Correlation between insulin‑like growth factor binding protein 3 and metastasis‑associated gene 1 protein in esophageal squamous cell carcinoma

Yang,Haiping; Xu,Lijuan; Qian,Haili; Niu,Xinqiang; Zhao,Dan; Zhao,Zhilong; Wu,Jun; Liu,Junfeng; Wang,Yanyu

doi:10.3892/mmr.2016.5046

Correlation between insulin‑like growth factor binding protein 3 and metastasis‑associated gene 1 protein in esophageal squamous cell carcinoma

Authors:
- Haiping Yang
- Lijuan Xu
- Haili Qian
- Xinqiang Niu
- Dan Zhao
- Zhilong Zhao
- Jun Wu
- Junfeng Liu
- Yanyu Wang
View Affiliations

Affiliations: Department of Thoracic and Cardiovascular Surgery, Beijing Luhe Hospital Affiliated to Capital Medical University, Beijing 101100, P.R. China, State Key Laboratory of Molecular Oncology, Cancer Hospital/Institute, Chinese Academy of Medical Sciences, Beijing 100021, P.R. China, Department of Thoracic Surgery, Cixian People's Hospital, Handan, Hebei 056500, P.R. China, Department of Pathology, Beijing Chest Hospital of Capital Medical University, Beijing 101100, P.R. China, Department of Cardiothoracics, Zhongshan Hospital, Dalian University, Dalian, Liaoning 116001, P.R. China, Department of Thoracic Surgery, Fourth Hospital, Hebei Medical University, Shijiazhuang, Hebei 050011, P.R. China
Published online on: March 28, 2016 https://doi.org/10.3892/mmr.2016.5046
Pages: 4143-4150
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The present study aimed to investigate the correlation between insulin‑like growth factor binding protein 3 (IGFBP‑3) and metastasis‑associated gene 1 (MTA1) protein, and the clinicopathological features and prognosis of esophageal squamous cell carcinoma (ESCC). Patients with ESCC who underwent surgical resection were enrolled in the current study, ESCC tissues and adjacent normal tissues (control) were obtained from 197 patients. The protein expression levels of IGFBP‑3 and MTA1 were detected using immunohistochemistry. The results demonstrated that the expression of IGFBP‑3 in ESCC tissues was significantly lower than in the adjacent normal tissues (27.4 vs. 40.6%; P<0.05), and was negatively correlated with smoking status, degree of tumor differentiation and lymph node metastasis (P<0.05). The expression of MTA1 protein in ESCC tissues was significantly higher than that of the adjacent tissues (42.1 vs. 11.2%; P<0.05), and was positively correlated with the tumor size, extent of tumor invasion and lymph node metastasis (P<0.05). No association was identified between the protein expression levels of IGFBP‑3 and MTA1. The protein expression levels of IGFBP‑3 and MTA1 were not independent risk factors for ESCC prognosis; however, the degree of tumor invasion (P=0.02) and rate of lymph node metastasis (P=0.027) were. IGFBP‑3 inhibits the proliferation and metastasis of ESCC; however, MTA1 promotes the proliferation and metastasis of ESCC. There is no interaction between IGFBP‑3 and MTA1 in ESCC, and they are not independent risk factors for ESCC prognosis.

View Figures

View References

1	Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI
2	Suntharalingam M: Definitive chemoradiation in the management of locally advanced esophageal cancer. Semin Radiat Oncol. 17:22–28. 2007. View Article : Google Scholar
3	Rohatgi PR, Swisher SG, Correa AM, Wu TT, Liao Z, Komaki R, Walsh G, Vaporciyan A, Lynch PM, Rice DC, et al: Failure patterns correlate with the proportion of residual carcinoma after preoperative chemoradiotherapy for carcinoma of the esophagus. Cancer. 104:1349–1355. 2005. View Article : Google Scholar : PubMed/NCBI
4	Di Fiore F, Lecleire S, Rigal O, Galais MP, Ben Soussan E, David I, Paillot B, Jacob JH and Michel P: Predictive factors of survival in patients treated with definitive chemoradiotherapy for squamous cell esophageal carcinoma. World J Gastroenterol. 12:4185–4190. 2006. View Article : Google Scholar : PubMed/NCBI
5	Nicolson GL, Nawa A, Toh Y, Taniguchi S, Nishimori K and Moustafa A: Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: Role in epithelial cancer cell invasion, proliferation and nuclear regulation. Clin Exp Metastasis. 20:19–24. 2003. View Article : Google Scholar : PubMed/NCBI
6	Toh Y, Ohga T, Endo K, Adachi E, Kusumoto H, Haraguchi M, Okamura T and Nicolson GL: Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. Int J Cancer. 110:362–367. 2004. View Article : Google Scholar : PubMed/NCBI
7	Holdaway IM, Mason BH, Lethaby AE, Singh V, Harvey VJ, Thompson PI and Evans BD: Serum insulin-like growth factor-I and insulin-like growth factor binding protein-3 following chemotherapy for advanced breast cancer. ANZ J Surg. 73:905–908. 2003. View Article : Google Scholar : PubMed/NCBI
8	Rajah R, Valentinis B and Cohen P: Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-beta1 on programmed cell death through a p53- and IGF-independent mechanism. J Biol Chem. 272:12181–12188. 1997. View Article : Google Scholar : PubMed/NCBI
9	Hankinson SE, Willett WC, Colditz GA, Hunter DJ, Michaud DS, Deroo B, Rosner B, Speizer FE and Pollak M: Circulating concentrations of insulin-like growth factor I and risk of breast cancer. Lancet. 351:1393–1396. 1998. View Article : Google Scholar : PubMed/NCBI
10	Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH and Pollak M: Plasma insulin-like growth factor-I and prostate cancer risk: A prospective study. Science. 279:563–566. 1998. View Article : Google Scholar : PubMed/NCBI
11	Yu H, Spitz MR, Mistry J, Gu J, Hong WK and Wu X: Plasma levels of insulin-like growth factor-I and lung cancer risk: A case-control study. J Natl Cancer Inst. 91:151–156. 1999. View Article : Google Scholar : PubMed/NCBI
12	Ma J, Pollak MN, Giovannucci E, Chan JM, Tao Y, Hennekens CH and Stampfer MJ: Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J Natl Cancer Inst. 91:620–625. 1999. View Article : Google Scholar : PubMed/NCBI
13	Chuang ST, Patton KT, Schafernak KT, Papavero V, Lin F, Baxter RC, Teh BT and Yang XJ: Over expression of insulin-like growth factor binding protein 3 in clear cell renal cell carcinoma. J Urol. 179:445–449. 2008. View Article : Google Scholar
14	Balasenthil S, Broaddus RR and Kumar R: Expression of metastasis-associated protein 1 (MTA1) in benign endometrium and endometrial adenocarcinomas. Hum Pathol. 37:656–661. 2006. View Article : Google Scholar : PubMed/NCBI
15	Rice TW, Blackstone EH and Rusch VW: 7th edition of the AJCC cancer staging manual: Esophagus and esophagogastric junction. Ann Surg Oncol. 17:1721–1724. 2010. View Article : Google Scholar : PubMed/NCBI
16	Yang HP, Liu JF, Rao J, Zhang XM, Qian HL, Niu XQ and Zhao ZL: Insulin-like growth factor binding protein-3 (IGFBP-3) genetic variant and the risk of esophageal squamous cell carcinoma in a Chinese population. Genet Mol Res. 13:4146–4153. 2014. View Article : Google Scholar : PubMed/NCBI
17	Hwa V, Oh Y and Rosenfeld RG: The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev. 20:761–787. 1999.PubMed/NCBI
18	Gui Y and Murphy LJ: Insulin-like growth factor (IGF)-binding protein-3 (IGFBP-3) binds to fibronectin (FN): Demonstration of IGF-I/IGFBP-3/fn ternary complexes in human plasma. J Clin Endocrinol Metab. 86:2104–2110. 2001.PubMed/NCBI
19	Yamada PM and Lee KW: Perspectives in mammalian IGFBP-3 biology: Local vs. systemic action. Am J Physiol Cell Physiol. 296:C954–C976. 2009. View Article : Google Scholar : PubMed/NCBI
20	Gill ZP, Perks CM, Newcomb PV and Holly JM: Insulin-like growth factor-binding protein (IGFBP-3) predisposes breast cancer cells to programmed cell death in a non-IGF-dependent manner. J Biol Chem. 272:25602–25607. 1997. View Article : Google Scholar : PubMed/NCBI
21	Collard TJ, Guy M, Butt AJ, Perks CM, Holly JM, Paraskeva C and Williams AC: Transcriptional upregulation of the insulin-like growth factor binding protein IGFBP-3 by sodium butyrate increases IGF-independent apoptosis in human colonic adenoma-derived epithelial cells. Carcinogenesis. 24:393–401. 2003. View Article : Google Scholar : PubMed/NCBI
22	Torng PL, Lee YC, Huang CY, Ye JH, Lin YS, Chu YW, Huang SC, Cohen P, Wu CW and Lin CT: Insulin-like growth factor binding protein-3 (IGFBP-3) acts as an invasion-metastasis suppressor in ovarian endometrioid carcinoma. Oncogene. 27:2137–2147. 2008. View Article : Google Scholar
23	Torng PL, Lin CW, Chan MW, Yang HW, Huang SC and Lin CT: Promoter methylation of IGFBP-3 and p53 expression in ovarian endometrioid carcinoma. Mol Cancer. 8:1202009. View Article : Google Scholar : PubMed/NCBI
24	Chang YS, Wang L, Liu D, Mao L, Hong WK, Khuri FR and Lee HY: Correlation between insulin-like growth factor-binding protein-3 promoter methylation and prognosis of patients with stage I non-small cell lung cancer. Clin Cancer Res. 8:3669–3675. 2002.PubMed/NCBI
25	Wang Z, Wang Z, Liang Z, Liu J, Shi W, Bai P, Lin X, Magaye R and Zhao J: Expression and clinical significance of IGF-1, IGFBP-3, and IGFBP-7 in serum and lung cancer tissues from patients with non-small cell lung cancer. Onco Targets Ther. 6:1437–1444. 2013.PubMed/NCBI
26	Aishima S, Basaki Y, Oda Y, Kuroda Y, Nishihara Y, Taguchi K, Taketomi A, Maehara Y, Hosoi F, Maruyama Y, et al: High expression of insulin-like growth factor binding protein-3 is correlated with lower portal invasion and better prognosis in human hepatocellular carcinoma. Cancer Sci. 97:1182–1190. 2006. View Article : Google Scholar : PubMed/NCBI
27	Walker G, MacLeod K, Williams AR, Cameron DA, Smyth JF and Langdon SP: Insulin-like growth factor binding proteins IGFBP3, IGFBP4, and IGFBP5 predict endocrine responsiveness in patients with ovarian cancer. Clin Cancer Res. 13:1438–1444. 2007. View Article : Google Scholar : PubMed/NCBI
28	Shariat SF, Lamb DJ, Kattan MW, Nguyen C, Kim J, Beck J, Wheeler TM and Slawin KM: Association of preoperative plasma levels of insulin-like growth factor I and insulin-like growth factor binding proteins-2 and -3 with prostate cancer invasion, progression, and metastasis. J Clin Oncol. 20:833–841. 2002. View Article : Google Scholar : PubMed/NCBI
29	Tas F, Karabulut S, Bilgin E, Tastekin D and Duranyildiz D: Clinical significance of serum insulin-like growth factor-1 (IGF-1) and insulin-like growth factor binding protein-3 (IGFBP-3) in patients with breast cancer. Tumour Biol. 35:9303–9309. 2014. View Article : Google Scholar : PubMed/NCBI
30	Tas F, Karabulut S, Serilmez M, Ciftci R and Duranyildiz D: Clinical significance of serum insulin-like growth factor-1 (IGF-1) and insulin like growth factor binding protein-3 (IGFBP-3) in patients with epithelial ovarian cancer. Tumour Biol. 35:3125–3132. 2014. View Article : Google Scholar
31	Seligson DB, Yu H, Tze S, Said J, Pantuck AJ, Cohen P and Lee KW: IGFBP-3 nuclear localization predicts human prostate cancer recurrence. Horm Cancer. 4:12–23. 2013. View Article : Google Scholar :
32	Kim YH, Sumiyoshi S, Hashimoto S, Masago K, Togashi Y, Sakamori Y, Okuda C, Mio T and Mishima M: Expressions of insulin-like growth factor receptor-1 and insulin-like growth factor binding protein 3 in advanced non-small-cell lung cancer. Clin Lung Cancer. 13:385–390. 2012. View Article : Google Scholar : PubMed/NCBI
33	Rohrmann S, Grote VA, Becker S, Rinaldi S, Tjønneland A, Roswall N, Grønbæk H, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, et al: Concentrations of IGF-I and IGFBP-3 and pancreatic cancer risk in the European prospective investigation into cancer and nutrition. Br J Cancer. 106:1004–1010. 2012. View Article : Google Scholar : PubMed/NCBI
34	Firth SM and Baxter RC: Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev. 23:824–854. 2002. View Article : Google Scholar : PubMed/NCBI
35	Grimberg A: Mechanisms by which IGF-I may promote cancer. Cancer Biol Ther. 2:630–635. 2003. View Article : Google Scholar : PubMed/NCBI
36	Buckbinder L, Talbott R, Velasco-Miguel S, Takenaka I, Faha B, Seizinger BR and Kley N: Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature. 377:646–649. 1995. View Article : Google Scholar : PubMed/NCBI
37	Binoux M: Insulin-like growth factor binding proteins (IGFBPs): Physiological and clinical implications. J Pediatr Endocrinol Metab. 9(Suppl 3): S285–S288. 1996.
38	Mehta HH, Gao Q, Galet C, Paharkova V, Wan J, Said J, Sohn JJ, Lawson G, Cohen P, Cobb LJ and Lee KW: IGFBP-3 is a metastasis suppression gene in prostate cancer. Cancer Res. 71:5154–5163. 2011. View Article : Google Scholar : PubMed/NCBI
39	Zhao L, He L, Zhang R, Cai MY, Liao YJ, Qian D, Xi M, Zeng YX, Xie D and Liu MZ: Low expression of IGFBP-3 predicts poor prognosis in patients with esophageal squamous cell carcinoma. Med Oncol. 29:2669–2676. 2012. View Article : Google Scholar
40	Jenkins PJ, Khalaf S, Ogunkolade W, McCarthy K, David T, Hands RE, Davies D and Bustin SA: Differential expression of IGF-binding protein-3 in normal and malignant colon and its influence on apoptosis. Endocr Relat Cancer. 12:891–901. 2005. View Article : Google Scholar : PubMed/NCBI
41	Toh Y, Pencil SD and Nicolson GL: A novel candidate metastasis-associated gene, mta1, differentially expressed in highly metastatic mammary adenocarcinoma cell lines. cDNA cloning, expression, and protein analyses. J Biol Chem. 269:22958–22963. 1994.PubMed/NCBI
42	Cui Q, Takiguchi S, Matsusue K, Toh Y and Yoshida MA: Assignment of the human metastasis-associated gene 1 (MTA1) to human chromosome band 14q32.3 by fluorescence in situ hybridization. Cytogenet Cell Genet. 93:139–140. 2001. View Article : Google Scholar : PubMed/NCBI
43	Roy S, Packman K, Jeffrey R and Tenniswood M: Histone deacetylase inhibitors differentially stabilize acetylated p53 and induce cell cycle arrest or apoptosis in prostate cancer cells. Cell Death Differ. 12:482–491. 2005. View Article : Google Scholar : PubMed/NCBI
44	Hofer MD, Menke A, Genze F, Gierschik P and Giehl K: Expression of MTA1 promotes motility and invasiveness of PANC-1 pancreatic carcinoma cells. Br J Cancer. 90:455–462. 2004. View Article : Google Scholar : PubMed/NCBI