Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment

Oncogenesis

Volumn 2, Issue , 2013, Pages

  Wong, G S ^a,b   Lee, J S ^c   Park, Y Y ^c   Klein Szanto, A J ^d   Waldron, T J ^a,b   Cukierman, E ^d   Herlyn, M ^e   Gimotty, P ^b,f   Nakagawa, H ^a,b   Rustgi, A K ^a,b,f  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d FOX CHASE CANCER CENTER   (United States)

^e WISTAR INSTITUTE   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

invasion; mutant p53; periostin; STAT1; tumor microenvironment

Indexed keywords

PROTEIN P53; STAT1 PROTEIN; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; EPITHELIUM CELL; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS TUMOR; EXTRACELLULAR MATRIX; IN VIVO STUDY; MISSENSE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT;

EID: 84881434842     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2013.17     Document Type: Article

References (48)

1. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med 2003; 349: 2241-2252. (Pubitemid 37485141)
2. Wang LS, Chow KC, Chi KH, Liu CC, Li WY, Chiu JH et al. Prognosis of esophageal squamous cell carcinoma: analysis of clinicopathological and biological factors. Am J Gastroenterol 1999; 94: 1933-1940.
3. Xu XC. Risk factors and gene expression in esophageal cancer. Methods Mol Biol 2009; 471: 335-360.
4. Sibilia M, Kroismayr R, Lichtenberger BM, Natarajan A, Hecking M, Holcmann M. The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 2007; 75: 770-787. (Pubitemid 350086174)
5. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009; 137: 413-431.
6. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat Rev Cancer 2009; 9: 701-713.
7. Muller PA, Vousden KH, Norman JC. p53 and its mutants in tumor cell migration and invasion. J Cell Biol 2011; 192: 209-218.
8. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004; 119: 847-860. (Pubitemid 40017690)
9. Lozano G, Behringer RR. New mouse models of cancer: single-cell knockouts. Proc Natl Acad Sci USA 2007; 104: 4245-4246. (Pubitemid 47186210)
10. McCabe ML, Dlamini Z. The molecular mechanisms of oesophageal cancer. Int Immunopharmacol 2005; 5: 1113-1130. (Pubitemid 40725707)
11. Christofori G. New signals from the invasive front. Nature 2006; 441: 444-450. (Pubitemid 44050139)
12. Beacham DA, Cukierman E. Stromagenesis: the changing face of fibroblastic microenvironments during tumor progression. Semin Cancer Biol 2005; 15: 329-341. (Pubitemid 41140303)
13. Chiodoni C, Colombo MP, Sangaletti S. Matricellular proteins: from homeostasis to inflammation, cancer, and metastasis. Cancer Metastasis Rev 2010; 29: 295-307.
14. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 2011; 17: 867-874.
15. McAllister SS, Gifford AM, Greiner AL, Kelleher SP, Saelzler MP, Ince TA et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008; 133: 994-1005. (Pubitemid 351787747)
16. Wong GS, Rustgi AK. Matricellular proteins: priming the tumour microenviron-ment for cancer development and metastasis. Br J Cancer 2013; 108: 755-761.
17. Fukunaga-Kalabis M, Santiago-Walker A, Herlyn M. Matricellular proteins produced by melanocytes and melanomas: in search for functions. Cancer Microenviron 2008; 1: 93-102.
18. Soltermann A, Tischler V, Arbogast S, Braun J, Probst-Hensch N, Weder W et al. Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer. Clin Cancer Res 2008; 14: 7430-7437.
19. Michaylira CZ, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R et al. Periostin, a cell adhesion molecule, facilitates invasion in the tumor micro-environment and annotates a novel tumor-invasive signature in esophageal cancer. Cancer Res 2010; 70: 5281-5292.
20. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H et al. 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: 1239-1249. (Pubitemid 29314070)
21. 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): 271-278. (Pubitemid 23251940)
22. Wong GS, Habibollahi P, Heidari P, Lee JS, Klein-Szanto AJ, Waldron TJ et al. Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology 2012; S0016-5085: 01546-01546.
23. Muller PA, Vousden KH. p53 mutations in cancer. Nat Cell Biol 2013; 15: 2-8.
24. Wang W, Kim SH, El-Deiry WS. Small-molecule modulators of p53 family signaling and antitumor effects in p53-deficient human colon tumor xenografts. Proc Natl Acad Sci USA 2006; 103: 11003-11008. (Pubitemid 44148408)
25. Su H, Hu N, Yang HH, Wang C, Takikita M, Wang QH et al. Global gene expression profiling and validation in esophageal squamous cell carcinoma and its association with clinical phenotypes. Clin Cancer Res 2011; 17: 2955-2966.
26. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M et al. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 2004; 5: 329-339. (Pubitemid 38482069)
27. Puglisi F, Puppin C, Pegolo E, Andreetta C, Pascoletti G, D'Aurizio F et al. Expression of periostin in human breast cancer. J Clin Pathol 2008; 61: 494-498. (Pubitemid 351518233)
28. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2012; 481: 85-89.
29. Petitjean A, Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor pheno-type: lessons from recent developments in the IARC TP53 database. Hum Mutat 2007; 28: 622-629. (Pubitemid 46744292)
30. Wiman KG. Pharmacological reactivation of mutant p53: from protein structure to the cancer patient. Oncogene 2010; 29: 4245-4252.
31. Bykov VJ, Selivanova G, Wiman KG. Small molecules that reactivate mutant p53. Eur J Cancer 2003; 39: 1828-1834. (Pubitemid 37311177)
32. Issaeva N, Bozko P, Enge M, Protopopova M, Verhoef LG, Masucci M et al. Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 2004; 10: 1321-1328. (Pubitemid 40022713)
33. Wang Y, Suh YA, Fuller MY, Jackson JG, Xiong S, Terzian T et al. Restoring expression of wild-type p53 suppresses tumor growth but does not cause tumor regression in mice with a p53 missense mutation. J Clin Invest 2011; 121: 893-904.
34. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011; 331: 1559-1564.
35. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-252.
36. Roberts DD. Emerging functions of matricellular proteins. Cell Mol Life Sci 2011; 68: 3133-3136.
37. Kwon Y, Cukierman E, Godwin AK. Differential expressions of adhesive molecules and proteases define mechanisms of ovarian tumor cell matrix penetration/invasion. PLoS One 2011; 6: e18872.
38. Sasaki H, Yu CY, Dai M, Tam C, Loda M, Auclair D et al. Elevated serum periostin levels in patients with bone metastases from breast but not lung cancer. Breast Cancer Res Treat 2003; 77: 245-252. (Pubitemid 36197639)
39. Sasaki H, Lo KM, Chen LB, Auclair D, Nakashima Y, Moriyama S et al. 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; 92: 869-873. (Pubitemid 32894097)
40. Siriwardena BS, Kudo Y, Ogawa I, Kitagawa M, Kitajima S, Hatano H et al. Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer. Br J Cancer 2006; 95: 1396-1403. (Pubitemid 44760092)
41. Khodarev NN, Roizman B, Weichselbaum RR. Molecular pathways: interferon/stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin Cancer Res 2012; 18: 3015-3021.
42. Khodarev NN, Minn AJ, Efimova EV, Darga TE, Labay E, Beckett M et al. Signal transducer and activator of transcription 1 regulates both cytotoxic and prosurvival functions in tumor cells. Cancer Res 2007; 67: 9214-9220. (Pubitemid 47535908)
43. Schultz J, Koczan D, Schmitz U, Ibrahim SM, Pilch D, Landsberg J et al. Tumor-promoting role of signal transducer and activator of transcription (Stat)1 in late-stage melanoma growth. Clin Exp Metastasis 2010; 27: 133-140.
44. Khodarev NN, Roach P, Pitroda SP, Golden DW, Bhayani M, Shao MY et al. STAT1 pathway mediates amplification of metastatic potential and resistance to therapy. PLoS One 2009; 4: e5821.
45. Wu Y, Antony S, Juhasz A, Lu J, Ge Y, Jiang G et al. Up-regulation and sustained activation of Stat1 are essential for interferon-gamma (IFN-gamma)-induced dual oxidase 2 (Duox2) and dual oxidase A2 (DuoxA2) expression in human pancreatic cancer cell lines. J Biol Chem 2011; 286: 12245-12256.
46. Smith C, Chang MY, Parker KH, Beury DW, DuHadaway JB, Flick HE et al. IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov 2012; 2: 722-735.
47. Okawa T, Michaylira CZ, Kalabis J, Stairs DB, Nakagawa H, Andl CD et al. 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: 2788-2803. (Pubitemid 350070724)
48. Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, Klein-Szanto AJ et al. Fibroblast-secreted hepatocyte growth factor plays a functional role in esopha-geal squamous cell carcinoma invasion. Proc Natl Acad Sci USA 2010; 107: 11026-11031.