation to promote morphogenesis and tissue remodeling. Matrix Biol 44–46:14–23. doi:10.1016/j.matbio.2015.02.006

    Article  PubMed  CAS  Google Scholar 

  62. Hwang EY, Jeong MS, Park EK, Kim JH, Jang SB (2014) Structural characterization and interaction of periostin and bone morphogenetic protein for regulation of collagen cross-linking. Biochem Biophys Res Commun 449(4):425–431. doi:10.1016/j.bbrc.2014.05.055

    Article  CAS  PubMed  Google Scholar 

  63. Garnero P (2012) The contribution of collagen crosslinks to bone strength. Bonekey Rep 1:182. doi:10.1038/bonekey.2012.182

    Article  PubMed  PubMed Central  Google Scholar 

  64. Trackman PC (2016) Enzymatic and non-enzymatic functions of the lysyl oxidase family in bone. Matrix Biol 52–54:7–18. doi:10.1016/j.matbio.2016.01.001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Takayama I, Tanabe H, Nishiyama T, Ito H, Amizuka N, Li M, Katsube KI, Kii I, Kudo A (2017) Periostin is required for matricellular localization of CCN3 in periodontal ligament of mice. J Cell Commun Signal 11(1):5–13. doi:10.1007/s12079-016-0371-5

    Article  PubMed  Google Scholar 

  66. Ratajczak-Wielgomas K, Dziegiel P (2015) The role of periostin in neoplastic processes. Folia Histochem Cytobiol 53(2):120–132. doi:10.5603/FHC.a2015.0014

    Article  PubMed  Google Scholar 

  67. Snider J, Kotlyar M, Saraon P, Yao Z, Jurisica I, Stagljar I (2015) Fundamentals of protein interaction network mapping. Mol Syst Biol 11(12):848. doi:10.15252/msb.20156351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res 45(D1):D362–D368. doi:10.1093/nar/gkw937

    Article  PubMed  Google Scholar 

  69. Ghatak S, Misra S, Norris RA, Moreno-Rodriguez RA, Hoffman S, Levine RA, Hascall VC, Markwald RR (2014) Periostin induces intracellular cross-talk between kinases and hyaluronan in atrioventricular valvulogenesis. J Biol Chem 289(12):8545–8561. doi:10.1074/jbc.M113.539882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Masuoka M, Shiraishi H, Ohta S, Suzuki S, Arima K, Aoki S, Toda S, Inagaki N, Kurihara Y, Hayashida S, Takeuchi S, Koike K, Ono J, Noshiro H, Furue M, Conway SJ, Narisawa Y, Izuhara K (2012) Periostin promotes chronic allergic inflammation in response to Th2 cytokines. J Clin Investig 122(7):2590–2600. doi:10.1172/JCI58978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Matsuzawa M, Arai C, Nomura Y, Murata T, Yamakoshi Y, Oida S, Hanada N, Nakamura Y (2015) Periostin of human periodontal ligament fibroblasts promotes migration of human mesenchymal stem cell through the alphavbeta3 integrin/FAK/PI3K/Akt pathway. J Periodontal Res 50(6):855–863. doi:10.1111/jre.12277

    Article  CAS  PubMed  Google Scholar 

  72. Utispan K, Sonongbua J, Thuwajit P, Chau-In S, Pairojkul C, Wongkham S, Thuwajit C (2012) Periostin activates integrin alpha5beta1 through a PI3K/AKT dependent pathway in invasion of cholangiocarcinoma. Int J Oncol 41(3):1110–1118. doi:10.3892/ijo.2012.1530

    Article  CAS  PubMed  Google Scholar 

  73. Xiao ZM, Wang XY, Wang AM (2015) Periostin induces chemoresistance in colon cancer cells through activation of the PI3K/Akt/survivin pathway. Biotechnol Appl Biochem 62(3):401–406. doi:10.1002/bab.1193

    Article  CAS  PubMed  Google Scholar 

  74. Yang L, Serada S, Fujimoto M, Terao M, Kotobuki Y, Kitaba S, Matsui S, Kudo A, Naka T, Murota H, Katayama I (2012) Periostin facilitates skin sclerosis via PI3K/Akt dependent mechanism in a mouse model of scleroderma. PLoS One 7(7):e41994. doi:10.1371/journal.pone.0041994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Huttlin EL, Bruckner RJ, Paulo JA, Cannon JR, Ting L, Baltier K, Colby G, Gebreab F, Gygi MP, Parzen H, Szpyt J, Tam S, Zarraga G, Pontano-Vaites L, Swarup S, White AE, Schweppe DK, Rad R, Erickson BK, Obar RA, Guruharsha KG, Li K, Artavanis-Tsakonas S, Gygi SP, Harper JW (2017) Architecture of the human interactome defines protein communities and disease networks. Nature 545(7655):505–509. doi:10.1038/nature22366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Huttlin EL, Ting L, Bruckner RJ, Gebreab F, Gygi MP, Szpyt J, Tam S, Zarraga G, Colby G, Baltier K, Dong R, Guarani V, Vaites LP, Ordureau A, Rad R, Erickson BK, Wuhr M, Chick J, Zhai B, Kolippakkam D, Mintseris J, Obar RA, Harris T, Artavanis-Tsakonas S, Sowa ME, De Camilli P, Paulo JA, Harper JW, Gygi SP (2015) The BioPlex network: a systematic exploration of the human interactome. Cell 162(2):425–440. doi:10.1016/j.cell.2015.06.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5(4):329–339

    Article  CAS  PubMed  Google Scholar 

  78. Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res 62(18):5358–5364

    CAS  PubMed  Google Scholar 

  79. Khurana S, Schouteden S, Manesia JK, Santamaria-Martinez A, Huelsken J, Lacy-Hulbert A, Verfaillie CM (2016) Outside-in integrin signalling regulates haematopoietic stem cell function via Periostin–Itgav axis. Nat Commun 7:13500. doi:10.1038/ncomms13500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Orecchia P, Conte R, Balza E, Castellani P, Borsi L, Zardi L, Mingari MC, Carnemolla B (2011) Identification of a novel cell binding site of periostin involved in tumour growth. Eur J Cancer 47(14):2221–2229. doi:10.1016/j.ejca.2011.04.026

    Article  CAS  PubMed  Google Scholar 

  81. Shao R, Bao S, Bai X, Blanchette C, Anderson RM, Dang T, Gishizky ML, Marks JR, Wang XF (2004) Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Mol Cell Biol 24(9):3992–4003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sugiyama A, Kanno K, Nishimichi N, Ohta S, Ono J, Conway SJ, Izuhara K, Yokosaki Y, Tazuma S (2016) Periostin promotes hepatic fibrosis in mice by modulating hepatic stellate cell activation via alphav integrin interaction. J Gastroenterol 51(12):1161–1174. doi:10.1007/s00535-016-1206-0

    Article  CAS  PubMed  Google Scholar 

  83. Tanabe H, Takayama I, Nishiyama T, Shimazaki M, Kii I, Li M, Amizuka N, Katsube K, Kudo A (2010) Periostin associates with Notch1 precursor to maintain Notch1 expression under a stress condition in mouse cells. PLoS One 5(8):e12234. doi:10.1371/journal.pone.0012234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. 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 

  85. Hong L, Shejiao D, Fenrong C, Gang Z, Lei D (2015) Periostin down-regulation attenuates the pro-fibrogenic response of hepatic stellate cells induced by TGF-beta1. J Cell Mol Med 19(10):2462–2468. doi:10.1111/jcmm.12636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Huang Y, Liu W, Xiao H, Maitikabili A, Lin Q, Wu T, Huang Z, Liu F, Luo Q, Ouyang G (2015) Matricellular protein periostin contributes to hepatic inflammation and fibrosis. Am J Pathol 185(3):786–797. doi:10.1016/j.ajpath.2014.11.002

    Article  CAS  PubMed  Google Scholar 

  87. Kaur H, Takefuji M, Ngai CY, Carvalho J, Bayer J, Wietelmann A, Poetsch A, Hoelper S, Conway SJ, Mollmann H, Looso M, Troidl C, Offermanns S, Wettschureck N (2016) Targeted ablation of periostin-expressing activated fibroblasts prevents adverse cardiac remodeling in mice. Circ Res 118(12):1906–1917. doi:10.1161/CIRCRESAHA.116.308643

    Article  CAS  PubMed  Google Scholar 

  88. Lorts A, Schwanekamp JA, Baudino TA, McNally EM, Molkentin JD (2012) Deletion of periostin reduces muscular dystrophy and fibrosis in mice by modulating the transforming growth factor-beta pathway. Proc Natl Acad Sci USA 109(27):10978–10983. doi:10.1073/pnas.1204708109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Lorts A, Schwanekamp JA, Elrod JW, Sargent MA, Molkentin JD (2009) Genetic manipulation of periostin expression in the heart does not affect myocyte content, cell cycle activity, or cardiac repair. Circ Res 104(1):e1–e7. doi:10.1161/CIRCRESAHA.108.188649

    Article  CAS  PubMed  Google Scholar 

  90. Nakama T, Yoshida S, Ishikawa K, Kobayashi Y, Zhou Y, Nakao S, Sassa Y, Oshima Y, Takao K, Shimahara A, Yoshikawa K, Hamasaki T, Ohgi T, Hayashi H, Matsuda A, Kudo A, Nozaki M, Ogura Y, Kuroda M, Ishibashi T (2015) Inhibition of choroidal fibrovascular membrane formation by new class of RNA interference therapeutic agent targeting periostin. Gene Ther 22(2):127–137. doi:10.1038/gt.2014.112

    Article  CAS  PubMed  Google Scholar 

  91. Nakama T, Yoshida S, Ishikawa K, Kubo Y, Kobayashi Y, Zhou Y, Nakao S, Hisatomi T, Ikeda Y, Takao K, Yoshikawa K, Matsuda A, Ono J, Ohta S, Izuhara K, Kudo A, Sonoda KH, Ishibashi T (2017) Therapeutic effect of novel single-stranded RNAi agent targeting periostin in eyes with retinal neovascularization. Mol Ther Nucleic Acids 6:279–289. doi:10.1016/j.omtn.2017.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Nam BY, Park JT, Kwon YE, Lee JP, Jung JH, Kim Y, Kim S, Park J, Um JE, Wu M, Han SH, Yoo TH, Kang SW (2017) Periostin-binding DNA aptamer treatment ameliorates peritoneal dialysis-induced peritoneal fibrosis. Mol Ther Nucleic Acids 7:396–407. doi:10.1016/j.omtn.2017.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Schwanekamp JA, Lorts A, Vagnozzi RJ, Vanhoutte D, Molkentin JD (2016) Deletion of periostin protects against atherosclerosis in mice by altering inflammation and extracellular matrix remodeling. Arterioscler Thromb Vasc Biol 36(1):60–68. doi:10.1161/ATVBAHA.115.306397

    CAS  PubMed  Google Scholar 

  94. Taniyama Y, Katsuragi N, Sanada F, Azuma J, Iekushi K, Koibuchi N, Okayama K, Ikeda-Iwabu Y, Muratsu J, Otsu R, Rakugi H, Morishita R (2016) Selective blockade of periostin exon 17 preserves cardiac performance in acute myocardial infarction. Hypertension 67(2):356–361. doi:10.1161/HYPERTENSIONAHA.115.06265

    CAS  PubMed  Google Scholar 

  95. Yokota K, Kobayakawa K, Saito T, Hara M, Kijima K, Ohkawa Y, Harada A, Okazaki K, Ishihara K, Yoshida S, Kudo A, Iwamoto Y, Okada S (2017) Periostin promotes scar formation through the interaction between pericytes and infiltrating monocytes/macrophages after spinal cord injury. Am J Pathol 187(3):639–653. doi:10.1016/j.ajpath.2016.11.010

    Article  CAS  PubMed  Google Scholar 

  96. Zhu M, Saxton RE, Ramos L, Chang DD, Karlan BY, Gasson JC, Slamon DJ (2011) Neutralizing monoclonal antibody to periostin inhibits ovarian tumor growth and metastasis. Mol Cancer Ther 10(8):1500–1508. doi:10.1158/1535-7163.MCT-11-0046

    Article  CAS  PubMed  Google Scholar 

  97. Turtle E, Chow N, Yang C, Sosa S, Bauer U, Brenner M, Solow-Cordero D, Ho WB (2012) Design and synthesis of procollagen C-proteinase inhibitors. Bioorg Med Chem Lett 22(24):7397–7401. doi:10.1016/j.bmcl.2012.10.067

    Article  CAS  PubMed  Google Scholar 

  98. Chang J, Lucas MC, Leonte LE, Garcia-Montolio M, Singh LB, Findlay AD, Deodhar M, Foot JS, Jarolimek W, Timpson P, Erler JT, Cox TR (2017) Pre-clinical evaluation of small molecule LOXL2 inhibitors in breast cancer. Oncotarget 8(16):26066–26078. doi:10.18632/oncotarget.15257

    PubMed  PubMed Central  Google Scholar 

  99. Hutchinson JH, Rowbottom MW, Lonergan D, Darlington J, Prodanovich P, King CD, Evans JF, Bain G (2017) Small molecule lysyl oxidase-like 2 (LOXL2) inhibitors: the identification of an inhibitor selective for LOXL2 over LOX. ACS Med Chem Lett 8(4):423–427. doi:10.1021/acsmedchemlett.7b00014

    Article  CAS  PubMed  Google Scholar 

  100. Rowbottom MW, Bain G, Calderon I, Lasof T, Lonergan D, Lai A, Huang F, Darlington J, Prodanovich P, Santini AM, King CD, Goulet L, Shannon KE, Ma GL, Nguyen K, MacKenna DA, Evans JF, Hutchinson JH (2017) Identification of 4-(aminomethyl)-6-(trifluoromethyl)-2-(phenoxy)pyridine derivatives as potent, selective, and orally efficacious inhibitors of the copper-dependent amine oxidase, lysyl oxidase-like 2 (LOXL2). J Med Chem 60(10):4403–4423. doi:10.1021/acs.jmedchem.7b00345

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Project for Cancer Research and Therapeutic Evolution (P-CREATE) (IK) from the Japan Agency for Medical Research and Development (AMED).

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  1. Common Facilities Unit, Integrated Research Group, Compass to Healthy Life Research Complex Program, RIKEN Cluster for Science and Technology Hub, 6-7-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo, 650-0047, Japan

    Isao Kii

  2. Pathophysiological and Health Science Team, Imaging Platform and Innovation Group, Division of Bio-Function Dynamics Imaging, RIKEN Center for Life Science Technologies, 6-7-3 Minatojima-minamimachi, Chuo-ku, Kobe, 650-0047, Japan

    Isao Kii & Harumi Ito

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  1. Isao Kii
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Kii, I., Ito, H. Periostin and its interacting proteins in the construction of extracellular architectures. Cell. Mol. Life Sci. 74, 4269–4277 (2017). https://doi.org/10.1007/s00018-017-2644-4

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