Top

Published in:

Open Access 01-12-2021 | Goiter | Short report

Periostin expression and its supposed roles in benign and malignant thyroid nodules: an immunohistochemical study of 105 cases

Authors: Kimihide Kusafuka, Masaru Yamashita, Tomohiro Iwasaki, Chinatsu Tsuchiya, Aki Kubota, Kazuki Hirata, Akinori Murakami, Aya Muramatsu, Kazumori Arai, Makoto Suzuki

Published in: Diagnostic Pathology | Issue 1/2021

Abstract

Background

Thyroid tumors are often difficult to histopathologically diagnose, particularly follicular adenoma (FA) and follicular carcinoma (FC). Papillary carcinoma (PAC) has several histological subtypes. Periostin (PON), which is a non-collagenous extracellular matrix molecule, has been implicated in tumor invasiveness. We herein aimed to elucidate the expression status and localization of PON in thyroid tumors.

Method

We collected 105 cases of thyroid nodules, which included cases of adenomatous goiter, FA, microcarcinoma (MIC), PAC, FC, poorly differentiated carcinoma (PDCa), and undifferentiated carcinoma (UCa), and immunohistochemically examined the PON expression patterns of these lesions.

Results

Stromal PON deposition was detected in PAC and MIC, particularly in the solid/sclerosing subtype, whereas FA and FC showed weak deposition on the fibrous capsule. However, the invasive and/or extracapsular regions of microinvasive FC showed quite strong PON expression. Except for it, we could not find any significant histopathological differences between FA and FC. There were no other significant histopathological differences between FA and FC. Although PDCa showed a similar PON expression pattern to PAC, UCa exhibited stromal PON deposition in its invasive portions and cytoplasmic expression in its carcinoma cells. Although there was only one case of UCa, it showed strong PON immunopositivity. PAC and MIC showed similar patterns of stromal PON deposition, particularly at the invasive front.

Conclusions

PON may play a role in the invasion of thyroid carcinomas, particularly PAC and UCa, whereas it may act as a barrier to the growth of tumor cells in FA and minimally invasive FC.

Available only for authorised users

Rosai J, Albores Saavedra J, Asioki S, Bolach ZW, Bogdova T, Chen H. Papillary carcinoma. In: Lloyd RV, Osamura RY, Kloppel G, Rosai J, editors. WHO classification of Tumours of endocrine organs. 4th ed. Lyon: IARC Press. 2017:81–91.

LiVolsi V, Abdulkader Nalib I, Baloch ZW, Bartolazzi A, Chan JKC, DeLellis RA. Follicular thyroidal carcinoma. In: Lloyd RV, Osamura RY, Kloppel G, Rosai J, editors. WHO classification of Tumours of endocrine organs. 4th ed. Lyon: IARC Press. 2017:92–5.

Santi A, Kugeratski FG, Zanivan S. Cancer associated fibroblasts: the architects of stroma remodeling. Proteomics. 2018;18(5-6):e1700167. https://doi.org/10.1002/pmic.201700167.CrossRefPubMed

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(7):1239–49. https://doi.org/10.1359/jbmr.1999.14.7.1239.CrossRefPubMed

Kudo A. Periostin in bone biology. Adv Exp Med Biol. 2019;1132:43–7. https://doi.org/10.1007/978-981-13-6657-4_5.CrossRefPubMed

Nuzzo PV, Rubagotti A, Zinoli L, Salvi S, Boccardo S, Boccardo F. The prognostic value of stromal and epithelial periostin expression in human breast cancer: correlation with clinical pathological features and mortality outcome. BMC Cancer. 2016;16(1):95. https://doi.org/10.1186/s12885-016-2139-y.CrossRefPubMedPubMedCentral

Shao R, Bao B, Bai X, Blanchette C, Anderson RM, Dang T, et al. 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;24(9):3992–4003. https://doi.org/10.1128/MCB.24.9.3992-4003.2004.CrossRefPubMedPubMedCentral

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(10):1396–403. https://doi.org/10.1038/sj.bjc.6603431.CrossRefPubMedPubMedCentral

Jang SY, Park SY, Lee HW, Choi Y-K, Park K-G, Yoon GS, et al. The combination of periostin overexpression and microvascular invasion in related to a poor prognosis for hepatocellular carcinoma. Gut Liver. 2016;10(6):948–54. https://doi.org/10.5009/gnl15481.CrossRefPubMedPubMedCentral

10.

Takeshita S, Kikuno R, Tezuka K, Amann E. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with insert protein fasciclin I. Biochem J. 1993;294(Pt1):271–8. https://doi.org/10.1042/bj2940271.CrossRefPubMedPubMedCentral

11.

Nunomura S, Nanri Y, Okawa M, Arima K, Mitamura Y, Yoshihara T, et al. Constitutive overexpression of periostin delays wound healing in mouse skin. Wound Repair Regen. 2018;26(1):6–15. https://doi.org/10.1111/wrr.12616.CrossRefPubMedPubMedCentral

12.

Cobo T, Viloria CG, Solares L, Fontanil T, Gonzalez-Chamorro E, De Carlos F, et al. Role of periostin in adhesion and migration of bone remodeling cells. PLoS One. 2016;11(1):e0147837. https://doi.org/10.1371/journal.pone.0147837.CrossRefPubMedPubMedCentral

13.

Zhao S, Wu H, Xia W, Chen X, Zhu S, Zhang S, et al. Periostin expression is upregulated and associated with myocardial fibrosis in human failing hearts. J Cardiol. 2014;63(5):373–8. https://doi.org/10.1016/j.jjcc.2013.09.013.CrossRefPubMed

14.

Braun N, Sen K, Alscher MD, Fritz P, Kimmel M, Morelle J, et al. Periostin: a matricellular protein involved in peritoneal injury during peritoneal dialysis. Perit Dial Int. 2013;33(5):515–28. https://doi.org/10.3747/pdi.2010.00259.CrossRefPubMedPubMedCentral

15.

Nuzzo PV, Buzzatti G, Ricci F, Rubagotti A, Argellati F, Zinoli L, et al. Periostin: a novel prognostic and therapeutic target for genitourinary cancer? Clin Genitourin Cancer. 2014;12(5):301–11. https://doi.org/10.1016/j.clgc.2014.02.005.CrossRefPubMed

16.

Takanami I, Abiko T, Koizumi S. Expression of periostin in patients with non-small-cell lung cancer: correlation with angiogenesis and lymphangiogenesis. Int J Biol Markers. 2008;23(3):182–6. https://doi.org/10.1177/172460080802300308.CrossRefPubMed

17.

Nissen NI, Karsdal M, Willumsen N. Collagens and cancer associated fibroblasts in the reactive stroma and its relation to cancer biology. J Exp Clin Cancer Res. 2019;38(1):115. https://doi.org/10.1186/s13046-019-1110-6.CrossRefPubMedPubMedCentral

18.

Oh HJ, Bae JM, Wen XY, Cho NY, Kim JH, Kang GH. Overexpression of POSTN in tumor stroma is a poor prognostic indicator of colorectal cancer. J Pathol Trans Med. 2017;51(3):306–13.CrossRef

19.

Ratajczak-Wielgomas K, Grzegrzolka J, Piotrowska A, Gomulkiewicz A, Witkiewicz W, Dziegial P. Periostin expression in cancer-associated fibroblasts of invasive ductal breast carcinoma. Oncol Rep. 2016;36(5):2745–54. https://doi.org/10.3892/or.2016.5095.CrossRefPubMed

20.

Kikuchi Y, Kunita A, Iwata C, Komura D, Nishiyama T, Shimazu K, et al. The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am J Pathol. 2014;184(3):859–70. https://doi.org/10.1016/j.ajpath.2013.11.012.CrossRefPubMed

21.

Bai Y, Kakudo K, Nakamura M, Ozaki T, Li Y, Liu Z, et al. Loss of cellular polarity/cohesiveness in the invasive front of papillary thyroid carcinoma and periostin expression. Cancer Lett. 2009;281(2):188–95. https://doi.org/10.1016/j.canlet.2009.02.043.CrossRefPubMed

22.

Bai Y, Nakamura M, Zhou G, Li Y, Liu Z, Ozaki T, et al. Novel isoforms of periostin expressed in the human thyroid. J Clin Med. 2010;1:13–20. https://doi.org/10.4137/JCM.S5899.CrossRef

23.

Kim CJ, Isono T, Tambe Y, Chano T, Okabe H, Okada Y, et al. Role of alternative splicing of periostin in human bladder carcinogenesis. Int J Oncol. 2008;32(1):161–9. https://doi.org/10.3892/ijo.32.1.161.CrossRefPubMed

24.

Saleh HA, Jin B, Barnwell J, Alzohaili O. Utility of immunohistochemical markers in differentiating benign from malignant follicular-derived thyroid nodules. Diagn Pathol. 2010;5(1). https://doi.org/10.1186/1746-1596-5-9.

25.

Prasad ML, Pellegata NS, Huang Y, Nagaraja HN, de la Chapelle A, Kloos RT. Galectin-3, fibronectin-1, CITED-1, HBME-1 and cytokeratin-19 immunohistochemistry is useful for the differential diagnosis of the thyroid tumors. Mod Pathol. 2005;18(1):48–57. https://doi.org/10.1038/modpathol.3800235.CrossRefPubMed

26.

Juan C-K, Kang Y-G, Bae J-S, Lim D-J, Choi Y-J, Lee K-Y. Unique patterns of tumor growth related with the risk of lymph node metastasis in papillary thyroid carcinoma. Mod Pathol. 2010;23(9):1201–8. https://doi.org/10.1038/modpathol.2010.116.CrossRef

Title: Periostin expression and its supposed roles in benign and malignant thyroid nodules: an immunohistochemical study of 105 cases
Authors: Kimihide Kusafuka
Masaru Yamashita
Tomohiro Iwasaki
Chinatsu Tsuchiya
Aki Kubota
Kazuki Hirata
Akinori Murakami
Aya Muramatsu
Kazumori Arai
Makoto Suzuki
Publication date: 01-12-2021
Publisher: BioMed Central
Keyword: Goiter
Published in: Diagnostic Pathology / Issue 1/2021
Electronic ISSN: 1746-1596
DOI: https://doi.org/10.1186/s13000-021-01146-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Periostin expression and its supposed roles in benign and malignant thyroid nodules: an immunohistochemical study of 105 cases

Abstract

Background

Method

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Method

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2021

Clear cell and papillary renal cell carcinomas in hereditary papillary renal cell carcinoma (HPRCC) syndrome: a case report

Pulmonary tumor with Notochordal differentiation: a case report and morphologic, Immunohistochemical and molecular study of benign Notochordal cell tumor originating in the lung

Kaposiform Hemangioendothelioma: clinicopathological characteristics of 8 cases of a rare vascular tumor and review of literature

Extranodal natural killer/T-cell lymphoma nasal type with extensive ocular tissue involvement: a case report

CpG islands in MyD88 and ASC/PYCARD/TMS1 promoter regions are differentially methylated in head and neck squamous cell carcinoma and primary lung squamous cell carcinoma

Pancreatic medullary carcinoma developed on a pancreatic intraductal papillary mucinous neoplasm with loss of MSH2 and MSH6 expression: a case report