Eps15 homology domain 1 promotes the evolution of papillary thyroid cancer by regulating endocytotic recycling of epidermal growth factor receptor

Liu,Yu; Liang,Yanan; Li,Ming; Liu,Duanyang; Tang,Jing; Yang,Weiwei; Tong,Dandan; Jin,Xiaoming

doi:10.3892/ol.2018.9200

Eps15 homology domain 1 promotes the evolution of papillary thyroid cancer by regulating endocytotic recycling of epidermal growth factor receptor

Authors:
- Yu Liu
- Yanan Liang
- Ming Li
- Duanyang Liu
- Jing Tang
- Weiwei Yang
- Dandan Tong
- Xiaoming Jin
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Affiliations: Department of Pathology, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China, Institute of Iodine Deficiency Disorders, Center for Endemic Disease Control, Chinese Center for Disease Control and Prevention, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
Published online on: July 24, 2018 https://doi.org/10.3892/ol.2018.9200
Pages: 4263-4270
Copyright : © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].

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Abstract

Papillary thyroid cancer (PTC) is the most common type of thyroid malignancy, and it is often observed to overexpress epidermal growth factor receptor (EGFR). Previous research has indicated that EH domain‑containing 1 (EHD1) is associated with EGFR‑mediated endocytotic recycling in multiple tumor types. The objective of the present study was to determine the protein expression levels and clinical significance of EHD1, EGFR, caveolin‑1 (CAV‑1) and RAB11 family interacting protein 3 (RAB11FIP3) in PTC. PTC specimens were analyzed for EHD1, EGFR, CAV‑1 and RAB11FIP3 expression via immunohistochemistry and western blotting. The associations between protein expression and clinicopathological features were assessed. EHD1, EGFR, CAV‑1 and RAB11FIP3 expression levels were increased in human PTC. Additionally, the expression level of EHD1 protein was significantly associated with tumor size, lymph node metastasis and EGFR expression (P<0.05). CAV‑1 was associated with tumor size and EGFR expression (P<0.05). EGFR was only associated with lymph node metastasis (P=0.027) and RAB11FIP3 was not associated with any clinicopathological characteristics. The correlations between EHD1 and EGFR (r=0.564, P<0.05), CAV‑1 (r=0.865, P<0.01) and RAB11FIP3 (r=0.504, P<0.05) were statistically significant. Overall, EHD1, CAV‑1 and RAB11FIP3, which are key proteins in endocytotic recycling, promote PTC tumorigenesis through the regulation of the transport of EGFR.

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1	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar : PubMed/NCBI
2	Mohammed AA and El-Shentenawy A: Advanced thyroid cancers: New era of treatment. Med Oncol. 31:492014. View Article : Google Scholar : PubMed/NCBI
3	Herbst RS: Review of epidermal growth factor receptor biology. Int J Radiat Oncol Biol Phys. 59 Suppl 2:S21–S26. 2004. View Article : Google Scholar
4	Hsu F, Nichol A, Toriumi T and De Caluwe A: Miliary metastases are associated with epidermal growth factor receptor mutations in non-small cell lung cancer: A population-based study. Acta Oncol. 56:1175–1180. 2017. View Article : Google Scholar : PubMed/NCBI
5	Cao WM, Gao Y and Wang XJ: Lack of epidermal growth factor receptor (EGFR)-activating mutations in triple-negative breast cancer in china. Breast Cancer Res. 17:1152015. View Article : Google Scholar : PubMed/NCBI
6	Tanaka Y, Terai Y, Tanabe A, Sasaki H, Sekijima T, Fujiwara S, Yamashita Y, Kanemura M, Ueda M, Sugita M, et al: Prognostic effect of epidermal growth factor receptor gene mutations and the aberrant phosphorylation of Akt and ERK in ovarian cancer. Cancer Boil Ther. 11:50–57. 2011. View Article : Google Scholar
7	Mallick UK and American Thyroid A: The revised American Thyroid Association management guidelines 2009 for patients with differentiated thyroid cancer: An evidence-based risk-adapted approach. Clin Oncol (R Coll Radiol). 22:472–474. 2010. View Article : Google Scholar : PubMed/NCBI
8	Tong D, Liang YN, Stepanova AA, Liu Y, Li X, Wang L, Zhang F and Vasilyeva NV: Increased Eps15 homology domain 1 and RAB11FIP3 expression regulate breast cancer progression via promoting epithelial growth factor receptor recycling. Tumour Biol. 39:10104283176910102017. View Article : Google Scholar : PubMed/NCBI
9	Wang S, Wang N, Zheng Y, Zhang J, Zhang F and Wang Z: Caveolin-1: An oxidative stress-related target for cancer prevention. Oxid Med Cell Longev. 2017:74540312017. View Article : Google Scholar : PubMed/NCBI
10	Nwosu ZC, Ebert MP, Dooley S and Meyer C: Caveolin-1 in the regulation of cell metabolism: A cancer perspective. Mol Cancer. 15:712016. View Article : Google Scholar : PubMed/NCBI
11	Moreno-Caceres J, Caja L, Mainez J, Mayoral R, Martín-Sanz P, Moreno-Vicente R, Del Pozo MÁ, Dooley S, Egea G and Fabregat I: Caveolin-1 is required for TGF-β-induced transactivation of the EGF receptor pathway in hepatocytes through the activation of the metalloprotease TACE/ADAM17. Cell Death Dis. 5:e13262014. View Article : Google Scholar : PubMed/NCBI
12	Xu L, Qu X, Li H, Li C, Liu J, Zheng H and Liu Y: Src/caveolin- 1-regulated EGFR activation antagonizes TRAIL-induced apoptosis in gastric cancer cells. Oncol Rep. 32:318–324. 2014. View Article : Google Scholar : PubMed/NCBI
13	Zhang J, Naslavsky N and Caplan S: Rabs and EHDs: Alternate modes for traffic control. Biosci Rep. 32:17–23. 2012. View Article : Google Scholar : PubMed/NCBI
14	Grant BD and Caplan S: Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic. 9:2043–2052. 2008. View Article : Google Scholar : PubMed/NCBI
15	Butterworth MB, Edinger RS, Silvis MR, Gallo LI, Liang X, Apodaca G, Frizzell RA and Johnson JP: Rab11b regulates the trafficking and recycling of the epithelial sodium channel (ENaC). Am J Physiol Renal Physiol. 302:F581–F590. 2012. View Article : Google Scholar : PubMed/NCBI
16	Bhuin T and Roy JK: Rab11 in disease progression. Int J Mol Cell Med. 4:1–8. 2015.PubMed/NCBI
17	Vetter M, Stehle R, Basquin C and Lorentzen E: Structure of Rab11-FIP3-Rabin8 reveals simultaneous binding of FIP3 and Rabin8 effectors to Rab11. Nat Struc Mol Boil. 22:695–702. 2015. View Article : Google Scholar
18	Takahashi S, Takei T, Koga H, Takatsu H, Shin HW and Nakayama K: Distinct roles of Rab11 and Arf6 in the regulation of Rab11-FIP3/arfophilin-1 localization in mitotic cells. Genes Cells. 16:938–950. 2011. View Article : Google Scholar : PubMed/NCBI
19	Collins LL, Simon G, Matheson J, Wu C, Miller MC, Otani T, Yu X, Hayashi S, Prekeris R and Gould GW: Rab11-FIP3 is a cell cycle-regulated phosphoprotein. BMC Cell Boil. 13:42012. View Article : Google Scholar
20	Iaea DB, Mao S, Lund FW and Maxfield FR: Role of STARD4 in sterol transport between the endocytic recycling compartment and the plasma membrane. Mol Biol Cell. 28:1111–1122. 2017. View Article : Google Scholar : PubMed/NCBI
21	Chung BM, Tom E, Zutshi N, Bielecki TA, Band V and Band H: Nexus of signaling and endocytosis in oncogenesis driven by non-small cell lung cancer-associated epidermal growth factor receptor mutants. World J Clin Oncol. 5:806–823. 2014. View Article : Google Scholar : PubMed/NCBI
22	Gao Y, Wang Y, Sun L, Meng Q, Cai L and Dong X: Expression of TGFβ-1 and EHD1 correlated with survival of non-small cell lung cancer. Tumour Biol. 35:9371–9380. 2014. View Article : Google Scholar : PubMed/NCBI
23	Meng Q, Xing Y, Ren T, Lu H, Xi Y, Jiang Z, Hu J, Li C, Sun L, Sun D and Cai L: Mammalian Eps15 homology domain 1 promotes metastasis in non-small cell lung cancer by inducing epithelial-mesenchymal transition. Oncotarget. 8:22433–22442. 2017.PubMed/NCBI
24	Hoop CL, Sivanandam VN, Kodali R, Srnec MN and van der Wel PC: Structural characterization of the caveolin scaffolding domain in association with cholesterol-rich membranes. Biochemistry. 51:90–99. 2012. View Article : Google Scholar : PubMed/NCBI
25	Lee YM and Lee JB: Prognostic value of epidermal growth factor receptor, p53 and galectin-3 expression in papillary thyroid carcinoma. J Int Med Res. 41:825–834. 2013. View Article : Google Scholar : PubMed/NCBI
26	Paskas S, Jankovic J, Marecko I, Išić Denčić T, Tatić S, Cvejić D and Savin S: Caveolin-1 expression in papillary thyroid carcinoma: Correlation with clinicopathological parameters and BRAF mutation status. Otolaryngol Head Neck Surg. 150:201–209. 2014. View Article : Google Scholar : PubMed/NCBI
27	Chen D, Qi W, Zhang P, Guan H and Wang L: Expression of the estrogen receptor α, progesterone receptor and epidermal growth factor receptor in papillary thyroid carcinoma tissues. Oncol Lett. 10:317–320. 2015. View Article : Google Scholar : PubMed/NCBI
28	Tang C, Yang L, Wang N, Li L, Xu M, Chen GG and Liu ZM: High expression of GPER1, EGFR and CXCR1 is associated with lymph node metastasis in papillary thyroid carcinoma. Int J Clin Exp Pathol. 7:3213–3223. 2014.PubMed/NCBI
29	Gidon A, Bardin S, Cinquin B, Boulanger J, Waharte F, Heliot L, de la Salle H, Hanau D, Kervrann C, Goud B and Salamero J: A Rab11A/myosin Vb/Rab11-FIP2 complex frames two late recycling steps of langerin from the ERC to the plasma membrane. Traffic. 13:815–833. 2012. View Article : Google Scholar : PubMed/NCBI
30	Naslavsky N, Rahajeng J, Sharma M, Jovic M and Caplan S: Interactions between EHD proteins and Rab11-FIP2: A role for EHD3 in early endosomal transport. Mol Boil Cell. 17:163–177. 2006. View Article : Google Scholar
31	Horgan CP, Oleksy A, Zhdanov AV, Lall PY, White IJ, Khan AR, Futter CE, McCaffrey JG and McCaffrey MW: Rab11-FIP3 is critical for the structural integrity of the endosomal recycling compartment. Traffic. 8:414–430. 2007. View Article : Google Scholar : PubMed/NCBI