Abstract
Annexin A10 (ANXA10) is a member of annexin A and has been reported to highly express in papillary thyroid carcinoma (PTC) tissues. Tumor susceptibility gene 101 (TSG101) also plays a role in PTC and is predicted to bind to ANXA10. This study intended to investigate whether ANXA10 could regulate PTC via binding to ANXA10. The expression of ANXA10 and TSG101 in normal thyroid follicular epithelial cell line and several PTC cell lines was analyzed using RT-qPCR and western blotting assays. Subsequently, PTC cell line BCPAP was silenced with ANXA10 followed by TSG101 overexpression or not, and then cell proliferation, apoptosis and mitogen-activated protein kinase (MAPK) signaling expression were assessed via MTT, colony formation, immunofluorescence staining, Tunel staining and western blotting assays. Besides, the interaction between ANXA10 and TSG101 was validated using Co-immunoprecipitation assay. ANXA10 and TSG101 expressions were up-regulated in PTC cell lines. ANXA10 silence inhibited proliferation, promoted apoptosis and inactivated MAPK/ extracellular regulated protein kinases (ERK) signaling pathway of BCPAP cells. Additionally, ANXA10 could bind to TSG101 and regulate its expression. However, the above effects of ANXA10 silence on BCPAP cells were all blocked by TSG101 overexpression. ANXA10 inhibited proliferation and promoted apoptosis of PTC cells via binding to TSG101, and these actions may depend on down-regulating MAPK/ERK pathway expression.
Similar content being viewed by others
Data availability
The experimental data will be available on the request.
References
Chua HH, Kameyama T, Mayeda A, Yeh TH (2019) Cancer-specifically Re-Spliced TSG101 mRNA promotes invasion and metastasis of nasopharyngeal carcinoma. Int J Molec Sci 20. https://doi.org/10.3390/ijms20030773
Evan GI, Vousden KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411:342–348. https://doi.org/10.1038/35077213
Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371. https://doi.org/10.1152/physrev.00030.2001
Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6:449–461. https://doi.org/10.1038/nrm1661
Hung MS et al. (2019) Cul4A modulates invasion and metastasis of lung cancer through regulation of ANXA10. Cancers 11. https://doi.org/10.3390/cancers11050618
Kitahara CM, Sosa JA (2016) The changing incidence of thyroid cancer. Nat Rev Endocrinol 12:646–653. https://doi.org/10.1038/nrendo.2016.110
Kodaira H et al (2019) ANXA10 induction by interaction with tumor-associated macrophages promotes the growth of esophageal squamous cell carcinoma. Pathol Int 69:135–147. https://doi.org/10.1111/pin.12771
Kumar B et al (2016) ESCRT-I protein Tsg101 plays a role in the post-macropinocytic trafficking and infection of endothelial cells by Kaposi’s sarcoma-associated herpesvirus. PLoS Pathog 12:e1005960. https://doi.org/10.1371/journal.ppat.1005960
Liu RT et al (2002) Overexpression of tumor susceptibility gene TSG101 in human papillary thyroid carcinomas. Oncogene 21:4830–4837. https://doi.org/10.1038/sj.onc.1205612
Liu Z et al (2014) TSG101 and PEG10 are prognostic markers in squamous cell/adenosquamous carcinomas and adenocarcinoma of the gallbladder. Oncol Lett 7:1128–1138. https://doi.org/10.3892/ol.2014.1886
Liu Z et al (2019) TSG101 promotes the proliferation, migration and invasion of hepatocellular carcinoma cells by regulating the PEG10. J Cell Mol Med 23:70–82. https://doi.org/10.1111/jcmm.13878
Liu X et al (2020) Upregulated lncRNA DLX6-AS1 underpins hepatocellular carcinoma progression via the miR-513c/Cul4A/ANXA10 axis. Cancer Gene Ther. https://doi.org/10.1038/s41417-020-00233-0
Liu X, Yang M, Guo Y, Lu X (2021) Annexin A10 is a novel prognostic biomarker of papillary thyroid cancer. Ir J Med Sci 190:59–65. https://doi.org/10.1007/s11845-020-02263-x
Munksgaard PP et al (2011) Low ANXA10 expression is associated with disease aggressiveness in bladder cancer. Br J Cancer 105:1379–1387. https://doi.org/10.1038/bjc.2011.404
Pessolano E et al. (2018) Annexin A1 may induce pancreatic cancer progression as a key player of extracellular vesicles effects as evidenced in the in vitro MIA PaCa-2 model system. Int J Mol Sci 19. https://doi.org/10.3390/ijms19123878
Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM (2014) Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Can Res 74:2913–2921. https://doi.org/10.1158/0008-5472.can-14-0155
Sabio G, Davis RJ (2014) TNF and MAP kinase signalling pathways. Semin Immunol 26:237–245. https://doi.org/10.1016/j.smim.2014.02.009
Sai XB, Makiyama T, Sakane H, Horii Y, Hiraishi H, Shirataki H (2015) TSG101, a tumor susceptibility gene, bidirectionally modulates cell invasion through regulating MMP-9 mRNA expression. BMC Cancer 15:933. https://doi.org/10.1186/s12885-015-1942-1
Seib CD, Sosa JA (2019) Evolving understanding of the epidemiology of thyroid cancer. Endocrinol Metab Clin North Am 48:23–35. https://doi.org/10.1016/j.ecl.2018.10.002
Shimizu T et al (2012) Annexin A10 in human oral cancer: biomarker for tumoral growth via G1/S transition by targeting MAPK signaling pathways. PLoS ONE 7:e45510. https://doi.org/10.1371/journal.pone.0045510
Srivastava M et al (2001) ANX7, a candidate tumor suppressor gene for prostate cancer. Proc Natl Acad Sci USA 98:4575–4580. https://doi.org/10.1073/pnas.071055798
Sun R et al (2019) Annexin10 promotes extrahepatic cholangiocarcinoma metastasis by facilitating EMT via PLA2G4A/PGE2/STAT3 pathway. EBioMedicine 47:142–155. https://doi.org/10.1016/j.ebiom.2019.08.062
Wang J, Zhao S, Wang F, Wang J, Zhang Y (2019) Prognostic Significance of Increased Expression of Annexin A10 (ANXA10) in Serous Epithelial Ovarian Cancer. Med Sci Monit 25:5666–5673. https://doi.org/10.12659/msm.915911
Xing M (2013) Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 13:184–199. https://doi.org/10.1038/nrc3431
Xu C, Zheng J (2019) siRNA against TSG101 reduces proliferation and induces G0/G1 arrest in renal cell carcinoma - involvement of c-myc, cyclin E1, and CDK2. Cell Mol Biol Lett 24:7. https://doi.org/10.1186/s11658-018-0124-y
Yi M, Schnitzer JE (2009) Impaired tumor growth, metastasis, angiogenesis and wound healing in annexin A1-null mice. Proc Natl Acad Sci USA 106:17886–17891. https://doi.org/10.1073/pnas.0901324106
Zang B, Zhao J, Chen C (2019) LncRNA PCAT-1 promoted ESCC progression via regulating ANXA10 expression by sponging miR-508-3p. Cancer Manag Res 11:10841–10849. https://doi.org/10.2147/cmar.s233983
Zhang Y et al (2011) Down-regulation of TSG101 by small interfering RNA inhibits the proliferation of breast cancer cells through the MAPK/ERK signal pathway. Histol Histopathol 26:87–94. https://doi.org/10.14670/hh-26.87
Zhu J, Wu J, Pei X, Tan Z, Shi J, Lubman DM (2017) Annexin A10 is a candidate marker associated with the progression of pancreatic precursor lesions to adenocarcinoma. PLoS ONE 12:e0175039. https://doi.org/10.1371/journal.pone.0175039
Funding
Young and Middle-aged Scientific Research Foundation of Wannan Medical College (WK2020F20).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wei, T., Zhu, X. Knockdown of ANXA10 inhibits proliferation and promotes apoptosis of papillary thyroid carcinoma cells by down-regulating TSG101 thereby inactivating the MAPK/ERK signaling pathway. J Bioenerg Biomembr 53, 429–440 (2021). https://doi.org/10.1007/s10863-021-09902-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10863-021-09902-7