ProteinChip technology is a useful method in the pathogenesis and diagnosis of endometriosis: a preliminary study
Open accessAbstract
Objective To test the feasibility of ProteinChip (Ciphergen Biosystems, Inc., Fremont, CA) technology as a proteomic tool in discovering and identifying proteins that are differentially expressed in endometrium, endometriotic tissue, and normal peritoneum from women with and without endometriosis.Design Differential analysis of protein expression in women with and without endometriosis.Setting University hospital.Patient(s) A total of nine patients during their secretory phase (days 20-22) were selected for this study on the basis of cycle phase and presence/or absence of endometriosis.Intervention(s) Twelve tissues used in the study included six endometrial biopsies from women with mild endometriosis (n = 3) and a normal pelvis (n = 3) as well as paired samples of peritoneal endometriotic lesions (n = 3) and macroscopically normal peritoneum biopsies (n = 3) from three women with endometriosis.Main outcome measure(s) Numerous expression differences were observed in the above comparisons, representing both up-regulation and down-regulation in protein and peptide expression levels.Result(s) Endometrial expression for a number of proteins and peptides in the range of 2.8-12.3 kDa was 3-24 times lower in women with endometriosis than in those without endometriosis. When compared with normal peritoneum, endometriotic lesions showed an increased expression for a set of proteins and peptides in the range of 3-96 kDa, and especially an up-regulated cluster of proteins between 22 and 23 kDa, identified to be transgelin, a smooth muscle actin-binding protein.Conclusion(s) This preliminary study demonstrated that differential protein profiling by using ProteinChip array technology is feasible, reproducible, and may be developed into a powerful tool for endometriosis research.
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In 2006, the first of these reports described reduced expression of a protein peak in secretory phase endometrium from women with mild endometriosis relative to controls.
“In 2006, the first of these reports described reduced expression of a protein peak in secretory phase endometrium from women with mild endometriosis relative to controls [133].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [133]
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Cites
Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018 · see citing works
Rw, N., Hertig, A. T., & Rock, J. A. (1950) · Fertility and Sterility · doi:10.1016/s0015-0282(16)30062-0 · Cited by 2,854 · see citing works
A comparison of selected mRNA and protein abundances in human liver
Anderson, L., & Seilhamer, J. (1997) · Electrophoresis · doi:10.1002/elps.1150180333 · Cited by 1,266 · see citing works
Zhang, Z., Bast, R. C., Yu, Y., Li, J., Sokoll, L. J., Rai, A. J., Rosenzweig, J. M., Cameron, B., Wang, Y. Y., Meng, X.-Y., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0746 · Cited by 929 · see citing works
Kao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696 · see citing works
Invited Review: Cross-bridge regulation by thin filament-associated proteins
Morgan, K. G., & Gangopadhyay, S. S. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.2.953 · Cited by 220 · see citing works
Smooth muscles are frequent components of endometriotic lesions
Anaf, V. (2000) · Human Reproduction · doi:10.1093/humrep/15.4.767 · Cited by 183 · see citing works
Becker, S. M., Cazares, L. H., Watson, P. A., Lynch, H. T., Semmes, O. J., Drake, R. R., & Laronga, C. (2004) · Annals of Surgical Oncology · doi:10.1245/aso.2004.03.557 · Cited by 87 · see citing works
P21(Cip1/WAF1) expression in the mouse testis before and after X irradiation
Beumer, T. L., Roepers‐Gajadien, H. L., Gademan, I. S., Rutgers, D. H., & de Rooij, D. G. (1997) · Molecular Reproduction and Development · doi:10.1002/(sici)1098-2795(199707)47:3 · Cited by 59 · see citing works
Review of proteomics with applications to genetic epidemiology
Sellers, T. A., & Yates, J. R. (2003) · Genetic Epidemiology · doi:10.1002/gepi.10226 · Cited by 52 · see citing works
Proteomic approaches in endometriosis research
Poliness, A. E., Healey, M., Brennecke, S. P., & Moses, E. K. (2004) · PROTEOMICS · doi:10.1002/pmic.200300791 · Cited by 40 · see citing works
TABIBZADEH, S. S. (2003) · Frontiers in bioscience · doi:10.2741/1045 · Cited by 39 · see citing works
Detection of a unique 32-kd protein in the peritoneal fluid of women with endometriosis
Nothnick, W. B., Curry, T. E., Muse, K. N., London, S. N., & Vernon, M. W. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56519-4 · Cited by 16 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Qian J, Hendrix M, Larsen WJ, Dorn GW 2nd, Lessard JL. Establish- ment and characterization of a conditionally immortalized smooth mus- cle/myometrial-like cell line. Mol Reprod Dev 1997;47:284 -94.
Cited by
Sorted by citations
Endometrial alterations in endometriosis: a systematic review of putative biomarkers
May, K. E., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr013 · Cited by 237 · see citing works
“Levels of IL-8 receptors (CXCR1 and 2) were increased in the endometrial epithelium of affected women (Ulukus et al., 2005).”
BackgroundResultInfluentialRahmioglu, N., Fassbender, A., Vitonis, A. F., Tworoger, S. S., Hummelshoj, L., D'Hooghe, T. M., Adamson, G. D., Giudice, L. C., Becker, C. M., Zondervan, K. T., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1208 · Cited by 227 · see citing works
Self-citationUpdate on biomarkers for the detection of endometriosis
Fassbender, A., Burney, R. O., F. O, D., D’Hooghe, T., & Giudice, L. (2015) · BioMed Research International · doi:10.1155/2015/130854 · Cited by 195 · see citing works
Self-citationEndometrial biomarkers for the non-invasive diagnosis of endometriosis
Gupta, D., Hull, M. L., Fraser, I. S., Miller, L., Bossuyt, P. M., JOHNSON, N. P., & Nisenblat, V. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012165 · Cited by 174 · see citing works
Fassbender, A., Vodolazkaia, A., Saunders, P., Lebovic, D., Waelkens, E., De Moor, B., & D'Hooghe, T. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.01.097 · Cited by 150 · see citing works
Self-citationDifferentially expressed genes in eutopic and ectopic endometrium of women with endometriosis
Meola, J., Silva, J. C. R. E., Dentillo, D. B., Silva, W. A., Veiga-Castelli, L. C., Bernardes, L. Â. D. S., Ferriani, R. A., de Paz, C. C. P., Giuliatti, S., & Martelli, L. R. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.058 · Cited by 120 · see citing works
Bokor, A., Kyama, C. M., Vercruysse, L., Fassbender, A., Gevaert, O., Vodolazkaia, A., De Moor, B., Fulop, V., & D'Hooghe, T. (2009) · Human Reproduction · doi:10.1093/humrep/dep283 · Cited by 128 · see citing works
“5), antineurofilament protein, anti-substance P (SP), anti-vasoactive intestinal peptide (VIP), anti-neuropeptide Y and anti-calcitonine gene-related polypeptide.”
BackgroundSelf-citationProteomic Analysis of the Luteal Endometrial Secretome
Scotchie, J. G., Fritz, M. A., Mocanu, M., Lessey, B. A., & Young, S. L. (2009) · Reproductive Sciences · doi:10.1177/1933719109337165 · Cited by 101 · see citing works
“Initial studies using proteomic techniques to investigate endometrial tissue protein expression in normal and pathologic states have found the techniques to be feasible and useful in broadening understanding of endometrial physiology.(9-11) However, we hypothesized that the secretome, defined as all secreted proteins,…”
BackgroundFassbender, A., Verbeeck, N., Börnigen, D., Kyama, C. M., Bokor, A., Vodolazkaia, A., Peeraer, K., Tomassetti, C., Meuleman, C., Gevaert, O., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des127 · Cited by 87 · see citing works
“The 3623 Da peak was selected to construct the diagnostic model for minimal to severe endometriosis, and was also differentially expressed in our previous SELDI-TOF MS study (Kyama et al., 2006).”
MethodResultSelf-citationAmetzazurra, A., Matorras, R., García-Velasco, J. A., Prieto, B., Simón, L., Martinez, A., & Nagore, D. (2008) · Human Reproduction · doi:10.1093/humrep/den450 · Cited by 85 · see citing works
Post-Translational Modifications and Protein-Specific Isoforms in Endometriosis Revealed by 2D DIGE
Stephens, A. N., Hannan, N. J., Rainczuk, A., Meehan, K. L., Chen, J., Nicholls, P. K., Rombauts, L. J. F., Stanton, P. G., Robertson, D. M., & Salamonsen, L. A. (2010) · Journal of Proteome Research · doi:10.1021/pr901131p · Cited by 76 · see citing works
Proteomic Profile of Uterine Luminal Fluid from Early Pregnant Ewes
Koch, J. M., Ramadoss, J., & Magness, R. R. (2010) · Journal of Proteome Research · doi:10.1021/pr100096b · Cited by 68 · see citing works
Sherwin, J. R. A., Sharkey, A. M., Mihalyi, A., Simsa, P., Catalano, R. D., & D'Hooghe, T. M. (2008) · Human Reproduction · doi:10.1093/humrep/den078 · Cited by 66 · see citing works
Self-citationSeeber, B., Sammel, M. D., Fan, X., Gerton, G. L., Shaunik, A., Chittams, J. L., & Barnhart, K. T. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.121 · Cited by 59 · see citing works
“A recent study testing the feasibility of using SELDI for proteomics research in endometriosis concluded that it is indeed a viable approach for studying this disease (23).”
Proteomic Analysis of Peritoneal Fluid in Women with Endometriosis
Ferrero, S., Gillott, D. J., Remorgida, V., Anserini, P., Leung, K., Ragni, N., & Grudzinskas, J. G. (2007) · Journal of Proteome Research · doi:10.1021/pr060680q · Cited by 55 · see citing works
Evaluation of endometrial biomarkers for semi-invasive diagnosis of endometriosis
Kyama, C. M., Mihalyi, A., Gevaert, O., Waelkens, E., Simsa, P., de Plas, R. V., Meuleman, C., Moor, B. D., & D’Hooghe, T. M. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.084 · Cited by 45 · see citing works
Self-citationEl-Kasti, M. M., Wright, C., Fye, H. K. S., Roseman, F., Kessler, B. M., & Becker, C. M. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.11.066 · Cited by 44 · see citing works
Gene expression signatures differentiate uterine endometrial stromal sarcoma from leiomyosarcoma
Davidson, B., Abeler, V. M., Hellesylt, E., Holth, A., Shih, I., Skeie-Jensen, T., Chen, L., Yang, Y., & Wang, T. (2012) · Gynecologic Oncology · doi:10.1016/j.ygyno.2012.11.021 · Cited by 42 · see citing works
“Higher TAGLN mRNA expression by qRT-PCR was found in endometriosis compared to patient-matched eutropic endometrium [61] and higher protein expression was observed in these lesions compared to normal peritoneum [62].”
ResultEmerging drugs in endometriosis
Mihalyi, A., Simsa, P., Kyama, C. M., Meuleman, C., Mwenda, J. M., & D’Hooghe, T. (2006) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.11.3.503 · Cited by 38 · see citing works
“With the possibilities provided by improved molecular technologies, it will hopefully become possible to identify biological features that are exclusively (or almost exclusively) present or absent in endometriosis, allowing specific targeting of ectopic lesions, and could open completely new horizons in the diagnosis…”
BackgroundSelf-citationHidalgo, G. D. S., Meola, J., Silva, J. C. R. E., de Paz, C. C. P., & Ferriani, R. A. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.052 · Cited by 38 · see citing works
Proteomic analysis of protein expression in the eutopic endometrium of women with endometriosis
ten Have, S., Fraser, I. S., Markham, R., Lam, A. M., & Matsumoto, I. (2007) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.200600743 · Cited by 36 · see citing works
“example it is known that there is increased angiogenesis and neurogenesis [15, 16] in the eutopic endometrium, but the changes have not been detected in this preliminary proteomic study.”
BackgroundMethodHou, Z., Sun, L., Gao, L., Liao, L., Mao, Y., & Liu, J. (2009) · Biomarkers · doi:10.3109/13547500903183970 · Cited by 30 · see citing works
“Recently, Protein-Chip technology has been applied to the study of protein expressed by the endometrium, endometriotic tissues and normal peritoneum obtained from women with and without endometriosis (Kyama et al. 2006).”
Method“Spot”-ting differences between the ectopic and eutopic endometrium of endometriosis patients
Chehna-Patel, N., Sachdeva, G., Gajbhiye, R., Warty, N. R., & Khole, V. V. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.01.048 · Cited by 25 · see citing works
Kyama, C. M., Overbergh, L., Mihalyi, A., Cuneo, S., Chai, D. C., Debrock, S., Mwenda, J. M., Mathieu, C., Nugent, N. P., & D’Hooghe, T. M. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.205 · Cited by 24 · see citing works
Self-citationFassbender, A., Simsa, P., Kyama, C. M., Waelkens, E., Mihalyi, A., Meuleman, C., Gevaert, O., Van de Plas, R., de Moor, B., & D'Hooghe, T. M. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-123 · Cited by 23 · see citing works
“peaks identified in EM samples in our previous studies [5,6] were not confirmed in the present study.”
InfluentialSelf-citationProteomics technologies in endometriosis
Ferrero, S., Gillott, D. J., Remorgida, V., Ragni, N., Venturini, P. L., & Grudzinskas, J. G. (2008) · Expert Review of Proteomics · doi:10.1586/14789450.5.5.705 · Cited by 23 · see citing works
Vehmas, A. P., Muth‐Pawlak, D., Huhtinen, K., Saloniemi-Heinonen, T., Jaakkola, K., Laajala, T. D., Kaprio, H., Suvitie, P. A., Aittokallio, T. A., Siitari, H., et al. (2014) · Journal of Proteome Research · doi:10.1021/pr500384n · Cited by 20 · see citing works
Yao, Z., Zhang, Y., Yan, J., & Yan, L. (2020) · Journal of Gynecology Obstetrics and Human Reproduction · doi:10.1016/j.jogoh.2020.102043 · Cited by 15 · see citing works
Integrated analysis of mRNA and protein expression profiling in tubal endometriosis
Qi, H., Zhang, H., Zhao, X., Qin, Y., Liang, G., He, X., & Zhang, J. (2020) · Reproduction · doi:10.1530/rep-19-0587 · Cited by 14 · see citing works
“Also, several studies have examined the proteome of eutopic endometrium (Kyama et al .”
Proteomics in the Diagnosis of Endometriosis: Opportunities and Challenges
Ferrero, S. (2018) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201800183 · Cited by 13 · see citing works
Marianowski, P., Szymusik, I., Malejczyk, J., Hibner, M., & Wielgoś, M. (2013) · PubMed · Cited by 12 · see citing works
Future of Endometriosis Research
Simsa, P., Mihalyi, A., Kyama, C. M., Mwenda, J. M., Fülöp, V., & D’Hooghe, T. M. (2007) · Women s Health · doi:10.2217/17455057.3.5.647 · Cited by 10 · see citing works
“A supportive high-throughput method for the microarray technology could be represented by the different matrix-assisted laser desorption/ionization and surface-enhanced laser desorption-ionization proteomics technologies, since the protein-expression pattern is also regulated at the translation level [45].”
MethodSelf-citationGhosh, D., Nagpal, S., Bhat, M. A., Geethadevi, A., Srivastava, A. K., Sharma, J. B., & Sengupta, J. (2015) · Journal of Reproductive Health and Medicine · doi:10.1016/j.jrhm.2015.06.003 · Cited by 9 · see citing works
Proteomics a Key Tool for a Better Understanding of Endometriosis: a Mini- Review
Fatemeh, N. M. G. B. B., & Gilany, K. (2011) · Cited by 9 · see citing works
Molecular Biology of Endometriosis
Sengupta, J., Geethadevi, A., Bhat, M. A., & Ghosh, D. (2016) · Human Reproduction · doi:10.1002/9781118849613.ch3 · Cited by 9 · see citing works
OMICs Studies and Endometriosis Biomarker Identification
Saare, M., Peters, M., Aints, A., Laisk, T., Salumets, A., & Altmäe, S. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_12 · Cited by 8 · see citing works
Endometriosis and Cytoskeletal Remodeling: The Functional Role of Actin-Binding Proteins
Arendt, W., Kleszczyński, K., Gagat, M., & Izdebska, M. (2025) · Cells · doi:10.3390/cells14050360 · Cited by 6 · see citing works
“Furthermore, Kyama et al. demonstrated that TAGLN was differentially expressed in endometriotic lesions obtained from peritoneal sites compared to normal peritoneum [83].”
Wen, Y., Whitin, J. C., Yu, T. T.-S., Cohen, H. J., Polan, M. L., & Chen, B. H. (2011) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2011.01690.x · Cited by 6 · see citing works
Elevated periostin in serum and peritoneal washing fluids as potential biomarkers for endometriosis
Zheng, Q., Lu, J., Li, R., Hu, C., & Liu, P. (2016) · Gynecological Endocrinology · doi:10.1080/09513590.2016.1190329 · Cited by 2 · see citing works
“Although laparoscopy is currently considered to be the gold standard for diagnosis of endometriosis, its high cost and potential surgical risk makes it hard to be widely used in the diagnosis of endometriosis [3].”
BackgroundProteomic Biomarkers for Endometriosis
Fassbender, A., Hubert, A., Waelkens, E., Dorien, O., & D’Hooghe, T. M. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_10 · Cited by 2 · see citing works
Self-citationSemi-invasive Diagnosis of Endometriosis Doctoral Thesis
Bokor, A. (2010) · Cited by 1 · see citing works
Identifying biomarkers for non-invasive diagnosis of endometriosis
Irungu, S. (2016) · UCL Discovery (University College London) · Cited by 1 · see citing works
Diagnosis of Endometriosis: Proteomics
Stephens, A. N., Rombauts, L. J. F., & Salamonsen, L. A. (2011) · doi:10.1002/9781444398519.ch31
Domı́nguez, F., & Simón, C. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-408134-5.00010-x
Vallvé-Juanico, J. (2018) · Tesis Doctorals en Xarxa (Consorci de Serveis Universitaris de Catalunya)
(2007) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3282ca75fc
- Authors
- Kyama, C. M., T’Jampens, D., Mihalyi, A., Simsa, P., Debrock, S., Waelkens, E., Landuyt, B., Meuleman, C., Fulop, V., Mwenda, J. M., & D’Hooghe, T. M.
- Affiliations
- Institute of Primate Research (KE)
- Universitair Ziekenhuis Leuven (BE)
- Corresponding author
- D’Hooghe, Thomas M.
- ORCID
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 2006-07
- Volume
- 86
- Issue
- 1
- Pages
- 203-209
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W2102695352
- Cited by
- 46
- References
- 13
- Citations by year
- 2025: 1 · 2020: 2 · 2018: 2 · 2017: 2 · 2016: 4 · 2015: 2 · 2014: 3 · 2013: 2 · 2012: 2
- FWCI
- 4.89
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, differentially expressed proteins, proteomics, endometrium, transgelin, endometriosis diagnosis, endometriosis pathogenesis
- MeSH terms
- Cells, Cultured, Endometriosis, Female, Humans, Pilot Projects, Proteins, Sensitivity and Specificity, Reproducibility of Results, Biomarkers, Gene Expression Profiling, Protein Array Analysis
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