Rapid actions of plasma membrane estrogen receptors regulate motility of mouse embryonic stem cells through a profilin-1/cofilin-1-directed kinase signaling pathway

Molecular Endocrinology

Volumn 26, Issue 8, 2012, Pages 1291-1303

  Yun, Seung Pil ^a   Ryu, Jung Min ^a   Kim, Mi Ok ^a   Park, Jae Hong ^a   Han, Ho Jae ^b  

^a Chonnam National University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; COFILIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR; F ACTIN; FOCAL ADHESION KINASE; FULVESTRANT; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROFILIN; PROTEIN CDC42; PROTEIN KINASE P60; PROTEIN PROFILIN 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ACTINS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; COFILIN 1; EMBRYONIC STEM CELLS; ENZYME ACTIVATION; ESTRADIOL; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION; MICE; PHOSPHORYLATION; PROFILINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; SERUM ALBUMIN, BOVINE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSCRIPTIONAL ACTIVATION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84864449366     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1002     Document Type: Article

References (50)

1. Park JH, Lee MY, Han HJ 2009 A potential role for caveolin-1 in estradiol-17-induced proliferation of mouse embryonic stem cells: involvement of Src, PI3K/Akt, and MAPKs pathways. Int J Biochem Cell Biol 41:659-665
2. Yun SP, Lee MY, Ryu JM, Song CH, Han HJ 2009 Role of HIF-1β and VEGF in human mesenchymal stem cell proliferation by 17-estradiol: involvement of PKC, PI3K/Akt, and MAPKs. Am J Physiol Cell Physiol 296:C317-C326
3. Zhou S, Zilberman Y, Wassermann K, Bain SD, Sadovsky Y, Gazit D 2001 Estrogen modulates estrogen receptor β and expression, osteogenic activity, and apoptosis in mesenchymal stem cells (MSCs) of osteoporotic mice. J Cell Biochem Suppl 36:144-155
4. Bjornstrom L, Sjoberg M 2005 Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19:833-842
5. Keung W, Chan ML, Ho EY, Vanhoutte PM, Man RY 2011 Nongenomic activation of adenylyl cyclase and protein kinase G by 17-estradiol in vascular smooth muscle of the rat superior mesenteric artery. Pharmacol Res 64:509-516
6. Ohshiro K, Schwartz AM, Levine PH, Kumar R 2012 Alternate estrogen receptors promote invasion of inflammatory breast cancer cells via non-genomic signaling. PLoS One 7:e30725
7. Fiorelli G, Gori F, Frediani U, Franceschelli F, Tanini A, Tosti-Guerra C, Benvenuti S, Gennari L, Becherini L, Brandi ML 1996 Membrane binding sites and non-genomic effects of estrogen in cultured human pre-osteoclastic cells. J Steroid Biochem Mol Biol 59:233-240
8. Kelly MJ, Wagner EJ 1999 Estrogen modulation of G-protein-coupled receptors. Trends Endocrinol Metab 10:369-374
9. Stirone C, Boroujerdi A, Duckles SP, Krause DN 2005 Estrogen receptor activation of phosphoinositide-3 kinase, akt, and nitric oxide signaling in cerebral blood vessels: rapid and long-term effects. Mol Pharmacol 67:105-113
10. Suzuki T, Yu HP, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH 2008 Estrogen-mediated activation of non-genomic pathway improves macrophages cytokine production following trauma-hemorrhage. J Cell Physiol 214:662-672
11. Han HJ, Heo JS, Lee YJ 2006 Estradiol-17 stimulates proliferation of mouse embryonic stem cells: involvement of MAPKs and CDKs as well as protooncogenes. Am J Physiol Cell Physiol 290: C1067-C1075
12. Liew CG, Moore H, Ruban L, Shah N, Cosgrove K, Dunne M, Andrews P 2005 Human embryonic stem cells: possibilities for human cell transplantation. Ann Med 37:521-532
13. Zhao X, Huang L, Yin Y, Fang Y, Zhao J, Chen J 2008 Estrogen induces endothelial progenitor cells proliferation and migration by estrogen receptors and PI3K-dependent pathways. Microvasc Res 75:45-52
14. Azios NG, Krishnamoorthy L, Harris M, Cubano LA, Cammer M, Dharmawardhane SF 2007 Estrogen and resveratrol regulate Rac and Cdc42 signaling to the actin cytoskeleton of metastatic breast cancer cells. Neoplasia 9:147-158
15. Giretti MS, Fu XD, De Rosa G, Sarotto I, Baldacci C, Garibaldi S, Mannella P, Biglia N, Sismondi P, Genazzani AR, Simoncini T 2008 Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS One 3:e2238
16. He YY, Cai B, Yang YX, Liu XL, Wan XP 2009 Estrogenic G protein-coupled receptor 30 signaling is involved in regulation of endometrial carcinoma by promoting proliferation, invasion potential, and interleukin-6 secretion via the MEK/ERK mitogen-activated protein kinase pathway. Cancer Sci 100:1051-1061
17. Sanchez AM, Flamini MI, Baldacci C, Goglia L, Genazzani AR, Simoncini T 2010 Estrogen receptor-β promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Mol Endocrinol 24:2114-2125
18. Sanchez AM, Flamini MI, Zullino S, Gopal S, Genazzani AR, Simoncini T 2011 Estrogen receptor-β promotes endothelial cell motility through focal adhesion kinase. Mol Hum Reprod 17:219-226
19. Hu J, Mukhopadhyay A, Craig AW 2011 Transducer of Cdc42-dependent actin assembly promotes epidermal growth factor-induced cell motility and invasiveness. J Biol Chem 286:2261-2272
20. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, Segall J, Eddy R, Miki H, Takenawa T, Condeelis J 2005 Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168:441-452
21. Yun SP, Ryu JM, Jang MW, Han HJ 2011 Interaction of profilin-1 and F-actin via a-arrestin-1/JNK signaling pathway involved in prostaglandin E2-induced human mesenchymal stem cells migration and proliferation. J Cell Physiol 226:559-571
22. Kobayashi M, Nishita M, Mishima T, Ohashi K, Mizuno K 2006 MAPKAPK-2-mediated LIM-kinase activation is critical for VEGF-induced actin remodeling and cell migration. EMBO J 25:713-726
23. Lamote I, Meyer E, Duchateau L, Burvenich C 2004 Influence of 17-estradiol, progesterone, and dexamethasone on diapedesis and viability of bovine blood polymorphonuclear leukocytes. J Dairy Sci 87:3340-3349
24. Chieng-Yane P, Bocquet A, Létienne R, Bourbon T, Sablayrolles S, Perez M, Hatem SN, Lompré AM, Le Grand B, David-Dufilho M 2011 Protease-activated receptor-1 antagonist F 16618 reduces arterial restenosis by down-regulation of tumor necrosis factor β and matrix metalloproteinase 7 expression, migration, and proliferation of vascular smooth muscle cells. J Pharmacol Exp Ther 336: 643-651
25. Park JH, Han HJ 2009 Caveolin-1 plays important role in EGF-induced migration and proliferation of mouse embryonic stem cells: involvement of PI3K/Akt and ERK. Am J Physiol Cell Physiol 297: C935-C944
26. Sørensen V, Zhen Y, Zakrzewska M, Haugsten EM, Walchli S, Nilsen T, Olsnes S, Wiedlocha A 2008 Phosphorylation of fibro-blast growth factor (FGF) receptor 1 at Ser777 by p38 mitogenactivated protein kinase regulates translocation of exogenous FGF1 to the cytosol and nucleus. Mol Cell Biol 28:4129-4141
27. Wiedĺocha A, Nilsen T, Wesche J, Sørensen V, Maĺecki J, Marcinkowska E, Olsnes S 2005 Phosphorylation-regulated nucleocytoplasmic trafficking of internalized fibroblast growth factor-1. Mol Biol Cell 16:794-810
28. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
29. Dos Santos EG, Dieudonne MN, Pecquery R, Le Moal V, Giudicelli Y, Lacasa D 2002 Rapid nongenomic E2 effects on p42/p44 MAPK, activator protein-1, and cAMP response element binding protein in rat white adipocytes. Endocrinology 143:930-940
30. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC 2001 Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-730
31. Marino M, Acconcia F, Bresciani F, Weisz A, Trentalance A 2002 Distinct nongenomic signal transduction pathways controlled by 17-estradiol regulate DNA synthesis and cyclin D1 gene transcription in HepG2 cells. Mol Biol Cell 13:3720-3729
32. Soderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, Landegren U 2006 Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3:995-1000
33. Hong SH, Nah HY, Lee YJ, Lee JW, Park JH, Kim SJ, Lee JB, Yoon HS, Kim CH 2004 Expression of estrogen receptor-β and-, glucocorticoid receptor, and progesterone receptor genes in human embryonic stem cells and embryoid bodies. Mol Cells 18:320-325
34. Lucas TF, Royer C, Siu ER, Lazari MF, Porto CS 2010 Expression and signaling of G protein-coupled estrogen receptor 1 (GPER) in rat Sertoli cells. Biol Reprod 83:307-317
35. Yuen GS, McEwen BS, Akama KT 2011 LIM kinase mediates estrogen action on the actin depolymerization factor cofilin. Brain Res 1379:44-52
36. Wyckoff MH, Chambliss KL, Mineo C, Yuhanna IS, Mendelsohn ME, Mumby SM, Shaul PW 2001 Plasma membrane estrogen receptors are coupled to endothelial nitric-oxide synthase through Gβi. J Biol Chem 276:27071-27076
37. Evinger AJ III, Levin ER 2005 Requirements for estrogen receptor β membrane localization and function. Steroids 70:361-363
38. Ignatov A, Ignatov T, Roessner A, Costa SD, Kalinski T 2010 Role of GPR30 in the mechanisms of tamoxifen resistance in breast cancer MCF-7 cells. Breast Cancer Res Treat 123:87-96
39. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ 2008 Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165-190
40. Fricke R, Gohl C, Dharmalingam E, Grevelhorster A, Zahedi B, Harden N, Kessels M, Qualmann B, Bogdan S 2009 Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr Biol 19:1429-1437
41. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P 2005 Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791-804
42. Bu W, Chou AM, Lim KB, Sudhaharan T, Ahmed S 2009 The Toca-1-N-WASP complex links filopodial formation to endocytosis. J Biol Chem 284:11622-11636
43. Bu W, Lim KB, Yu YH, Chou AM, Sudhaharan T, Ahmed S 2010 Cdc42 interaction with N-WASP and Toca-1 regulates membrane tubulation, vesicle formation and vesicle motility: implications for endocytosis. PLoS One 5:e12153
44. Yang L, Wang L, Zheng Y 2006 Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol Biol Cell 17:4675-4685
45. Kang F, Purich DL, Southwick FS 1999 Profilin promotes barbed-end actin filament assembly without lowering the critical concentration. J Biol Chem 274:36963-36972
46. Konakahara S, Ohashi K, Mizuno K, Itoh K, Tsuji T 2004 CD29 integrin and LIMK1/cofilin-mediated actin reorganization regulates the migration of haematopoietic progenitor cells underneath bone marrow stromal cells. Genes Cells 9:345-358
47. Pantaloni D, Carlier MF 1993 How profilin promotes actin filament assembly in the presence of thymosin 4. Cell 75:1007-1014
48. McGough A, Pope B, Chiu W, Weeds A 1997 Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138:771-781
49. Yamaguchi H, Condeelis J 2007 Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773:642-652
50. Wu N, Zhang W, Yang Y, Liang YL, Wang LY, Jin JW, Cai XM, Zha XL 2006 Profilin 1 obtained by proteomic analysis in all-trans retinoic acid-treated hepatocarcinoma cell lines is involved in inhibition of cell proliferation and migration. Proteomics 6:6095-6106