Estrogens and PTP1B function in a novel pathway to regulate aromatase enzymatic activity in breast cancer cells

Endocrinology

Volumn 153, Issue 11, 2012, Pages 5157-5166

  Barone, Ines ^a   Giordano, Cinzia ^a   Malivindi, Rocco ^a   Lanzino, Marilena ^a   Rizza, Pietro ^a   Casaburi, Ivan ^a   Bonofiglio, Daniela ^a   Catalano, Stefania ^a   Andò, Sebastiano ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AROMATASE; ESTRADIOL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE 1B; PROTEIN TYROSINE PHOSPHATASE INHIBITOR;

ARTICLE; BREAST CANCER; CANCER CELL; CELL STRAIN MCF 7; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ESTROGEN ACTIVITY; HUMAN; HUMAN CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AROMATASE; BREAST NEOPLASMS; CELL LINE, TUMOR; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84867768388     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1561     Document Type: Article

References (49)

1. Sasano H, Nagura H, Harada N, Goukon Y, Kimura M 1994 Immunolocalization of aromatase and other steroidogenic enzyme in human breast disorders. Hum Patol 25:530-535 (Pubitemid 24173872)
2. Sourdaine P, Mullen P, White R, Telford J, Parker MG, Miller WR 1996 Aromatase activity and CYP19 gene expression in breast cancers. J Steroid Biochem Mol Biol 59:191-198 (Pubitemid 27036271)
3. Maggiolini M, Carpino A, Bonofiglio D, Pezzi V, Rago V, Marsico S, Picard D, Andò S 2001 The direct proliferative stimulus of dehydroepiandrosterone on MCF-7 breast cancer cells is potentiated by overexpression of aromatase. Mol Cell Endocrinol 184:163-171 (Pubitemid 32994806)
4. Yue W, Zhou D, Chen S, Brodie A, 1994 A new nude mouse model for postmenopausal breast cancer using MCF-7 cells transfected with the human aromatase gene. Cancer Res 54:5092-5095 (Pubitemid 24313482)
5. Tekmal RR, Ramachandra N, Gubba S, Durgam VR, Mantione J, Toda K, Shizuta Y, Dillehay DL 1996 Overexpression of int-5/aromatase in mammary glands of transgenic mice results in the induction of hyperplasia and nuclear abnormalities. Cancer Res 56:3180-3185 (Pubitemid 26242957)
6. Sun XZ, Zhou D, Chen S 1997 Autocrine and paracrine actions of breast tumor aromatase. A three-dimensional cell culture study involving aromatase transfected MCF-7 and T-47D cells. J Steroid Biochem Mol Biol 63:29-36 (Pubitemid 28018134)
7. Gill K, Kirma N, Tekmal RR 2001 Overexpression of aromatase in transgenic male mice in the induction of gynecomastia and other biochemical changes in mammary glands. J Steroid Biochem Mol Biol 77:13-18 (Pubitemid 32455349)
8. Simpson ER, Michael MD, Agarwal VR, Hinshelwood MM, Bulun SE, Zhao Y, 1997 Expression of the CYP19 (aromatase) gene: an unusual case of alternative promoter usage. FASEB J 11:29-36 (Pubitemid 27076321)
9. Bulun SE, Sebastian S, Takayama K, Suzuki T, Sasano H, Shozu M 2003 The human CYP19 (aromatase P450) gene: update on physiologic roles and genomic organization of promoters. J Steroid Biochem Mol Bio 86:219-224 (Pubitemid 37412560)
10. Balthazart J, Baillien M, Ball GF 2001 Phosphorylation processes mediate rapid changes of brain aromatase activity. J Steroid Biochem Mol Biol 79:261-277 (Pubitemid 34162529)
11. Balthazart J, Baillien M, Ball GF 2006 Rapid control of brain aromatase activity by glutamatergic imputs. Endocrinology 147:359-366 (Pubitemid 43004289)
12. Shozu M, Sumitani H, Murakami K, Segawa T, Yang HJ, Inoue M 2001 Regulation of aromatase activity in bone-derived cells: possible role of mitogen-activated protein kinase. J Steroid Biochem Mol Biol 79:61-65 (Pubitemid 34158779)
13. Yue W, Wang JP, Conaway MR, Li Y, Santen RJ 2003 Adaptive hypersensitivity following long-term estrogen deprivation: involvement of multiple signal pathways. J Steroid Biochem Mol Biol 86:265-274 (Pubitemid 37412565)
14. Kinoshita Y, Chen S 2003 Induction of aromatase (CYP19) expression in breast cancer cells through a nongenomic action of estrogen receptor α. Cancer Res 63:3546-3555 (Pubitemid 36793034)
15. Su B, Wong C, Hong Y, Chen S 2011 Growth factor signaling enhances aromatase activity of breast cancer cells via post-transcriptional mechanisms. J Steroid Biochem Mol Biol 123:101-108
16. Charlier TD, Harada N, Balthazart J, Cornil CA 2011 Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 152:4199-4210
17. Miller TW, Shin I, Kagawa N, Evans DB, Waterman MR, Arteaga CL 2008 Aromatase is phosphorylated in situ at serine-118. J Steroid Biochem Mol Biol 112:95-101
18. Catalano S, Barone I, Giordano C, Rizza P, Qi H, Gu G, Malivindi R, Bonofiglio D, Andò S 2009 Rapid estradiol/ERα signaling enhances aromatase enzymatic activity in breast cancer cells. Mol Endocrinol 23:1634-1645
19. Novak B, Kapuy O, Domingo-Sananes MR, Tyson JJ 2010 Regulated protein kinases and phosphatases in cell cycle decisions. Curr Opin Cell Biol 22:801-808
20. Lingamanaidu V, Ravichandran LV, Chen H, Li Y, Quon MJ 2001 Phosphorylation of PTP1B at Ser50 by Akt impairs its ability to dephosphorylate the insulin receptor. Mol Endocrinol 15:1768-1780 (Pubitemid 32939307)
21. Yip SC, Saha S, Chernoff J 2010 PTP1B: a double agent in metabolism and oncogenesis. Trends Biochem Sci 35:442-449
22. Chernoff J 1999 Protein tyrosine phosphatases as negative regulators of mitogenic signaling. J Cell Physiol 180:173-181 (Pubitemid 29297194)
23. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, Ramachandran C, Gresser MJ, Tremblay ML, Kennedy BP 1999 Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283:1544-1548
24. Goldstein BJ, Bittner-Kowalczyk A, White MF, Harbeck M 2000 Tyrosine dephosphorylation and deactivation of insulin receptor substrate-1 by protein-tyrosine phosphatase 1B. Possible facilitation by the formation of a ternary complex with the Grb2 adaptor protein. J Biol Chem 275:4283-4289 (Pubitemid 30094668)
25. Myers MP, Andersen JN, Cheng A, Tremblay ML, Horvath CM, Parisien JP, Salmeen A, Barford D, Tonks NK 2001 TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem 276: 47771-47774
26. Lund IK, Hansen JA, Andersen HS, Møller NP, Billestrup N 2005 Mechanism of protein tyrosine phosphatase 1B-mediated inhibition of leptin signalling. J Mol Endocrinol 34:339-351 (Pubitemid 40585186)
27. Arnold SF, Melamed M, Vorojeikina DP, Notides AC, Sasson S, 1997 Estradiol-binding mechanism and binding capacity of the human estrogen receptor is regulated by tyrosine phosphorylation. Mol Endocrinol 11:48-53 (Pubitemid 27021253)
28. LaMontagne Jr KR, Hannon G, Tonks NK 1998 Protein tyrosine phosphatase PTP1B suppresses p210 bcr-abl-induced transformation of rat-1 fibroblasts and promotes differentiation of K562 cells. Proc Natl Acad Sci USA 95:14094-14099 (Pubitemid 28549326)
29. Arias-Salgado EG, Haj F, Dubois C, Moran B, Kasirer-Friede A, Furie BC, Furie B, Neel BG, Shattil SJ 2005 PTP-1B is an essential positive regulator of platelet integrin signaling. J Cell Biol 170:837-845 (Pubitemid 41242115)
30. Eden ER, White IJ, Tsapara A, Futter CE 2010 Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat Cell Biol 12:267-272
31. Bjorge JD, Pang A, Fujita DJ 2000 Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem 275:41439-41446 (Pubitemid 32054980)
32. Bentires-Alj M, Neel BG 2007 Protein-tyrosine phosphatase 1B is required for HER2/Neu-induced breast cancer. Cancer Res 67:2420-2424 (Pubitemid 46548925)
33. Julien SG, Dubé N, Read M, Penney J, Paquet M, Han Y, Kennedy BP, Muller WJ, Tremblay ML 2007 Protein tyrosine phosphatase1B deficiency or inhibition delays ErbB2-induced mammary tumorigenesis and protects from lung metastasis. Nat Genet 39:338-346 (Pubitemid 46328486)
34. Wiener JR, Kerns BJ, Harvey EL, Conaway MR, Iglehart JD, Berchuck A, Bast Jr RC 1994 Overexpression of the protein tyrosine phosphatase PTP1B in human breast cancer: association with p185c-erbB-2 protein expression. J Natl Cancer Inst 86:372-378
35. Castoria G, Migliaccio A, Bilancio A, Di Domenico M, de Falco A, Lombardi M, Fiorentino R, Varricchio L, Barone MV, Auricchio F 2001 PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. EMBO J 20:6050-6059 (Pubitemid 33049280)
36. Stoica GE, Franke TF, Wellstein A, Czubayko F, List HJ, Reiter R, Morgan E, Martin MB, Stoica A 2003 Estradiol rapidly activates Akt via the ErbB2 signaling pathway. Mol Endocrinol 17:818-830 (Pubitemid 36539574)
37. Miller WR 2006 Aromatase and the breast: regulation and clinical aspects. Maturitas 54:335-341
38. Santen RJ, Yue W, Naftolin F, Mor G, Berstein L 1999 The potential of aromatase inhibitors in breast cancer prevention. Endoc-Relat Cancer 6:235-243 (Pubitemid 29260058)
39. Altundag K, Ibrahim NK 2006 Aromatase inhibitors in breast cancer: an overview. Oncologist 11:553-562 (Pubitemid 43967611)
40. Brown-Shimer S, Johnson KA, Hill DE, Bruskin AM 1992 Effect of protein tyrosine phosphatase 1B expression on transformation by the human neu oncogene. Cancer Res 52:478-482
41. Liu F, Sells MA, Chernoff J 1998 Transformation suppression by protein tyrosine phosphatase 1B requires a functional SH3 ligand. Mol Cell Biol 18:250-259 (Pubitemid 28021036)
42. Arregui CO, Balsamo J, Lilien J 1998 Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J Cell Biol 143:861-873 (Pubitemid 28512577)
43. Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG 1992 The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 68:545-560
44. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD 1994 Aromatase cytocrome P450, the enzyme responsible for estrogen biosyntesis. Endocr Rev 15:342-355 (Pubitemid 24180792)
45. Flint AJ, Gebbink MF, Franza Jr BR, Hill DE, Tonks NK 1993 Multi-site phosphorylation of the protein tyrosine phosphatase, PTP1B: identification of cell cycle regulated and phorbol ester stimulated sites of phosphorylation. EMBO J 12:1937-1946 (Pubitemid 23157710)
46. Shifrin VI, Davis RJ, Neel BG 1997 Phosphorylation of protein-tyrosine phosphatase PTP-1B on identical sites suggests activation of a common signaling pathway during mitosis and stress response in mammalian cells. J Biol Chem 272:2957-2962 (Pubitemid 27053347)
47. Migliaccio A, Di Domenico M, Castoria G, de Falco A, Bontempo P, Nola E, Auricchio F 1996 Tyrosine kinase/p21 ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 15:1292-1300
48. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK 2000 Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541
49. Hall JM, Couse JF, Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signalling. J Biol Chem 276:36869-36872