Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2012

Open Access 01-12-2012 | Research

S100P Expression in response to sex steroids during the implantation window in human endometrium

Authors: Dan Zhang, Chengbin Ma, Xiaoli Sun, Hexia Xia, Wei Zhang

Published in: Reproductive Biology and Endocrinology | Issue 1/2012

Login to get access

Abstract

Background

S100P, a protein originally detected in the human placenta, has been found to play an important role in the development and invasion of tumors. Interestingly, we have recently discovered using data mining that S100P was considerably up-regulated during the window of implantation in the human endometrium, but little further information has been available.

Methods

Real-time PCR and immunofluorescence were performed to examine the expression and location of S100P in the human endometrium and endometrial cells. Estrogen and progesterone were added to the cultured cells to test the response of S100P to sex steroids.

Results

A dramatic peak, approximately a 100-fold increase in comparison with the proliferative and early- and late-secretory phases, was observed in the endometrium during the mid-secretory phase, which corresponds to the time of embryo implantation. Progesterone regulated the expression of S100P in both primary endometrial epithelial and stromal cells, but estrogen had no significant effect.

Conclusions

The results indicate that S100P participates in the periodic change of the endometrium under the regulation of progesterone, may be used as a unique biomarker of the receptive endometrium and play an important role in embryo implantation.
Appendix
Available only for authorised users
Literature
1.
Achache H, Revel A: Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update. 2006, 12 (6): 731-746. 10.1093/humupd/dml004.CrossRefPubMed
2.
Wilcox AJ, Baird DD, Weinberg CR: Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999, 340 (23): 1796-1799. 10.1056/NEJM199906103402304.CrossRefPubMed
3.
Salamonsen LA, Nie G, Hannan NJ, Dimitriadis E: Society for reproductive biology Founders' lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod Fertil Dev. 2009, 21 (7): 923-934. 10.1071/RD09145.CrossRefPubMed
4.
Zhang D, Sun C, Ma C, Dai H, Zhang W: Data mining of spatial-temporal expression of genes in the human endometrium during the window of implantation. Reprod Sci. 2012, 19 (10): 1085-1098. 10.1177/1933719112442248.CrossRefPubMed
5.
Becker T, Gerke V, Kube E, Weber K: S100P, A novel Ca(2+)-binding protein from human placenta. CDNA cloning, recombinant protein expression and Ca2+ binding properties. Eur J Biochem. 1992, 207 (2): 541-547. 10.1111/j.1432-1033.1992.tb17080.x.CrossRefPubMed
6.
Bulk E, Hascher A, Liersch R, Mesters RM, Diederichs S, Sargin B, Gerke V, Hotfilder M, Vormoor J, Berdel WE, Serve H, Muller-Tidow C: Adjuvant therapy with small hairpin RNA interference prevents non-small cell lung cancer metastasis development in mice. Cancer Res. 2008, 68 (6): 1896-1904. 10.1158/0008-5472.CAN-07-2390.CrossRefPubMed
7.
Abd El All H: Smooth muscle actin and s100p on non germinal centre diffuse large B cell lymphoma are adverse prognostic factors: pilot study. Diagn Pathol. 2007, 2: 9-10.1186/1746-1596-2-9.PubMedCentralCrossRefPubMed
8.
Amelung JT, Buhrens R, Beshay M, Reymond MA: Key genes in lung cancer translational research: a meta-analysis. Pathobiology. 2010, 77 (2): 53-63. 10.1159/000278292.CrossRefPubMed
9.
Arumugam T, Ramachandran V, Logsdon CD: Effect of cromolyn on S100P interactions with RAGE and pancreatic cancer growth and invasion in mouse models. J Natl Cancer Inst. 2006, 98 (24): 1806-1818. 10.1093/jnci/djj498.PubMedCentralCrossRefPubMed
10.
Arumugam T, Simeone DM, Schmidt AM, Logsdon CD: S100P Stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem. 2004, 279 (7): 5059-5065.CrossRefPubMed
11.
Arumugam T, Simeone DM, Van Golen K, Logsdon CD: S100P Promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res. 2005, 11 (15): 5356-5364. 10.1158/1078-0432.CCR-05-0092.CrossRefPubMed
12.
Bartling B, Rehbein G, Simm A, Silber RE, Hofmann HS: Porcupine expression is associated with the expression of S100P and other cancer-related molecules in non-small cell lung carcinoma. Int J Oncol. 2010, 36 (4): 1015-1021.CrossRefPubMed
13.
Basu GD, Azorsa DO, Kiefer JA, Rojas AM, Tuzmen S, Barrett MT, Trent JM, Kallioniemi O, Mousses S: Functional evidence implicating S100P in prostate cancer progression. Int J Cancer. 2008, 123 (2): 330-339. 10.1002/ijc.23447.CrossRefPubMed
14.
Gibadulinova A, Tothova V, Pastorek J, Pastorekova S: Transcriptional regulation and functional implication of S100P in cancer. Amino Acids. 2010, 41 (4): 885-892.CrossRefPubMed
15.
Hamada S, Satoh K, Hirota M, Kanno A, Ishida K, Umino J, Ito H, Kikuta K, Kume K, Masamune A, Katayose Y, Unno M, Shimosegawa T: Calcium-binding protein S100P is a novel diagnostic marker of cholangiocarcinoma. Cancer Sci. 2011, 102 (1): 150-156. 10.1111/j.1349-7006.2010.01757.x.CrossRefPubMed
16.
Shiota M, Tsunoda T, Song Y, Yokomizo A, Tada Y, Oda Y, Naito S: Enhanced S100 calcium-binding protein P expression sensitizes human bladder cancer cells to cisplatin. BJU Int. 2010, 107 (7): 1148-1153.CrossRefPubMed
17.
Nakata K, Nagai E, Ohuchida K, Hayashi A, Miyasaka Y, Aishima S, Oda Y, Mizumoto K, Tanaka M, Tsuneyoshi M: S100P Is a novel marker to identify intraductal papillary mucinous neoplasms. Hum Pathol. 2010, 41 (6): 824-831. 10.1016/j.humpath.2009.11.007.CrossRefPubMed
18.
Levy M, Lin F, Xu H, Dhall D, Spaulding BO, Wang HL: S100P, von hippel-lindau gene product, and IMP3 serve as a useful immunohistochemical panel in the diagnosis of adenocarcinoma on endoscopic bile duct biopsy. Hum Pathol. 2010, 41 (9): 1210-1219. 10.1016/j.humpath.2010.01.014.CrossRefPubMed
19.
20.
Riesewijk A, Martin J, van Os R, Horcajadas JA, Polman J, Pellicer A, Mosselman S, Simon C: Gene expression profiling of human endometrial receptivity on days LH + 2 versus LH + 7 by microarray technology. Mol Hum Reprod. 2003, 9 (5): 253-264. 10.1093/molehr/gag037.CrossRefPubMed
21.
Diaz-Gimeno P, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Alama P, Pellicer A, Simon C: A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2010, 95 (1): 50-60.CrossRefPubMed
22.
Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC: Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006, 147 (3): 1097-1121.CrossRefPubMed
23.
Murray MJ, Lessey BA: Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis. Semin Reprod Endocrinol. 1999, 17 (3): 275-290. 10.1055/s-2007-1016235.CrossRefPubMed
24.
Kodaman PH, Taylor HS: Hormonal regulation of implantation. Obstet Gynecol Clin North Am. 2004, 31 (4): 745-766, ix. 10.1016/j.ogc.2004.08.008.CrossRefPubMed
25.
Paulson RJ: Hormonal induction of endometrial receptivity. Fertil Steril. 2011, 96 (3): 530-535. 10.1016/j.fertnstert.2011.07.1097.CrossRefPubMed
26.
Noyes RW, Hertig AT, Rock J: Dating the endometrial biopsy. Am J Obstet Gynecol. 1975, 122 (2): 262-263.PubMed
27.
Arnold JT, Kaufman DG, Seppala M, Lessey BA: Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod. 2001, 16 (5): 836-845. 10.1093/humrep/16.5.836.CrossRefPubMed
28.
29.
Egorina EM, Sovershaev MA, Osterud B: In-cell western assay: a new approach to visualize tissue factor in human monocytes. J Thromb Haemost. 2006, 4 (3): 614-620. 10.1111/j.1538-7836.2005.01781.x.CrossRefPubMed
30.
Tong XM, Lin XN, Song T, Liu L, Zhang SY: Calcium-binding protein S100P is highly expressed during the implantation window in human endometrium. Fertil Steril. 2010, 94 (4): 1510-1518. 10.1016/j.fertnstert.2009.07.1667.CrossRefPubMed
31.
Parkkila S, Pan PW, Ward A, Gibadulinova A, Oveckova I, Pastorekova S, Pastorek J, Martinez AR, Helin HO, Isola J: The calcium-binding protein S100P in normal and malignant human tissues. BMC Clin Pathol. 2008, 8: 2-10.1186/1472-6890-8-2.PubMedCentralCrossRefPubMed
32.
Popovici RM, Betzler NK, Krause MS, Luo M, Jauckus J, Germeyer A, Bloethner S, Schlotterer A, Kumar R, Strowitzki T, von Wolff M: Gene expression profiling of human endometrial-trophoblast interaction in a coculture model. Endocrinology. 2006, 147 (12): 5662-5675. 10.1210/en.2006-0916.CrossRefPubMed
33.
Whiteman HJ, Weeks ME, Dowen SE, Barry S, Timms JF, Lemoine NR, Crnogorac-Jurcevic T: The role of S100P in the invasion of pancreatic cancer cells is mediated through cytoskeletal changes and regulation of Cathepsin D. Cancer Res. 2007, 67 (18): 8633-8642. 10.1158/0008-5472.CAN-07-0545.CrossRefPubMed
34.
Koltzscher M, Neumann C, Konig S, Gerke V: Ca2 + −Dependent binding and activation of dormant ezrin by dimeric S100P. Mol Biol Cell. 2003, 14 (6): 2372-2384. 10.1091/mbc.E02-09-0553.PubMedCentralCrossRefPubMed
35.
Filipek A, Jastrzebska B, Nowotny M, Kuznicki J: CacyBP/SIP, a calcyclin and siah-1-interacting protein, binds EF-hand proteins of the S100 family. J Biol Chem. 2002, 277 (32): 28848-28852. 10.1074/jbc.M203602200.CrossRefPubMed
36.
Chen Q, Zhang Y, Lu J, Wang Q, Wang S, Cao Y, Wang H, Duan E: Embryo-uterine cross-talk during implantation: the role of Wnt signaling. Mol Hum Reprod. 2009, 15 (4): 215-221. 10.1093/molehr/gap009.CrossRefPubMed
37.
McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK: Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Clin Endocrinol Metab. 2001, 86 (8): 3665-3674. 10.1210/jc.86.8.3665.CrossRefPubMed
38.
Nakamura H, Kimura T, Ogita K, Nakamura T, Takemura M, Shimoya K, Koyama S, Tsujie T, Koyama M, Murata Y: NF-kappaB activation at implantation window of the mouse uterus. Am J Reprod Immunol. 2004, 51 (1): 16-21. 10.1046/j.8755-8920.2003.00116.x.CrossRefPubMed
39.
Heng S, Cervero A, Simon C, Stephens AN, Li Y, Zhang J, Paule S, Rainczuk A, Singh H, Quinonero A, Tapia A, Velasquez L, Salamonsen L, Rombauts LJ, Nie G: Proprotein convertase 5/6 is critical for embryo implantation in women: regulating receptivity by cleaving EBP50, modulating ezrin binding, and membrane-cytoskeletal interactions. Endocrinology. 2011, 152 (12): 5041-5052. 10.1210/en.2011-1273.CrossRefPubMed
40.
Wang Q, Williamson M, Bott S, Brookman-Amissah N, Freeman A, Nariculam J, Hubank MJ, Ahmed A, Masters JR: Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer. Oncogene. 2007, 26 (45): 6560-6565. 10.1038/sj.onc.1210472.CrossRefPubMed
41.
Hammacher A, Thompson EW, Williams ED: Interleukin-6 is a potent inducer of S100P, which is up-regulated in androgen-refractory and metastatic prostate cancer. Int J Biochem Cell Biol. 2005, 37 (2): 442-450. 10.1016/j.biocel.2004.07.011.CrossRefPubMed
42.
Hamada S, Satoh K, Hirota M, Fujibuchi W, Kanno A, Umino J, Ito H, Satoh A, Kikuta K, Kume K, Masamune A, Shimosegawa T: Expression of the calcium-binding protein S100P is regulated by bone morphogenetic protein in pancreatic duct epithelial cell lines. Cancer Sci. 2009, 100 (1): 103-110. 10.1111/j.1349-7006.2008.00993.x.CrossRefPubMed
43.
Chandramouli A, Mercado-Pimentel ME, Hutchinson A, Gibadulinova A, Olson ER, Dickinson S, Shanas R, Davenport J, Owens J, Bhattacharyya AK, Regan JW, Pastorekova S, Arumugam T, Logsdon CD, Nelson MA: The induction of S100p expression by the prostaglandin E (PGE)/EP4 receptor signaling pathway in colon cancer cells. Cancer Biol Ther. 2010, 10 (10): 1056-1066. 10.4161/cbt.10.10.13373.PubMedCentralCrossRefPubMed
44.
Kino T, Manoli I, Kelkar S, Wang Y, Su YA, Chrousos GP: Glucocorticoid receptor (GR) beta has intrinsic, GRalpha-independent transcriptional activity. Biochem Biophys Res Commun. 2009, 381 (4): 671-675. 10.1016/j.bbrc.2009.02.110.PubMedCentralCrossRefPubMed
45.
Namba T, Homan T, Nishimura T, Mima S, Hoshino T, Mizushima T: Up-regulation of S100P expression by non-steroidal anti-inflammatory drugs and its role in anti-tumorigenic effects. J Biol Chem. 2009, 284 (7): 4158-4167.CrossRefPubMed
46.
Averboukh L, Liang P, Kantoff PW, Pardee AB: Regulation of S100P expression by androgen. Prostate. 1996, 29 (6): 350-355. 10.1002/(SICI)1097-0045(199612)29:6<350::AID-PROS2>3.0.CO;2-C.CrossRefPubMed
47.
Bray JD, Jelinsky S, Ghatge R, Bray JA, Tunkey C, Saraf K, Jacobsen BM, Richer JK, Brown EL, Winneker RC, Horwitz KB, Lyttle CR: Quantitative analysis of gene regulation by seven clinically relevant progestins suggests a highly similar mechanism of action through progesterone receptors in T47D breast cancer cells. J Steroid Biochem Mol Biol. 2005, 97 (4): 328-341. 10.1016/j.jsbmb.2005.06.032.CrossRefPubMed
Metadata
Title
S100P Expression in response to sex steroids during the implantation window in human endometrium
Authors
Dan Zhang
Chengbin Ma
Xiaoli Sun
Hexia Xia
Wei Zhang
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2012
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-10-106

Other articles of this Issue 1/2012

Reproductive Biology and Endocrinology 1/2012 Go to the issue

Research

Prostaglandin receptors EP and FP are regulated by estradiol and progesterone in the uterus of ovariectomized rats

Research

Evaluation of developmental changes in bovine in vitro produced embryos following exposure to bovine Herpesvirus type 5

Research

Effect of hCG priming on embryonic development of immature oocytes collected from unstimulated women with polycystic ovarian syndrome

Review

Hormonal, functional and genetic biomarkers in controlled ovarian stimulation: tools for matching patients and protocols

Research

Late morfofunctional alterations of the Sertoli cell caused by doxorubicin administered to prepubertal rats

Research

Ovarian reaction and estrus manifestation in delayed puberty gilts after treatment with equine chorionic gonadotropin