SALL4 is a marker of poor prognosis in serous ovarian carcinoma promoting invasion and metastasis
Open accessAbstract
Spalt-like transcription factor 4 (SALL4) is a transcription factor which is able to regulate development and embryonic stem cell pluripotency, and it is also involved in some tumor progression. However, the role of SALL4 in serous ovarian carcinoma (SOC) is still controversial. In this study, we determined the SALL4 expression in ovarian carcinoma (OC) cell lines and SOC tissues, and explored the clinical value of SALL4 in SOC. The SALL4 mRNA and protein expression in OC cell lines were examined by real-time PCR and western blotting. The SALL4 protein expression of 91 SOC tissue samples were examined by immunohistochemistry, and the correlation with clinicopathologic features as well as the survivals of SOC patients were analyzed. The invasion potential of OC cells were determined by cytoskeleton immunofluorescence, wound-healing, Transwell and colony formation assays. Our study found SALL4 mRNA and protein were highly expressed in OC cell lines, especially in HO-8910PM. SALL4 protein was highly expressed in SOC tissues, and positively associated with advanced FIGO stage, high histological grade, lymph node involvement, distant metastasis, recurrence and death of SOC (all P<0.05). Survival analysis showed that high expression of SALL4 indicated poorer overall and progression-free survival (P<0.05). Univariate and multivariate analysis showed that SALL4 is an independent marker for prognosis prediction (P<0.05). SALL4 ectopic expression significantly increased the migration, invasion and proliferation capacity of OC cells. In contrast, inhibition of SALL4 markedly decreased these capacities in vitro. In addition, SALL4-interference changed critical signaling involved in cancer progression. In conclusion, SALL4 was highly expressed and correlated with poor prognosis in SOC patients, promoting invasion and metastasis of OC cells. SALL4 could be a novel molecular target and prognostic marker for SOC.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
SALL4 is a zinc finger transcription factor important for many cancers, most notably hepatocellular carcinoma (HCC).
“SALL4 is a zinc finger transcription factor that is important for many cancers, most notably hepatocellular carcinoma (HCC) (Yong et al, 2013), lung cancer (Kobayashi et al, 2011a), ovarian cancer (Yang et al, 2016), breast cancer (Kobayashi et al, 2011b), myelodysplastic syndrome (MDS) (Liu et al, 2022), and acute myeloid leukemia (AML) (Li et al, 2013; Ma et al, 2006).”
From Targeting transcription factors through an IMiD independent zinc finger domain (2025) · cites this paper as Yang et al, 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Jemal, A., Tiwari, R. C., Murray, T., Ghafoor, A., Samuels, A., Ward, E., Feuer, E. J., & Thun, M. J. (2004) · CA: A Cancer Journal for Clinicians · doi:10.3322/canjclin.54.1.8 · Cited by 3,984 · see citing works
Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits
Polyak, K., & Weinberg, R. A. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2620 · Cited by 3,302 · see citing works
Rubin, M., & Stephen, C. D. (1993) · Cited by 3,161 · see citing works
Jayson, G. C., Kohn, E. C., Kitchener, H. C., & Ledermann, J. A. (2014) · The Lancet · doi:10.1016/s0140-6736(13)62146-7 · Cited by 1,853 · see citing works
The biology of ovarian cancer: new opportunities for translation
Bast, R. C., Hennessy, B. T., & Mills, G. B. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2644 · Cited by 1,362 · see citing works
Cannistra, S. (1993) · New England Journal of Medicine · doi:10.1056/nejmra041842 · Cited by 957 · see citing works
Recent progress in the diagnosis and treatment of ovarian cancer
Jelovac, D., & Armstrong, D. K. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20113 · Cited by 779 · see citing works
Epithelial-mesenchymal transitions: insights from development
Lim, J., & Thiery, J. P. (2012) · Development · doi:10.1242/dev.071209 · Cited by 661 · see citing works
Zhang, J., Tam, W.-L., Tong, G. Q., Wu, Q., Chan, H.-Y., Soh, B.-S., Lou, Y., Yang, J., Ma, Y., Chai, L., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1481 · Cited by 568 · see citing works
EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness
Sànchez‐Tilló, E., Liu, Y., de Barrios, O., Siles, L., Fanlo, L., Cuatrecasas, M., Darling, D. S., Dean, D. C., Castells, A., & Postigo, A. A. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1122-2 · Cited by 520 · see citing works
Yang, D., Sun, Y., Hu, L., Zheng, H., Ji, P., Pecot, C. V., Zhao, Y., Reynolds, S. M., Cheng, H., Rupaimoole, R., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2012.12.020 · Cited by 395 · see citing works
Al-Baradie, R., Yamada, K., St. Hilaire, C., Chan, W.-M., Andrews, C., McIntosh, N., Nakano, M., Martonyi, E. J., Raymond, W. R., Okumura, S., et al. (2002) · The American Journal of Human Genetics · doi:10.1086/343821 · Cited by 314 · see citing works
Cao, L., Shao, M., Schilder, J. M., Guise, T. A., Mohammad, K. S., & Matei, D. E. (2011) · Oncogene · doi:10.1038/onc.2011.429 · Cited by 224 · see citing works
Ma, Y., Cui, W., Yang, J., Qu, J., Di, C., Amin, H. M., Lai, R., Ritz, J., Krause, D. S., & Chai, L. (2006) · Blood · doi:10.1182/blood-2006-02-001594 · Cited by 215 · see citing works
SALL4 Expression in Germ Cell and Non–Germ Cell Tumors
Miettinen, M., Wang, Z., McCue, P. A., Sarlomo‐Rikala, M., Ryś, J., Biernat, W., Lasota, J. P., & Lee, Y.-S. (2014) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000116 · Cited by 205 · see citing works
Functional Antagonism between Sall4 and Plzf Defines Germline Progenitors
Hobbs, R. M., Fagoonee, S., Papa, A., Webster, K. A., Altruda, F., Nishinakamura, R., Chai, L., & Pandolfi, P. P. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.004 · Cited by 188 · see citing works
Kohlhase, J., Schubert, L., Liebers, M., Rauch, A., Becker, K., Mohammed, S. N., Newbury-Ecob, R., & Reardon, W. (2003) · Journal of Medical Genetics · doi:10.1136/jmg.40.7.473 · Cited by 185 · see citing works
Differential roles of Sall4 isoforms in embryonic stem cell pluripotency
Rao, S., Zhen, S., Roumiantsev, S., McDonald, L. T., Yuan, G.-C., & Orkin, S. H. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00419-10 · Cited by 173 · see citing works
SALL4, a novel marker for human gastric carcinogenesis and metastasis
Zhang, L., Xu, Z., Xu, X., Zhang, B., Wu, H., Wang, M., Zhang, X., Yang, T., Cai, J., Yan, Y., et al. (2013) · Oncogene · doi:10.1038/onc.2013.495 · Cited by 122 · see citing works
SALL4: An emerging cancer biomarker and target
Zhang, X., Yuan, X., Zhu, W., Qian, H., & Xu, W. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.11.037 · Cited by 100 · see citing works
SALL4 is a new target in endometrial cancer
Li, A., Jiao, Y., Yong, K. J., Wang, F., Gao, C., Yan, B., Srivastava, S., Lim, G. S. D., Tang, P., He, Y., et al. (2013) · Oncogene · doi:10.1038/onc.2013.529 · Cited by 100 · see citing works
Watanabe (2011) · International Journal of Oncology · doi:10.3892/ijo.2011.929 · Cited by 82 · see citing works
Overexpression of SALL4 in lung cancer and its importance in cell proliferation
Watanabe, N. (2011) · Oncology Reports · doi:10.3892/or.2011.1374 · Cited by 78 · see citing works
SALL4 is directly activated by TCF/LEF in the canonical Wnt signaling pathway
Böhm, J., Sustmann, C., Wilhelm, C., & Kohlhase, J. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.07.124 · Cited by 77 · see citing works
SALL4 as a new biomarker for early colorectal cancers
Khales, S. A., Abbaszadegan, M. R., Abdollahi, A., Raeisossadati, R., Tousi, M. F., & Forghanifard, M. M. (2014) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-014-1808-y · Cited by 72 · see citing works
Davidson, B., Holth, A., Hellesylt, E., Tan, T. Z., Huang, R. Y., Trope, C. G., Nesland, J. M., & Thiery, J. P. (2014) · Human Pathology · doi:10.1016/j.humpath.2014.10.004 · Cited by 63 · see citing works
An Oct4‐Sall4‐Nanog network controls developmental progression in the pre‐implantation mouse embryo
Tan, M. H., Au, K. F., Leong, D. E., Foygel, K., Wong, W. H., & Yao, M. W. M. (2013) · Molecular Systems Biology · doi:10.1038/msb.2012.65 · Cited by 63 · see citing works
A SALL4/MLL/HOXA9 pathway in murine and human myeloid leukemogenesis.
Li, A.-L., Yang, Y., Gao, C., Lu, J., Jeong, H.-W., Liu, B.-H., Tang, P., Yao, X.-P., Neuberg, D., Huang, G., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci62891 · Cited by 48 · see citing works
Oncofetal Gene SALL4 in Aggressive Hepatocellular Carcinoma
Hopkins, L., Rowe, I. A. C., & Houlihan, D. D. (2013) · New England Journal of Medicine · doi:10.1056/nejmc1308785 · Cited by 45 · see citing works
Yi, B.-R., Kim, T., Kim, Y.-S., & Choi, K. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2695 · Cited by 40 · see citing works
Trinh, D. T., Shibata, K., Hirosawa, T., Umezu, T., Mizuno, M., Kajiyama, H., & Kikkawa, F. (2012) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2011.01798.x · Cited by 36 · see citing works
Sall4 isoforms act during proximal–distal and anterior–posterior axis formation in the mouse embryo
Uez, N., Lickert, H., Kohlhase, J., de Angelis, M. H., Kühn, R., Wurst, W., & Floß, T. (2008) · genesis · doi:10.1002/dvg.20421 · Cited by 33 · see citing works
Chao, T., Yo, Y.-T., Liao, Y.-P., Wang, Y.-C., Su, P., Huang, T., & Lai, H. (2012) · Gynecologic Oncology · doi:10.1016/j.ygyno.2012.12.018 · Cited by 26 · see citing works
SALL4: Engine of Cell Stemness
Xiong, J. (2014) · Current Gene Therapy · doi:10.2174/1566523214666140825125138 · Cited by 25 · see citing works
Flagged first, then by citations
2 of the 36 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Da, C.-L., Liu, Y., Zhan, Y., Liu, K., & Wang, R. (2016) · Oncology Reports · doi:10.3892/or.2016.4661 · Cited by 84 · see citing works
SALL4 Oncogenic Function in Cancers: Mechanisms and Therapeutic Relevance
Sun, B., Xu, L., Bi, W., & Ou, W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042053 · Cited by 53 · see citing works
SALL 4 induces radioresistance in nasopharyngeal carcinoma via the ATM /Chk2/p53 pathway
Nie, X., Guo, E., Wu, C., Liu, D., Sun, W., Zhang, L., Long, G., Mei, Q., Wu, K., Xiong, H., et al. (2019) · Cancer Medicine · doi:10.1002/cam4.2056 · Cited by 46 · see citing works
SALL4 promotes glycolysis and chromatin remodeling via modulating HP1α-Glut1 pathway
Kim, J., Xu, S., Xiong, L., Yu, L., Fu, X., & Xu, Y. (2017) · Oncogene · doi:10.1038/onc.2017.265 · Cited by 40 · see citing works
Oncofetal gene SALL4 and prognosis in cancer: A systematic review with meta-analysis
Nicolè, L., Sanavia, T., Veronese, N., Cappellesso, R., Luchini, C., Dabrilli, P., & Fassina, A. (2017) · Oncotarget · doi:10.18632/oncotarget.14952 · Cited by 39 · see citing works
Itou, J., Li, W., Ito, S., Tanaka, S., Matsumoto, Y., Sato, F., & Toi, M. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000245 · Cited by 25 · see citing works
Functional and clinical significance of SALL4 in breast cancer
Dirican, E., & Akkіprіk, M. (2016) · Tumor Biology · doi:10.1007/s13277-016-5150-7 · Cited by 23 · see citing works
The new advance of SALL4 in cancer: Function, regulation, and implication
Abouelnazar, F. A., Zhang, X., Wang, M., Zhang, J., Yu, D. B., Zang, X., Zhang, J., Li, Y., Xu, J., Yang, Q., et al. (2023) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.24927 · Cited by 17 · see citing works
Li, J., Zhang, Y., Tao, X., You, Q., Zheng, T., He, Z., & Ou, J. (2020) · Annals of Translational Medicine · doi:10.21037/atm-20-7939 · Cited by 16 · see citing works
Yamada, Y., & Yamada, Y. (2018) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.94.016 · Cited by 16 · see citing works
A pan-cancer study of spalt-like transcription factors 1/2/3/4 as therapeutic targets
Ma, T., Shi, S., Jiang, H., Chen, X., Xu, D., Ding, X., Zhang, H., & Yang, X. (2021) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2021.109016 · Cited by 15 · see citing works
BMI‑1 promotes invasion and metastasis in endometrial adenocarcinoma and is a poor prognostic factor
Yu, J., Chen, L., Bao, Z., Liu, Y., Liu, G., Li, F., & Li, L. (2020) · Oncology Reports · doi:10.3892/or.2020.7539 · Cited by 14 · see citing works
Sharbatoghli, M., Shamshiripour, P., Fattahi, F., Kalantari, E., Shams, Z. H., Panahi, M., Totonchi, M., Asadi-Lari, Z., Madjd, Z., & Zanjani, L. S. (2022) · Journal of Ovarian Research · doi:10.1186/s13048-021-00921-x · Cited by 14 · see citing works
Pluripotency Stemness and Cancer: More Questions than Answers
Hatina, J., Kripnerová, M., Houdek, Z., Pešta, M., & Tichánek, F. (2021) · Advances in experimental medicine and biology · doi:10.1007/5584_2021_663 · Cited by 12 · see citing works
Kei, S., & Adeyi, O. A. (2019) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2019-0226-ra · Cited by 8 · see citing works
Di, C., Sun, J. Y., Zhang, H., Zhou, P., & Kong, J. (2018) · PubMed Central · Cited by 8 · see citing works
Higher expression of SALL4 predicts poor cancer prognosis: A meta-analysis
Shen, H., Li, L., Wang, D., Yang, S., Chen, X., Zhou, S., Zhong, S., Zhao, J., & Tang, J. (2017) · Cancer Biomarkers · doi:10.3233/cbm-160052 · Cited by 7 · see citing works
Diagnostic Value of SALL4 and OCT3/4 in Pediatric Testicular Tumors
Bîcă, O. D., Ciongradi, C. I., Ivănuță, M., Ianole, V., Sârbu, I., Cojocaru, E., Bîcă, D. E., & Lozneanu, L. (2024) · Diagnostics · doi:10.3390/diagnostics14131454 · Cited by 6 · see citing works
Huang, X., Zhu, J., Li, Y., Yu, Y., & Tang, J. Y. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.763480 · Cited by 5 · see citing works
Assessment of Molecular Markers in Pediatric Ovarian Tumors: Romanian Single-Center Experience
Bîcă, O. D., Ciongradi, C. I., Benchia, D., Sârbu, I., Alecsa, M., Cristofor, A. E., Bîcă, D. E., & Lozneanu, L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126752 · Cited by 5 · see citing works
Atılgan, A. O., Özen, Ö., Reyhan, A. N. H., & Ayhan, A. (2022) · International Journal of Surgical Pathology · doi:10.1177/10668969221134695 · Cited by 5 · see citing works
Ohadi, F., Rahgozar, S., & Ghodousi, E. S. (2020) · Cancer Management and Research · doi:10.2147/cmar.s240469 · Cited by 5 · see citing works
Targeting transcription factors through an IMiD independent zinc finger domain
Liu, B. H., Liu, M., Radhakrishnan, S., Dai, M.-Y., Jaladanki, C. K., Gao, C., Tang, J. P., Kumari, K., Go, M. L., Vu, K. A. L., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-025-00241-3 · Cited by 8 · see citing works
“…is important for many cancers, most notably hepatocellular carcinoma (HCC) (Yong et al, 2013), lung cancer (Kobayashi et al, 2011a), ovarian cancer (Yang et al, 2016), breast cancer (Kobayashi et al, 2011b), myelodysplastic syndrome (MDS) (Liu et al, 2022), and acute myeloid leukemia (AML) (Li et…”
Vastrad, B. M., & Vastrad, C. M. (2024) · Egyptian Journal of Medical Human Genetics · doi:10.1186/s43042-024-00572-9 · Cited by 4 · see citing works
Kang, C., Hong, J., Kim, H., Jo, J., Seo, J., Lee, J., & Lee, S. (2025) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5c00501 · Cited by 3 · see citing works
SALL4 as a Useful Marker for the Distinction of Various Gestational Trophoblastic Disease Subtypes
Trécourt, A., Donzel, M., Gaillot-Durand, L., Bolze, P., Golfier, F., Descargues, P., Hajri, T., Mauduit, C., Devouassoux‐Shisheboran, M., & Allias, F. (2025) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000002358 · Cited by 3 · see citing works
Wang, Q., Liu, L., Li, D., Gao, L., & Zhang, M. (2022) · Pathology International · doi:10.1111/pin.13285 · Cited by 3 · see citing works
Molecular Diagnosis in Ovarian Carcinoma
Dwivedi, S., Misra, R., Purohit, P., Vishnoi, J. R., Pareek, P., Goel, A., Khattri, S., Sharma, P., Pant, K. K., & Misra, S. (2019) · Springer eBooks · doi:10.1007/978-981-13-5877-7_19 · Cited by 3 · see citing works
Harb, O. A., Salem, A., Haggag, R., Abdesalam, W., & Salim, R. A. (2016) · International Journal of Advanced Research · doi:10.21474/ijar01/917
- Authors
- YANG, M., XIE, X., & DING, Y.
- Affiliations
- Second Xiangya Hospital of Central South University (CN)
- Venue
- Oncology Reports
- Publisher
- Spandidos Publications
- Published
- 2016-01-05
- Volume
- 35
- Issue
- 3
- Pages
- 1796-1806
- ISSN
- 1021-335X (ISSN-L)
- 1791-2431
- OpenAlex
- W2225450423
- Cited by
- 30
- References
- 36
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 1 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 3
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Oncology Reports (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Keywords
- SALL4, serous ovarian cancer, prognostic factors, tumor invasion, metastasis, cell migration, cell proliferation, overall survival, progression-free survival, transcription factors, molecular targets
- MeSH terms
- Carcinoma, Ovarian Epithelial, Adult, Aged, Female, Humans, Middle Aged, Neoplasm Invasiveness, Neoplasm Metastasis, Neoplasm Recurrence, Local, Neoplasms, Glandular and Epithelial, Ovarian Neoplasms, Prognosis, Transcription Factors, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic, Cystadenocarcinoma, Serous, Disease-Free Survival, Cell Line, Tumor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
