Periostin, a Cell Adhesion Molecule, Facilitates Invasion in the Tumor Microenvironment and Annotates a Novel Tumor-invasive Signature in Esophageal Cancer

Overview

Journal Cancer Res

Specialty Oncology

Date 2010 Jun 3

PMID 20516120

Citations 73

Authors

Carmen Z Michaylira

Gabrielle S Wong

Charles G Miller

Christie M Gutierrez

Hiroshi Nakagawa

Rachel Hammond

Andres J Klein-Szanto

Ju-Seog Lee

Sang Bae Kim

Meenhard Herlyn

J Alan Diehl

Phyllis Gimotty

Anil K Rustgi

Affiliations

Soon will be listed here.

Abstract

Human squamous cell cancers are the most common epithelially derived malignancies. One example is esophageal squamous cell carcinoma (ESCC), which is associated with a high mortality rate that is related to a propensity for invasion and metastasis. Here, we report that periostin, a highly expressed cell adhesion molecule, is a key component of a novel tumor-invasive signature obtained from an organotypic culture model of engineered ESCC. This tumor-invasive signature classifies with human ESCC microarrays, underscoring its utility in human cancer. Genetic modulation of periostin promotes tumor cell migration and invasion as revealed in gain-of-loss and loss-of-function experiments. Inhibition of epidermal growth factor receptor signaling and restoration of wild-type p53 function were each found to attenuate periostin, suggesting the interdependence of two common genetic alterations with periostin function. Collectively, our studies reveal periostin as an important mediator of ESCC tumor invasion and they indicate that organotypic (three-dimensional) culture can offer an important tool to discover novel biological effectors in cancer.

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References

Sasaki H, Dai M, Auclair D, Kaji M, Fukai I, Kiriyama M . Serum level of the periostin, a homologue of an insect cell adhesion molecule, in thymoma patients. Cancer Lett. 2001; 172(1):37-42. DOI: 10.1016/s0304-3835(01)00633-4. View

Sasaki H, Yu C, Dai M, Tam C, Loda M, Auclair D . Elevated serum periostin levels in patients with bone metastases from breast but not lung cancer. Breast Cancer Res Treat. 2003; 77(3):245-52. DOI: 10.1023/a:1021899904332. View

Xu X . Risk factors and gene expression in esophageal cancer. Methods Mol Biol. 2008; 471:335-60. DOI: 10.1007/978-1-59745-416-2_17. View

Sasaki H, Dai M, Auclair D, Fukai I, Kiriyama M, Yamakawa Y . Serum level of the periostin, a homologue of an insect cell adhesion molecule, as a prognostic marker in nonsmall cell lung carcinomas. Cancer. 2001; 92(4):843-8. DOI: 10.1002/1097-0142(20010815)92:4<843::aid-cncr1391>3.0.co;2-p. View

Kudo Y, Ogawa I, Kitajima S, Kitagawa M, Kawai H, Gaffney P . Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Res. 2006; 66(14):6928-35. DOI: 10.1158/0008-5472.CAN-05-4540. View

Calza S, Valentini D, Pawitan Y . Normalization of oligonucleotide arrays based on the least-variant set of genes. BMC Bioinformatics. 2008; 9:140. PMC: 2324100. DOI: 10.1186/1471-2105-9-140. View

Takeshita S, Kikuno R, Tezuka K, Amann E . Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J. 1993; 294 ( Pt 1):271-8. PMC: 1134594. DOI: 10.1042/bj2940271. View

Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M . Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell. 2004; 5(4):329-39. DOI: 10.1016/s1535-6108(04)00081-9. View

Butcher J, Norris R, Hoffman S, Mjaatvedt C, Markwald R . Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol. 2006; 302(1):256-66. PMC: 1913192. DOI: 10.1016/j.ydbio.2006.09.048. View

10.

Parkin D, Bray F, Ferlay J, Pisani P . Global cancer statistics, 2002. CA Cancer J Clin. 2005; 55(2):74-108. DOI: 10.3322/canjclin.55.2.74. View

11.

Lehrbach D, Nita M, Cecconello I . Molecular aspects of esophageal squamous cell carcinoma carcinogenesis. Arq Gastroenterol. 2004; 40(4):256-61. DOI: 10.1590/s0004-28032003000400011. View

12.

Lindner V, Wang Q, Conley B, Friesel R, Vary C . Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration. Arterioscler Thromb Vasc Biol. 2004; 25(1):77-83. DOI: 10.1161/01.ATV.0000149141.81230.c6. View

13.

Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H . 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; 14(7):1239-49. DOI: 10.1359/jbmr.1999.14.7.1239. View

14.

Nair K, Naidoo R, Chetty R . Expression of cell adhesion molecules in oesophageal carcinoma and its prognostic value. J Clin Pathol. 2005; 58(4):343-51. PMC: 1770622. DOI: 10.1136/jcp.2004.018036. View

15.

Okawa T, Michaylira C, Kalabis J, Stairs D, Nakagawa H, Andl C . The functional interplay between EGFR overexpression, hTERT activation, and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induces tumor development, invasion, and differentiation. Genes Dev. 2007; 21(21):2788-803. PMC: 2045132. DOI: 10.1101/gad.1544507. View

16.

Mueller M, Fusenig N . Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004; 4(11):839-49. DOI: 10.1038/nrc1477. View

17.

Gillan L, Matei D, Fishman D, Gerbin C, Karlan B, Chang D . 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; 62(18):5358-64. View

18.

Cavallaro U, Christofori G . Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer. 2004; 4(2):118-32. DOI: 10.1038/nrc1276. View

19.

Siriwardena B, Kudo Y, Ogawa I, Kitagawa M, Kitajima S, Hatano H . Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer. Br J Cancer. 2006; 95(10):1396-403. PMC: 2360586. DOI: 10.1038/sj.bjc.6603431. View

20.

Baril P, Gangeswaran R, Mahon P, Caulee K, Kocher H, Harada T . Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: role of the beta4 integrin and the PI3k pathway. Oncogene. 2006; 26(14):2082-94. DOI: 10.1038/sj.onc.1210009. View