Sex-specific lung diseases: Effect of oestrogen on cultured cells and in animal models

European Respiratory Review

Volumn 22, Issue 129, 2013, Pages 302-311

  Shim, Bosung ^a   Pacheco Rodriguez, Gustavo ^a   Kato, Jiro ^a   Darling, Thomas N ^b   Vaughan, Martha ^a   Moss, Joel ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b Uniformed Services University of the Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANASTROZOLE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; EXEMESTANE; FULVESTRANT; LETROZOLE; RALOXIFENE; RAPAMYCIN; TAMOXIFEN; TOREMIFENE;

BENIGN METASTASISING LEIOMYOMA; CELL CULTURE; DRUG MECHANISM; ESTROGEN METABOLISM; EXPERIMENTAL ANIMAL; HUMAN; LEIOMYOMA; LIVER HEMANGIOMA; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; LUNG DISEASE; LUNG FIBROSIS; LYMPHANGIOLEIOMYOMATOSIS; NONHUMAN; PREVALENCE; REVIEW; RISK FACTOR; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ESTRADIOL; FEMALE; HUMANS; LUNG; LUNG DISEASES; MALE; PREVALENCE; SEX DISTRIBUTION; SEX FACTORS; SIGNAL TRANSDUCTION;

EID: 84883373329     PISSN: 09059180     EISSN: 16000617     Source Type: Journal    
DOI: 10.1183/09059180.00002813     Document Type: Review

References (129)

1. Ryu JH, Moss J, Beck GJ, et al. The NHLBI lymphangioleiomyomatosis registry: characteristics of 230 patients at enrollment. Am J Respir Crit Care Med 2006; 173: 105-111.
2. Pitts S, Oberstein EM, Glassberg MK. Benign metastasizing leiomyoma and lymphangioleiomyomatosis: sexspecific diseases? Clin Chest Med 2004; 25: 343-360.
3. Muscat JE, Wynder EL. Lung cancer pathology in smokers, ex-smokers and never smokers. Cancer Lett 1995; 88: 1-5.
4. Badesch DB, Raskob GE, Elliott CG, et al. Pulmonary arterial hypertension: baseline characteristics from the REVEAL Registry. Chest 2010; 137: 376-387.
5. Cottin V, Cordier JF. Combined pulmonary fibrosis and emphysema in connective tissue disease. Curr Opin Pulm Med 2012; 18: 418-427.
6. Gribbin J, Hubbard RB,Lle Jeune I, et al. Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax 2006; 61: 980-985.
7. Baumgartner KB, Samet JM, Stidley CA, et al. Cigarette smoking: a risk factor for idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 1997; 155: 242-248.
8. Kornum JB, Christensen S, Grijota M, et al. The incidence of interstitial lung disease 1995-2005: a Danish nationwide population-based study. BMC Pulm Med 2008; 8: 24.
9. Coultas DB, Zumwalt RE, Black WC, et al. The epidemiology of interstitial lung diseases. Am J Respir Crit Care Med 1994; 150: 967-972.
10. Vassallo R, Ryu JH, Schroeder DR, et al. Clinical outcomes of pulmonary Langerhans'-cell histiocytosis in adults. N Engl J Med 2002; 346: 484-490.
11. Travis WD, Hunninghake G, King TE Jr, et al. Idiopathic nonspecific interstitial pneumonia: report of an American Thoracic Society project. Am J Respir Crit Care Med 2008; 177: 1338-1347.
12. Portnoy J, Veraldi KL, Schwarz MI, et al. Respiratory bronchiolitis-interstitial lung disease: long-term outcome. Chest 2007; 131: 664-671.
13. de Marco R, Locatelli F, Sunyer J, et al. Differences in incidence of reported asthma related to age in men and women. A retrospective analysis of the data of the European Respiratory Health Survey. Am J Respir Crit Care Med 2000; 162: 68-74.
14. Choi IS. Gender-specific asthma treatment. Allergy Asthma Imunol Res 2011; 3: 74-80.
15. Leynaert B, Sunyer J, Garcia-Esteban R, et al. Gender differences in prevalence, diagnosis and incidence of allergic and non-allergic asthma: a population-based cohort. Thorax 2012; 67: 625-631.
16. Akinbami LJ, Liu X. Chronic obstructive pulmonary disease among adults aged 18 and over in the United States, 1998-2009. NCHS Data Brief 2011; 1-8.
17. Aryal S, Diaz-Guzman E, Mannino DM. COPD and gender differences: an update. Transl Res 2013 [Epub ahead of print DOI: 10.1016/j.trsl.2013.04.003].
18. Cote CG, Chapman KR. Diagnosis and treatment considerations for women with COPD. Int J Clin Pract 2009; 63: 486-493.
19. Townsend EA, Miller VM, Prakash YS. Sex differences and sex steroids in lung health and disease. Endocr Rev 2012; 33: 1-47.
20. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
21. Schiavina M, Di Scioscio V, Contini P, et al. Pulmonary lymphangioleiomyomatosis in a karyotypically normal man without tuberous sclerosis complex. Am J Respir Crit Care Med 2007; 176: 96-98.
22. Ryu JH, Sykes AM, Lee AS, et al. Cystic lung disease is not uncommon in men with tuberous sclerosis complex. Respir Med 2012; 106: 1586-1590.
23. Henderson BE, Feigelson HS. Hormonal carcinogenesis. Carcinogenesis 2000; 21: 427-433.
24. Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest 2006; 116: 561-570.
25. Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev 2011; 32: 81-151.
26. Di Nardo G, Gilardi G. Human aromatase: perspectives in biochemistry and biotechnology. Biotechnol Appl Biochem 2013; 60: 92-101.
27. Simpson ER, Mahendroo MS, Means GD, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 1994; 15: 342-355.
28. Ghosh D, Griswold J, Erman M, et al. Structural basis for androgen specificity and oestrogen synthesis in human aromatase. Nature 2009; 457: 219-223.
29. Parl FF, Dawling S, Roodi N, et al. Estrogen metabolism and breast cancer: a risk model. Ann N Y Acad Sci 2009; 1155: 68-75.
30. Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 2001; 276: 36869-36872.
31. Losel R, Wehling M. Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 2003; 4: 46-56.
32. Mueller MD, Vigne JL, Minchenko A, et al. Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci USA 2000; 97: 10972-10977.
33. Stoner M, Wormke M, Saville B, et al. Estrogen regulation of vascular endothelial growth factor gene expression in ZR-75 breast cancer cells through interaction of estrogen receptor alpha and SP proteins. Oncogene 2004; 23: 1052-1063.
34. Pedram A, Razandi M, Aitkenhead M, et al. Integration of the non-genomic and genomic actions of estrogen. Membrane-initiated signaling by steroid to transcription and cell biology. J Biol Chem 2002; 277: 50768-50775.
35. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol 2007; 25: 561-570.
36. Travis WD, Travis LB, Devesa SS. Lung cancer. Cancer 1995; 75: 191-202.
37. Wakelee HA, Chang ET, Gomez SL, et al. Lung cancer incidence in never smokers. J Clin Oncol 2007; 25: 472-478.
38. Jemal A, Ward E, Thun M. Declining death rates reflect progress against cancer. PLoS One 2010; 5: e9584.
39. Taioli E, Wynder EL. Re: Endocrine factors and adenocarcinoma of the lung in women. J Natl Cancer Inst 1994; 86: 869-870.
40. Marquez-Garban DC, Chen HW, Goodglick L, et al. Targeting aromatase and estrogen signaling in human nonsmall cell lung cancer. Ann N Y Acad Sci 2009; 1155: 194-205.
41. Weinberg OK, Marquez-Garban DC, Fishbein MC, et al. Aromatase inhibitors in human lung cancer therapy. Cancer Res 2005; 65: 11287-11291.
42. Stabile LP, Davis AL, Gubish CT, et al. Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor alpha and beta and show biological responses to estrogen. Cancer Res 2002; 62: 2141-2150.
43. Mah V, Seligson DB, Li A, et al. Aromatase expression predicts survival in women with early-stage non small cell lung cancer. Cancer Res 2007; 67: 10484-10490.
44. Beattie CW, Hansen NW, Thomas PA. Steroid receptors in human lung cancer. Cancer Res 1985; 45: 4206-4214.
45. Marquez-Garban DC, Mah V, Alavi M, et al. Progesterone and estrogen receptor expression and activity in human non-small cell lung cancer. Steroids 2011; 76: 910-920.
46. Mollerup S, Jorgensen K, Berge G, et al. Expression of estrogen receptors alpha and beta in human lung tissue and cell lines. Lung Cancer 2002; 37: 153-159.
47. Niikawa H, Suzuki T, Miki Y, et al. Intratumoral estrogens and estrogen receptors in human non-small cell lung carcinoma. Clin Cancer Res 2008; 14: 4417-4426.
48. Pietras RJ, Marquez DC, Chen HW, et al. Estrogen and growth factor receptor interactions in human breast and non-small cell lung cancer cells. Steroids 2005; 70: 372-381.
49. Stabile LP, Dacic S, Land SR, et al. Combined analysis of estrogen receptor beta-1 and progesterone receptor expression identifies lung cancer patients with poor outcome. Clin Cancer Res 2011; 17: 154-164.
50. Gruber CJ, TschugguelW, Schneeberger C, et al. Production and actions of estrogens. N Engl JMed 2002; 346: 340-352.
51. Kawai H, Ishii A, Washiya K, et al. Combined overexpression of EGFR and estrogen receptor alpha correlates with a poor outcome in lung cancer. Anticancer Res 2005; 25: 4693-4698.
52. Schwartz AG, Prysak GM, Murphy V, et al. Nuclear estrogen receptor beta in lung cancer: expression and survival differences by sex. Clin Cancer Res 2005; 11: 7280-7287.
53. Skov BG, Fischer BM, Pappot H. Oestrogen receptor beta over expression in males with non-small cell lung cancer is associated with better survival. Lung Cancer 2008; 59: 88-94.
54. Wu CT, Chang YL, Shih JY, et al. The significance of estrogen receptor beta in 301 surgically treated non-small cell lung cancers. J Thorac Cardiovasc Surg 2005; 130: 979-986.
55. Dougherty SM, Mazhawidza W, Bohn AR, et al. Gender difference in the activity but not expression of estrogen receptors alpha and beta in human lung adenocarcinoma cells. Endocr Relat Cancer 2006; 13: 113-134.
56. Hershberger PA, Vasquez AC, Kanterewicz B, et al. Regulation of endogenous gene expression in human non-small cell lung cancer cells by estrogen receptor ligands. Cancer Res 2005; 65: 1598-1605.
57. Kato S, Endoh H, Masuhiro Y, et al. Activation of the estrogen receptor through phosphorylation by mitogenactivated protein kinase. Science 1995; 270: 1491-1494.
58. Stabile LP, Lyker JS, Gubish CT, et al. Combined targeting of the estrogen receptor and the epidermal growth factor receptor in non-small cell lung cancer shows enhanced antiproliferative effects. Cancer Res 2005; 65: 1459-1470.
59. Marquez-Garban DC, Chen HW, Fishbein MC, et al. Estrogen receptor signaling pathways in human non-small cell lung cancer. Steroids 2007; 72: 135-143.
60. Stabile LP, Siegfried JM. Estrogen receptor pathways in lung cancer. Curr Oncol Rep 2004; 6: 259-267.
61. Jarzynka MJ, Guo P, Bar-Joseph I, et al. Estradiol and nicotine exposure enhances A549 bronchioloalveolar carcinoma xenograft growth in mice through the stimulation of angiogenesis. Int J Oncol 2006; 28: 337-344.
62. Hammoud Z, Tan B, Badve S, et al. Estrogen promotes tumor progression in a genetically defined mouse model of lung adenocarcinoma. Endocr Relat Cancer 2008; 15: 475-483.
63. Zheng S, El-Naggar AK, Kim ES, et al. A genetic mouse model for metastatic lung cancer with gender differences in survival. Oncogene 2007; 26: 6896-6904.
64. Banka CL, Lund CV, Nguyen MT, et al. Estrogen induces lung metastasis through a host compartment-specific response. Cancer Res 2006; 66: 3667-3672.
65. Wang XY, Wang Y, Liu HC. Tamoxifen lowers the MMP-9/TIMP-1 ratio and inhibits the invasion capacity of ERpositive non-small cell lung cancer cells. Biomed Pharmacother 2011; 65: 525-528.
66. Kato J, Zhu J, Liu C, et al. ADP-ribosylarginine hydrolase regulates cell proliferation and tumorigenesis. Cancer Res 2011; 71: 5327-5335.
67. Moss J, Vaughan M, eds. ADP-ribosylating Toxins and G Proteins: Insights into Signal Transduction. Washington, American Society for Microbiology Press, 1990.
68. Williamson KC, Moss J. Mono-ADP-ribosyltransferases and ADP-ribosylarginine hydrolase: a mono-ADPribosylation cycle in animal cells. In: Moss J, Vaughan M, eds. ADP-ribosylating Toxins and G Proteins: Insights into Signal Transduction. Washington, American Society for Microbiology Press, 1990; pp. 493-510.
69. Okazaki IJ, Moss J. Glycosylphosphatidylinositol-anchored and secretory isoforms of mono-ADP-ribosyltransferases. J Biol Chem 1998; 273: 23617-23620.
70. Okazaki IJ, Moss J. Characterization of glycosylphosphatidylinositiol-anchored, secreted, and intracellular vertebrate mono-ADP-ribosyltransferases. Annu Rev Nutr 1999; 19: 485-509.
71. Zolkiewska A, Moss J. Integrin alpha 7 as substrate for a glycosylphosphatidylinositol-anchored ADPribosyltransferase on the surface of skeletal muscle cells. J Biol Chem 1993; 268: 25273-25276.
72. Oka S, Kato J, Moss J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem 2006; 281: 705-713.
73. Ono T, Kasamatsu A, Oka S, et al. The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADPribose, a product of the Sir2 family of acetyl-histone deacetylases. Proc Natl Acad Sci USA 2006; 103: 16687-16691.
74. Kasamatsu A, Nakao M, Smith BC, et al. Hydrolysis of O-acetyl-ADP-ribose isomers by ADP-ribosylhydrolase 3. J Biol Chem 2011; 286: 21110-21117.
75. Moss J, Jacobson MK, Stanley SJ. Reversibility of arginine-specific mono(ADP-ribosyl)ation: identification in erythrocytes of an ADP-ribose-L-arginine cleavage enzyme. Proc Natl Acad Sci USA 1985; 82: 5603-5607.
76. Moss J, Stanley SJ, Nightingale MS, et al. Molecular and immunological characterization of ADP-ribosylarginine hydrolases. J Biol Chem 1992; 267: 10481-10488.
77. Kitaichi M, Nishimura K, Itoh H, et al. Pulmonary lymphangioleiomyomatosis: a report of 46 patients including a clinicopathologic study of prognostic factors. Am J Respir Crit Care Med 1995; 151: 527-533.
78. Chu SC, Horiba K, Usuki J, et al. Comprehensive evaluation of 35 patients with lymphangioleiomyomatosis. Chest 1999; 115: 1041-1052.
79. Urban T, Lazor R, Lacronique J, et al. Pulmonary lymphangioleiomyomatosis. A study of 69 patients. Groupe d'Etudes et de Recherche sur les Maladies "Orphelines" Pulmonaires (GERM"O"P). Medicine (Baltimore) 1999; 78: 321-337.
80. Johnson SR, Tattersfield AE. Clinical experience of lymphangioleiomyomatosis in the UK. Thorax 2000; 55: 1052-1057.
81. Taveira-Da Silva AM, Pacheco-Rodriguez G, Moss J. The natural history of lymphangioleiomyomatosis: markers of severity, rate of progression and prognosis. Lymphat Res Biol 2010; 8: 9-19.
82. Costello LC, Hartman TE, Ryu JH. High frequency of pulmonary lymphangioleiomyomatosis in women with tuberous sclerosis complex. Mayo Clin Proc 2000; 75: 591-594.
83. Crino PB, Nathanson KL, Henske EP. The tuberous sclerosis complex. N Engl J Med 2006; 355: 1345-1356.
84. Huang J, Manning BD. The TSC1-TSC2 complex: a molecular switchboard controlling cell growth. Biochem J 2008; 412: 179-190.
85. Goncharova EA, Goncharov DA, Eszterhas A, et al. Tuberin regulates p70 S6 kinase activation and ribosomal protein S6 phosphorylation. A role for the TSC2 tumor suppressor gene in pulmonary lymphangioleiomyomatosis (LAM). J Biol Chem 2002; 277: 30958-30967.
86. Ruvinsky I, Sharon N, Lerer T, et al. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 2005; 19: 2199-2211.
87. Fingar DC, Salama S, Tsou C, et al. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 2002; 16: 1472-1487.
88. Sabatini DM. mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 2006; 6: 729-734.
89. Kayser K, Zink S, Schneider T, et al. Benign metastasizing leiomyoma of the uterus: documentation of clinical, immunohistochemical and lectin-histochemical data of ten cases. Virchows Arch 2000; 437: 284-292.
90. Esteban JM, Allen WM, Schaerf RH. Benign metastasizing leiomyoma of the uterus: histologic and immunohistochemical characterization of primary and metastatic lesions. Arch Pathol Lab Med 1999; 123: 960-962.
91. Henske EP, McCormack FX. Lymphangioleiomyomatosis-a wolf in sheep's clothing. J Clin Invest 2012; 122: 3807-3816.
92. Crooks DM, Pacheco-Rodriguez G, De Castro RM, et al. Molecular and genetic analysis of disseminated neoplastic cells in lymphangioleiomyomatosis. Proc Natl Acad Sci USA 2004; 101: 17462-17467.
93. Darling TN, Pacheco-Rodriguez G, Gorio A, et al. Lymphangioleiomyomatosis and TSC2-/-cells. Lymphat Res Biol 2010; 8: 59-69.
94. Taveira-Da Silva AM, Alford CE, Levens ED, et al. Favorable response to antigonadal therapy for a benign metastasizing leiomyoma. Obstet Gynecol 2012; 119: 438-442.
95. Banner AS, Carrington CB, Emory WB, et al. Efficacy of oophorectomy in lymphangioleiomyomatosis and benign metastasizing leiomyoma. N Engl J Med 1981; 305: 204-209.
96. Lewis EI, Chason RJ, Decherney AH, et al. Novel hormone treatment of benign metastasizing leiomyoma: an analysis of five cases and literature review. Fertil Steril 2013; 99: 2017-2024.
97. Logginidou H, Ao X, Russo I, et al. Frequent estrogen and progesterone receptor immunoreactivity in renal angiomyolipomas from women with pulmonary lymphangioleiomyomatosis. Chest 2000; 117: 25-30.
98. Patton KT, Cheng L, Papavero V, et al. Benign metastasizing leiomyoma: clonality, telomere length and clinicopathologic analysis. Mod Pathol 2006; 19: 130-140.
99. Jautzke G, Muller-Ruchholtz E, Thalmann U. Immunohistological detection of estrogen and progesterone receptors in multiple and well differentiated leiomyomatous lung tumors in women with uterine leiomyomas (so-called benign metastasizing leiomyomas). A report on 5 cases. Pathol Res Pract 1996; 192: 215-223.
100. Yoon G, Kim TJ, Sung CO, et al. Benign metastasizing leiomyoma with multiple lymph node metastasis: a case report. Cancer Res Treat 2011; 43: 131-133.
101. Maurer RA. Estradiol regulates the transcription of the prolactin gene. J Biol Chem 1982; 257: 2133-2136.
102. Terasaki Y, Yahiro K, Pacheco-Rodriguez G, et al. Effects of prolactin on TSC2-null Eker rat cells and in pulmonary lymphangioleiomyomatosis. Am J Respir Crit Care Med 2010; 182: 531-539.
103. Howe SR, Gottardis MM, Everitt JI, et al. Estrogen stimulation and tamoxifen inhibition of leiomyoma cell growth in vitro and in vivo. Endocrinology 1995; 136: 4996-5003.
104. Yu J, Astrinidis A, Howard S, et al. Estradiol and tamoxifen stimulate LAM-associated angiomyolipoma cell growth and activate both genomic and nongenomic signaling pathways. Am J Physiol Lung Cell Mol Physiol 2004; 286: L694-L700.
105. Yu JJ, Robb VA, Morrison TA, et al. Estrogen promotes the survival and pulmonary metastasis of tuberin-null cells. Proc Natl Acad Sci USA 2009; 106: 2635-2640.
106. Hodges LC, Hunter DS, Bergerson JS, et al. An in vivo/in vitro model to assess endocrine disrupting activity of xenoestrogens in uterine leiomyoma. Ann N Y Acad Sci 2001; 948: 100-111.
107. Hunter DS, Hodges LC, Eagon PK, et al. Influence of exogenous estrogen receptor ligands on uterine leiomyoma: evidence from an in vitro/in vivo animal model for uterine fibroids. Environ Health Perspect 2000; 108: Suppl. 5 829-834
108. Liu F, Lunsford EP, Tong J, et al. Real-time monitoring of tumorigenesis, dissemination, and drug response in a preclinical model of lymphangioleiomyomatosis/tuberous sclerosis complex. PLoS One 2012; 7: e38589.
109. Clements D, Asprey SL, McCulloch TA, et al. Analysis of the oestrogen response in an angiomyolipoma derived xenograft model. Endocr Relat Cancer 2009; 16: 59-72.
110. Astrinidis A, Cash TP, Hunter DS, et al. Tuberin, the tuberous sclerosis complex 2 tumor suppressor gene product, regulates Rho activation, cell adhesion and migration. Oncogene 2002; 21: 8470-8476.
111. Lamb RF, Roy C, Diefenbach TJ, et al. The TSC1 tumour suppressor hamartin regulates cell adhesion through ERM proteins and the GTPase Rho. Nat Cell Biol 2000; 2: 281-287.
112. Glassberg MK, Elliot SJ, Fritz J, et al. Activation of the estrogen receptor contributes to the progression of pulmonary lymphangioleiomyomatosis via matrix metalloproteinase-induced cell invasiveness. J Clin Endocrinol Metab 2008; 93: 1625-1633.
113. Matsui K, Takeda K, Yu ZX, et al. Role for activation of matrix metalloproteinases in the pathogenesis of pulmonary lymphangioleiomyomatosis. Arch Pathol Lab Med 2000; 124: 267-275.
114. Seyama K, Kumasaka T, Kurihara M, et al. Lymphangioleiomyomatosis: a disease involving the lymphatic system. Lymphat Res Biol 2010; 8: 21-31.
115. Glasgow CG, El-Chemaly S, Moss J. Lymphatics in lymphangioleiomyomatosis and idiopathic pulmonary fibrosis. Eur Respir Rev 2012; 21: 196-206.
116. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008; 294: L152-L160.
117. Gharaee-Kermani M, Hatano K, Nozaki Y, et al. Gender-based differences in bleomycin-induced pulmonary fibrosis. Am J Pathol 2005; 166: 1593-1606.
118. Tofovic SP, Zhang X, Jackson EK, et al. 2-methoxyestradiol attenuates bleomycin-induced pulmonary hypertension and fibrosis in estrogen-deficient rats. Vascul Pharmacol 2009; 51: 190-197.
119. Haston CK, Wang M, Dejournett RE, et al. Bleomycin hydrolase and a genetic locus within the MHC affect risk for pulmonary fibrosis in mice. Hum Mol Genet 2002; 11: 1855-1863.
120. Voltz JW, Card JW, Carey MA, et al. Male sex hormones exacerbate lung function impairment after bleomycininduced pulmonary fibrosis. Am J Respir Cell Mol Biol 2008; 39: 45-52.
121. Brass DM, McGee SP, Dunkel MK, et al. Gender influences the response to experimental silica-induced lung fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2010; 299: L664-L671.
122. Lekgabe ED, Royce SG, Hewitson TD, et al. The effects of relaxin and estrogen deficiency on collagen deposition and hypertrophy of nonreproductive organs. Endocrinology 2006; 147: 5575-5583.
123. Lipton A, Demers LM, Harvey HA, et al. Letrozole (CGS 20267). A phase I study of a new potent oral aromatase inhibitor of breast cancer. Cancer 1995; 75: 2132-2318.
124. Shang Y. Molecular mechanisms of oestrogen and SERMs in endometrial carcinogenesis. Nat Rev Cancer 2006; 6: 360-368.
125. Shen H, Yuan Y, Sun J, et al. Combined tamoxifen and gefitinib in non-small cell lung cancer shows antiproliferative effects. Biomed Pharmacother 2010; 64: 88-92.
126. Bissler JJ, McCormack FX, Young LR, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med 2008; 358: 140-151.
127. Glasgow CG, Steagall WK, Taveira-Dasilva A, et al. Lymphangioleiomyomatosis (LAM): molecular insights lead to targeted therapies. Respir Med 2010; 104: Suppl. 1 S45-S58.
128. El-Hashemite N, Walker V, Kwiatkowski DJ. Estrogen enhances whereas tamoxifen retards development of Tsc mouse liver hemangioma: a tumor related to renal angiomyolipoma and pulmonary lymphangioleiomyomatosis. Cancer Res 2005; 65: 2474-2481.
129. Li C, Zhou X, Sun Y, et al. Faslodex inhibits estradiol-induced ECM dynamics and lung metastasis in a model of LAM. Am J Respir Cell Mol Biol 2013; 49: 132-142.