Estrogen and testosterone in concert with EFNB3 regulate vascular smooth muscle cell contractility and blood pressure

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 7, 2016, Pages H861-H872

  Wang, Yujia ^a   Wu, Zenghui ^a   Thorin, Eric ^b   Tremblay, Johanne ^a   Lavoie, Julie L ^a,c   Luo, Hongyu ^a   Peng, Junzheng ^a   Qi, Shijie ^a   Wu, Tao ^d   Chen, Fei ^d   Shen, Jianzhong ^d   Hu, Shenjiang ^d   Wu, Jiangping ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MONTREAL HEART INSTITUTE   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Blood pressure; Ephrinb3; Estrogen

Indexed keywords

CALCIUM ION; EPHRIN B3; ESTROGEN; MESSENGER RNA; MYOSIN LIGHT CHAIN KINASE; SEX HORMONE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CATECHOLAMINE URINE LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GENE DELETION; GENE INACTIVATION; GENETIC RISK; HYPERTENSION; IMMUNOFLUORESCENCE MICROSCOPY; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SMOOTH MUSCLE CONTRACTILITY; TARGET CELL; VASCULAR SMOOTH MUSCLE CELL; WILD TYPE; ANIMAL; BLOOD PRESSURE; C57BL MOUSE; METABOLISM; MOUSE; MUSCLE CONTRACTION; PHYSIOLOGY; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; BLOOD PRESSURE; EPHRIN-B3; ESTROGENS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; TESTOSTERONE; VASOCONSTRICTION;

EID: 84983749021     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00873.2015     Document Type: Article

References (55)

1. Anonymous. Unified nomenclature for Eph family receptors, and their ligands, the ephrins. Eph Nomenclature Committee. Cell 90: 403–404, 1997.
2. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251–263, 2002.
3. Benten WP, Lieberherr M, Giese G, Wrehlke C, Stamm O, Sekeris CE, Mossmann H, Wunderlich F. Functional testosterone receptors in plasma membranes of T cells. FASEB J 13: 123–133, 1999.
4. Brozovich FV. Myosin light chain phosphatase–it gets around. Circ Res 90: 500–502, 2002.
5. Danzo BJ. The effects of environmental hormones on reproduction. Cell Mol Life Sci 54: 1249–1264, 1998.
6. Davy A, Bush JO, Soriano P. Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol 4: e315, 2006.
7. Dong HL, OBrien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL. GRIP: A synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386: 279–284, 1997.
8. Dravis C, Wu T, Chumley MJ, Yokoyama N, Wei S, Wu DK, Marcus DC, Henkemeyer M. EphB2 and ephrin-B2 regulate the ionic homeostasis of vestibular endolymph. Hear Res 223: 93–104, 2007.
9. 2C-adrenoceptors and cold-induced constriction of cutaneous arteries. Am J Physiol Heart Circ Physiol 293: H1955–H1961, 2007.
10. Evans PD, Bayliss A, Reale V. GPCR-mediated rapid, nongenomic actions of steroids: comparisons between DmDopEcR and GPER1 (GPR30). Gen Comp Endocrinol 195: 157–163, 2014.
11. Farhat MY, Lavigne MC, Ramwell PW. The vascular protective effects of estrogen. FASEB J 10: 615–624, 1996.
12. Flanagan JG, Vanderhaeghen P. The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21: 309–345, 1998.
13. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 124: 161-173, 2006.
14. Giembycz MA, Newton R. Beyond the dogma: novel beta2-adrenoceptor signalling in the airways. Eur Respir J 27: 1286–1306, 2006.
15. Golovina VA, Blaustein MP. Preparation of primary cultured mesenteric artery smooth muscle cells for fluorescent imaging and physiological studies. Nat Protoc 1: 2681–2687, 2006.
16. Gui Y, Zheng XL, Zheng J, Walsh MP. Inhibition of rat aortic smooth muscle contraction by 2-methoxyestradiol. Am J Physiol Heart Circ Physiol 295: H1935–H1942, 2008.
17. Hashimoto T, Karasawa T, Saito A, Miyauchi N, Han GD, Hayasaka K, Shimizu F, Kawachi H. Ephrin-B1 localizes at the slit diaphragm of the glomerular podocyte. Kidney Int 72: 954–964, 2007.
18. Huang C, Jacobson K, Schaller MD. MAP kinases and cell migration. J Cell Sci 117: 4619–4628, 2004.
19. Kawano Y, Fukata Y, Oshiro N, Amano M, Nakamura T, Ito M, Matsumura F, Inagaki M, Kaibuchi K. Phosphorylation of myosinbinding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J Cell Biol 147: 1023–1038, 1999.
20. Kerkhofs S, Denayer S, Haelens A, Claessens F. Androgen receptor knockout and knock-in mouse models. J Mol Endocrinol 42: 11–17, 2009.
21. Koga M, Hirano K, Nishimura J, Nakano H, Kanaide H. Endotheliumdependent and independent enhancement of vascular contractility in the ovariectomized rabbit. J Soc Gynecol Investig 11: 272–279, 2004.
22. Konstantinova I, Nikolova G, Ohara-Imaizumi M, Meda P, Kucera T, Zarbalis K, Wurst W, Nagamatsu S, Lammert E. EphA-Ephrin-Amediated beta cell communication regulates insulin secretion from pancreatic islets. Cell 129: 359–370, 2007.
23. Kullander K, Croll SD, Zimmer M, Pan L, McClain J, Hughes V, Zabski S, DeChiara TM, Klein R, Yancopoulos GD, Gale NW. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev 15: 877–888, 2001.
24. Lavoie JL, Lake-Bruse KD, Sigmund CD. Increased blood pressure in transgenic mice expressing both human renin and angiotensinogen in the renal proximal tubule. Am J Physiol Renal Physiol 286: F965–F971, 2004.
25. Levin ER. Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19: 1951–1959, 2005.
26. Lu Q, Lu Z, Liu Q, Guo L, Ren H, Fu J, Jiang Q, Clarke PR, Zhang C. Chromatin-bound NLS proteins recruit membrane vesicles and nucleoporins for nuclear envelope assembly via importin-alpha/beta. Cell Res 22: 1562–1575, 2012.
27. Luo H, Charpentier T, Wang X, Qi S, Han B, Wu T, Terra R, Lamarre A, Wu J. Efnb1 and Efnb2 proteins regulate thymocyte development, peripheral T cell differentiation, and antiviral immune responses and are essential for interleukin-6 (IL-6) signaling. J Biol Chem 286: 41135–41152, 2011.
28. Luo H, Wan X, Wu Y, Wu J. Cross-linking of EphB6 resulting in signal transduction and apoptosis in Jurkat cells. J Immunol 167: 1362–1370, 2001.
29. Luo H, Wu Z, Qi S, Jin W, Han B, Wu J. Ephrinb1 and Ephrinb2 are associated with interleukin-7 receptor alpha and retard its internalization from the cell surface. J Biol Chem 286: 44976–44987, 2011.
30. Luo H, Wu Z, Tremblay J, Thorin E, Peng J, Lavoie JL, Hu B, Stoyanova E, Cloutier G, Qi S, Wu T, Cameron M, Wu J. Receptor tyrosine kinase Ephb6 regulates vascular smooth muscle contractility and modulates blood pressure in concert with sex hormones. J Biol Chem 287: 6819–6829, 2012.
31. Luo H, Yu G, Tremblay J, Wu J. EphB6-null mutation results in compromised T cell function. J Clin Invest 114: 1762–1773, 2004.
32. Luo H, Yu G, Wu Y, Wu J. EphB6 crosslinking results in costimulation of T cells. J Clin Invest 110: 1141–1150, 2002.
33. Miller JR, Silver PJ, Stull JT. The role of myosin light chain kinase phosphorylation in beta-adrenergic relaxation of tracheal smooth muscle. Mol Pharmacol 24: 235–242, 1983.
34. Muranyi A, Derkach D, Erdodi F, Kiss A, Ito M, Hartshorne DJ. Phosphorylation of Thr695 and Thr850 on the myosin phosphatase target subunit: inhibitory effects and occurrence in A7r5 cells. FEBS Lett 579: 6611–6615, 2005.
35. Nelson LR, Bulun SE. Estrogen production and action. J Am Acad Dermatol 45: S116–124, 2001.
36. Nikolova Z, Djonov V, Zuercher G, Andres AC, Ziemiecki A. Celltype specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis. J Cell Sci 111: 2741–2751, 1998.
37. Ogita H, Kunimoto S, Kamioka Y, Sawa H, Masuda M, Mochizuki N. EphA4-mediated Rho activation via Vsm-RhoGEF expressed specifically in vascular smooth muscle cells. Circ Res 93: 23–31, 2003.
38. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133: 38–52, 2008.
39. Prossnitz ER, Barton M. Estrogen biology: new insights into GPER function and clinical opportunities. Mol Cell Endocrinol 389: 71–83, 2014.
40. 2+/calmodulin of an exogenous myosin light chain kinase in mouse arteries. J Physiol 587: 2599–2612, 2009.
41. Roman-Blas JA, Castaneda S, Largo R, Herrero-Beaumont G. Osteoarthritis associated with estrogen deficiency. Arthritis Res Ther 11: 241, 2009.
42. Segura I, Essmann CL, Weinges S, Acker-Palmer A. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat Neurosci 10: 301–310, 2007.
43. Tanaka M, Kamata R, Yanagihara K, Sakai R. Suppression of gastric cancer dissemination by ephrin-B1-derived peptide. Cancer Sci 101: 87–93, 2010.
44. Tanaka M, Kamo T, Ota S, Sugimura H. Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion. EMBO J 22: 847–858, 2003.
45. Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93: 741–753, 1998.
46. Wang Y, Thorin E, Luo H, Tremblay J, Lavoie JL, Wu Z, Peng J, Qi S, Wu J. EPHB4 protein expression in vascular smooth muscle cells regulates their contractility, and EPHB4 deletion leads to hypotension in mice. J Biol Chem 290: 14235–14244, 2015.
47. Wilkinson DG. Eph receptors and ephrins: regulators of guidance and assembly. Int Rev Cytol 196: 177–244, 2000.
48. Wu J, Luo H. Recent advances on T-cell regulation by receptor tyrosine kinases. Curr Opin Hematol 12: 292–297, 2005.
49. Wu Z, Luo H, Thorin E, Tremblay J, Peng J, Lavoie JL, Wang Y, Qi S, Wu T, Wu J. Possible role of Efnb1 protein, a ligand of Eph receptor tyrosine kinases, in modulating blood pressure. J Biol Chem 287: 15557-15569, 2012.
50. Yu G, Luo H, Wu Y, Wu J. Ephrin B2 induces T cell costimulation. J Immunol 171: 106–114, 2003.
51. Yu G, Luo H, Wu Y, Wu J. EphrinB1 is essential in T-cell-T-cell co-operation during T-cell activation. J Biol Chem 279: 55531–55539, 2004.
52. Yu G, Luo H, Wu Y, Wu J. Mouse ephrinB3 augments T-cell signaling and responses to T-cell receptor ligation. J Biol Chem 278: 47209–47216, 2003.
53. Yu G, Mao J, Wu Y, Luo H, Wu J. Ephrin-B1 is critical in T-cell development. J Biol Chem 281: 10222–10229, 2006.
54. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T, Matsuo K. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4: 111–121, 2006.
55. Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, Hodgin J, Shaul PW, Thoren P, Smithies O, Gustafsson JA, Mendelsohn ME. Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science 295: 505–508, 2002.