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Deciphering the molecular and physiological connections between obesity and breast cancer |
Zhao HE, Andy B. CHEN, Gen-Sheng FENG( ) |
| Department of Pathology, School of Medicine, and Section of Molecular Biology, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093-0864, USA |
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Abstract Obesity is associated with the higher risk of breast cancer in postmenopausal women. The leptin signaling pathway is recognized to primarily regulate energy balance and associated with breast cancer. Furthermore, the estrogen signaling pathway plays a critical role in breast carcinogenesis. In this review, we discuss how obesity is linked to breast cancer via cross-talk of leptin and estrogen pathways.
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Corresponding Author(s):
FENG Gen-Sheng,Email:gfeng@ucsd.edu
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Issue Date: 01 June 2011
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| 1 |
Antal M C, Krust A, Chambon P, Mark M (2008). Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERβ-null mutant. Proc Natl Acad Sci USA , 105(7): 2433–2438
doi: 10.1073/pnas.0712029105 pmid:18268329
|
| 2 |
Asseryanis E, Ruecklinger E, Hellan M, Kubista E, Singer C F (2004). Breast cancer size in postmenopausal women is correlated with body mass index and androgen serum levels. Gynecol Endocrinol , 18(1): 29–36
doi: 10.1080/09513590310001651759 pmid:15106362
|
| 3 |
Barash I A, Cheung C C, Weigle D S, Ren H, Kabigting E B, Kuijper J L, Clifton D K, Steiner R A (1996). Leptin is a metabolic signal to the reproductive system. Endocrinology , 137(7): 3144–3147
doi: 10.1210/en.137.7.3144 pmid:8770941
|
| 4 |
Barness L A, Opitz J M, Gilbert-Barness E (2007). Obesity: genetic, molecular, and environmental aspects. Am J Med Genet A , 143A(24): 3016–3034
doi: 10.1002/ajmg.a.32035 pmid:18000969
|
| 5 |
Binai N A, Damert A, Carra G, Steckelbroeck S, L?wer J, L?wer R, Wessler S (2010). Expression of estrogen receptor alpha increases leptin-induced STAT3 activity in breast cancer cells. Int J Cancer , 127(1): 55–66
pmid:19876927
|
| 6 |
Catalano S, Mauro L, Marsico S, Giordano C, Rizza P, Rago V, Montanaro D, Maggiolini M, Panno M L, Andó S (2004). Leptin induces, via ERK1/ERK2 signal, functional activation of estrogen receptor alpha in MCF-7 cells. J Biol Chem , 279(19): 19908–19915
doi: 10.1074/jbc.M313191200 pmid:14985328
|
| 7 |
Cave N J, Backus R C, Marks S L, Klasing K C (2007). Oestradiol, but not genistein, inhibits the rise in food intake following gonadectomy in cats, but genistein is associated with an increase in lean body mass. J Anim Physiol Anim Nutr (Berl) , 91(9-10): 400–410
doi: 10.1111/j.1439-0396.2006.00667.x pmid:17845247
|
| 8 |
Chehab F F, Lim M E, Lu R (1996). Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet , 12(3): 318–320
doi: 10.1038/ng0396-318 pmid:8589726
|
| 9 |
Cleary M P, Grande J P, Juneja S C, Maihle N J (2004a). Diet-induced obesity and mammary tumor development in MMTV-neu female mice. Nutr Cancer , 50(2): 174–180
doi: 10.1207/s15327914nc5002_7 pmid:15623464
|
| 10 |
Cleary M P, Juneja S C, Phillips F C, Hu X, Grande J P, Maihle N J (2004b). Leptin receptor-deficient MMTV-TGF-α/Lepr(db)Lepr(db) female mice do not develop oncogene-induced mammary tumors. Exp Biol Med (Maywood) , 229(2): 182–193
pmid:14734797
|
| 11 |
Cleary M P, Phillips F C, Getzin S C, Jacobson T L, Jacobson M K, Christensen T A, Juneja S C, Grande J P, Maihle N J (2003). Genetically obese MMTV-TGF-alpha/Lep(ob)Lep(ob) female mice do not develop mammary tumors. Breast Cancer Res Treat , 77(3): 205–215
doi: 10.1023/A:1021891825399 pmid:12602920
|
| 12 |
Cooke P S, Heine P A, Taylor J A, Lubahn D B (2001). The role of estrogen and estrogen receptor-alpha in male adipose tissue. Mol Cell Endocrinol , 178(1-2): 147–154
doi: 10.1016/S0303-7207(01)00414-2 pmid:11403904
|
| 13 |
Couse J F, Lindzey J, Grandien K, Gustafsson J A, Korach K S (1997). Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERα) and estrogen receptor-beta (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology , 138(11): 4613–4621 9348186
doi: 10.1210/en.138.11.4613
|
| 14 |
Dang Z, L?wik C W (2004). The balance between concurrent activation of ERs and PPARs determines daidzein-induced osteogenesis and adipogenesis. J Bone Miner Res , 19(5): 853–861
doi: 10.1359/jbmr.040120 pmid:15068509
|
| 15 |
Dieudonné M N, Leneveu M C, Giudicelli Y, Pecquery R (2004). Evidence for functional estrogen receptors α and β in human adipose cells: regional specificities and regulation by estrogens. Am J Physiol Cell Physiol , 286(3): C655–C661
doi: 10.1152/ajpcell.00321.2003 pmid:14761887
|
| 16 |
Dieudonne M N, Machinal-Quelin F, Serazin-Leroy V, Leneveu M C, Pecquery R, Giudicelli Y (2002). Leptin mediates a proliferative response in human MCF7 breast cancer cells. Biochem Biophys Res Commun , 293(1): 622–628
doi: 10.1016/S0006-291X(02)00205-X pmid:12054648
|
| 17 |
Dogan S, Hu X, Zhang Y, Maihle N J, Grande J P, Cleary M P (2007). Effects of high-fat diet and/or body weight on mammary tumor leptin and apoptosis signaling pathways in MMTV-TGF-α mice. Breast Cancer Res , 9(6): R91
doi: 10.1186/bcr1840 pmid:18162139
|
| 18 |
Donato G B, Fuchs S C, Oppermann K, Bastos C, Spritzer P M (2006). Association between menopause status and central adiposity measured at different cutoffs of waist circumference and waist-to-hip ratio. Menopause , 13(2): 280–285
doi: 10.1097/01.gme.0000177907.32634.ae pmid:16645541
|
| 19 |
Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M (2000). Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development , 127(19): 4277–4291
pmid:10976058
|
| 20 |
Farag N H, Matthews S C, Brzezinski E, Nelesen R A, Mills P J (2004). Relationship between central obesity and cardiovascular hemodynamic indices in postmenopausal women. Fertil Steril , 81(2): 465–467
doi: 10.1016/j.fertnstert.2003.08.007 pmid:14967394
|
| 21 |
Foryst-Ludwig A, Clemenz M, Hohmann S, Hartge M, Sprang C, Frost N, Krikov M, Bhanot S, Barros R, Morani A, Gustafsson J A, Unger T, Kintscher U (2008). Metabolic actions of estrogen receptor α (ERα) are mediated by a negative cross-talk with PPARγ. PLoS Genet , 4(6): e1000108
doi: 10.1371/journal.pgen.1000108 pmid:18584035
|
| 22 |
Fusco R, Galgani M, Procaccini C, Franco R, Pirozzi G, Fucci L, Laccetti P, Matarese G (2010). Cellular and molecular crosstalk between leptin receptor and estrogen receptor-α in breast cancer: molecular basis for a novel therapeutic setting. Endocr Relat Cancer , 17(2): 373–382
doi: 10.1677/ERC-09-0340 pmid:20410173
|
| 23 |
Gambino Y P, Maymó J L, Pérez-Pérez A, Due?as J L, Sánchez-Margalet V, Calvo J C, Varone C L (2010). 17β-estradiol enhances leptin expression in human placental cells through genomic and nongenomic actions. Biol Reprod , 83(1): 42–51
doi: 10.1095/biolreprod.110.083535 pmid:20237333
|
| 24 |
Gao Q, Mezei G, Nie Y, Rao Y, Choi C S, Bechmann I, Leranth C, Toran-Allerand D, Priest C A, Roberts J L, Gao X B, Mobbs C, Shulman G I, Diano S, Horvath T L (2007). Anorectic estrogen mimics leptin’s effect on the rewiring of melanocortin cells and Stat3 signaling in obese animals. Nat Med , 13(1): 89–94
doi: 10.1038/nm1525 pmid:17195839
|
| 25 |
Garofalo C, Sisci D, Surmacz E (2004). Leptin interferes with the effects of the antiestrogen ICI 182,780 in MCF-7 breast cancer cells. Clin Cancer Res , 10(19): 6466–6475
doi: 10.1158/1078-0432.CCR-04-0203 pmid:15475434
|
| 26 |
Geisler J, Haynes B, Ekse D, Dowsett M, L?nning P E (2007). Total body aromatization in postmenopausal breast cancer patients is strongly correlated to plasma leptin levels. J Steroid Biochem Mol Biol , 104(1-2): 27–34
doi: 10.1016/j.jsbmb.2006.09.040 pmid:17350249
|
| 27 |
Geisler J G, Zawalich W, Zawalich K, Lakey J R, Stukenbrok H, Milici A J, Soeller W C (2002). Estrogen can prevent or reverse obesity and diabetes in mice expressing human islet amyloid polypeptide. Diabetes , 51(7): 2158–2169
doi: 10.2337/diabetes.51.7.2158 pmid:12086946
|
| 28 |
Gonzalez R R, Cherfils S, Escobar M, Yoo J H, Carino C, Styer A K, Sullivan B T, Sakamoto H, Olawaiye A, Serikawa T, Lynch M P, Rueda B R (2006). Leptin signaling promotes the growth of mammary tumors and increases the expression of vascular endothelial growth factor (VEGF) and its receptor type two (VEGF-R2). J Biol Chem , 281(36): 26320–26328
doi: 10.1074/jbc.M601991200 pmid:16825198
|
| 29 |
Goulart A C, Zee R Y, Rexrode K M (2009). Estrogen receptor 1 gene polymorphisms and decreased risk of obesity in women. Metabolism , 58(6): 759–764
doi: 10.1016/j.metabol.2009.01.003 pmid:19375130
|
| 30 |
Grossmann M E, Nkhata K J, Mizuno N K, Ray A, Cleary M P (2008). Effects of adiponectin on breast cancer cell growth and signaling. Br J Cancer , 98(2): 370–379
doi: 10.1038/sj.bjc.6604166 pmid:18182989
|
| 31 |
Gu J M, Xiao W J, He J W, Zhang H, Hu W W, Hu Y Q, Li M, Liu Y J, Fu W Z, Yu J B, Gao G, Yue H, Ke Y H, Zhang Z L (2009). Association between VDR and ESR1 gene polymorphisms with bone and obesity phenotypes in Chinese male nuclear families. Acta Pharmacol Sin , 30(12): 1634–1642
doi: 10.1038/aps.2009.169 pmid:19960008
|
| 32 |
Han C, Zhang H T, Du L, Liu X, Jing J, Zhao X, Yang X, Tian B (2005). Serum levels of leptin, insulin, and lipids in relation to breast cancer in China. Endocrine , 26(1): 19–24
doi: 10.1385/ENDO:26:1:019 pmid:15805581
|
| 33 |
Heine P A, Taylor J A, Iwamoto G A, Lubahn D B, Cooke P S (2000). Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc Natl Acad Sci USA , 97(23): 12729–12734
doi: 10.1073/pnas.97.23.12729 pmid:11070086
|
| 34 |
Ishikawa M, Kitayama J, Nagawa H (2004). Enhanced expression of leptin and leptin receptor (OB-R) in human breast cancer. Clin Cancer Res , 10(13): 4325–4331
doi: 10.1158/1078-0432.CCR-03-0749 pmid:15240518
|
| 35 |
Jarde T, Caldefie-Chézet F, Damez M, Mishellany F, Penault-Llorca F, Guillot J, Vasson M P (2008). Leptin and leptin receptor involvement in cancer development: a study on human primary breast carcinoma. Oncol Rep , 19(4): 905–911
pmid:18357374
|
| 36 |
Jen K L, Djuric Z, DiLaura N M, Buison A, Redd J N, Maranci V, Hryniuk W M (2004). Improvement of metabolism among obese breast cancer survivors in differing weight loss regimens. Obes Res , 12(2): 306–312
doi: 10.1038/oby.2004.38 pmid:14981223
|
| 37 |
Jian W X, Yang Y J, Long J R, Li Y N, Deng F Y, Jiang D K, Deng H W (2005). Estrogen receptor α gene relationship with peak bone mass and body mass index in Chinese nuclear families. J Hum Genet , 50(9): 477–482
doi: 10.1007/s10038-005-0281-5 pmid:16160748
|
| 38 |
Jiang H, Yu J, Guo H, Song H, Chen S (2008). Upregulation of survivin by leptin/STAT3 signaling in MCF-7 cells. Biochem Biophys Res Commun , 368(1): 1–5
doi: 10.1016/j.bbrc.2007.04.004 pmid:18242580
|
| 39 |
Kim H S (2009). Leptin and leptin receptor expression in breast cancer. Cancer Res Treat , 41(3): 155–163
doi: 10.4143/crt.2009.41.3.155 pmid:19809565
|
| 40 |
Koda M, Sulkowska M, Kanczuga-Koda L, Jarzabek K, Sulkowski S (2007). Expression of leptin and its receptor in female breast cancer in relation with selected apoptotic markers. Folia Histochem Cytobiol , 45(Suppl 1): S187–S191
pmid:18292831
|
| 41 |
Kurzer M S (2002). Hormonal effects of soy in premenopausal women and men. J Nutr , 132(3): 570S–573S
pmid:11880595
|
| 42 |
Liang Y Q, Akishita M, Kim S, Ako J, Hashimoto M, Iijima K, Ohike Y, Watanabe T, Sudoh N, Toba K, Yoshizumi M, Ouchi Y (2002). Estrogen receptor beta is involved in the anorectic action of estrogen. Int J Obes Relat Metab Disord , 26(8): 1103–1109
doi: 10.1038/sj.ijo.0802054 pmid:12119576
|
| 43 |
Liu C L, Chang Y C, Cheng S P, Chern S R, Yang T L, Lee J J, Guo I C, Chen C P (2007). The roles of serum leptin concentration and polymorphism in leptin receptor gene at codon 109 in breast cancer. Oncology , 72(1-2): 75–81
doi: 10.1159/000111097 pmid:18004080
|
| 44 |
Maccio A, Madeddu C, Gramignano G, Mulas C, Floris C, Massa D, Astara G, Chessa P, Mantovani G (2010). Correlation of body mass index and leptin with tumor size and stage of disease in hormone-dependent postmenopausal breast cancer: preliminary results and therapeutic implications. J Mol Med , 88(7): 677–686
doi: 10.1007/s00109-010-0611-8 pmid:20339829
|
| 45 |
Magoffin D A, Weitsman S R, Aagarwal S K, Jakimiuk A J (1999). Leptin regulation of aromatase activity in adipose stromal cells from regularly cycling women. Ginekol Pol , 70(1): 1–7
pmid:10349800
|
| 46 |
Malik N M, Carter N D, Murray J F, Scaramuzzi R J, Wilson C A, Stock M J (2001). Leptin requirement for conception, implantation, and gestation in the mouse. Endocrinology , 142(12): 5198–5202
doi: 10.1210/en.142.12.5198 pmid:11713215
|
| 47 |
Marttunen M B, Andersson S, Hietanen P, Karonen S L, Koistinen H A, Koivisto V A, Tiitinen A, Ylikorkala O (2000). Antiestrogenic tamoxifen and toremifene increase serum leptin levels in postmenopausal breast cancer patients. Maturitas , 35(2): 175–179
doi: 10.1016/S0378-5122(00)00121-3 pmid:10924844
|
| 48 |
McMurtry V, Simeone A M, Nieves-Alicea R, Tari A M (2009). Leptin utilizes Jun N-terminal kinases to stimulate the invasion of MCF-7 breast cancer cells. Clin Exp Metastasis , 26(3): 197–204
doi: 10.1007/s10585-008-9231-x pmid:19112600
|
| 49 |
Meza-Munoz D E, Fajardo M E, Pérez-Luque E L, Malacara J M (2006). Factors associated with estrogen receptors-α (ER-α) and -β (ER-β) and progesterone receptor abundance in obese and non obese pre- and post-menopausal women. Steroids , 71(6): 498–503
doi: 10.1016/j.steroids.2006.01.011 pmid:16566954
|
| 50 |
Miyoshi Y, Funahashi T, Tanaka S, Taguchi T, Tamaki Y, Shimomura I, Noguchi S (2006). High expression of leptin receptor mRNA in breast cancer tissue predicts poor prognosis for patients with high, but not low, serum leptin levels. Int J Cancer , 118(6): 1414–1419
doi: 10.1002/ijc.21543 pmid:16206269
|
| 51 |
Mounzih K, Lu R, Chehab F F (1997). Leptin treatment rescues the sterility of genetically obese ob/ob males. Endocrinology , 138(3): 1190–1193
doi: 10.1210/en.138.3.1190 pmid:9048626
|
| 52 |
Musatov S, Chen W, Pfaff D W, Mobbs C V, Yang X J, Clegg D J, Kaplitt M G, Ogawa S (2007). Silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA , 104(7): 2501–2506
doi: 10.1073/pnas.0610787104 pmid:17284595
|
| 53 |
Naaz A, Zakroczymski M, Heine P, Taylor J, Saunders P, Lubahn D, Cooke P S (2002). Effect of ovariectomy on adipose tissue of mice in the absence of estrogen receptor alpha (ERα): a potential role for estrogen receptor beta (ERβ). Horm Metab Res , 34(11-12): 758–763
doi: 10.1055/s-2002-38259 pmid:12660895
|
| 54 |
Nilsson M, Dahlman I, Rydén M, Nordstr?m E A, Gustafsson J A, Arner P, Dahlman-Wright K (2007). Oestrogen receptor α gene expression levels are reduced in obese compared to normal weight females. Int J Obes (Lond) , 31(6): 900–907
doi: 10.1038/sj.ijo.0803528 pmid:17224934
|
| 55 |
Nkhata K J, Ray A, Dogan S, Grande J P, Cleary M P (2009a). Mammary tumor development from T47-D human breast cancer cells in obese ovariectomized mice with and without estradiol supplements. Breast Cancer Res Treat , 114(1): 71–83
doi: 10.1007/s10549-008-9991-7 pmid:18392696
|
| 56 |
Nkhata K J, Ray A, Schuster T F, Grossmann M E, Cleary M P (2009b). Effects of adiponectin and leptin co-treatment on human breast cancer cell growth. Oncol Rep , 21(6): 1611–1619
pmid:19424644
|
| 57 |
Ohlsson C, Hellberg N, Parini P, Vidal O, Bohlooly-Y M, Rudling M, Lindberg M K, Warner M, Angelin B, Gustafsson J A (2000). Obesity and disturbed lipoprotein profile in estrogen receptor-α-deficient male mice. Biochem Biophys Res Commun , 278(3): 640–645
doi: 10.1006/bbrc.2000.3827 pmid:11095962
|
| 58 |
Okazaki R, Inoue D, Shibata M, Saika M, Kido S, Ooka H, Tomiyama H, Sakamoto Y, Matsumoto T (2002). Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) α or β. Endocrinology , 143(6): 2349–2356
doi: 10.1210/en.143.6.2349 pmid:12021200
|
| 59 |
Okumura M, Yamamoto M, Sakuma H, Kojima T, Maruyama T, Jamali M, Cooper D R, Yasuda K (2002). Leptin and high glucose stimulate cell proliferation in MCF-7 human breast cancer cells: reciprocal involvement of PKC-α and PPAR expression. Biochim Biophys Acta , 1592(2): 107–116
pmid:12379472
|
| 60 |
Okura T, Koda M, Ando F, Niino N, Ohta S, Shimokata H (2003). Association of polymorphisms in the estrogen receptor α gene with body fat distribution. Int J Obes Relat Metab Disord , 27(9): 1020–1027
doi: 10.1038/sj.ijo.0802378 pmid:12917706
|
| 61 |
Ozet A, Arpaci F, Yilmaz M I, Ayta H, Ozturk B, Komurcu S, Yavuz A A, Tezcan Y, Acikel C (2001). Effects of tamoxifen on the serum leptin level in patients with breast cancer. Jpn J Clin Oncol , 31(9): 424–427
doi: 10.1093/jjco/hye097 pmid:11689595
|
| 62 |
Percik R, Stumvoll M (2009). Obesity and cancer. Exp Clin Endocrinol Diabetes , 117(10): 563–566
doi: 10.1055/s-0029-1241870 pmid:19924603
|
| 63 |
Perera C N, Chin H G, Duru N, Camarillo I G (2008). Leptin-regulated gene expression in MCF-7 breast cancer cells: mechanistic insights into leptin-regulated mammary tumor growth and progression. J Endocrinol , 199(2): 221–233
doi: 10.1677/JOE-08-0215 pmid:18715880
|
| 64 |
Picó C, Puigserver P, Oliver P, Palou A (1998). 2-Methoxyestradiol, an endogenous metabolite of 17beta-estradiol, inhibits adipocyte proliferation. Mol Cell Biochem , 189(1-2): 1–7
doi: 10.1023/A:1006835124149 pmid:9879647
|
| 65 |
Pischon T, N?thlings U, Boeing H (2008). Obesity and cancer. Proc Nutr Soc , 67(2): 128–145
doi: 10.1017/S0029665108006976 pmid:18412987
|
| 66 |
Qiu J, Ogus S, Mounzih K, Ewart-Toland A, Chehab F F (2001). Leptin-deficient mice backcrossed to the BALB/cJ genetic background have reduced adiposity, enhanced fertility, normal body temperature, and severe diabetes. Endocrinology , 142(8): 3421–3425
doi: 10.1210/en.142.8.3421 pmid:11459786
|
| 67 |
Ray A, Nkhata K J, Cleary M P (2007). Effects of leptin on human breast cancer cell lines in relationship to estrogen receptor and HER2 status. Int J Oncol , 30(6): 1499–1509
pmid:17487372
|
| 68 |
Revillion F, Charlier M, Lhotellier V, Hornez L, Giard S, Baranzelli M C, Djiane J, Peyrat J P (2006). Messenger RNA expression of leptin and leptin receptors and their prognostic value in 322 human primary breast cancers. Clin Cancer Res , 12(7 Pt 1): 2088–2094
doi: 10.1158/1078-0432.CCR-05-1904 pmid:16609020
|
| 69 |
Saxena N K, Taliaferro-Smith L, Knight B B, Merlin D, Anania F A, O’Regan R M, Sharma D (2008). Bidirectional crosstalk between leptin and insulin-like growth factor-I signaling promotes invasion and migration of breast cancer cells via transactivation of epidermal growth factor receptor. Cancer Res , 68(23): 9712–9722
doi: 10.1158/0008-5472.CAN-08-1952 pmid:19047149
|
| 70 |
Saxena N K, Vertino P M, Anania F A, Sharma D (2007). leptin-induced growth stimulation of breast cancer cells involves recruitment of histone acetyltransferases and mediator complex to CYCLIN D1 promoter via activation of Stat3. J Biol Chem , 282(18): 13316–13325
doi: 10.1074/jbc.M609798200 pmid:17344214
|
| 71 |
Snoussi K, Strosberg A D, Bouaouina N, Ben Ahmed S, Helal A N, Chouchane L (2006). Leptin and leptin receptor polymorphisms are associated with increased risk and poor prognosis of breast carcinoma. BMC Cancer , 6(1): 38
doi: 10.1186/1471-2407-6-38 pmid:16504019
|
| 72 |
Tagawa N, Yuda R, Kubota S, Wakabayashi M, Yamaguchi Y, Kiyonaga D, Mori N, Minamitani E, Masuzaki H, Kobayashi Y (2009). 17Beta-estradiol inhibits 11β-hydroxysteroid dehydrogenase type 1 activity in rodent adipocytes. J Endocrinol , 202(1): 131–139
doi: 10.1677/JOE-09-0021 pmid:19380458
|
| 73 |
Tchernof A, Poehlman E T, Després J P (2000). Body fat distribution, the menopause transition, and hormone replacement therapy. Diabetes Metab , 26(1): 12–20
pmid:10705099
|
| 74 |
Tessitore L, Vizio B, Pesola D, Cecchini F, Mussa A, Argiles J M, Benedetto C (2004). Adipocyte expression and circulating levels of leptin increase in both gynaecological and breast cancer patients. Int J Oncol , 24(6): 1529–1535
pmid:15138597
|
| 75 |
Ueki S, Oguma M, Usami A, Kamada Y, Kato H, Kamada R, Takeda M, Ito W, Tanigai T, Kayaba H, Chihara J (2009). Regulation of peroxisome proliferator-activated receptor-γ expression in human eosinophils by estradiol. Int Arch Allergy Immunol , 149(Suppl 1): 51–56
doi: 10.1159/000210654 pmid:19494505
|
| 76 |
Yin N, Wang D, Zhang H, Yi X, Sun X, Shi B, Wu H, Wu G, Wang X, Shang Y (2004). Molecular mechanisms involved in the growth stimulation of breast cancer cells by leptin. Cancer Res , 64(16): 5870–5875
doi: 10.1158/0008-5472.CAN-04-0655 pmid:15313931
|
| 77 |
Yu W, Gu J C, Liu J Z, Wang S H, Wang Y, Zhang Z T, Ma X M, Song M M (2010). Regulation of estrogen receptors α and β in human breast carcinoma by exogenous leptin in nude mouse xenograft model. Chin Med J (Engl) , 123(3): 337–343
pmid:20193256
|
| 78 |
Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman J M (1994). Positional cloning of the mouse obese gene and its human homologue. Nature , 372(6505): 425–432
doi: 10.1038/372425a0 pmid:7984236
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