Home LiteratureArticle Details
PMID: 19308325 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

The multifaceted role of periostin in tumorigenesis.

Cellular and molecular life sciences : CMLS ·Vol. 66 ·No. 14 ·2009-07-00 ·Pages 2219-30

Ruan K, Bao S, Ouyang G

Abstract

Periostin, also called osteoblast-specific factor 2 (OSF-2), is a member of the fasciclin family and a disulfide-linked cell adhesion protein that has been shown to be expressed preferentially in the periosteum and periodontal ligaments, where it acts as a critical regulator of bone and tooth formation and maintenance. Furthermore, periostin plays an important role in cardiac development. Recent clinical evidence has also revealed that periostin is involved in the development of various tumors, such as breast, lung, colon, pancreatic, and ovarian cancers. Periostin interacts with multiple cell-surface receptors, most notably integrins, and signals mainly via the PI3-K/Akt and other pathways to promote cancer cell survival, epithelial-mesenchymal transition (EMT), invasion, and metastasis. In this review, aspects related to the function of periostin in tumorigenesis are summarized.

MeSH Terms
Cell Adhesion Molecules/genetics,metabolism,physiology Cell Proliferation Cell Survival Humans Neoplasm Invasiveness/genetics Neoplasm Metastasis/genetics Neoplasms/classification,genetics,metabolism
Chemicals
Cell Adhesion Molecules POSTN protein, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ruan Kai
Key Laboratory of the Ministry of Education for Cell Biology and Tumor Cell Engineering, School of Life Sciences, Xiamen University, Xiamen, China.
Bao Shideng
Ouyang Gaoliang
References (100)
100 references, click to expand
  1. Expression of periostin in human breast cancer.
    J Clin Pathol. 2008 Apr;61(4):494-8 PMID: 17938160
  2. Molecular requirements for epithelial-mesenchymal transition during tumor progression.
    Curr Opin Cell Biol. 2005 Oct;17(5):548-58 PMID: 16098727
  3. BRCA1 5083del19 mutant allele selectively up-regulates periostin expression in vitro and in vivo.
    Clin Cancer Res. 2008 Nov 1;14(21):6797-803 PMID: 18980973
  4. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration.
    Physiol Genomics. 2003 Aug 15;14(3):261-71 PMID: 12799472
  5. The matrix reorganized: extracellular matrix remodeling and integrin signaling.
    Curr Opin Cell Biol. 2006 Oct;18(5):463-71 PMID: 16919434
  6. 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. 2004 May;24(9):3992-4003 PMID: 15082792
  7. Matricellular proteins: Extracellular modulators of bone development, remodeling, and regeneration.
    Bone. 2006 Jun;38(6):749-57 PMID: 16412713
  8. The dominance of the microenvironment in breast and ovarian cancer.
    Semin Cancer Biol. 2002 Apr;12(2):97-104 PMID: 12027581
  9. Osteopontin prevents curcumin-induced apoptosis and promotes survival through Akt activation via alpha v beta 3 integrins in human gastric cancer cells.
    Exp Biol Med (Maywood). 2008 Dec;233(12):1537-45 PMID: 18849546
  10. Altered patterns of gene expression in response to myocardial infarction.
    Circ Res. 2000 May 12;86(9):939-45 PMID: 10807865
  11. Tornado extraction: a method to enrich and purify RNA from the nephrogenic zone of the neonatal rat kidney.
    Kidney Int. 2002 Sep;62(3):763-9 PMID: 12164857
  12. Regulation of cyclooxygenase-2 and periostin by Wnt-3 in mouse mammary epithelial cells.
    J Biol Chem. 2000 Oct 13;275(41):32046-51 PMID: 10884377
  13. The microenvironment of the tumour-host interface.
    Nature. 2001 May 17;411(6835):375-9 PMID: 11357145
  14. Serum level of the periostin, a homologue of an insect cell adhesion molecule, in thymoma patients.
    Cancer Lett. 2001 Oct 22;172(1):37-42 PMID: 11595127
  15. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?
    Nat Rev Cancer. 2007 Jun;7(6):415-28 PMID: 17508028
  16. 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. 2002 Sep 15;62(18):5358-64 PMID: 12235007
  17. Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families.
    Nat Genet. 1994 Dec;8(4):399-404 PMID: 7894493
  18. Positional control of cell fate through joint integrin/receptor protein kinase signaling.
    Annu Rev Cell Dev Biol. 2003;19:173-206 PMID: 14570568
  19. Expression and function of periostin-isoforms in bone.
    J Cell Biochem. 2004 Aug 1;92(5):1044-61 PMID: 15258926
  20. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway.
    EMBO J. 1997 May 15;16(10):2783-93 PMID: 9184223
  21. Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer.
    Br J Cancer. 2006 Nov 20;95(10):1396-403 PMID: 17060937
  22. Role of transforming growth factor Beta in human cancer.
    J Clin Oncol. 2005 Mar 20;23(9):2078-93 PMID: 15774796
  23. Cancer susceptibility and the functions of BRCA1 and BRCA2.
    Cell. 2002 Jan 25;108(2):171-82 PMID: 11832208
  24. Elevated serum periostin levels in patients with bone metastases from breast but not lung cancer.
    Breast Cancer Res Treat. 2003 Feb;77(3):245-52 PMID: 12602924
  25. Human microvascular endothelial cells immortalized with human telomerase catalytic protein: a model for the study of in vitro angiogenesis.
    Biochem Biophys Res Commun. 2004 Sep 3;321(4):788-94 PMID: 15358096
  26. Periostin family of proteins: therapeutic targets for heart disease.
    Anat Rec A Discov Mol Cell Evol Biol. 2005 Dec;287(2):1205-12 PMID: 16240445
  27. Distinct mechanisms of tumor invasion and metastasis.
    Trends Mol Med. 2007 Dec;13(12):535-41 PMID: 17981506
  28. Hypoxia-responsive growth factors upregulate periostin and osteopontin expression via distinct signaling pathways in rat pulmonary arterial smooth muscle cells.
    J Appl Physiol (1985). 2004 Oct;97(4):1550-8; discussion 1549 PMID: 15121739
  29. Suppression of anchorage-independent growth of human cancer cell lines by the TRIF52/periostin/OSF-2 gene.
    Exp Cell Res. 2002 Sep 10;279(1):91-9 PMID: 12213217
  30. Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals.
    J Allergy Clin Immunol. 2006 Jul;118(1):98-104 PMID: 16815144
  31. Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer.
    Clin Cancer Res. 2008 Nov 15;14(22):7430-7 PMID: 19010860
  32. Induction of angiogenesis during the transition from hyperplasia to neoplasia.
    Nature. 1989 May 4;339(6219):58-61 PMID: 2469964
  33. Human periostin gene expression in normal tissues, tumors and melanoma: evidences for periostin production by both stromal and melanoma cells.
    Mol Cancer. 2007 Dec 17;6:80 PMID: 18086302
  34. Periostin is expressed in pericryptal fibroblasts and cancer-associated fibroblasts in the colon.
    J Histochem Cytochem. 2008 Aug;56(8):753-64 PMID: 18443362
  35. Complex networks orchestrate epithelial-mesenchymal transitions.
    Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42 PMID: 16493418
  36. Effects of pressure overload on extracellular matrix expression in the heart of the atrial natriuretic peptide-null mouse.
    Hypertension. 2003 Jul;42(1):88-95 PMID: 12756220
  37. Cell cycle checkpoints: preventing an identity crisis.
    Science. 1996 Dec 6;274(5293):1664-72 PMID: 8939848
  38. Periostin is down-regulated in high grade human bladder cancers and suppresses in vitro cell invasiveness and in vivo metastasis of cancer cells.
    Int J Cancer. 2005 Oct 20;117(1):51-8 PMID: 15880581
  39. A novel mechanism for the regulation of osteoblast differentiation: transcription of periostin, a member of the fasciclin I family, is regulated by the bHLH transcription factor, twist.
    J Cell Biochem. 2002;86(4):792-804 PMID: 12210745
  40. Taking the study of cancer cell survival to a new dimension.
    Cell. 2002 Dec 27;111(7):923-5 PMID: 12507419
  41. Transduction of a mesenchyme-specific gene periostin into 293T cells induces cell invasive activity through epithelial-mesenchymal transformation.
    J Biol Chem. 2006 Jul 14;281(28):19700-8 PMID: 16702213
  42. Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: role of the beta4 integrin and the PI3k pathway.
    Oncogene. 2007 Mar 29;26(14):2082-94 PMID: 17043657
  43. Genome instability: a mechanistic view of its causes and consequences.
    Nat Rev Genet. 2008 Mar;9(3):204-17 PMID: 18227811
  44. Expression of Periostin, homologous with an insect cell adhesion molecule, as a prognostic marker in non-small cell lung cancers.
    Jpn J Cancer Res. 2001 Aug;92(8):869-73 PMID: 11509119
  45. The activation of Akt/PKB signaling pathway and cell survival.
    J Cell Mol Med. 2005 Jan-Mar;9(1):59-71 PMID: 15784165
  46. Expression of periostin in patients with non-small cell lung cancer: correlation with angiogenesis and lymphangiogenesis.
    Int J Biol Markers. 2008 Jul-Sep;23(3):182-6 PMID: 18949745
  47. Functional role of periostin in development and wound repair: implications for connective tissue disease.
    J Cell Commun Signal. 2008 Jun;2(1-2):9-17 PMID: 18642132
  48. Serum level of the periostin, a homologue of an insect cell adhesion molecule, as a prognostic marker in nonsmall cell lung carcinomas.
    Cancer. 2001 Aug 15;92(4):843-8 PMID: 11550156
  49. Periostin creates a tumor-supportive microenvironment in the pancreas by sustaining fibrogenic stellate cell activity.
    Gastroenterology. 2007 Apr;132(4):1447-64 PMID: 17408641
  50. Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer.
    Cancer Res. 2006 Jul 15;66(14):6928-35 PMID: 16849536
  51. Matricellular proteins: extracellular modulators of cell function.
    Curr Opin Cell Biol. 2002 Oct;14(5):608-16 PMID: 12231357
  52. Periostin induction in tumor cell line explants and inhibition of in vitro cell growth by anti-periostin antibodies.
    Carcinogenesis. 2005 May;26(5):908-15 PMID: 15731169
  53. Integrin signaling.
    Science. 1999 Aug 13;285(5430):1028-32 PMID: 10446041
  54. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment?
    Cancer Cell. 2005 Jan;7(1):17-23 PMID: 15652746
  55. Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas.
    Mod Pathol. 2008 Aug;21(8):1044-53 PMID: 18487994
  56. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells.
    Cell. 1992 Nov 13;71(4):543-6 PMID: 1423612
  57. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I.
    Biochem J. 1993 Aug 15;294 ( Pt 1):271-8 PMID: 8363580
  58. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway.
    Cancer Cell. 2004 Apr;5(4):329-39 PMID: 15093540
  59. Importance of the bone marrow microenvironment in inducing the angiogenic response in multiple myeloma.
    Oncogene. 2006 Jul 20;25(31):4257-66 PMID: 16518413
  60. Drosophila fasciclin I, a neural cell adhesion molecule, has a phosphatidylinositol lipid membrane anchor that is developmentally regulated.
    J Biol Chem. 1990 Sep 5;265(25):15104-9 PMID: 2394715
  61. Periostin expression by epicardium-derived cells is involved in the development of the atrioventricular valves and fibrous heart skeleton.
    Differentiation. 2008 Sep;76(7):809-19 PMID: 18294225
  62. Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase.
    Dev Biol. 2007 Feb 1;302(1):256-66 PMID: 17070513
  63. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair.
    Nat Med. 2007 Aug;13(8):962-9 PMID: 17632525
  64. Secreted protein acidic, rich in cysteine (SPARC), mediates cellular survival of gliomas through AKT activation.
    J Biol Chem. 2004 Dec 10;279(50):52200-9 PMID: 15469933
  65. Epithelial-mesenchymal transitions in tumour progression.
    Nat Rev Cancer. 2002 Jun;2(6):442-54 PMID: 12189386
  66. Periostin, secreted from stromal cells, has biphasic effect on cell migration and correlates with the epithelial to mesenchymal transition of human pancreatic cancer cells.
    Int J Cancer. 2008 Jun 15;122(12):2707-18 PMID: 18381746
  67. Osteopontin: regulation in tumor metastasis.
    Cancer Metastasis Rev. 2008 Mar;27(1):103-18 PMID: 18049863
  68. Periostin is expressed within the developing teeth at the sites of epithelial-mesenchymal interaction.
    Dev Dyn. 2004 Apr;229(4):857-68 PMID: 15042709
  69. Neonatal and adult cardiovascular pathophysiological remodeling and repair: developmental role of periostin.
    Ann N Y Acad Sci. 2008 Mar;1123:30-40 PMID: 18375575
  70. Vascular-specific growth factors and blood vessel formation.
    Nature. 2000 Sep 14;407(6801):242-8 PMID: 11001067
  71. Differential gene expression between normal and tumor-derived ovarian epithelial cells.
    Cancer Res. 2000 Dec 1;60(23):6744-9 PMID: 11118061
  72. Establishment of cell lines that exhibit pluripotency from miniature swine periodontal ligaments.
    Arch Oral Biol. 2007 Oct;52(10):1002-8 PMID: 17543882
  73. Integrins and cancer.
    Curr Opin Cell Biol. 1996 Oct;8(5):724-30 PMID: 8939661
  74. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses.
    Nature. 2001 Jun 21;411(6840):969-74 PMID: 11418864
  75. BMP-2 induces cell migration and periostin expression during atrioventricular valvulogenesis.
    Dev Biol. 2008 Mar 15;315(2):383-96 PMID: 18261719
  76. Periostin: novel diagnostic and therapeutic target for cancer.
    Histol Histopathol. 2007 Oct;22(10):1167-74 PMID: 17616943
  77. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium.
    Cancer Cell. 2002 Sep;2(3):205-16 PMID: 12242153
  78. Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis.
    J Orthop Res. 2004 May;22(3):520-5 PMID: 15099630
  79. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  80. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues.
    J Cell Biochem. 2007 Jun 1;101(3):695-711 PMID: 17226767
  81. Extracellular matrix protein betaig-h3/TGFBI promotes metastasis of colon cancer by enhancing cell extravasation.
    Genes Dev. 2008 Feb 1;22(3):308-21 PMID: 18245446
  82. Sensing the environment: a historical perspective on integrin signal transduction.
    Nat Cell Biol. 2002 Apr;4(4):E83-90 PMID: 11944041
  83. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  84. Patterns of gene expression associated with BMP-2-induced osteoblast and adipocyte differentiation of mesenchymal progenitor cell 3T3-F442A.
    J Bone Miner Metab. 2000;18(3):132-9 PMID: 10783846
  85. periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype.
    Mol Cell Biol. 2005 Dec;25(24):11131-44 PMID: 16314533
  86. RGD-CAP ((beta)ig-h3) enhances the spreading of chondrocytes and fibroblasts via integrin alpha(1)beta(1).
    Biochim Biophys Acta. 1999 Aug 12;1451(1):196-205 PMID: 10446401
  87. Identification and characterization of a novel Schwann and outflow tract endocardial cushion lineage-restricted periostin enhancer.
    Dev Biol. 2007 Jul 15;307(2):340-55 PMID: 17540359
  88. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1.
    Science. 1994 Oct 7;266(5182):66-71 PMID: 7545954
  89. Putting tumours in context.
    Nat Rev Cancer. 2001 Oct;1(1):46-54 PMID: 11900251
  90. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution.
    Nucleic Acids Res. 2006 Mar 06;34(5):1416-26 PMID: 16522651
  91. Osteopontin promotes ovarian cancer progression and cell survival and increases HIF-1alpha expression through the PI3-K/Akt pathway.
    Cancer Sci. 2008 Oct;99(10):1901-7 PMID: 19016748
  92. Many roads lead to oncogene-induced senescence.
    Oncogene. 2008 May 1;27(20):2801-9 PMID: 18193093
  93. cDNA cloning and sequence analysis of beta ig-h3, a novel gene induced in a human adenocarcinoma cell line after treatment with transforming growth factor-beta.
    DNA Cell Biol. 1992 Sep;11(7):511-22 PMID: 1388724
  94. Osteopontin: role in cell signaling and cancer progression.
    Trends Cell Biol. 2006 Feb;16(2):79-87 PMID: 16406521
  95. Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration.
    Arterioscler Thromb Vasc Biol. 2005 Jan;25(1):77-83 PMID: 15514205
  96. Advances of AKT pathway in human oncogenesis and as a target for anti-cancer drug discovery.
    Curr Cancer Drug Targets. 2008 Feb;8(1):2-6 PMID: 18288938
  97. Zebrafish periostin is required for the adhesion of muscle fiber bundles to the myoseptum and for the differentiation of muscle fibers.
    Dev Biol. 2004 Mar 15;267(2):473-87 PMID: 15013807
  98. Expression of the periostin mRNA level in neuroblastoma.
    J Pediatr Surg. 2002 Sep;37(9):1293-7 PMID: 12194119
  99. Expression of periostin and its clinicopathological relevance in gastric cancer.
    World J Gastroenterol. 2007 Oct 21;13(39):5261-6 PMID: 17876898
  100. 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. 1999 Jul;14(7):1239-49 PMID: 10404027
Article Info
Journal
Cellular and molecular life sciences : CMLS
Abbr.
Cell Mol Life Sci
ISSN
1420-9071
Published
2009-07-00
Epub
2009-00-24
Pages
2219-30
Language
English
Region
Switzerland
NLM ID
9705402
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]