Role of annexin A3 in breast cancer (Review)
- Authors:
- Published online on: May 12, 2022 https://doi.org/10.3892/mco.2022.2544
- Article Number: 111
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Copyright: © Ozturk . This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
1. Introduction and background
Annexins are a family of proteins occurring in a variety of cell types (1). They bind calcium and phospholipids to form calcium-dependent ion voltage channels (2). Annexins also have roles in events such as coagulation inhibition, endocytosis, exocytosis, signal transduction, proliferation and programmed cell death, and it has been suggested that calcium binding underlies these effects of annexins (3,4). There are a total of 12 different annexin proteins in mammals. These proteins are named as A1-A11 and A13(5).
Changes in annexin expression have been demonstrated to be associated with various pathologies, including asthma (6), atherosclerosis (7), autoimmune diseases (8) and Alzheimer's disease (9).
In the present review, the associations of annexin A3 (ANXA3) with breast cancer were investigated. Since there are numerous studies indicating that ANXA3 has a key role in certain cancer types such as breast cancer, the present review focused on this protein.
Associations of ANXA3 with various malignant neoplasms have been reported, including breast cancer (10-19), colorectal cancer (20-23), prostate cancer (24-26), nasopharyngeal carcinoma (27), pancreatic cancer (28), hepatocellular carcinoma (29-33), renal carcinoma (34), thyroid cancer (35), osteosarcoma (36), gastric cancer (37-41) and lung cancer (42-46).
ANXA3, also called placental anticoagulant protein a3 or lipocortin 3, is encoded on 4q13-q22(6). The ANXA3 molecule has two isoforms with a molecular weight of 36 kDa (containing 323 amino acids) and 33 kDa (containing 284 amino acids) (5,47). Although most neoplasms express only the 36 kDa form, certain cells express both isoforms, or cells such as myeloid cells, prostate adenocarcinoma cells, rat brain cells, may express only one of the two isoforms (33 or 36 kDa) (25,48-50). Le Cabec et al (48) reported that both isoforms of 33 and 36 kDa were expressed in myeloblast HL-60 cells. In this study, ANXA3 expression was analyzed by western blot. It was indicated that the expression of the 33 kDA form was higher and that the expression of the 36 kDa form was lower in renal cell carcinoma cells compared to primary cell cultures. This result revealed that both isoforms may have different roles in the carcinogenesis process (47,51). To date, no studies have been performed to differentiate between 36- and 33-kDa ANXA3 by identifying the individual contribution to cancer development and progression.
ANXA has a variable N-terminal region and a fixed C-terminal region. The C-terminal region consists of four or eight annexin repeats. Each of the annexin repeats consists of ~70 amino acids containing phospholipid and Ca2+ binding sites (52). The N-terminal region of annexins, which causes different biological activities and functions, consists of 20-200 amino acids (53,54). ANXA3 contains an N-terminus, four additional repeat domains and a C-terminus. Unlike the 36 kDa isoform, the 33 kDa isoform of ANXA3 does not have the first 39 amino acid residues of the N-terminal region (19). The N-terminus of ANXA3 is involved in the regulation of membrane binding with the tryptophan 5 (W5) domain and non-specific permeability. N-terminal loss or W5 mutation may be observed in the 33-kDA isoform of the ANXA3 molecule. These conditions also alter the membrane interaction by increasing the cellular Ca2+ flux (55).
A literature search was performed for the present review via Web of Science, PubMed, MEDLINE and EMBASE to retrieve studies published between January 1, 1990 and January 1, 2022, using the keywords ‘annexin A3’, ‘breast cancer’, ‘role’, ‘annexin’, ‘drug resistance’ and ‘chemotherapy’. Initially, 14,834 entries were retrieved. Among them, 1,041 studies were open access and available. A total of 1,041 studies were viewed and 888 studies were excluded, as they did not appear relevant to the study subject (based on their titles or abstracts), while 153 studies were retained. Subsequently, 144 studies were excluded for the following reasons: Unsuitable study design (based on their titles or abstracts), duplication, abstract only (the full papers were not accesible), language, insufficient information and other reasons (insufficient number of patients, letters to the editor etc.). Finally, the 9 studies remaining were analyzed in detail and included in the present review. The number of patients in these 9 studies, the method by which the ANXA3 molecule was analyzed, the ANXA3 expression results and the potential roles of this protein are summarized in Table I.
Table IDetails of the 9 papers on the role of ANXA3 in breast cancer included in the present review. |
2. Role of ANXA3 in breast cancer development and progression
A previous study suggested that ANCA3 is associated with tumor progression and may be a potential prognostic marker (13). In that study, ANXA3 expression in patients with breast cancer was evaluated by western blot analysis. Furthermore, ANXA3 was inhibited by RNA interference in MDA-MB-231 cancer cells and the effects on proliferation, colonization and invasion were observed. In addition, the ANXA3 levels of 30 patients with breast cancer were evaluated by immunohistochemistry and their association with survival was determined. ANXA3 levels were observed to be higher in MDA-MB-231, HCC-70 and HCC-1954 cells compared to non-cancerous cell lines. It was also observed that ANXA3 silencing suppressed the invasion, wound healing and colonization properties of MDA-MB-231 and HCC-1954 cells. ANXA3 expression was indicated to be closely related to tumor size and high ANXA3 levels were associated with decreased survival rates (13).
In another related study, the mechanisms of the effects of ANXA3 in breast cancer cells were investigated (14). The expression of ANXA3 was observed to be significantly higher in MDA-MB-231 cells than in MCF-7 cells. Following knockdown of ANXA3, which was confirmed by western blot analysis, the percentage of G0/1 cells in the cell cycle and the apoptosis rate were indicated to be significantly higher and the proliferation rate was lower compared with that in the control groups. In the wound healing test, the migratory ability of MDA-MB-231-Sh cells was shown to be significantly lower than that of MDA-MB-231-NC and MDA-MB-231 cells. Furthermore, the cell invasion capacity was lower in MDA-MB-231 cells with ANXA3 knockdown. This study demonstrated that ANXA3 is associated with the proliferation, apoptosis, migration and invasion of breast cancer cells (14).
Li et al (17) investigated the roles of ANXA3 in breast cancer in vivo in a study using subcutaneous tumors in mice. A total of 18 mice were divided into three groups and inoculated with either native MDA-MB-231 cells, negative control-transfected MDA-MB-231 or MDA-MB-231 cells with ANXA3 knockdown. Flow cytometry was used to evaluate cell proliferation and reverse transcription-quantitative (RT-q)PCR was used to determine ANXA3 mRNA expression. Slower tumor growth was reported for the transfection group. In addition, the tumor weight was observed to be significantly lower in the transfection group (P<0.01). ANXA3 levels in the transfection group were indicated to be significantly lower than those in the other groups (P<0.01). A lower proliferation index and higher G0/1 population were also observed in the transfection group (P<0.01). This study suggested that ANXA3 regulates tumor cell proliferation and growth and may be used as a therapeutic target (17).
3. Effect of ANXA3 on patient prognosis
Zhou et al (10) performed a study of 309 patients; higher levels of ANXA3 were detected in cancerous tissue compared to adjacent tissue and ANXA3 levels were reported to be associated with lymphatic metastasis (P=0.001) and tumor grade (P=0.004). ANXA3 and lymphatic metastases were identified as independent risk factors affecting survival. Higher levels of ANXA3 were detected in cases of triple-negative breast cancer compared to other types (P<0.002). No significant difference was observed between groups of different ages, tumor size, stage or menopausal status and ANXA3 levels (P>0.05). The results of that study suggested an association between ANXA3 and the progression of breast cancer, which is due to increased lymphatic metastasis. This study also indicated that ANXA3 may be a prognostic marker in breast cancer (10).
In another study, ANXA3 levels were investigated in 60 patients with breast cancer (11). In addition, the effect of RNA interference with ANXA3 on apoptosis of breast cancer cells was investigated. The results suggested that ANXA3 levels were higher in breast cancer compared to normal breast tissues. ANXA3 in carcinoma tissues was also reported to be closely associated with tumor size and axillary metastasis. Kaplan-Meier analysis indicated a significant negative association between high levels of ANXA3 and survival, and ANXA3 overexpression was indicated to be inversely proportional to Bax staining and the apoptosis index. The findings of this study suggested that ANXA3 may be a novel prognostic marker and have a role in the regulation of apoptosis (11).
The clinical implication of ANXA3 in cancer cells vs. normal cells was investigated in a study involving 81 cancer patients. ANXA3 mRNA levels in the samples were determined by RT-qPCR and ANXA3 protein expression was detected by western blot analysis. Proliferation indices were compared between cancer cells and normal cells using flow cytometry. The correlations between gene and protein expression levels of ANXA3 and the proliferation indices of cancer cells were also calculated. ANXA3 levels were observed to be significantly higher in breast cancer tissues than in normal cells. It was observed that ANXA3 levels were significantly higher in triple-negative cases compared to luminal A and B types. By contrast, no significant difference in expression levels was observed among other subtypes. It was reported that the proliferation indices of breast cancer cells were significantly higher and were positively correlated with ANXA3. This study revealed that ANXA3 expression may have an important role in cancer development and metastasis and may be an important biomarker in prognosis (15).
4. ANXA3 as a therapeutic target
A study was published that included 219 patients with breast cancer, 192 patients with benign breast pathology and 630 healthy controls (12). The ANXA3 levels of these individuals were determined by mass spectrometry and ELISA. Serum ANXA3 levels were indicated to be significantly higher in patients with benign pathology compared to the other groups (P<0.0005). In addition, ANXA3 was determined to be highly expressed in benign and well-differentiated malignant tumour cells. This study demonstrated that ANXA3 is a novel marker in breast tumors, may serve as a therapeutic target and has a role in the migration of neoplastic cells (12).
Du et al (16) investigated the relationship of ANXA3 with metastasis and drug resistance in breast cancer. In this study, ANXA3 expression levels were observed to be significantly higher in breast cancer tissues. In vitro and in vivo analyses indicated that invasion decreased and cell proliferation increased after inhibition of ANXA3. One of the most important contributions of this study was the finding that ANXA3 inhibition increases sensitivity to doxorubicin by increasing drug uptake. Doxorubicin and ANXA3 degradation appeared to suppress tumor growth and metastasis. This study demonstrated the role of ANXA3 in the growth and metastasis of breast cancer and indicated that ANXA3 downregulation may be a novel therapeutic strategy for the treatment of breast cancer (16).
Zhu et al (18) investigated the relationship between ANXA3 and chemotherapy efficacy in a study that included 158 patients with breast cancer. A total of 83 patients were treated with epirubicin + cyclophosphamide + 5-fluorouracil (CEF group) and 75 patients were treated with epirubicin + cyclophosphamide + docetaxel (TEC group). Tissue samples were obtained from each patient prior to and 10 days after chemotherapy administration to detect ANXA3 expression, which was determined by RT-qPCR. Significant differences in the rates of remission and progressive disease were reported between the groups (Z=10.716, P=0.013). The clinical efficacy rate in the TEC group was determined to be significantly higher (P<0.05). It was also observed that there was no significant difference between the two groups in terms of bone marrow suppression (P>0.05). While there was no difference between the two groups in terms of ANXA3 levels prior to chemotherapy, ANXA3 levels after chemotherapy were determined to be lower in the TEC group (P<0.05). This study revealed that, compared to the CEF regimen, the TEC regimen may improve clinicopathological efficacy, inhibit ANXA3 expression and improve the prognosis of patients (18).
5. Comparison with similar studies
The article published by Yang et al (51) is a review reporting the effect of ANXA3 in cancer. However, the present study is only a review article focusing on breast cancer. Therefore, this previous study is more comprehensive; however, it does not include 3 research articles (11,12,18) examined in the present study.
Although the review article by Liu et al (19) reporting the effect of ANXA3 in cancer is similar to the present study, the present article is only a review on breast cancer. Furthermore, this previous study does not include 2 research articles (12,18) examined in the present study.
6. Conclusions
To date, numerous studies have been performed with the aim of investigating the relationship between ANXA3 expression and breast cancer. In these studies, the role of ANXA3 in the development, spread, prognosis and treatment processes of breast cancer were investigated. These studies indicated that ANXA3 levels were higher in breast cancer cells than in normal cells, with a significant inverse association between strong ANXA3 expression and survival. Based on the present review, ANXA3 expression is associated with growth, proliferation, apoptosis and invasion of breast cancer cells, and the level of ANXA3 is an important biomarker for the prognosis of breast cancer. Furthermore, ANXA3 is a potential therapeutic target for the treatment of breast cancer. Multicenter studies should be performed with larger patient groups to better understand the roles of ANXA3 in breast cancer and other malignant tumors and develop it as a target and marker for effective treatment programs. These studies will be promising for the treatment and prognosis of breast cancer.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
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Authors' contributions
AO was responsible for the conception and design of the review, performed the literature search and selection, wrote the manuscript and edited it. AO read and approved the final manuscript to be published. Data authentication is not applicable.
Ethics approval and consent to participate
Not applicable.
Patient consent for publication
Not applicable.
Competing interests
The author declares that he has no competing interests.
Author's information
Author's ORCID no is: 0000-0003-4525-3477.
References
Edwards HC and Crumpton MJ: Ca(2+)-dependent phospholipid and arachidonic acid binding by the placental annexins VI and IV. Eur J Biochem. 198:121–129. 1991.PubMed/NCBI View Article : Google Scholar | |
Liemann S and Lewit-Bentley A: Annexins: A novel family of calcium- and membrane-binding proteins in search of a function. Structure. 3:233–237. 1995.PubMed/NCBI View Article : Google Scholar | |
Pepinsky RB, Tizard R, Mattaliano RJ, Sinclair LK, Miller GT, Browning JL, Chow EP, Burne C, Huang KS, Pratt D, et al: Five distinct calcium and phospholipid binding proteins share homology with lipocortin I. J Biol Chem. 263:10799–10811. 1988.PubMed/NCBI | |
Ernst JD, Hoye E, Blackwood RA and Jaye D: Purification and characterization of an abundant cytosolic protein from human neutrophils that promotes Ca2(+)-dependent aggregation of isolated specific granules. J Clin Invest. 85:1065–1071. 1990.PubMed/NCBI View Article : Google Scholar | |
Mussunoor S and Murray GI: The role of annexins in tumour development and progression. J Pathol. 216:131–140. 2008.PubMed/NCBI View Article : Google Scholar | |
Gerke V and Moss SE: Annexins: From structure to function. Physiol Rev. 82:331–371. 2002.PubMed/NCBI View Article : Google Scholar | |
Hedhli N, Falcone DJ, Huang B, Cesarman-Maus G, Kraemer R, Zhai H, Tsirka SE, Santambrogio L and Hajjar KA: The annexin A2/S100A10 system in health and disease: Emerging paradigms. J Biomed Biotechnol. 2012(406273)2012.PubMed/NCBI View Article : Google Scholar | |
Weiss R, Bitton A, Ben Shimon M, Elhaik Goldman S, Nahary L, Cooper I, Benhar I, Pick CG and Chapman J: Annexin A2, autoimmunity, anxiety and depression. J Autoimmun. 73:92–99. 2016.PubMed/NCBI View Article : Google Scholar | |
Sohma H, Imai S, Takei N, Honda H, Matsumoto K, Utsumi K, Matsuki K, Hashimoto E, Saito T and Kokai Y: Evaluation of annexin A5 as a biomarker for Alzheimer's disease and dementia with lewy bodies. Front Aging Neurosci. 5(15)2013.PubMed/NCBI View Article : Google Scholar | |
Zhou T, Li Y, Yang L, Tang T, Zhang L and Shi J: Annexin A3 as a prognostic biomarker for breast cancer: A retrospective study. Biomed Res Int. 2017(2603685)2017.PubMed/NCBI View Article : Google Scholar | |
Zeng C, Ke Z, Song Y, Yao Y, Hu X, Zhang M, Li H and Yin J: Annexin A3 is associated with a poor prognosis in breast cancer and participates in the modulation of apoptosis in vitro by affecting the Bcl-2/Bax balance. Exp Mol Pathol. 95:23–31. 2013.PubMed/NCBI View Article : Google Scholar | |
Zeidan B, Jackson TR, Larkin SE, Cutress RI, Coulton GR, Ashton-Key M, Murray N, Packham G, Gorgoulis V, Garbis SD and Townsend PA: Annexin A3 is a mammary marker and a potential neoplastic breast cell therapeutic target. Oncotarget. 6:21421–21427. 2015.PubMed/NCBI View Article : Google Scholar | |
Kim JY, Jung EJ, Park HJ, Lee JH, Song EJ, Kwag SJ, Park JH, Park T, Jeong SH, Jeong CY, et al: Tumor-suppressing effect of silencing of annexin A3 expression in breast cancer. Clin Breast Cancer. 18:e713–e719. 2018.PubMed/NCBI View Article : Google Scholar | |
Zhou T, Li Y, Yang L, Liu L, Ju Y and Li C: Silencing of ANXA3 expression by RNA interference inhibits the proliferation and invasion of breast cancer cells. Oncol Rep. 37:388–398. 2017.PubMed/NCBI View Article : Google Scholar | |
Zhou T, Liu S, Yang L, Ju Y and Li C: The expression of ANXA3 and its relationship with the occurrence and development of breast cancer. J BUON. 23:713–719. 2018.PubMed/NCBI | |
Du R, Liu B, Zhou L, Wang D, He X, Xu X, Zhang L, Niu C and Liu S: Downregulation of annexin A3 inhibits tumor metastasis and decreases drug resistance in breast cancer. Cell Death Dis. 9(126)2018.PubMed/NCBI View Article : Google Scholar | |
Li J, Zhou T, Liu L, Ju YC, Chen YT, Tan ZR and Wang J: The regulatory role of annexin 3 in a nude mouse bearing a subcutaneous xenograft of MDA-MB-231 human breast carcinoma. Pathol Res Pract. 214:1719–1725. 2018.PubMed/NCBI View Article : Google Scholar | |
Zhu S, Li Y, Wang Y, Cao J, Li X, Wang J and Wang X: Efficacy of neoadjuvant chemotherapy and annexin A3 expression in breast cancer. J BUON. 24:522–528. 2019.PubMed/NCBI | |
Liu C, Li N, Liu G and Feng X: Annexin A3 and cancer. Oncol Lett. 22(834)2021.PubMed/NCBI View Article : Google Scholar | |
Xu R, Yin J, Zhang Y and Zhang S: Annexin A3 depletion overcomes resistance to oxaliplatin in colorectal cancer via the MAPK signaling pathway. J Cell Biochem. 120:14585–14593. 2019.PubMed/NCBI View Article : Google Scholar | |
Yang L, Men WL, Yan KM, Tie J, Nie YZ and Xiao HJ: MiR-340-5p is a potential prognostic indicator of colorectal cancer and modulates ANXA3. Eur Rev Med Pharmacol Sci. 22:4837–4845. 2018.PubMed/NCBI View Article : Google Scholar | |
Bai Z, Wang J, Wang T, Li Y, Zhao X, Wu G, Yang Y, Deng W and Zhang Z: The MiR-495/annexin A3/P53 axis ınhibits the ınvasion and EMT of colorectal cancer cells. Cell Physiol Biochem. 44:1882–1895. 2017.PubMed/NCBI View Article : Google Scholar | |
Xie YQ, Fu D, He ZH and Tan QD: Prognostic value of annexin A3 in human colorectal cancer and its correlation with hypoxia-inducible factor-1α. Oncol Lett. 6:1631–1635. 2013.PubMed/NCBI View Article : Google Scholar | |
Köllermann J, Schlomm T, Bang H, Schwall GP, von Eichel-Streiber C, Simon R, Schostak M, Huland H, Berg W, Sauter G, et al: Expression and prognostic relevance of annexin A3 in prostate cancer. Eur Urol. 54:1314–1323. 2008.PubMed/NCBI View Article : Google Scholar | |
Hamelin-Peyron C, Vlaeminck-Guillem V, Haïdous H, Schwall GP, Poznanović S, Gorius-Gallet E, Michel S, Larue A, Guillotte M, Ruffion A, et al: Prostate cancer biomarker annexin A3 detected in urines obtained following digital rectal examination presents antigenic variability. Clin Biochem. 47:901–908. 2014.PubMed/NCBI View Article : Google Scholar | |
Schostak M, Schwall GP, Poznanović S, Groebe K, Müller M, Messinger D, Miller K, Krause H, Pelzer A, Horninger W, et al: Annexin A3 in urine: A highly specific noninvasive marker for prostate cancer early detection. J Urol. 181:343–353. 2009.PubMed/NCBI View Article : Google Scholar | |
Qu S, Li XY, Liang ZG, Li L, Huang ST, Li JQ, Li DR and Zhu XD: Protein expression of nucleophosmin, annexin A3 and nm23-H1 correlates with human nasopharyngeal carcinoma radioresistance in vivo. Oncol Lett. 12:615–620. 2016.PubMed/NCBI View Article : Google Scholar | |
Wan X, Guo D, Zhu Q and Qu R: microRNA-382 suppresses the progression of pancreatic cancer through the PI3K/Akt signaling pathway by inhibition of Anxa3. Am J Physiol Gastrointest Liver Physiol. 319:G309–G322. 2020.PubMed/NCBI View Article : Google Scholar | |
Ma XL, Jiang M, Zhao Y, Wang BL, Shen MN, Zhou Y, Zhang CY, Sun YF, Chen JW, Hu B, et al: Application of serum annexin A3 in diagnosis, outcome prediction and therapeutic response evaluation for patients with hepatocellular carcinoma. Ann Surg Oncol. 25:1686–1694. 2018.PubMed/NCBI View Article : Google Scholar | |
Pan QZ, Pan K, Weng DS, Zhao JJ, Zhang XF, Wang DD, Lv L, Jiang SS, Zheng HX and Xia JC: Annexin A3 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma. Mol Carcinog. 54:598–607. 2015.PubMed/NCBI View Article : Google Scholar | |
Pan QZ, Pan K, Wang QJ, Weng DS, Zhao JJ, Zheng HX, Zhang XF, Jiang SS, Lv L, Tang Y, et al: Annexin A3 as a potential target for immunotherapy of liver cancer stem-like cells. Stem Cells. 33:354–366. 2015.PubMed/NCBI View Article : Google Scholar | |
Tong M, Che N, Zhou L, Luk ST, Kau PW, Chai S, Ngan ES, Lo CM, Man K, Ding J, et al: Efficacy of annexin A3 blockade in sensitizing hepatocellular carcinoma to sorafenib and regorafenib. J Hepatol. 69:826–839. 2018.PubMed/NCBI View Article : Google Scholar | |
Zhu Q, Pan QZ, Zhong AL, Hu H, Zhao JJ, Tang Y, Hu WM, Li M, Weng DS, Chen MY, et al: Annexin A3 upregulates the infiltrated neutrophil-lymphocyte ratio to remodel the immune microenvironment in hepatocellular carcinoma. Int Immunopharmacol. 89(107139)2020.PubMed/NCBI View Article : Google Scholar | |
Bombelli S, Torsello B, De Marco S, Lucarelli G, Cifola I, Grasselli C, Strada G, Bovo G, Perego RA and Bianchi C: 36-kDa annexin A3 isoform negatively modulates lipid storage in clear cell renal cell carcinoma cells. Am J Pathol. 190:2317–2326. 2020.PubMed/NCBI View Article : Google Scholar | |
Jung EJ, Moon HG, Park ST, Cho BI, Lee SM, Jeong CY, Ju YT, Jeong SH, Lee YJ, Choi SK, et al: Decreased annexin A3 expression correlates with tumor progression in papillary thyroid cancer. Proteomics Clin Appl. 4:528–537. 2010.PubMed/NCBI View Article : Google Scholar | |
Zeng X, Wang S, Gui P, Wu H and Li Z: Expression and significance of annexin A3 in the osteosarcoma cell lines HOS and U2OS. Mol Med Rep. 20:2583–2590. 2019.PubMed/NCBI View Article : Google Scholar | |
Wang J, Jia X, Meng X, Li Y, Wu W, Zhang X, Xu H and Cui J: Annexin A3 may play an important role in ochratoxin-induced malignant transformation of human gastric epithelium cells. Toxicol Lett. 313:150–158. 2019.PubMed/NCBI View Article : Google Scholar | |
Takahashi H, Kaniwa N, Saito Y, Sai K, Hamaguchi T, Shirao K, Shimada Y, Matsumura Y, Ohtsu A, Yoshino T, et al: Construction of possible integrated predictive index based on EGFR and ANXA3 polymorphisms for chemotherapy response in fluoropyrimidine-treated Japanese gastric cancer patients using a bioinformatic method. BMC Cancer. 15(718)2015.PubMed/NCBI View Article : Google Scholar | |
Zhai JM, Sun SJ, Wang W and Zeng C: Expression of annexin A3 in gastric cancer and its correlation with proliferation and apoptosis. Asian Pac J Cancer Prev. 15:3001–3004. 2014.PubMed/NCBI View Article : Google Scholar | |
Yu SY, Li Y, Fan LQ, Zhao Q, Tan BB and Liu Y: Impact of annexin A3 expression in gastric cancer cells. Neoplasma. 61:257–264. 2014.PubMed/NCBI View Article : Google Scholar | |
Wang K and Li J: Overexpression of ANXA3 is an independent prognostic indicator in gastric cancer and its depletion suppresses cell proliferation and tumor growth. Oncotarget. 7:86972–86984. 2016.PubMed/NCBI View Article : Google Scholar | |
Jın YF, Huang YT and Chen PF: ANXA3 deletion inhibits the resistance of lung cancer cells to oxaliplatin. Eur Rev Med Pharmacol Sci. 24:3741–3748. 2020.PubMed/NCBI View Article : Google Scholar | |
Liu YF, Liu QQ, Zhang YH and Qiu JH: Annexin A3 knockdown suppresses lung adenocarcinoma. Anal Cell Pathol (Amst). 2016(4131403)2016.PubMed/NCBI View Article : Google Scholar | |
Wang C, Xiao Q, Li YW, Zhao C, Jia N, Li RL, Cao SS, Cui J, Wang L, Wu Y and Wen AD: Regulatory mechanisms of annexin-induced chemotherapy resistance in cisplatin resistant lung adenocarcinoma. Asian Pac J Cancer Prev. 15:3191–3194. 2014.PubMed/NCBI View Article : Google Scholar | |
Wang L, Li X, Ren Y, Geng H, Zhang Q, Cao L, Meng Z, Wu X, Xu M and Xu K: Cancer-associated fibroblasts contribute to cisplatin resistance by modulating ANXA3 in lung cancer cells. Cancer Sci. 110:1609–1620. 2019.PubMed/NCBI View Article : Google Scholar | |
Liu YF, Xiao ZQ, Li MX, Li MY, Zhang PF, Li C, Li F, Chen YH, Yi H, Yao HX and Chen ZC: Quantitative proteome analysis reveals annexin A3 as a novel biomarker in lung adenocarcinoma. J Pathol. 217:54–64. 2009.PubMed/NCBI View Article : Google Scholar | |
Bianchi C, Bombelli S, Raimondo F, Torsello B, Angeloni V, Ferrero S, Di Stefano V, Chinello C, Cifola I, Invernizzi L, et al: Primary cell cultures from human renal cortex and renal-cell carcinoma evidence a differential expression of two spliced isoforms of annexin A3. Am J Pathol. 176:1660–1670. 2010.PubMed/NCBI View Article : Google Scholar | |
Le Cabec V, Russo-Marie F and Maridonneau-Parini I: Differential expression of two forms of annexin 3 in human neutrophils and monocytes and along their differentiation. Biochem Biophys Res Commun. 189:1471–1476. 1992.PubMed/NCBI View Article : Google Scholar | |
Nishiura H, Yamanegi K, Kawabe M, Kato-Kogoe N, Yamada N and Nakasho K: Annexin A3 plays a role in cytoplasmic calcium oscillation by extracellular calcium in the human promyelocytic leukemia HL-60 cells differentiated by phorbol-12-myristate-13-acetate. Exp Mol Pathol. 97:241–246. 2014.PubMed/NCBI View Article : Google Scholar | |
Junker H, Suofu Y, Venz S, Sascau M, Herndon JG, Kessler C, Walther R and Popa-Wagner A: Proteomic identification of an upregulated isoform of annexin A3 in the rat brain following reversible cerebral ischemia. Glia. 55:1630–1637. 2007.PubMed/NCBI View Article : Google Scholar | |
Yang L, Lu P, Yang X, Li K and Qu S: Annexin A3, a calcium-dependent phospholipid-binding protein: Implication in cancer. Front Mol Biosci. 8(716415)2021.PubMed/NCBI View Article : Google Scholar | |
Boye TL and Nylandsted J: Annexins in plasma membrane repair. Biol Chem. 397:961–969. 2016.PubMed/NCBI View Article : Google Scholar | |
Rescher U and Grewal T: Highlight: Annexins in health and disease. Biol Chem. 397:947–948. 2016.PubMed/NCBI View Article : Google Scholar | |
Purvis GSD, Solito E and Thiemermann C: Annexin-A1: Therapeutic potential in microvascular disease. Front Immunol. 10(938)2019.PubMed/NCBI View Article : Google Scholar | |
Hofmann A, Raguénès-Nicol C, Favier-Perron B, Mesonero J, Huber R, Russo-Marie F and Lewit-Bentley A: The annexin A3-membrane interaction is modulated by an N-terminal tryptophan. Biochemistry. 39:7712–7721. 2000.PubMed/NCBI View Article : Google Scholar |