Expression of nodal, cripto, SMAD3, phosphorylated SMAD3, and SMAD4 in the proliferative endometrium of women with endometriosis

Reproductive Sciences

Volumn 22, Issue 5, 2015, Pages 527-533

  Cruz, Cynthia Dela ^a   Del Puerto, Helen L ^a   Rocha, Ana Luiza L ^a   Cavallo, Inês K ^a   Clarizia, Alessandra D ^a   Petraglia, Felice ^b   Reis, Fernando M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

Cripto; endometriosis; endometrium; Nodal; SMADs

Indexed keywords

PROTEIN CRIPTO; PROTEIN NODAL; SMAD3 PROTEIN; SMAD4 PROTEIN; UNCLASSIFIED DRUG; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MESSENGER RNA; NODAL PROTEIN, HUMAN; SIGNAL PEPTIDE; SMAD3 PROTEIN, HUMAN; SMAD4 PROTEIN, HUMAN; TDGF1 PROTEIN, HUMAN; TUMOR PROTEIN;

ADULT; ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CASE CONTROL STUDY; CELL PROLIFERATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; YOUNG ADULT;

ADULT; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL PROLIFERATION; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM PROTEINS; NODAL PROTEIN; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; SMAD4 PROTEIN; YOUNG ADULT;

EID: 84930744984     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719114549855     Document Type: Article

References (41)

1. Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction. 2006 ; 132 (2). 217-232
2. Papageorgiou I, Nicholls PK, Wang F, et al. Expression of nodal signalling components in cycling human endometrium and in endometrial cancer. Reprod Biol Endocrinol. 2009 ; 7: 122
3. Torres PB, Florio P, Galleri L, Reis FM, Borges LE, Petraglia F. Activin A, activin receptor type II, nodal, and cripto mRNA are expressed by eutopic and ectopic endometrium in women with ovarian endometriosis. Reprod Sci. 2009 ; 16 (8). 727-733
4. Godkin JD, Dore JJ. Transforming growth factor beta and the endometrium. Rev Reprod. 1998 ; 3 (1). 1-6
5. Kumar A, Novoselov V, Celeste AJ, Wolfman NM, ten Dijke P, Kuehn MR. Nodal signaling uses activin and transforming growth factor-beta receptor-regulated Smads. J Biol Chem. 2001 ; 276 (1). 656-661
6. Quail DF, Siegers GM, Jewer M, Postovit LM. Nodal signalling in embryogenesis and tumourigenesis. Int J Biochem Cell Biol. 2013 ; 45 (4). 885-898
7. Shen MM. Nodal signaling: developmental roles and regulation. Development. 2007 ; 134 (6). 1023-1034
8. Brandenberger R, Wei H, Zhang S, et al. Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation. Nat Biotechnol. 2004 ; 22 (6). 707-716
9. Vallier L, Touboul T, Chng Z, et al. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways. PLoS One. 2009 ; 4 (6). e6082
10. Brennan J, Lu CC, Norris DP, Rodriguez TA, Beddington RS, Robertson EJ. Nodal signalling in the epiblast patterns the early mouse embryo. Nature. 2001 ; 411 (6840). 965-969
11. Kenney NJ, Adkins HB, Sanicola M. Nodal and Cripto-1: embryonic pattern formation genes involved in mammary gland development and tumorigenesis. J Mammary Gland Biol Neoplasia. 2004 ; 9 (2). 133-144
12. Harrison CA, Gray PC, Vale WW, Robertson DM. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol Metab. 2005 ; 16 (2). 73-78
13. Tsuchida K, Nakatani M, Uezumi A, Murakami T, Cui X. Signal transduction pathway through activin receptors as a therapeutic target of musculoskeletal diseases and cancer. Endocr J. 2008 ; 55 (1). 11-21
14. Schier AF. Nodal morphogens. Cold Spring Harb Perspect Biol. 2009 ; 1 (5). a003459
15. Schier AF, Shen MM. Nodal signalling in vertebrate development. Nature. 2000 ; 403 (6766). 385-389
16. Yeo C, Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol Cell. 2001 ; 7 (5). 949-957
17. Yan YT, Liu JJ, Luo Y, et al. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol Cell Biol. 2002 ; 22 (13). 4439-449
18. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997 ; 24 (2). 235-258
19. Centini G, Lazzeri L, Dores D, et al. Chronic pelvic pain and quality of life in women with and without endometriosis. J Endometr. 2013 ; 5 (1). 27-33
20. Rogers PA, D'Hooghe TM, Fazleabas A, et al. Priorities for endometriosis research: recommendations from an international consensus workshop. Reprod Sci. 2009 ; 16 (4). 335-346
21. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 2012 ; 98 (3). 511-519
22. Vercellini P, Vigano P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014 ; 10 (5). 261-275
23. Oliveira FR, Dela Cruz C, Del Puerto HL, Vilamil QT, Reis FM, Camargos AF. Stem cells: are they the answer to the puzzling etiology of endometriosis?. Histol Histopathol. 2012 ; 27 (1). 23-29
24. Wakefield LM, Hill CS. Beyond TGFbeta: roles of other TGFbeta superfamily members in cancer. Nat Rev Cancer. 2013 ; 13 (5). 328-341
25. Postovit LM, Seftor EA, Seftor RE, Hendrix MJ. Targeting Nodal in malignant melanoma cells. Expert Opin Ther Targets. 2007 ; 11 (4). 497-505
26. Quail DF, Walsh LA, Zhang G, et al. Embryonic protein nodal promotes breast cancer vascularization. Cancer Res. 2012 ; 72 (15). 3851-3863
27. Rocha AL, Carrarelli P, Novembri R, et al. Altered expression of activin, cripto, and follistatin in the endometrium of women with endometrioma. Fertil Steril. 2011 ; 95 (7). 2241-2246
28. Fuhrich DG, Lessey BA, Savaris RF. Comparison of HSCORE assessment of endometrial beta3 integrin subunit expression with digital HSCORE using computerized image analysis (ImageJ). Anal Quant Cytol Histol. 2013 ; 35 (4). 210-216
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001 ; 25 (4). 402-408
30. Munksgaard PS, Blaakaer J. The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations. Gynecol Oncol. 2012 ; 124 (1). 164-169
31. Vlahos NF, Economopoulos KP, Fotiou S. Endometriosis, in vitro fertilisation and the risk of gynaecological malignancies, including ovarian and breast cancer. Best Pract Res Clin Obstet Gynaecol. 2010 ; 24 (1). 39-50
32. Lee CC, Jan HJ, Lai JH, et al. Nodal promotes growth and invasion in human gliomas. Oncogene. 2010 ; 29 (21). 3110-3123
33. Quail DF, Zhang G, Walsh LA, et al. Embryonic morphogen nodal promotes breast cancer growth and progression. PLoS One. 2012 ; 7 (11). e48237
34. Strizzi L, Hardy KM, Kirschmann DA, Ahrlund-Richter L, Hendrix MJ. Nodal expression and detection in cancer: experience and challenges. Cancer Res. 2012 ; 72 (8). 1915-1920
35. Jones RL, Salamonsen LA, Zhao YC, Ethier JF, Drummond AE, Findlay JK. Expression of activin receptors, follistatin and betaglycan by human endometrial stromal cells; consistent with a role for activins during decidualization. Mol Hum Reprod. 2002 ; 8 (4). 363-374
36. Zimmerman CM, Padgett RW. Transforming growth factor beta signaling mediators and modulators. Gene. 2000 ; 249 (1-2). 17-30
37. Luo X, Xu J, Chegini N. The expression of Smads in human endometrium and regulation and induction in endometrial epithelial and stromal cells by transforming growth factor-beta. J Clin Endocrinol Metab. 2003 ; 88 (10). 4967-4976
38. Jeruss JS, Sturgis CD, Rademaker AW, Woodruff TK. Down-regulation of activin, activin receptors, and Smads in high-grade breast cancer. Cancer Res. 2003 ; 63 (13). 3783-3790
39. Mabuchi Y, Yamoto M, Minami S, Umesaki N. Immunohistochemical localization of inhibin and activin subunits, activin receptors and Smads in ovarian endometriosis. Int J Mol Med. 2010 ; 25 (1). 17-23
40. Miyaki M, Kuroki T. Role of Smad4 (DPC4) inactivation in human cancer. Biochem Biophys Res Commun. 2003 ; 306 (4). 799-804
41. Heikkinen PT, Nummela M, Leivonen SK, et al. Hypoxia-activated Smad3-specific dephosphorylation by PP2A. J Biol Chem. 2010 ; 285 (6). 3740-3749