Effect of ligand-activated estrogen receptor Β on lymphoma growth in vitro and in vivo

Leukemia

Volumn 25, Issue 7, 2011, Pages 1103-1110

  Yakimchuk, K ^a   Iravani, M ^a   Hasni, M S ^a   Rhonnstad P ^b   Nilsson, S ^b   Jondal, M ^a   Okret, S ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Karo Bio   (Sweden)

Author keywords

agonists; apoptosis; cell proliferation; estrogen receptor b; lymphomas; tumor growth

Indexed keywords

DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR BETA; KB 9520; LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA; MALE; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR VOLUME;

EID: 85027950956     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.68     Document Type: Article

References (54)

1. Huber JC, Schneeberger C, Tempfer CB. Genetic modelling of the estrogen metabolism as a risk factor of hormone-dependent disorders. Maturitas 2002; 42: 1-12. (Pubitemid 34521716)
2. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87: 905-931. (Pubitemid 47084672)
3. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997; 138: 863-870. (Pubitemid 27089735)
4. Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 1997; 82: 4258-4265. (Pubitemid 27525550)
5. Shim GJ, Gherman D, Kim HJ, Omoto Y, Iwase H, Bouton D et al. Differential expression of oestrogen receptors in human secondary lymphoid tissues. J Pathol 2006; 208: 408-414. (Pubitemid 43210528)
6. Cheng G, Weihua Z, Warner M, Gustafsson JA° . Estrogen receptors ER alpha and ER beta in proliferation in the rodent mammary gland. Proc Natl Acad Sci USA 2004; 101: 3739-3746. (Pubitemid 38386631)
7. Wada-Hiraike O, Hiraike H, Okinaga H, Imamov O, Barros RP, Morani A et al. Role of estrogen receptor beta in uterine stroma and epithelium: insights from estrogen receptor beta/mice. Proc Natl Acad Sci USA 2006; 103: 18350-18355. (Pubitemid 44872762)
8. Omoto Y, Imamov O, Warner M, Gustafsson JA° . Estrogen receptor alpha and imprinting of the neonatal mouse ventral prostate by estrogen. Proc Natl Acad Sci USA 2005; 102: 1484-1489. (Pubitemid 40214366)
9. Imamov O, Morani A, Shim GJ, Omoto Y, Thulin-Andersson C, Warner M et al. Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc Natl Acad Sci USA 2004; 101: 9375-9380. (Pubitemid 38821066)
10. Cheng G, Li Y, Omoto Y, Wang Y, Berg T, Nord M et al. Differential regulation of estrogen receptor (ER)alpha and ERbeta in primate mammary gland. J Clin Endocrinol Metab 2005; 90: 435-444. (Pubitemid 40116692)
11. Wada-Hiraike O, Imamov O, Hiraike H, Hultenby K, Schwend T, Omoto Y et al. Role of estrogen receptor beta in colonic epithelium. Proc Natl Acad Sci USA 2006; 103: 2959-2964.
12. Morani A, Barros RP, Imamov O, Hultenby K, Arner A, Warner M et al. Lung dysfunction causes systemic hypoxia in estrogen receptor beta knockout (ERbeta) mice. Proc Natl Acad Sci USA 2006; 103: 7165-7169.
13. Shim GJ, Wang L, Andersson S, Nagy N, Kis LL, Zhang Q et al. Disruption of the estrogen receptor beta gene in mice causes myeloproliferative disease resembling chronic myeloid leukemia with lymphoid blast crisis. Proc Natl Acad Sci USA 2003; 100: 6694-6699. (Pubitemid 36675339)
14. Hartman J, Lindberg K, Morani A, Inzunza J, Ström A, Gustafsson JA° . Estrogen receptor beta inhibits angiogenesis and growth of T47D breast cancer xenografts. Cancer Res 2006; 66: 11207-11213. (Pubitemid 46009948)
15. Hartman J, Edvardsson K, Lindberg K, Zhao C, Williams C, StrömA et al. Tumor repressive functions of estrogen receptor beta in SW480 colon cancer cells. Cancer Res 2009; 69: 6100-6106.
16. Catovsky D, Fooks J, Richards S. Prognostic factors in chronic lymphocytic leukaemia: the importance of age, sex and response to treatment in survival. A report from the MRC CLL 1 trial. MRC Working Party on Leukaemia in Adults. Br J Haematol 1989; 72: 141-149. (Pubitemid 19151132)
17. Forsythe A, Breland T, Majumdar S, Elkin TD, Johnson D, Megason G. Gender differences in incidence rates of childhood B-precursor acute lymphocytic leukemia in Mississippi. J Pediatr Oncol Nurs 2010; 27: 164-167.
18. Abouyabis AN, Shenoy PJ, Lechowicz MJ, Flowers CR. Incidence and outcomes of the peripheral T-cell lymphoma subtypes in the United States. Leuk Lymphoma 2008; 49: 2099-2107.
19. Alexander DD, Mink PJ, Adami HO, Chang ET, Cole P, Mandel JS et al. The non-Hodgkin lymphomas: a review of the epidemiologic literature. Int J Cancer 2007; 120(Suppl 12): 1-39. (Pubitemid 46732571)
20. Mbulaiteye SM, Biggar RJ, Bhatia K, Linet MS, Devesa SS. Sporadic childhood Burkitt lymphoma incidence in the United States during 1992-2005. Pediatr Blood Cancer 2009; 53: 366-370.
21. Geller ML, Chlebowski RT. HT and breast cancer risk. Fertil Steril 2003; 80(Suppl 4): 5-9; quiz 54-55.
22. Neves ECM. Association of ovarian and uterine cancers with postmenopausal hormonal treatments. Clin Obstet Gynecol 2008; 51: 607-617.
23. Mohler ML, Narayanan R, Coss CC, Hu K, He Y, Wu Z et al. Estrogen receptor beta selective nonsteroidal estrogens: seeking clinical indications. Expert Opin Ther Pat 2010; 20: 507-534.
24. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 2001; 44: 4230-4251. (Pubitemid 33095330)
25. Zhou F, Rouse BT, Huang L. Prolonged survival of thymomabearing mice after vaccination with a soluble protein antigen entrapped in liposomes: a model study. Cancer Res 1992; 52: 6287-6291.
26. Rhönnstad PKE, Apelqvist T, Wennersta° l M, Cheng A. Novel estrogen receptor ligands. Patent application No. WO2009/127686, 2009.
27. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA . Mouse estrogen receptor beta forms estrogen response element-binding heterodimers with estrogen receptor alpha. Mol Endocrinol 1997; 11: 1486-1496. (Pubitemid 27366759)
28. Saji S, Jensen EV, Nilsson S, Rylander T, Warner M, Gustafsson JA° . Estrogen receptors alpha and beta in the rodent mammary gland. Proc Natl Acad Sci USA 2000; 97: 337-342. (Pubitemid 30055832)
29. Patrone C, Cassel TN, Pettersson K, Piao YS, Cheng G, Ciana P et al. Regulation of postnatal lung development and homeostasis by estrogen receptor beta. Mol Cell Biol 2003; 23: 8542-8552. (Pubitemid 37441291)
30. Helguero LA, Faulds MH, Gustafsson JA° , Haldosén LA. Estrogen receptors alfa (ERalpha) and beta (ERbeta) differentially regulate proliferation and apoptosis of the normal murine mammary epithelial cell line HC11. Oncogene 2005; 24: 6605-6616. (Pubitemid 41486791)
31. Simonoska R, Stenberg AE, Duan M, Yakimchuk K, Fridberger A, Sahlin L et al. Inner ear pathology and loss of hearing in estrogen receptor-beta deficient mice. J Endocrinol 2009; 201: 397-406.
32. Warner M, Gustafsson JA° . The role of estrogen receptor beta (ERbeta) in malignant diseasesFa new potential target for antiproliferative drugs in prevention and treatment of cancer. Biochem Biophys Res Commun 2010; 396: 63-66.
33. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson JA° , Nilsson S. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 1998; 54: 105-112. (Pubitemid 28337592)
34. Bahr GF, Mikel U, Klein G. Localization and quantitation of EBVassociated nuclear antigen (EBNA) in Raji cells. Beitr Pathol 1975; 155: 72-78.
35. Klein G, Zeuthen J, Terasaki P, Billing R, Honig R, Jondal M et al. Inducibility of the Epstein-Barr virus (EBV) cycle and surface marker properties of EBV-negative lymphoma lines and their in vitro EBV-converted sublines. Int J Cancer 1976; 18: 639-652.
36. Schmidt S, Rainer J, Riml S, Ploner C, Jesacher S, Achmü ller C et al. Identification of glucocorticoid-response genes in children with acute lymphoblastic leukemia. Blood 2006; 107: 2061-2069. (Pubitemid 43292367)
37. Ström A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA° . Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci USA 2004; 101: 1566-1571. (Pubitemid 38236167)
38. Vivar OI, Zhao X, Saunier EF, Griffin C, Mayba OS, Tagliaferri M et al. Estrogen receptor beta binds to and regulates three distinct classes of target genes. J Biol Chem 2010; 285: 22059-22066.
39. Jamadar-Shroff V, Papich MG, Suter SE. Soy-derived isoflavones inhibit the growth of canine lymphoid cell lines. Clin Cancer Res 2009; 15: 1269-1276.
40. Villamil JA, Henry CJ, Hahn AW, Bryan JN, Tyler JW, Caldwell CW. Hormonal and sex impact on the epidemiology of canine lymphoma. J Cancer Epidemiol 2009; 2009: 591753.
41. Park BW, Kim KS, Heo MK, Ko SS, Hong SW, Yang WI et al. Expression of estrogen receptor-beta in normal mammary and tumor tissues: is it protective in breast carcinogenesis? Breast Cancer Res Treat 2003; 80: 79-85. (Pubitemid 36851287)
42. Waliszewski P, Blaszczyk M, Wolinska-Witort E, Drews M, Snochowski M, Hurst RE. Molecular study of sex steroid receptor gene expression in human colon and in colorectal carcinomas. J Surg Oncol 1997; 64: 3-11. (Pubitemid 27082000)
43. Rody A, Holtrich U, Solbach C, Kourtis K, von Minckwitz G, Engels K et al. Methylation of estrogen receptor beta promoter correlates with loss of ER-beta expression in mammary carcinoma and is an early indication marker in premalignant lesions. Endocr Relat Cancer 2005; 12: 903-916. (Pubitemid 41815784)
44. Zhao C, Lam EW, Sunters A, Enmark E, De Bella MT, Coombes RC et al. Expression of estrogen receptor beta isoforms in normal breast epithelial cells and breast cancer: regulation by methylation. Oncogene 2003; 22: 7600-7606. (Pubitemid 37464093)
45. Roger P, Sahla ME, Mäkelä S, Gustafsson JA° , Baldet P, Rochefort H. Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors. Cancer Res 2001; 61: 2537-2541. (Pubitemid 32685835)
46. Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I et al. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation. Eur J Cancer 2003; 39: 1251-1258. (Pubitemid 36579196)
47. Batistatou A, Stefanou D, Goussia A, Arkoumani E, Papavassiliou AG, Agnantis NJ. Estrogen receptor beta (ERbeta) is expressed in brain astrocytic tumors and declines with dedifferentiation of the neoplasm. J Cancer Res Clin Oncol 2004; 130: 405-410. (Pubitemid 39044343)
48. Fujimura T, Takahashi S, Urano T, Ogawa S, Ouchi Y, Kitamura T et al. Differential expression of estrogen receptor beta (ERbeta) and its C-terminal truncated splice variant ERbetacx as prognostic predictors in human prostatic cancer. Biochem Biophys Res Commun 2001; 289: 692-699. (Pubitemid 33152289)
49. Mor G, Sapi E, Abrahams VM, Rutherford T, Song J, Hao XY et al. Interaction of the estrogen receptors with the Fas ligand promoter in human monocytes. J Immunol 2003; 170: 114-122. (Pubitemid 36026130)
50. Subramanian M, Shaha C. Oestrogen modulates human macrophage apoptosis via differential signalling through oestrogen receptor-alpha and beta. J Cell Mol Med 2009; 13: 2317-2329.
51. McPherson SJ, Hussain S, Balanathan P, Hedwards SL, Niranjan B, Grant M et al. Estrogen receptor-beta activated apoptosis in benign hyperplasia and cancer of the prostate is androgen independent and TNFalpha mediated. Proc Natl Acad Sci USA 2010; 107: 3123-3128.
52. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007; 28: 521-574. (Pubitemid 47236336)
53. Cutolo M, Brizzolara R, Atzeni F, Capellino S, Straub RH, Puttini PC. The immunomodulatory effects of estrogens: clinical relevance in immune-mediated rheumatic diseases. Ann N Y Acad Sci 2010; 1193: 36-42.
54. Kalaitzidis D, Gilmore TD. Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol Metab 2005; 16: 46-52. (Pubitemid 40270849)