Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 8701386, 9 pages
https://doi.org/10.1155/2017/8701386
Research Article

Heterogeneous Periostin Expression in Different Histological Variants of Papillary Thyroid Carcinoma

1Department of Morphofunctional Sciences I-Histology, Pathology, “Grigore T. Popa” University of Medicine and Pharmacy, Iasi, Romania
2Department of Pathology, Institute of Legal Medicine, Iasi, Romania
3Department of Pathology, “Sf. Spiridon” County Clinical Emergency Hospital, Iasi, Romania

Correspondence should be addressed to Cornelia Amalinei; moc.oohay@ienilama_ailenroc

Received 7 April 2017; Revised 19 November 2017; Accepted 3 December 2017; Published 25 December 2017

Academic Editor: Fotios Loupakis

Copyright © 2017 Simona Eliza Giusca et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. A. LiVosi, J. Albores-Saavedra, S. L. Asa et al., “Papillary carcinoma,” in World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of Endocrine Organs, pp. 57–66, IARC Press, Lyon, France, 2004. View at Google Scholar
  2. S. Erhamamci, M. Reyhan, N. E. Kocer, G. N. Nursal, N. Torun, and A. F. Yapar, “Simultaneous occurrence of medullary and differentiated thyroid carcinomas. Report of 4 cases and brief review of the literature,” Hellenic Journal of Nuclear Medicine, vol. 17, no. 2, pp. 148–152, 2014. View at Google Scholar · View at Scopus
  3. S. Takeshita, R. Kikuno, K. Tezuka, and E. Amann, “Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I,” Biochemical Journal, vol. 294, no. 1, pp. 271–278, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Horiuchi, N. Amizuka, S. Takeshita 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 β,” Journal of Bone and Mineral Research, vol. 14, no. 7, pp. 1239–1249, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. R. A. Norris, R. A. Moreno-Rodriguez, Y. Sugi et al., “Periostin regulates atrioventricular valve maturation,” Developmental Biology, vol. 316, no. 2, pp. 200–213, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. D. W. Hamilton, “Functional role of periostin in development and wound repair: implications for connective tissue disease,” Journal of Cell Communication and Signaling, vol. 2, no. 1-2, pp. 9–17, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Ruan, S. Bao, and G. Ouyang, “The multifaceted role of periostin in tumorigenesis,” Cellular and Molecular Life Sciences, vol. 66, no. 14, pp. 2219–2230, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Gillan, D. Matei, D. A. Fishman, C. S. Gerbin, B. Y. Karlan, and D. D. Chang, “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 Research, vol. 62, no. 18, pp. 5358–5364, 2002. View at Google Scholar
  9. I. T. Tai, M. Dai, and L. B. Chen, “Periostin induction in tumor cell line explants and inhibition of in vitro cell growth by anti-periostin antibodies,” Carcinogenesis, vol. 26, no. 5, pp. 908–915, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Kudo, B. S. M. S. Siriwardena, H. Hatano, I. Ogawa, and T. Takata, “Periostin: Novel diagnostic and therapeutic target for cancer,” Histology and Histopathology, vol. 22, no. 10-12, pp. 1167–1174, 2007. View at Google Scholar · View at Scopus
  11. P. V. Nuzzo, G. Buzzatti, F. Ricci et al., “Periostin: A novel prognostic and therapeutic target for genitourinary cancer?” Clinical Genitourinary Cancer, vol. 12, no. 5, pp. 301–311, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Zhu, M. S. Fejzo, L. Anderson et al., “Periostin promotes ovarian cancer angiogenesis and metastasis,” Gynecologic Oncology, vol. 119, no. 2, pp. 337–344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Morra and H. Moch, “Periostin expression and epithelial-mesenchymal transition in cancer: a review and an update,” Virchows Archiv, vol. 459, no. 5, pp. 465–475, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Ratajczak-Wielgomas and P. Dziegiel, “The role of periostin in neoplastic processes,” Folia Histochemica et Cytobiologica, vol. 53, no. 2, pp. 120–132, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. B. S. M. S. Siriwardena, Y. Kudo, I. Ogawa et al., “Periostin is frequently overexpressed and enhances invasion and angiogenesis in oral cancer,” British Journal of Cancer, vol. 95, no. 10, pp. 1396–1403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Chang, T. C. Lee, J. C. Li et al., “Differential expression of osteoblast-specific factor 2 and polymeric immunoglobulin receptor genes in nasopharyngeal carcinoma,” Head & Neck, vol. 27, no. 10, pp. 873–882, 2005. View at Google Scholar
  17. Y. Kudo, I. Ogawa, S. Kitajima et al., “Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer,” Cancer Research, vol. 66, no. 14, pp. 6928–6935, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Shao, S. Bao, X. Bai et al., “Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression,” Molecular and Cellular Biology, vol. 24, no. 9, pp. 3992–4003, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Puglisi, C. Puppin, E. Pegolo et al., “Expression of periostin in human breast cancer,” Journal of Clinical Pathology, vol. 61, no. 4, pp. 494–498, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Zhang, G. Zhang, J. Li, Q. Tao, and W. Tang, “The expression analysis of periostin in human breast cancer,” Journal of Surgical Research, vol. 160, no. 1, pp. 102–106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Xu, H. Xu, Y. Ren et al., “Cancer stem cell-related gene periostin: a novel prognostic marker for breast cancer,” PLoS ONE, vol. 7, no. 10, Article ID e46670, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Contié, N. Voorzanger-Rousselot, J. Litvin, P. Clézardin, and P. Garnero, “Increased expression and serum levels of the stromal cell-secreted protein periostin in breast cancer bone metastases,” International Journal of Cancer, vol. 128, no. 2, pp. 352–360, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. P. V. Nuzzo, A. Rubagotti, L. Zinoli, S. Salvi, S. Boccardo, and F. Boccardo, “The prognostic value of stromal and epithelial periostin expression in human breast cancer: Correlation with clinical pathological features and mortality outcome,” BMC Cancer, vol. 16, no. 1, article no. 95, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Zhu, R. E. Saxton, L. Ramos et al., “Neutralizing monoclonal antibody to periostin inhibits ovarian tumor growth and metastasis,” Molecular Cancer Therapeutics, vol. 10, no. 8, pp. 1500–1508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. K. U. Choi, J. S. Yun, I. H. Lee et al., “Lysophosphatidic acid-induced expression of periostin in stromal cells: Prognoistic relevance of periostin expression in epithelial ovarian cancer,” International Journal of Cancer, vol. 128, no. 2, pp. 332–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Y. Karlan, J. Dering, C. Walsh et al., “POSTN/TGFBI-associated stromal signature predicts poor prognosis in serous epithelial ovarian cancer,” Gynecologic Oncology, vol. 132, no. 2, pp. 334–342, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Tsunoda, B. Furusato, Y. Takashima et al., “The increased expression of periostin during early stages of prostate cancer and advanced stages of cancer stroma,” The Prostate, vol. 69, no. 13, pp. 1398–1403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Tischler, F. R. Fritzsche, P. J. Wild et al., “Periostin is up-regulated in high grade and high stage prostate cancer,” BMC Cancer, vol. 10, article no. 273, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Sun, X. Zhao, K. Xu et al., “Periostin: A promising target of therapeutical intervention for prostate cancer,” Journal of Translational Medicine, vol. 9, no. 1, article no. 99, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. P. V. Nuzzo, A. Rubagotti, L. Zinoli et al., “Prognostic value of stromal and epithelial periostin expression in human prostate cancer: correlation with clinical pathological features and the risk of biochemical relapse or death,” BMC Cancer, vol. 12, article 625, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Castronovo, D. Waltregny, P. Kischel et al., “A chemical proteomics approach for the identification of accessible antigens expressed in human kidney cancer,” Molecular & Cellular Proteomics, vol. 5, no. 11, pp. 2083–2091, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Dahinden, B. Ingold, P. Wild et al., “Mining tissue microarray data to uncover combinations of biomarker expression patterns that improve intermediate staging and grading of clear cell renal cell cancer,” Clinical Cancer Research, vol. 16, no. 1, pp. 88–98, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Morra, M. Rechsteiner, S. Casagrande et al., “Relevance of periostin splice variants in renal cell carcinoma,” The American Journal of Pathology, vol. 179, no. 3, pp. 1513–1521, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Baril, R. Gangeswaran, P. C. Mahon et al., “Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: role of the β4 integrin and the PI3k pathway,” Oncogene, vol. 26, no. 14, pp. 2082–2094, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. Q.-W. Ben, X.-L. Jin, L. Jun, X. Cai, F. Yuan, and Y.-Z. Yuan, “Periostin, a matrix specific protein, is associated with proliferation and invasion of pancreatic cancer,” Oncology Reports, vol. 25, no. 3, pp. 709–716, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. J.-S. Li, G.-W. Sun, X.-Y. Wei, and W.-H. Tang, “Expression of periostin and its clinicopathological relevance in gastric cancer,” World Journal of Gastroenterology, vol. 13, no. 39, pp. 5261–5266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Kikuchi, A. Kunita, C. Iwata et al., “The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation,” The American Journal of Pathology, vol. 184, no. 3, pp. 859–870, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Lv, R. Liu, J. Fu et al., “Epithelial cell-derived periostin functions as a tumor suppressor in gastric cancer through stabilizing p53 and E-cadherin proteins via the Rb/E2F1/p14ARF/Mdm2 signaling pathway,” Cell Cycle, vol. 13, no. 18, pp. 2962–2974, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Bao, G. Ouyang, X. Bai et al., “Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway,” Cancer Cell, vol. 5, no. 4, pp. 329–339, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. Z.-M. Xiao, X.-Y. Wang, and A.-M. Wang, “Periostin induces chemoresistance in colon cancer cells through activation of the PI3K/Akt/survivin pathway,” Biotechnology and Applied Biochemistry, vol. 62, no. 3, pp. 401–406, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. M.-O. Riener, F. R. Fritzsche, C. Soll et al., “Expression of the extracellular matrix protein periostin in liver tumours and bile duct carcinomas,” Histopathology, vol. 56, no. 5, pp. 600–606, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Y. Jang, S. Y. Park, H. W. Lee et al., “The combination of periostin overexpression and microvascular invasion is related to a poor prognosis for hepatocellular carcinoma,” Gut and Liver, vol. 10, no. 6, pp. 948–954, 2016. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Sasaki, D. Auclair, I. Fukai et al., “Serum level of the periostin, a homologue of an insect cell adhesion molecule, as a prognostic marker in nonsmall cell lung carcinomas,” Cancer, vol. 92, no. 4, pp. 843–848, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Soltermann, V. Tischler, S. Arbogast et al., “Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer,” Clinical Cancer Research, vol. 14, no. 22, pp. 7430–7437, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Morra, M. Rechsteiner, S. Casagrande et al., “Characterization of periostin isoform pattern in non-small cell lung cancer,” Lung Cancer, vol. 76, no. 2, pp. 183–190, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. L.-Z. Hong, X.-W. Wei, J.-F. Chen, and Y. Shi, “Overexpression of periostin predicts poor prognosis in non-small cell lung cancer,” Oncology Letters, vol. 6, no. 6, pp. 1595–1603, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Schramm, I. Opitz, S. Thies et al., “Prognostic significance of epithelial-mesenchymal transition in malignant pleural mesothelioma,” European Journal of Cardio-Thoracic Surgery, vol. 37, no. 3, pp. 566–572, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Sasaki, Y. Sato, S. Kondo et al., “Expression of the periostin mRNA level in neuroblastoma,” Journal of Pediatric Surgery, vol. 37, no. 9, pp. 1293–1297, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. B. Tian, Y. Zhang, and J. Zhang, “Periostin is a new potential prognostic biomarker for glioma,” Tumor Biology, vol. 35, no. 6, pp. 5877–5883, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. W. Zhou, S. Q. Ke, Z. Huang et al., “Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth,” Nature Cell Biology, vol. 17, no. 2, pp. 170–182, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. A. M. Mikheev, S. A. Mikheeva, A. D. Trister et al., “Periostin is a novel therapeutic target that predicts and regulates glioma malignancy,” Neuro-Oncology, vol. 17, no. 3, pp. 372–382, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. F. L. Greene, D. L. Page, I. D. Fleming et al., Eds., AJCC Cancer Staging Handbook, Springer, New York, NY, USA, 6th edition, 2002.
  53. W. Jia, W. Wang, C.-S. Ji et al., “Coexpression of periostin and EGFR in patients with esophageal squamous cell carcinoma and their prognostic significance,” OncoTargets and Therapy, vol. 9, pp. 5133–5142, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. P.-L. Sung, Y.-H. Jan, S.-C. Lin et al., “Periostin in tumor microenvironment is associated with poor prognosis and platinum resistance in epithelial ovarian carcinoma,” Oncotarget , vol. 7, no. 4, pp. 4036–4047, 2016. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Litvin, A.-H. Selim, M. O. Montgomery et al., “Expression and function of periostin-isoforms in bone,” Journal of Cellular Biochemistry, vol. 92, no. 5, pp. 1044–1061, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Litvin, S. Zhu, R. Norris, and R. Markwald, “Periostin family of proteins: Therapeutic targets for heart disease,” Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology, vol. 287, no. 2, pp. 1205–1212, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. C. J. Kim, T. Isono, Y. Tambe et al., “Role of alternative splicing of periostin in human bladder carcinogenesis,” International Journal of Oncology, vol. 32, no. 1, pp. 161–169, 2008. View at Google Scholar · View at Scopus
  58. Y. Bai, M. Nakamura, G. Zhou et al., “Novel isoforms of periostin expressed in the human thyroid,” Japanese Clinical Medicine, vol. 1, pp. 13–20, 2010. View at Publisher · View at Google Scholar
  59. S. Hoersch and M. A. Andrade-Navarro, “Periostin shows increased evolutionary plasticity in its alternatively spliced region,” BMC Evolutionary Biology, vol. 10, no. 1, article no. 30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Kudo, “Periostin in fibrillogenesis for tissue regeneration: Periostin actions inside and outside the cell,” Cellular and Molecular Life Sciences, vol. 68, no. 19, pp. 3201–3207, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. S. J. Conway, K. Izuhara, Y. Kudo et al., “The role of periostin in tissue remodeling across health and disease,” Cellular and Molecular Life Sciences, vol. 71, no. 7, pp. 1279–1288, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Utispan, J. Sonongbua, P. Thuwajit et al., “Periostin activates integrin α5β1 through a PI3K/AKT-dependent, pathway in invasion of cholangiocarcinoma,” International Journal of Oncology, vol. 41, no. 3, pp. 1110–1118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Lv, W. Wang, W. Jia et al., “High-level expression of periostin is closely related to metastatic potential and poor prognosis of hepatocellular carcinoma,” Medical Oncology, vol. 30, no. 1, pp. 1–9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Li, S. Oparil, W. Feng, and Y.-F. Chen, “Hypoxia-responsive growth factors upregulate periostin and osteopontin expression via distinct signaling pathways in rat pulmonary arterial smooth muscle cells,” Journal of Applied Physiology, vol. 97, no. 4, pp. 1550–1558, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. W. Yan and R. Shao, “Transduction of a mesenchyme-specific gene periostin into 293T cells induces cell invasive activity through epithelial-mesenchymal transformation,” The Journal of Biological Chemistry, vol. 281, no. 28, pp. 19700–19708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. C. J. Kim, K. Sakamoto, Y. Tambe, and H. Inoue, “Opposite regulation of epithelial-to-mesenchymal transition and cell invasiveness by periostin between prostate and bladder cancer cells,” International Journal of Oncology, vol. 38, no. 6, pp. 1759–1766, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. Kudo, S. Iizuka, M. Yoshida et al., “Periostin directly and indirectly promotes tumor lymphangiogenesis of head and neck cancer,” PLoS ONE, vol. 7, no. 8, Article ID e44488, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. Ø. Fluge, O. Bruland, L. A. Akslen, J. R. Lillehaug, and J. E. Varhaug, “Gene expression in poorly differentiated papillary thyroid carcinomas,” Thyroid, vol. 16, no. 2, pp. 161–175, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. Y. Bai, K. Kakudo, M. Nakamura et al., “Loss of cellular polarity/cohesiveness in the invasive front of papillary thyroid carcinoma and periostin expression,” Cancer Letters, vol. 281, no. 2, pp. 188–195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Puppin, D. Fabbro, M. Dima et al., “High periostin expression correlates with aggressiveness in papillary thyroid carcinomas,” Journal of Endocrinology, vol. 197, no. 2, pp. 401–408, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Hu, W. Wang, H.-C. Zhou, and X.-F. Shang, “High expression of periostin is dramatically associated with metastatic potential and poor prognosis of patients with osteosarcoma,” World Journal of Surgical Oncology, vol. 12, no. 1, article no. 287, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. N. Fukushima, Y. Kikuchi, T. Nishiyama, A. Kudo, and M. Fukayama, “Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas,” Modern Pathology, vol. 21, no. 8, pp. 1044–1053, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. R. A. Morris, B. Damon, V. Mironov et al., “Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues,” Journal of Cellular Biochemistry, vol. 101, no. 3, pp. 695–711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. G. Takayama, K. Arima, T. Kanaji et al., “Periostin: A novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals,” The Journal of Allergy and Clinical Immunology, vol. 118, no. 1, pp. 98–104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Gunia, A. Jain, S. Koch et al., “Periostin expression correlates with pT-stage, grading and tumour size, and independently predicts cancer-specific survival in surgically treated penile squamous cell carcinomas,” Journal of Clinical Pathology, vol. 66, no. 4, pp. 297–301, 2013. View at Publisher · View at Google Scholar · View at Scopus