Effect of hypoxia‑HIF‑1α‑periostin axis in thyroid cancer

Yang,Ye; Yang,Ye; Wu,Junyi; Wu,Junyi; Zhu,Huiqin; Zhu,Huiqin; Shi,Xiaoqin; Shi,Xiaoqin; Liu,Jun; Liu,Jun; Li,Yang; Li,Yang; Wang,Min; Wang,Min

doi:10.3892/or.2024.8716

Effect of hypoxia‑HIF‑1α‑periostin axis in thyroid cancer

Authors:
- Ye Yang
- Junyi Wu
- Huiqin Zhu
- Xiaoqin Shi
- Jun Liu
- Yang Li
- Min Wang
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Affiliations: Department of Obstetrics and Gynecology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Hongkou, Shanghai 200080, P.R. China, Department of General Surgery, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Hongkou, Shanghai 200080, P.R. China, Department of General Surgery, Dongtai People's Hospital, Dongtai, Jiangsu 224200, P.R. China, Department of Pathology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Hongkou, Shanghai 200080, P.R. China
Published online on: February 22, 2024 https://doi.org/10.3892/or.2024.8716
Article Number: 57
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The incidence of thyroid carcinoma (TC) has exhibited a rapid increase in recent years. A proportion of TCs exhibit aggressive behavior. The present study aimed to investigate the potential role of hypoxia‑hypoxia inducible factor 1 subunit α (HIF‑1α)‑periostin axis in the progression of TC. The upregulation of periostin and HIF‑1α expression levels was detected in 95 clinical TC tissues as compared with normal thyroid tissues. Hypoxia promoted the viability and invasion of TC cells and this effect was inhibited by the downregulation of periostin. Hypoxia also induced the Warburg effect in TC and this effect was inhibited by the silencing of periostin. Further investigations revealed that hypoxia activated HIF‑1α, which in turn regulated the expression of periostin. Immunoprecipitation and dual luciferase reporter assays demonstrated that HIF‑1α upregulated the expression of periostin by binding to the promoter of periostin. On the whole, these findings suggest the existence of a hypoxia‑HIF‑1α‑periostin axis in TC and indicate the role of this axis in the progression of TC.

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1	Wang J, Yu F, Shang Y, Ping Z and Liu L: Thyroid cancer: Incidence and mortality trends in China, 2005–2015. Endocrine. 68:163–173. 2020. View Article : Google Scholar : PubMed/NCBI
2	La Vecchia C, Malvezzi M, Bosetti C, Garavello W, Bertuccio P, Levi F and Negri E: Thyroid cancer mortality and incidence: A global overview. Int J Cancer. 136:2187–2195. 2015. View Article : Google Scholar : PubMed/NCBI
3	Hughes DT, Haymart MR, Miller BS, Gauger PG and Doherty GM: The most commonly occurring papillary thyroid cancer in the United States is now a microcarcinoma in a patient older than 45 years. Thyroid. 21:231–236. 2011. View Article : Google Scholar : PubMed/NCBI
4	Lim H, Devesa SS, Sosa JA, Check D and Kitahara CM: Trends in thyroid cancer incidence and mortality in the United States, 1974–2013. JAMA. 317:1338–1348. 2017. View Article : Google Scholar : PubMed/NCBI
5	Ibrahimpasic T, Ghossein R, Shah JP and Ganly I: Poorly differentiated carcinoma of the thyroid gland: Current status and future prospects. Thyroid. 29:311–321. 2019. View Article : Google Scholar : PubMed/NCBI
6	Dettmer MS, Schmitt A, Komminoth P and Perren A: Poorly differentiated thyroid carcinoma: An underdiagnosed entity. Pathologe. 41 (Suppl 1):S1–S8. 2020. View Article : Google Scholar
7	González-González L and Alonso J: Periostin: A matricellular protein with multiple functions in cancer development and progression. Front Oncol. 8:2252018. View Article : Google Scholar : PubMed/NCBI
8	Liu Y, Huang Z, Cui D and Ouyang G: The multiaspect functions of periostin in tumor progression. Adv Exp Med Biol. 1132:125–136. 2019. View Article : Google Scholar : PubMed/NCBI
9	Wang M, Gui C, Qiu S, Tang J and Peng Z: Periostin silencing suppresses the aggressive phenotype of thyroid carcinoma cells by suppressing the Akt/thyroid stimulating hormone receptor axis. Cytotechnology. 70:275–284. 2018. View Article : Google Scholar : PubMed/NCBI
10	Schwartz L, Supuran CT and Alfarouk KO: The Warburg effect and the hallmarks of cancer. Anticancer Agents Med Chem. 17:164–170. 2017. View Article : Google Scholar : PubMed/NCBI
11	Wang HJ, Hsieh YJ, Cheng WC, Lin CP, Lin YS, Yang SF, Chen CC, Izumiya Y, Yu JS, Kung HJ, et al: JMJD5 regulates PKM2 nuclear translocation and reprograms HIF-1α-mediated glucose metabolism. Proc Natl Acad Sci USA. 111:279–284. 2014. View Article : Google Scholar : PubMed/NCBI
12	Semenza GL: HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol. 13:167–171. 2001. View Article : Google Scholar : PubMed/NCBI
13	Semenza GL: Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE. 2007:cm82007. View Article : Google Scholar : PubMed/NCBI
14	Kierans SJ and Taylor CT: Regulation of glycolysis by the hypoxia-inducible factor (HIF): Implications for cellular physiology. J Physiol. 599:23–37. 2021. View Article : Google Scholar : PubMed/NCBI
15	Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC and Haugen BR: Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab. 93:4331–4341. 2008. View Article : Google Scholar : PubMed/NCBI
16	Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET and Eliceiri KW: ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics. 18:5292017. View Article : Google Scholar : PubMed/NCBI
17	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
18	Vander Heiden MG, Cantley LC and Thompson CB: Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science. 324:1029–1033. 2009. View Article : Google Scholar : PubMed/NCBI
19	Sonnenberg-Riethmacher E, Miehe M and Riethmacher D: Periostin in allergy and inflammation. Front Immunol. 12:7221702021. View Article : Google Scholar : PubMed/NCBI
20	Ratajczak-Wielgomas K and Dziegiel P: The role of periostin in neoplastic processes. Folia Histochem Cytobiol. 53:120–132. 2015. View Article : Google Scholar : PubMed/NCBI
21	Yamaguchi Y: Periostin in skin tissue and skin-related diseases. Allergol Int. 63:161–170. 2014. View Article : Google Scholar
22	Kudo Y, Iizuka S, Yoshida M, Nguyen PT, Siriwardena SB, Tsunematsu T, Ohbayashi M, Ando T, Hatakeyama D, Shibata T, et al: Periostin directly and indirectly promotes tumor lymphangiogenesis of head and neck cancer. PLoS One. 7:e444882012. View Article : Google Scholar : PubMed/NCBI
23	Zhang Y, Zhang G, Li J, Tao Q and Tang W: The expression analysis of periostin in human breast cancer. J Surg Res. 160:102–106. 2010. View Article : Google Scholar : PubMed/NCBI
24	Utispan K, Thuwajit P, Abiko Y, Charngkaew K, Paupairoj A, Chau-in S and Thuwajit C: Gene expression profiling of cholangiocarcinoma-derived fibroblast reveals alterations related to tumor progression and indicates periostin as a poor prognostic marker. Mol Cancer. 9:132010. View Article : Google Scholar : PubMed/NCBI
25	Kikuchi Y, Kunita A, Iwata C, Komura D, Nishiyama T, Shimazu K, Takeshita K, Shibahara J, Kii I, Morishita Y, et al: The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am J Pathol. 184:859–870. 2014. View Article : Google Scholar : PubMed/NCBI
26	Kusafuka K, Yamashita M, Iwasaki T, Tsuchiya C, Kubota A, Hirata K, Murakami A, Muramatsu A, Arai K and Suzuki M: Periostin expression and its supposed roles in benign and malignant thyroid nodules: An immunohistochemical study of 105 cases. Diagn Pathol. 16:862021. View Article : Google Scholar : PubMed/NCBI
27	Giusca SE, Amalinei C, Lozneanu L, Ciobanu Apostol D, Andriescu EC, Scripcariu A, Balan R, Avadanei ER and Căruntu ID: Heterogeneous periostin expression in different histological variants of papillary thyroid carcinoma. Biomed Res Int. 2017:87013862017. View Article : Google Scholar : PubMed/NCBI
28	Bai Y, Kakudo K, Nakamura M, Ozaki T, Li Y, Liu Z, Mori I, Miyauchi A and Zhou G: Loss of cellular polarity/cohesiveness in the invasive front of papillary thyroid carcinoma and periostin expression. Cancer Lett. 281:188–195. 2009. View Article : Google Scholar : PubMed/NCBI
29	Bai Y, Nakamura M, Zhou G, Li Y, Liu Z, Ozaki T, Mori I and Kakudo K: Novel isoforms of periostin expressed in the human thyroid. Jpn Clin Med. 1:13–20. 2010. View Article : Google Scholar : PubMed/NCBI
30	Fluge Ø, Bruland O, Akslen LA, Lillehaug JR and Varhaug JE: Gene expression in poorly differentiated papillary thyroid carcinomas. Thyroid. 16:161–175. 2006. View Article : Google Scholar : PubMed/NCBI
31	Lee JW, Bae SH, Jeong JW, Kim SH and Kim KW: Hypoxia-inducible factor (HIF-1)alpha: Its protein stability and biological functions. Exp Mol Med. 36:1–12. 2004. View Article : Google Scholar : PubMed/NCBI
32	Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER and Ratcliffe PJ: The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 399:271–275. 1999. View Article : Google Scholar : PubMed/NCBI
33	Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS and Kaelin WG Jr: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O₂ sensing. Science. 292:464–468. 2001. View Article : Google Scholar : PubMed/NCBI
34	Formenti F, Constantin-Teodosiu D, Emmanuel Y, Cheeseman J, Dorrington KL, Edwards LM, Humphreys SM, Lappin TR, McMullin MF, McNamara CJ, et al: Regulation of human metabolism by hypoxia-inducible factor. Proc Natl Acad Sci USA. 107:12722–12727. 2010. View Article : Google Scholar : PubMed/NCBI
35	Ruas JL, Poellinger L and Pereira T: Role of CBP in regulating HIF-1-mediated activation of transcription. J Cell Sci. 118:301–311. 2005. View Article : Google Scholar : PubMed/NCBI
36	Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD and Semenza GL: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 16:4604–4613. 1996. View Article : Google Scholar : PubMed/NCBI
37	Kim JW, Tchernyshyov I, Semenza GL and Dang CV: HIF-1-mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3:177–185. 2006. View Article : Google Scholar : PubMed/NCBI
38	Schmid T, Zhou J and Brüne B: HIF-1 and p53: Communication of transcription factors under hypoxia. J Cell Mol Med. 8:423–431. 2004. View Article : Google Scholar : PubMed/NCBI
39	Kudo A: Introductory review: Periostin-gene and protein structure. Cell Mol Life Sci. 74:4259–4268. 2017. View Article : Google Scholar : PubMed/NCBI
40	Srinivasan S, Guha M, Dong DW, Whelan KA, Ruthel G, Uchikado Y, Natsugoe S, Nakagawa H and Avadhani NG: Disruption of cytochrome c oxidase function induces the Warburg effect and metabolic reprogramming. Oncogene. 35:1585–1595. 2016. View Article : Google Scholar : PubMed/NCBI
41	Zhang Z, Nie F, Kang C, Chen B, Qin Z, Ma J, Ma Y and Zhao X: Increased periostin expression affects the proliferation, collagen synthesis, migration and invasion of keloid fibroblasts under hypoxic conditions. Int J Mol Med. 34:253–261. 2014. View Article : Google Scholar : PubMed/NCBI
42	Aukkarasongsup P, Haruyama N, Matsumoto T, Shiga M and Moriyama K: Periostin inhibits hypoxia-induced apoptosis in human periodontal ligament cells via TGF-β signaling. Biochem Biophys Res Commun. 441:126–132. 2013. View Article : Google Scholar : PubMed/NCBI
43	Guo X, Xue H, Shao Q, Wang J, Guo X, Chen X, Zhang J, Xu S, Li T, Zhang P, et al: Hypoxia promotes glioma-associated macrophage infiltration via periostin and subsequent M2 polarization by upregulating TGF-beta and M-CSFR. Oncotarget. 7:80521–80542. 2016. View Article : Google Scholar : PubMed/NCBI
44	Liu Y, Gao F and Song W: Periostin contributes to arsenic trioxide resistance in hepatocellular carcinoma cells under hypoxia. Biomed Pharmacother. 88:342–348. 2017. View Article : Google Scholar : PubMed/NCBI
45	Vaupel P and Multhoff G: Revisiting the Warburg effect: Historical dogma versus current understanding. J Physiol. 599:1745–1757. 2021. View Article : Google Scholar : PubMed/NCBI
46	Yang Z, Huang R, Wei X, Yu W, Min Z and Ye M: The SIRT6-autophagy-Warburg effect axis in papillary thyroid cancer. Front Oncol. 10:12652020. View Article : Google Scholar : PubMed/NCBI
47	Semenza GL: Hypoxia-inducible factor 1: Regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta. 1813:1263–1268. 2011. View Article : Google Scholar : PubMed/NCBI
48	Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ and Semenza GL: Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 283:10892–10903. 2008. View Article : Google Scholar : PubMed/NCBI
49	Ordureau A, Münch C and Harper JW: Quantifying ubiquitin signaling. Mol Cell. 58:660–676. 2015. View Article : Google Scholar : PubMed/NCBI
50	Zhang W: The mitophagy receptor FUN14 domain-containing 1 (FUNDC1): A promising biomarker and potential therapeutic target of human diseases. Genes Dis. 8:640–654. 2020. View Article : Google Scholar : PubMed/NCBI
51	Zhang W, Ren H, Xu C, Zhu C, Wu H, Liu D, Wang J, Liu L, Li W, Ma Q, et al: Hypoxic mitophagy regulates mitochondrial quality and platelet activation and determines severity of I/R heart injury. Elife. 5:e214072016. View Article : Google Scholar : PubMed/NCBI