Regulation of human chorionic gonadotropin beta subunit expression in ovarian cancer

Article

Śliwa, A., Kubiczak, M., Szczerba, A., Walkowiak, G., Nowak-Markwitz, E., Burczynska, B., Butler, S., Iles, R., Białas, P. and Jankowska, A. 2019. Regulation of human chorionic gonadotropin beta subunit expression in ovarian cancer. BMC cancer. 19 (1), pp. 1-9. https://doi.org/10.1186/s12885-019-5960-2
TypeArticle
TitleRegulation of human chorionic gonadotropin beta subunit expression in ovarian cancer
AuthorsŚliwa, A., Kubiczak, M., Szczerba, A., Walkowiak, G., Nowak-Markwitz, E., Burczynska, B., Butler, S., Iles, R., Białas, P. and Jankowska, A.
Abstract

Expression of human chorionic gonadotropin beta subunit by cancers is extensively documented, yet regulation of the multiple genes that can code for this protein is poorly understood. The aim of the study was to examine the mechanisms regulating CGB gene expression in ovarian cancer. Expression of CGB genes and SP1, SP3, TFAP2A transcription factor genes was evaluated by RT-qPCR. The methylation status of CGB genes promoter regions was examined by methylation-specific PCR. mRNA arising from multiple CGB genes was detected in both ovarian control and malignant tissues. However, expression of CGB3-9 genes was shown to be significantly higher in malignant than healthy ovarian tissues. CGB1 and CGB2 transcripts were shown to be present in 20% of ovarian cancers, but were not detected in any of the control samples. Malignant tissues were characterized by DNA demethylation of CGB promoter regions. In ovarian cancer CGB expression positively correlated with TFAP2A transcripts level and expression of TFAP2A transcription factor was significantly higher in cancer than in control tissues. In contrast SP3 expression level was significantly lower in ovarian tumours than in control ovarian tissue. In ovarian cancers increased expression of human chorionic gonadotropin beta subunit is associated with demethylation of CGB promoter regions. CGB3-9 expression level strongly correlates with expression of the TFAP2A transcription factor. Presence of mRNA arising from CGB1 and CGB2 genes appears to be a unique feature of a subset of ovarian cancers.

KeywordsAP2 transcription factor, DNA methylation, Gene expression regulation, Human chorionic gonadotropin beta subunit, Ovarian cancer
Research GroupBiomarkers for Cancer group
PublisherBioMed Central
JournalBMC cancer
ISSN1471-2407
Publication dates
Online30 Jul 2019
Print31 Dec 2019
Publication process dates
Deposited15 Aug 2019
Accepted19 Jul 2019
Output statusPublished
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© The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Digital Object Identifier (DOI)https://doi.org/10.1186/s12885-019-5960-2
LanguageEnglish
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Neven, P., Iles, R., Carter, P., Shepherd, J. and Chard, T. 1994. Diurnal variation of urinary "hCG beta subunit core fragment" production evaluated in patients with gynecological neoplasms. Clinical Chemistry. 40 (3), pp. 484-485.
Characterisation of the differential expression of marker antigens by normal and malignant endometrial epithelium
Chatzaki, E., Gallagher, C., Iles, R., Ind, T., Nouri, A., Bax, C. and Grudzinskas, J. 1994. Characterisation of the differential expression of marker antigens by normal and malignant endometrial epithelium. British journal of cancer. 69 (6), pp. 1010-1014.
Serum placental-type alkaline phosphatase activity in women with squamous and glandular malignancies of the reproductive tract
Ind, T., Iles, R., Carter, P., Lowe, D., Shepherd, J., Hudson, C. and Chard, T. 1994. Serum placental-type alkaline phosphatase activity in women with squamous and glandular malignancies of the reproductive tract. Journal of Clinical Pathology. 47 (11), pp. 1035-1037.
Measurement of urinary beta core fragment of human chorionic gonadotrophin in women with vulvovaginal malignancy and its prognostic significance
Carter, P., Iles, R., Neven, P., Ind, T., Shepherd, J. and Chard, T. 1995. Measurement of urinary beta core fragment of human chorionic gonadotrophin in women with vulvovaginal malignancy and its prognostic significance. British journal of cancer. 71 (2), pp. 350-353.
The effects of beta-human chorionic gonadotrophin on the in vitro growth of bladder cancer cell lines
Gillott, D., Iles, R. and Chard, T. 1996. The effects of beta-human chorionic gonadotrophin on the in vitro growth of bladder cancer cell lines. British journal of cancer. 73 (3), pp. 323-326.
The temporary anatomical structures prominent in the first trimester may be fulfilling exchange functions assigned to the placenta in the second and third trimester
Docherty, S., Iles, R., Wathen, N. and Chard, T. 1996. The temporary anatomical structures prominent in the first trimester may be fulfilling exchange functions assigned to the placenta in the second and third trimester. Human Reproduction. 11 (6), pp. 1157-1161.
Prognostic significance of the bcl-2 apoptotic family of proteins in primary and recurrent cervical cancer
Crawford, R., Caldwell, C., Iles, R., Lowe, D., Shepherd, J. and Chard, T. 1998. Prognostic significance of the bcl-2 apoptotic family of proteins in primary and recurrent cervical cancer. British journal of cancer. 78 (2), pp. 210-214.
Concentrations of placental protein 14 in uterine flushings from infertile women: validation of the collection technique and method of expression of results
Hamilton, J., Iles, R., Gunn, L., Wilson, C., Lower, A., Chard, T. and Grudzinskas, J. 1998. Concentrations of placental protein 14 in uterine flushings from infertile women: validation of the collection technique and method of expression of results. Human Reproduction. 13 (12), pp. 3357-3362.
The prognostic significance of beta human chorionic gonadotrophin and its metabolites in women with cervical carcinoma
Crawford, R., Iles, R., Carter, P., Caldwell, C., Shepherd, J. and Chard, T. 1998. The prognostic significance of beta human chorionic gonadotrophin and its metabolites in women with cervical carcinoma. Journal of Clinical Pathology. 51 (9), pp. 685-688.
Cross-Reaction with luteinizing hormone ß-Core is responsible for the age-dependent increase of immunoreactive ß-Core fragment of human chorionic gonadotropin in women with nonmalignant conditions
Iles, R., Javid, M., Gunn, L. and Chard, T. 1999. Cross-Reaction with luteinizing hormone ß-Core is responsible for the age-dependent increase of immunoreactive ß-Core fragment of human chorionic gonadotropin in women with nonmalignant conditions. Clinical Chemistry. 45, pp. 532-538.
The beta-subunit of human chorionic gonadotrophin exists as a homodimer
Butler, S., Laidler, P., Porter, J., Kicman, A., Chard, T., Cowan, D. and Iles, R. 1999. The beta-subunit of human chorionic gonadotrophin exists as a homodimer. Journal of molecular endocrinology. 22, pp. 185-192.
Clinical and endocrinological changes after electro-acupuncture treatment in patients with osteoarthritis of the knee
Ahsin, S., Saleem, S., Bhatti, A., Aslam, M. and Iles, R. 2009. Clinical and endocrinological changes after electro-acupuncture treatment in patients with osteoarthritis of the knee. Pain. 147 (1-3), pp. 60-66. https://doi.org/10.1016/j.pain.2009.08.004
Capillary electrophoresis of human follicular fluid
Wen, S., Perrett, D., Patel, P., Li, N., Docherty, S., Tozer, A. and Iles, R. 2009. Capillary electrophoresis of human follicular fluid. Journal of Chromatography B. 877 (31), pp. 3946-3952. https://doi.org/10.1016/j.jchromb.2009.09.046
The role of glycosylation in regulating glycoprotein hormone free alpha subunit and free beta subunit combination in the extra-embryonic coelomic fluid of early pregnancy
Blithe, D. and Iles, R. 1995. The role of glycosylation in regulating glycoprotein hormone free alpha subunit and free beta subunit combination in the extra-embryonic coelomic fluid of early pregnancy. Endocrinology. 136 (3), pp. 903-910. https://doi.org/10.1210/en.136.3.903
Can biological markers improve the management of breast cancer patients?
Leake, R., Anderson, L., Dowsett, M., Iles, R., Nicholson, R., Robertson, J., Walker, R. and UKCCR Biomarker group 2000. Can biological markers improve the management of breast cancer patients? British journal of cancer. 82 (10), pp. 1625-1626. https://doi.org/10.1054/bjoc.2000.1159
Biological markers: maintaining standards
Leake, R., Anderson, L., Dowsett, M., Iles, R., Nicholson, R., Robertson, J., Walker, R. and UKCCCR Biomarker group 2000. Biological markers: maintaining standards. British journal of cancer. 82 (10), pp. 1627-1628. https://doi.org/10.1054/bjoc.2000.1158
Determination of the glycoforms of human chorionic gonadotropin b-core fragment by matrix-assisted laser desoption/ionisation time of flight mass spectrometry
Jacoby, E., Kicman, A., Laidler, P. and Iles, R. 2000. Determination of the glycoforms of human chorionic gonadotropin b-core fragment by matrix-assisted laser desoption/ionisation time of flight mass spectrometry. Clinical Chemistry. 46 (11), pp. 1796-1803.
Regulation of endometrial cancer cell growth by luteinising hormone (LH) and follicle stimulating hormone (FSH)
Davies, S., Bax, C., Chatzaki, E., Chard, T. and Iles, R. 2000. Regulation of endometrial cancer cell growth by luteinising hormone (LH) and follicle stimulating hormone (FSH). British journal of cancer. 83 (12), pp. 1730-1734. https://doi.org/10.1054/bjoc.2000.1507
The increase in bladder carcinoma cell population induced by the free beta subunit of human chorionic gonadotrophin is a result of an anti-apoptotic effect and not cell proliferation
Butler, S., Ikram, M., Mathieu, S. and Iles, R. 2000. The increase in bladder carcinoma cell population induced by the free beta subunit of human chorionic gonadotrophin is a result of an anti-apoptotic effect and not cell proliferation. British journal of cancer. 82 (9), pp. 1553-1556. https://doi.org/10.1054/bjoc.2000.1177
The analysis of human amniotic fluid using capillary electrophoresis.
Stewart, C., Iles, R. and Perrett, D. 2001. The analysis of human amniotic fluid using capillary electrophoresis. Electrophoresis. 22 (6), pp. 1136-1142. https://doi.org/10.1002/1522-2683()22:6<1136::AID-ELPS1136>3.0.CO;2-A
High concentrations of CA 125 in uterine flushings: influence of cause of infertility and menstrual cycle day.
Hamilton, J., Iles, R., Gunn, L., Wilson, C., Lower, A. and Grudzinskas, J. 2002. High concentrations of CA 125 in uterine flushings: influence of cause of infertility and menstrual cycle day. Gynecological endocrinology..
Reduction of bladder cancer cell growth in response to hCGb CTP37 vaccinated mouse serum.
Butler, S., Staite, E. and Iles, R. 2003. Reduction of bladder cancer cell growth in response to hCGb CTP37 vaccinated mouse serum. Oncology research. 14 (2), pp. 93-100.
Identification of post-translational modifications resulting from LH beta polymorphisms by matrix-assisted laser desorption time-of-flight mass spectrometric analysis of pituitary LH beta core fragment
Jacoby, E., Kicman, A. and Iles, R. 2003. Identification of post-translational modifications resulting from LH beta polymorphisms by matrix-assisted laser desorption time-of-flight mass spectrometric analysis of pituitary LH beta core fragment. Journal of molecular endocrinology. 30 (2), pp. 239-252. https://doi.org/10.1677/jme.0.0300239
The recently identified homodimeric beta-beta subunit of human chorionic gonadotrophin (hCGbb) is no more biologically active than the free beta subunit (hCGb)
Butler, S. and Iles, R. 2004. The recently identified homodimeric beta-beta subunit of human chorionic gonadotrophin (hCGbb) is no more biologically active than the free beta subunit (hCGb). Tumor Biology. 25 (1-2), pp. 18-23. https://doi.org/10.1159/000077719
Serum amino-terminal propeptide of type 1 procollagen (P1NP) in prostate cancer: a potential predictor of bone metastases and prognosticator for disease progression and survival.
Thurairaja, R., Iles, R., Jefferson, K., McFarlane, J. and Persad, R. 2006. Serum amino-terminal propeptide of type 1 procollagen (P1NP) in prostate cancer: a potential predictor of bone metastases and prognosticator for disease progression and survival. Urologia internationalis. 76 (1), pp. 67-71.
Immunoassay detection of human chorionic gonadotrophin beta (hCGb) expression by prostate cancer is of no clinical significance
Otite, U., Baithun, S., Chinegwundon, F., Nargund, V. and Iles, R. 2006. Immunoassay detection of human chorionic gonadotrophin beta (hCGb) expression by prostate cancer is of no clinical significance. Tumor Biology. 27, pp. 181-186.
Gonadotropins and prostate cancer: revisited.
Thwaini, A., Naase, M., Chinegwundon, F., Baithun, S., Ghali, L., Shergill, I. and Iles, R. 2006. Gonadotropins and prostate cancer: revisited. Urologia internationalis. 77 (4), pp. 289-296. https://doi.org/10.1159/000096330
Ectopic hCGbeta expression by epithelial cancer: malignant behaviour, metastasis and inhibition of tumor cell apoptosis
Iles, R. 2007. Ectopic hCGbeta expression by epithelial cancer: malignant behaviour, metastasis and inhibition of tumor cell apoptosis. Molecular and Cellular Endocrinology. 260-26, pp. 264-270. https://doi.org/10.1016/j.mce.2006.02.019
An introduction to mass spectrometry based proteomics-detection and characterization of gonadotropins and related molecules
Kicman, A., Parkin, M. and Iles, R. 2007. An introduction to mass spectrometry based proteomics-detection and characterization of gonadotropins and related molecules. Molecular and Cellular Endocrinology. 260-26, pp. 212-227. https://doi.org/10.1016/j.mce.2006.02.022
Towards the development of an electrochemical biosensor for hCGβ detection
Kassanos, P., Iles, R., Bayford, R. and Demosthenous, A. 2008. Towards the development of an electrochemical biosensor for hCGβ detection. Physiological Measurement. 29 (6), pp. S241-S254. https://doi.org/10.1088/0967-3334/29/6/S21
The role of glycoprotein hormones in endometrial cancer. (in Part 7: Hormones & hormone receptor)
Bax, C., Davies, S., Chatzaki, E., Butler, S. and Iles, R. 2003. The role of glycoprotein hormones in endometrial cancer. (in Part 7: Hormones & hormone receptor). in: Nishida, M. and Kuramoto, H. (ed.) Cell and molecular biology of endometrial carcinoma. London Springer. pp. 195-206
Molecular cell biology and genetic disorders
Iles, R. 2009. Molecular cell biology and genetic disorders. in: Kumar, P. and Clark, M. (ed.) Kumar & Clark’s clinical medicine. Edinburgh Elsevier Saunders. pp. 19-52
Chapter 1: Basic sciences: the cell.
Iles, R. 2008. Chapter 1: Basic sciences: the cell. in: Nargund, V., Raghavan, D. and Sandler, H. (ed.) Urological oncology. London Springer. pp. 3-36
Human chorionic gonadotropin isoforms in the diagnosis of ectopic pregnancy
Iles, R., Borrelli, P., Butler, S. and Staite, E. 2003. Human chorionic gonadotropin isoforms in the diagnosis of ectopic pregnancy. Clinical Chemistry. 49 (12), pp. 2045-2049. https://doi.org/10.1373/clinchem.2003.022095
The free monomeric beta subunit of human chorionic gonadotrophin (hCG beta) and the recently identified homodimeric beta-beta subunit (hCG beta beta) both have autocrine growth effects
Butler, S. and Iles, R. 2004. The free monomeric beta subunit of human chorionic gonadotrophin (hCG beta) and the recently identified homodimeric beta-beta subunit (hCG beta beta) both have autocrine growth effects. Tumor Biology. 25 (1-2), pp. 18-23. https://doi.org/10.1159/000077719
Enhanced affinity capture MALDI-TOF MS: orientation of an immunoglobulin G using recombinant protein G
Iles, R., Bansal, S., Jacoby, E., Neubert, H., Cowan, D. and Kicman, A. 2002. Enhanced affinity capture MALDI-TOF MS: orientation of an immunoglobulin G using recombinant protein G. Analytical Chemistry. 74 (15), pp. 3677-3683. https://doi.org/10.1021/ac025558z
Identification of placental transforming growth factor-beta and bikunin metabolites as contaminants of pharmaceutical human chorionic gonadotrophin preparations by proteomic techniques
Iles, R., Kicman, A., Malatos, S. and Neubert, H. 2005. Identification of placental transforming growth factor-beta and bikunin metabolites as contaminants of pharmaceutical human chorionic gonadotrophin preparations by proteomic techniques. Molecular and Cellular Proteomics. 4 (7), pp. 984-992. https://doi.org/10.1074/mcp.M500085-MCP200
Ectopic human chorionic gonadotropin beta secretion by epithelial tumors and human chorionic gonadotropin beta-induced apoptosis in Kaposi's sarcoma: is there a connection?
Iles, R. and Butler, S. 2003. Ectopic human chorionic gonadotropin beta secretion by epithelial tumors and human chorionic gonadotropin beta-induced apoptosis in Kaposi's sarcoma: is there a connection? Clinical Cancer Research. 9 (13), pp. 4666-4673.
Human granulosa-lutein cell in vitro production of progesterone, inhibin A, inhibin B, and activin A are dependent on follicular size and not the presence of the oocyte
Wen, S., Tozer, A., Li, D., Docherty, S., Al-Shawaf, T. and Iles, R. 2008. Human granulosa-lutein cell in vitro production of progesterone, inhibin A, inhibin B, and activin A are dependent on follicular size and not the presence of the oocyte. Fertility and Sterility. 89 (5), pp. 1406-1413. https://doi.org/10.1016/j.fertnstert.2007.03.086
Follicular fluid levels of inhibin A, inhibin B, and activin A levels reflect changes in follicle size but are not independent markers of the oocyte's ability to fertilize
Wen, S., Tozer, A., Butler, S., Bell, C., Docherty, S. and Iles, R. 2006. Follicular fluid levels of inhibin A, inhibin B, and activin A levels reflect changes in follicle size but are not independent markers of the oocyte's ability to fertilize. Fertility and Sterility. 85 (6), pp. 1723-1729. https://doi.org/10.1016/j.fertnstert.2005.11.058
The effects of 'coasting' on follicular fluid concentrations of vascular endothelial growth factor in women at risk of developing ovarian hyperstimulation syndrome
Tozer, A., Iles, R., Iammarrone, E., Gillott, C., Al-Shawaf, T. and Grudzinskas, J. 2004. The effects of 'coasting' on follicular fluid concentrations of vascular endothelial growth factor in women at risk of developing ovarian hyperstimulation syndrome. Human Reproduction. 19 (3), pp. 522-528. https://doi.org/10.1093/humrep/deh096
Characteristics of populations of granulosa cells from individual follicles in women undergoing 'coasting' during controlled ovarian stimulation (COS) for IVF
Tozer, A., Iles, R., Iammarrone, E., Gillott, C., Wen, S., Al-Shawaf, T. and Grudzinskas, J. 2004. Characteristics of populations of granulosa cells from individual follicles in women undergoing 'coasting' during controlled ovarian stimulation (COS) for IVF. Human Reproduction. 19 (11), pp. 2561-2568. https://doi.org/10.1093/humrep/deh487