Intercellular adhesion molecule 1 is a sensitive and diagnostically useful immunohistochemical marker of papillary thyroid cancer (PTC) and of PTC‑like nuclear alterations in Hashimoto's thyroiditis

Zhang,Ke; Ge,Shu‑Jian; Lin,Xiao‑Yan; Lv,Bei‑Bei; Cao,Zhi‑Xin; Li,Jia‑Mei; Xu,Jia‑Wen; Wang,Qiang‑Xiu

doi:10.3892/ol.2016.4104

Intercellular adhesion molecule 1 is a sensitive and diagnostically useful immunohistochemical marker of papillary thyroid cancer (PTC) and of PTC‑like nuclear alterations in Hashimoto's thyroiditis

Authors:
- Ke Zhang
- Shu‑Jian Ge
- Xiao‑Yan Lin
- Bei‑Bei Lv
- Zhi‑Xin Cao
- Jia‑Mei Li
- Jia‑Wen Xu
- Qiang‑Xiu Wang
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Affiliations: Department of Nuclear Medicine, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong 250021, P.R. China, Department of Science and Education, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong 250021, P.R. China, Department of Pathology, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong 250021, P.R. China
Published online on: January 14, 2016 https://doi.org/10.3892/ol.2016.4104
Pages: 1722-1730
Copyright: © Zhang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Intercellular adhesion molecule 1 (ICAM‑1) is important in the progression of inflammatory responses. Recently, increased levels of ICAM‑1 have been reported in a number of types of malignancy. The present study aimed to investigate ICAM‑1 expression in papillary thyroid cancer (PTC) and in Hashimoto's thyroiditis (HT) with PTC‑like nuclear alterations, and to assess the predictive value of ICAM‑1 in thyroid lesions. ICAM‑1 expression was retrospectively investigated in 132 consecutive cases of PTC, 72 cases of HT, 10 of follicular cancer, 15 of follicular adenoma, 16 of nodular goiter and 8 samples of normal thyroid tissue using immunohistochemical analyses, and in 42 PTC patients using western blotting. ICAM‑1 expression was not detected in normal follicular cells, follicular lesions (adenoma and cancer) and benign nodular hyperplasia, but was frequently overexpressed in PTC cells. ICAM‑1 overexpression was associated with extra‑thyroidal invasion and lymph node metastasis; no association was found with age, gender, tumor size, multifocality, pathological stage, recurrence or distant metastasis. ICAM‑1 expression in HT patients with PTC‑like nuclear alterations was significantly higher than that in HT cases with non‑PTC‑like features. Compared with antibodies against cytokeratin 19, galectin‑3 and Hector Battifora mesothelial‑1, ICAM‑1 was the most sensitive marker for the detection of PTC‑like features in HT. These findings demonstrate that ICAM‑1 expression is upregulated in PTC and in HT with PTC‑like nuclear alterations. This feature may be an important factor in the progression of cancer of the thyroid gland.

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1	Cheema Y, Repplinger D, Elson D and Chen H: Is tumor size the best predictor of outcome for papillary thyroid cancer? Ann Surg Oncol. 13:1524–1528. 2006. View Article : Google Scholar : PubMed/NCBI
2	Hayes SH and Seigel GM: Immunoreactivity of ICAM-1 in human tumors, metastases and normal tissues. Int J Clin Exp Pathol. 2:553–560. 2009.PubMed/NCBI
3	Chen H, Hernandez W, Shriver MD, Ahaghotu CA and Kittles RA: ICAM gene cluster SNPs and prostate cancer risk in African Americans. Hum Genet. 120:69–76. 2006. View Article : Google Scholar : PubMed/NCBI
4	Rosette C, Roth RB, Oeth P, Braun A, Kammerer S, Ekblom J and Denissenko MF: Role of ICAM1 in invasion of human breast cancer cells. Carcinogenesis. 26:943–950. 2005. View Article : Google Scholar : PubMed/NCBI
5	Usami Y, Ishida K, Sato S, Kishino M, Kiryu M, Ogawa Y, Okura M, Fukuda Y and Toyosawa S: Intercellular adhesion molecule-1 (ICAM-1) expression correlates with oral cancer progression and induces macrophage/cancer cell adhesion. Int J Cancer. 133:568–578. 2013. View Article : Google Scholar : PubMed/NCBI
6	Nakashima M, Eguchi K, Ishikawa N, Yamashita I, Sakai M, Ida H, Kawabe Y, Ito K and Nagataki S: Expression of adhesion molecule ICAM-1 (CD54) in thyroid papillary adenocarcinoma. J Endocrinol Invest. 17:843–848. 1994. View Article : Google Scholar : PubMed/NCBI
7	Buitrago D, Keutgen XM, Crowley M, Filicori F, Aldailami H, Hoda R, Liu YF, Hoda RS, Scognamiglio T, Jin M, et al: Intercellular adhesion molecule-1 (ICAM-1) is upregulated in aggressive papillary thyroid carcinoma. Ann Surg Oncol. 19:973–980. 2012. View Article : Google Scholar : PubMed/NCBI
8	DeLellis RA and Williams ED: Tumours of the thyroid and parathyroid. World Health Organization Classification of Tumours. Pathology and Genetics of Endocrine Organs (Lyon). IARC Press. 58–70. 2004.
9	Edge SB and Compton CC: The American Joint Committee on Cancer: The 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 17:1471–1474. 2010. View Article : Google Scholar : PubMed/NCBI
10	Cvejic D, Savin S, Petrovic I, Paunovic I, Tatic S, Krgovic K and Havelka M: Galectin-3 expression in papillary microcarcinoma of the thyroid. Histopathology. 47:209–214. 2005. View Article : Google Scholar : PubMed/NCBI
11	Cheema Y, Olson S, Elson D and Chen H: What is the biology and optimal treatment for papillary microcarcinoma of the thyroid? J Surg Res. 134:160–162. 2006. View Article : Google Scholar : PubMed/NCBI
12	Kabaker AS, Tublin ME, Nikiforov YE, Armstrong MJ, Hodak SP, Stang MT, McCoy KL, Carty SE and Yip L: Suspicious ultrasound characteristics predict BRAF V600E-positive papillary thyroid carcinoma. Thyroid. 22:585–589. 2012. View Article : Google Scholar : PubMed/NCBI
13	Scognamiglio T, Hyjek E, Kao J and Chen YT: Diagnostic usefulness of HBME1, galectin-3, CK19 and CITED1 and evaluation of their expression in encapsulated lesions with questionable features of papillary thyroid carcinoma. Am J Clin Pathol. 126:700–708. 2006. View Article : Google Scholar : PubMed/NCBI
14	El Demellawy D, Nasr A and Alowami S: Application of CD56, P63 and CK19 immunohistochemistry in the diagnosis of papillary carcinoma of the thyroid. Diagn Pathol. 3:52008. View Article : Google Scholar : PubMed/NCBI
15	Rossi ED, Straccia P, Palumbo M, Stigliano E, Revelli L, Lombardi CP, Santeusanio G, Pontecorvi A and Fadda G: Diagnostic and prognostic role of HBME-1, galectin-3, and β-catenin in poorly differentiated and anaplastic thyroid carcinomas. Appl Immunohistochem Mol Morphol. 21:237–241. 2013.PubMed/NCBI
16	Liu S, Li N, Yu X, Xiao X, Cheng K, Hu J, Wang J, Zhang D, Cheng S and Liu S: Expression of intercellular adhesion molecule 1 by hepatocellular carcinoma stem cells and circulating tumor cells. Gastroenterology. 144:1031–1041. 2013. View Article : Google Scholar : PubMed/NCBI
17	Jenkinson C, Elliott V, Menon U, Apostolidou S, Fourkala OE, Gentry-Maharaj A, Pereira SP, Jacobs I, Cox TF, Greenhalf W, et al: Evaluation in pre-diagnosis samples discounts ICAM-1 and TIMP-1 as biomarkers for earlier diagnosis of pancreatic cancer. J Proteomics. 113:400–402. 2015. View Article : Google Scholar : PubMed/NCBI
18	Lin YC, Shun CT, Wu MS and Chen CC: A novel anticancer effect of thalidomide: Inhibition of intercellular adhesion molecule-1-mediated cell invasion and metastasis through suppression of nuclear factor-kappaB. Clin Cancer Res. 12:7165–7173. 2006. View Article : Google Scholar : PubMed/NCBI
19	Jankovic B, Le KT and Hershman JM: Clinical review: Hashimoto's thyroiditis and papillary thyroid carcinoma: Is there a correlation? J Clin Endocrinol Metab. 98:474–482. 2013. View Article : Google Scholar : PubMed/NCBI
20	Ahn D, Heo SJ, Park JH, Kim JH, Sohn JH, Park JY, Park SK and Park J: Clinical relationship between Hashimoto's thyroiditis and papillary thyroid cancer. Acta Oncol. 50:1228–1234. 2011. View Article : Google Scholar : PubMed/NCBI
21	Cheng V, Brainard J and Nasr C: Co-occurrence of papillary thyroid carcinoma and primary lymphoma of the thyroid in a patient with long-standing Hashimoto's thyroiditis. Thyroid. 22:647–650. 2012. View Article : Google Scholar : PubMed/NCBI
22	Tafani M, De Santis E, Coppola L, Perrone GA, Carnevale I, Russo A, Pucci B, Carpi A, Bizzarri M and Russo MA: Bridging hypoxia, inflammation and estrogen receptors in thyroid cancer progression. Biomed Pharmacother. 68:1–5. 2014. View Article : Google Scholar : PubMed/NCBI
23	Muzza M, Degl'Innocenti D, Colombo C, Perrino M, Ravasi E, Rossi S, Cirello V, Beck-Peccoz P, Borrello MG and Fugazzola L: The tight relationship between papillary thyroid cancer, autoimmunity and inflammation: Clinical and molecular studies. Clin Endocrinol (Oxf). 72:702–708. 2010. View Article : Google Scholar : PubMed/NCBI
24	Prasad ML, Huang Y, Pellegata NS, de la Chapelle A and Kloos RT: Hashimoto's thyroiditis with papillary thyroid carcinoma (PTC)-like nuclear alterations express molecular markers of PTC. Histopathology. 45:39–46. 2004. View Article : Google Scholar : PubMed/NCBI
25	Sadow PM, Heinrich MC, Corless CL, Fletcher JA and Nose V: Absence of BRAF, NRAS, KRAS, HRAS mutations and RET/PTC gene rearrangements distinguishes dominant nodules in Hashimoto thyroiditis from papillary thyroid carcinomas. Endocr Pathol. 21:73–79. 2010. View Article : Google Scholar : PubMed/NCBI
26	Rhoden KJ, Unger K, Salvatore G, Yilmaz Y, Vovk V, Chiappetta G, Qumsiyeh MB, Rothstein JL, Fusco A, Santoro M, et al: RET/papillary thyroid cancer rearrangement in nonneoplastic thyrocytes: Follicular cells of Hashimoto's thyroiditis share low-level recombination events with a subset of papillary carcinoma. J Clin Endocrinol Metab. 91:2414–2423. 2006. View Article : Google Scholar : PubMed/NCBI
27	Lun Y, Wu X, Xia Q, Han Y, Zhang X, Liu Z, Wang F, Duan Z, Xin S and Zhang J: Hashimoto's thyroiditis as a risk factor of papillary thyroid cancer may improve cancer prognosis. Otolaryngol Head Neck Surg. 148:396–402. 2013. View Article : Google Scholar : PubMed/NCBI
28	Konturek A, Barczyński M, Wierzchowski W, Stopa M and Nowak W: Coexistence of papillary thyroid cancer with Hashimoto thyroiditis. Langenbecks Arch Surg. 398:389–394. 2013. View Article : Google Scholar : PubMed/NCBI
29	Di Pasquale M, Rothstein JL and Palazzo JP: Pathologic features of Hashimoto's-associated papillary thyroid carcinomas. Hum Pathol. 32:24–30. 2001. View Article : Google Scholar : PubMed/NCBI
30	Unger P, Ewart M, Wang BY, Gan L, Kohtz DS and Burstein DE: Expression of p63 in papillary thyroid carcinoma and in Hashimoto's thyroiditis: A pathobiologic link? Hum Pathol. 34:764–769. 2003. View Article : Google Scholar : PubMed/NCBI
31	Burstein DE, Nagi C, Wang BY and Unger P: Immunohistochemical detection of p53 homolog p63 in solid cell nests, papillary thyroid carcinoma and hashimoto's thyroiditis: A stem cell hypothesis of papillary carcinoma oncogenesis. Hum Pathol. 35:465–473. 2004. View Article : Google Scholar : PubMed/NCBI
32	Royer MC, Zhang H, Fan CY and Kokoska MS: Genetic alterations in papillary thyroid carcinoma and hashimoto thyroiditis: An analysis of hOGG1 loss of heterozygosity. Arch Otolaryngol Head Neck Surg. 136:240–242. 2010. View Article : Google Scholar : PubMed/NCBI