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International Journal of Endocrinology
Volume 2017, Article ID 8475701, 13 pages
https://doi.org/10.1155/2017/8475701
Review Article

Gender, Estrogen, and Obliterative Lesions in the Lung

Department of Environmental & Occupational Health, Florida International University, Miami, FL, USA

Correspondence should be addressed to Quentin Felty; ude.uif@qytlef

Received 21 November 2016; Revised 20 February 2017; Accepted 7 March 2017; Published 2 April 2017

Academic Editor: Mario Maggi

Copyright © 2017 Hamza Assaggaf and Quentin Felty. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Tam, D. Morrish, S. Wadsworth, D. Dorscheid, S. F. Man, and D. D. Sin, “The role of female hormones on lung function in chronic lung diseases,” BMC Womens Health, vol. 11, no. 1, p. 24, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Rossouw, “Coronary heart disease in menopausal women: implications of primary and secondary prevention trials of hormones,” Maturitas, vol. 51, no. 1, pp. 51–63, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. The Coronary Drug Project, “Initial findings leading to modifications of its research protocol,” JAMA, vol. 214, no. 7, pp. 1303–1313, 1970. View at Google Scholar
  4. The Coronary Drug Project, “Findings leading to discontinuation of the 2.5-mg/day estrogen group,” JAMA, vol. 226, no. 6, pp. 652–657, 1973. View at Google Scholar
  5. E. P. Benditt and J. M. Benditt, “Evidence for a monoclonal origin of human atherosclerotic plaques,” Proceedings of the National Academy of Sciences of the United States of America, vol. 70, no. 4, pp. 1753–1756, 1973. View at Google Scholar
  6. Q. Felty, K. P. Singh, and D. Roy, “Estrogen-induced G(1)/S transition of G(0)-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling,” Oncogene, vol. 24, no. 31, pp. 4883–4893, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. Q. Felty, W. C. Xiong, D. Sun et al., “Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers,” Biochemistry, vol. 44, no. 18, pp. 6900–6909, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. Q. Felty and D. Roy, “Estrogen, mitochondria, and growth of cancer and non-cancer cells,” Journal of Carcinogenesis, vol. 4, no. 1, p. 1, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. G. F. Konings, N. L. Reynaert, B. Delvoux et al., “Increased levels of enzymes involved in local estradiol synthesis in chronic obstructive pulmonary disease,” Molecular and Cellular Endocrinology, vol. 443, pp. 23–31, 2017. View at Publisher · View at Google Scholar
  10. J. Parkash, Q. Felty, and D. Roy, “Estrogen exerts a spatial and temporal influence on reactive oxygen species generation that precedes calcium uptake in high-capacity mitochondria: implications for rapid nongenomic signaling of cell growth,” Biochemistry, vol. 45, no. 9, pp. 2872–2881, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Marino, P. Galluzzo, and P. Ascenzi, “Estrogen signaling multiple pathways to impact gene transcription,” Current Genomics, vol. 7, no. 8, pp. 497–508, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Roy and J. G. Liehr, “Temporary decrease in renal quinone reductase activity induced by chronic administration of estradiol to male Syrian hamsters. Increased superoxide formation by redox cycling of estrogen,” The Journal of Biological Chemistry, vol. 263, no. 8, pp. 3646–3651, 1988. View at Google Scholar
  13. J. G. Liehr and D. Roy, “Free radical generation by redox cycling of estrogens,” Free Radical Biology & Medicine, vol. 8, no. 4, pp. 415–423, 1990. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Behl, T. Skutella, F. Lezoualc'h et al., “Neuroprotection against oxidative stress by estrogens: structure-activity relationship,” Molecular Pharmacology, vol. 51, no. 4, pp. 535–541, 1997. View at Google Scholar
  15. W. Abplanalp, M. D. Scheiber, K. Moon, B. Kessel, J. H. Liu, and M. T. Subbiah, “Evidence for the role of high density lipoproteins in mediating the antioxidant effect of estrogens,” European Journal of Endocrinology, vol. 142, no. 1, pp. 79–83, 2000. View at Publisher · View at Google Scholar
  16. X. Cheng, I. Shimizu, Y. Yuan et al., “Effects of estradiol and progesterone on tumor necrosis factor alpha-induced apoptosis in human hepatoma HuH-7 cells,” Life Sciences, vol. 79, no. 21, pp. 1988–1994, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Comeglio, A. Morelli, I. Cellai et al., “Opposite effects of tamoxifen on metabolic syndrome-induced bladder and prostate alterations: a role for GPR30/GPER?” Prostate, vol. 74, no. 1, pp. 10–28, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Vignozzi, M. Gacci, I. Cellai et al., “Fat boosts, while androgen receptor activation counteracts, BPH-associated prostate inflammation,” Prostate, vol. 73, no. 8, pp. 789–800, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Vignozzi, I. Cellai, R. Santi et al., “Antiinflammatory effect of androgen receptor activation in human benign prostatic hyperplasia cells,” The Journal of Endocrinology, vol. 214, no. 1, pp. 31–43, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. J. A. Clayton and F. S. Collins, “Policy: NIH to balance sex in cell and animal studies,” Nature, vol. 509, no. 7500, pp. 282–283, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Speroff, R. H. Glass, and N. G. Kase, Eds., Clinical Gynecologic Endocrinology and Infertility, Lippincott Williams & Wilkins, Baltimore, 6th edition, 1999.
  22. R. A. Hess, “Estrogen in the adult male reproductive tract: a review,” Reproductive Biology and Endocrinology, vol. 1, no. 1, p. 52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. J. F. Dunn, B. C. Nisula, and D. Rodbard, “Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma,” The Journal of Clinical Endocrinology and Metabolism, vol. 53, no. 1, pp. 58–68, 1981. View at Publisher · View at Google Scholar
  24. M. R. Becklake and F. Kauffmann, “Gender differences in airway behaviour over the human life span,” Thorax, vol. 54, no. 12, pp. 1119–1138, 1999. View at Publisher · View at Google Scholar
  25. D. Massaro, L. B. Clerch, and G. D. Massaro, “Estrogen receptor-alpha regulates pulmonary alveolar loss and regeneration in female mice: morphometric and gene expression studies,” American Journal of Physiology. Lung Cellular and Molecular Physiology, vol. 293, no. 1, pp. L222–L228, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Patrone, T. N. Cassel, K. Pettersson et al., “Regulation of postnatal lung development and homeostasis by estrogen receptor beta,” Molecular and Cellular Biology, vol. 23, no. 23, pp. 8542–8552, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. A. J. Chu and S. A. Rooney, “Estrogen stimulation of surfactant synthesis,” Pediatric Pulmonology, vol. 1, no. 3, pp. S110–S114, 1985. View at Google Scholar
  28. J. S. Torday and H. C. Nielsen, “The sex difference in fetal lung surfactant production,” Experimental Lung Research, vol. 12, no. 1, pp. 1–19, 1987. View at Google Scholar
  29. T. R. Martin, R. G. Castile, J. J. Fredberg, M. E. Wohl, and J. Mead, “Airway size is related to sex but not lung size in normal adults,” Journal of Applied Physiology (1985), vol. 63, no. 5, pp. 2042–2047, 1987. View at Google Scholar
  30. S. Carranza-Lira, F. Hernandez, M. Sanchez, S. Murrieta, A. Hernandez, and C. Sandoval, “Prolactin secretion in molar and normal pregnancy,” International Journal of Gynaecology and Obstetrics, vol. 60, no. 2, pp. 137–141, 1998. View at Google Scholar
  31. C. E. Ventetuolo, G. L. Baird, R. G. Barr et al., “Higher estradiol and lower dehydroepiandrosterone-sulfate levels are associated with pulmonary arterial hypertension in men,” American Journal of Respiratory and Critical Care Medicine, vol. 193, no. 10, pp. 1168–1175, 2016. View at Publisher · View at Google Scholar
  32. K. M. Mair, A. F. Wright, N. Duggan et al., “Sex-dependent influence of endogenous estrogen in pulmonary hypertension,” American Journal of Respiratory and Critical Care Medicine, vol. 190, no. 4, pp. 456–467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Cakan, M. Aldemir, M. Topcuoglu, and U. Altug, “Role of testosterone/estradiol ratio in predicting the efficacy of tamoxifen citrate treatment in idiopathic oligoasthenoteratozoospermic men,” Urologia Internationalis, vol. 83, no. 4, pp. 446–451, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Niikawa, T. Suzuki, Y. Miki et al., “Intratumoral estrogens and estrogen receptors in human non-small cell lung carcinoma,” Clinical Cancer Research, vol. 14, no. 14, pp. 4417–4426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Taniuchi, F. Fujishima, Y. Miki et al., “Tissue concentrations of estrogens and aromatase immunolocalization in interstitial pneumonia of human lung,” Molecular and Cellular Endocrinology, vol. 392, no. 1-2, pp. 136–143, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Labrie, “Extragonadal synthesis of sex steroids: intracrinology,” Annales d'endocrinologie, vol. 64, no. 2, pp. 95–107, 2003. View at Publisher · View at Google Scholar
  37. D. Roy, M. Morgan, C. Yoo et al., “Integrated bioinformatics, environmental epidemiologic and genomic approaches to identify environmental and molecular links between endometriosis and breast cancer,” International Journal of Molecular Sciences, vol. 16, no. 10, pp. 25285–25322, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Roy, Q. Cai, Q. Felty, and S. Narayan, “Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers,” Journal of Toxicology and Environmental Health. Part B, Critical Reviews, vol. 10, no. 4, pp. 235–257, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Roy, S. Sarkar, and Q. Felty, “Levels of IL-1 beta control stimulatory/inhibitory growth of cancer cells,” Frontiers in Bioscience, vol. 11, pp. 889–898, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Groth, B. Vrugt, M. Brock, R. Speich, S. Ulrich, and L. C. Huber, “Inflammatory cytokines in pulmonary hypertension,” Respiratory Research, vol. 15, no. 1, p. 47, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Chaouat, L. Savale, C. Chouaid et al., “Role for interleukin-6 in COPD-related pulmonary hypertension,” Chest, vol. 136, no. 3, pp. 678–687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. M. K. Steiner, O. L. Syrkina, N. Kolliputi, E. J. Mark, C. A. Hales, and A. B. Waxman, “Interleukin-6 overexpression induces pulmonary hypertension,” Circulation Research, vol. 104, no. 2, pp. 236–244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Isse, S. M. Specht, J. G. Lunz III, L. I. Kang, Y. Mizuguchi, and A. J. Demetris, “Estrogen stimulates female biliary epithelial cell interleukin-6 expression in mice and humans,” Hepatology, vol. 51, no. 3, pp. 869–880, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. R. E. Kleiger, M. Boxer, R. E. Ingham, and D. C. Harrison, “Pulmonary hypertension in patients using oral contraceptives. A report of six cases,” Chest, vol. 69, no. 2, pp. 143–147, 1976. View at Google Scholar
  45. J. H. Morse, E. M. Horn, and R. J. Barst, “Hormone replacement therapy: a possible risk factor in carriers of familial primary pulmonary hypertension,” Chest, vol. 116, no. 3, p. 847, 1999. View at Publisher · View at Google Scholar · View at Scopus
  46. N. S. Irey and H. J. Norris, “Intimal vascular lesions associated with female reproductive steroids,” Archives of Pathology, vol. 96, no. 4, pp. 227–234, 1973. View at Google Scholar
  47. L. Sweeney and N. F. Voelkel, “Estrogen exposure, obesity and thyroid disease in women with severe pulmonary hypertension,” European Journal of Medical Research, vol. 14, no. 10, pp. 433–442, 2009. View at Publisher · View at Google Scholar
  48. A. Shen, M. D. Iseman, J. A. Waldron, and T. E. King, “Exacerbation of pulmonary lymphangioleiomyomatosis by exogenous estrogens,” Chest, vol. 91, no. 5, pp. 782–785, 1987. View at Publisher · View at Google Scholar
  49. I. Wahedna, S. Cooper, J. Williams, I. C. Paterson, J. R. Britton, and A. E. Tattersfield, “Relation of pulmonary lymphangio-leiomyomatosis to use of the oral contraceptive pill and fertility in the UK: a national case control study,” Thorax, vol. 49, no. 9, pp. 910–914, 1994. View at Publisher · View at Google Scholar · View at Scopus
  50. R. T. Chlebowski, H. Wakelee, M. Pettinger et al., “Estrogen plus progestin and lung cancer: follow-up of the women’s health initiative randomized trial,” Clinical Lung Cancer, vol. 17, no. 1, pp. 10–17, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Montani, E. M. Lau, A. Descatha et al., “Occupational exposure to organic solvents: a risk factor for pulmonary veno-occlusive disease,” The European Respiratory Journal, vol. 46, no. 6, pp. 1721–1731, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. G. N. Rallis, V. A. Boumba, V. A. Sakkas et al., “Residues of selected polychlorinated biphenyls (PCB) and organochlorine pesticides (OCP) in postmortem lungs from Epirus, northwestern Greece,” Journal of Toxicology and Environmental Health. Part a, vol. 77, no. 13, pp. 767–775, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. D. O. Carpenter, “Exposure to and health effects of volatile PCBs,” Reviews on Environmental Health, vol. 30, no. 2, pp. 81–92, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Hansen, M. Granström, D. Rytter et al., “Prenatal exposure to persistent organic pollutants and offspring allergic sensitization and lung function at 20 years of age,” Clinical & Experimental Allergy, vol. 46, no. 2, pp. 329–336, 2016. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Kreiss, M. M. Zack, R. D. Kimbrough, L. L. Needham, A. L. Smrek, and B. T. Jones, “Association of blood pressure and polychlorinated biphenyl levels,” Jama, vol. 245, no. 24, pp. 2505–2509, 1981. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Gustavsson and C. Hogstedt, “A cohort study of Swedish capacitor manufacturing workers exposed to polychlorinated biphenyls (PCBs),” American Journal of Industrial Medicine, vol. 32, no. 3, pp. 234–239, 1997. View at Publisher · View at Google Scholar
  57. A. Goncharov, R. F. Haase, A. Santiago-Rivera et al., “High serum PCBs are associated with elevation of serum lipids and cardiovascular disease in a Native American population,” Environmental Research, vol. 106, no. 2, pp. 226–239, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Tokunaga and K. Kataoka, “A longitudinal analysis on the association of serum lipids and lipoproteins concentrations with blood polychlorinated biphenyls level in chronic “Yusho” patients,” Fukuoka Igaku Zasshi, vol. 94, no. 5, pp. 110–117, 2003. View at Google Scholar
  59. A. V. Sergeev and D. O. Carpenter, “Hospitalization rates for coronary heart disease in relation to residence near areas contaminated with persistent organic pollutants and other pollutants,” Environmental Health Perspectives, vol. 113, no. 5, pp. 756–761, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. B. M. Backlin, E. Persson, C. J. Jones, and V. Dantzer, “Polychlorinated biphenyl (PCB) exposure produces placental vascular and trophoblastic lesions in the mink (Mustela vison): a light and electron microscopic study,” APMIS, vol. 106, no. 8, pp. 785–799, 1998. View at Publisher · View at Google Scholar
  61. C. J. Charlier, A. I. Albert, L. Zhang, N. G. Dubois, and G. J. Plomteux, “Polychlorinated biphenyls contamination in women with breast cancer,” Clinica Chimica Acta, vol. 347, no. 1-2, pp. 177–181, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Carroll-Turpin, V. Hebert, T. Chotibut et al., “4,4′-Methylenedianiline alters serotonergic transport in a novel, sex-specific model of pulmonary arterial hypertension in rats,” Toxicological Sciences, vol. 147, no. 1, pp. 235–245, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Midoro-Horiuti, R. Tiwari, C. S. Watson, and R. M. Goldblum, “Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups,” Environmental Health Perspectives, vol. 118, no. 2, pp. 273–277, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Andersson and E. Brittebo, “Proangiogenic effects of environmentally relevant levels of bisphenol A in human primary endothelial cells,” Archives of Toxicology, vol. 86, no. 3, pp. 465–474, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. L. J. Akinbami, J. E. Moorman, and X. Liu, “Asthma prevalence, health care use, and mortality: United States, 2005-2009,” National Health Statistics Reports, vol. 12, no. 32, pp. 1–14, 2011. View at Publisher · View at Google Scholar
  66. B. Leynaert, J. Sunyer, R. Garcia-Esteban et al., “Gender differences in prevalence, diagnosis and incidence of allergic and non-allergic asthma: a population-based cohort,” Thorax, vol. 67, no. 7, pp. 625–631, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Tam, D. Morrish, S. Wadsworth, D. Dorscheid, S. F. Man, and D. D. Sin, “The role of female hormones on lung function in chronic lung diseases,” BMC Womens Health, vol. 11, no. 1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. R. S. Bonds and T. Midoro-Horiuti, “Estrogen effects in allergy and asthma,” Current Opinion in Allergy and Clinical Immunology, vol. 13, no. 1, pp. 92–99, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. M. K. Han, D. Postma, D. M. Mannino et al., “Gender and chronic obstructive pulmonary disease: why it matters,” American Journal of Respiratory and Critical Care Medicine, vol. 176, no. 12, pp. 1179–1184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. D. R. Gold, X. Wang, D. Wypij, F. E. Speizer, J. H. Ware, and D. W. Dockery, “Effects of cigarette smoking on lung function in adolescent boys and girls,” The New England Journal of Medicine, vol. 335, no. 13, pp. 931–937, 1996. View at Publisher · View at Google Scholar · View at Scopus
  71. S. S. Salvi and P. J. Barnes, “Chronic obstructive pulmonary disease in non-smokers,” Lancet, vol. 374, no. 2, pp. 733–743, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Santos, V. I. Peinado, J. Ramirez et al., “Characterization of pulmonary vascular remodelling in smokers and patients with mild COPD,” The European Respiratory Journal, vol. 19, no. 4, pp. 632–638, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. C. L. Harness-Brumley, A. C. Elliott, D. B. Rosenbluth, D. Raghavan, and R. Jain, “Gender differences in outcomes of patients with cystic fibrosis,” Journal of Women's Health (2002), vol. 23, no. 12, pp. 1012–1020, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. S. H. Chotirmall, S. G. Smith, C. Gunaratnam et al., “Effect of estrogen on pseudomonas mucoidy and exacerbations in cystic fibrosis,” The New England Journal of Medicine, vol. 366, no. 21, pp. 1978–1986, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. H. J. Choi, Y. S. Chung, H. J. Kim et al., “Signal pathway of 17beta-estradiol-induced MUC5B expression in human airway epithelial cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 40, no. 2, pp. 168–178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. E. P. Henske and F. X. McCormack, “Lymphangioleiomyomatosis - a wolf in sheep’s clothing,” The Journal of Clinical Investigation, vol. 122, no. 11, pp. 3807–3816, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Yano, “Exacerbation of pulmonary lymphangioleiomyomatosis by exogenous oestrogen used for infertility treatment,” Thorax, vol. 57, no. 12, pp. 1085–1086, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Adachi, Y. Miki, R. Saito et al., “Intracrine steroid production and mammalian target of rapamycin pathways in pulmonary lymphangioleiomyomatosis,” Human Pathology, vol. 46, no. 11, pp. 1685–1693, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Jemal, R. Siegel, J. Xu, and E. Ward, “Cancer statistics, 2010,” CA: A Cancer Journal for Clinicians, vol. 60, no. 5, pp. 277–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. B. Shim, G. Pacheco-Rodriguez, J. Kato, T. N. Darling, M. Vaughan, and J. Moss, “Sex-specific lung diseases: effect of oestrogen on cultured cells and in animal models,” European Respiratory Review, vol. 22, no. 129, pp. 302–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. V. Mah, D. B. Seligson, A. Li et al., “Aromatase expression predicts survival in women with early-stage non small cell lung cancer,” Cancer Research, vol. 67, no. 21, pp. 10484–10490, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. R. M. Tuder, J. C. Marecki, A. Richter, I. Fijalkowska, and S. Flores, “Pathology of pulmonary hypertension,” Clinics in Chest Medicine, vol. 28, no. 1, pp. 23–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. D. B. Badesch, G. E. Raskob, C. G. Elliott et al., “Pulmonary arterial hypertension: baseline characteristics from the REVEAL registry,” Chest, vol. 137, no. 2, pp. 376–387, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Humbert, O. Sitbon, A. Chaouat et al., “Pulmonary arterial hypertension in France: results from a national registry,” American Journal of Respiratory and Critical Care Medicine, vol. 173, no. 9, pp. 1023–1030, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Rich, D. R. Dantzker, S. M. Ayres et al., “Primary pulmonary hypertension. A national prospective study,” Annals of Internal Medicine, vol. 107, no. 2, pp. 216–223, 1987. View at Publisher · View at Google Scholar
  86. A. Taraseviciute and N. F. Voelkel, “Severe pulmonary hypertension in postmenopausal obese women,” European Journal of Medical Research, vol. 11, no. 5, pp. 198–202, 2006. View at Google Scholar
  87. M. Rabinovitch, W. J. Gamble, O. S. Miettinen, and L. Reid, “Age and sex influence on pulmonary hypertension of chronic hypoxia and on recovery,” The American Journal of Physiology, vol. 240, no. 1, pp. H62–H72, 1981. View at Google Scholar
  88. M. Y. Farhat, M. F. Chen, T. Bhatti, A. Iqbal, S. Cathapermal, and P. W. Ramwell, “Protection by oestradiol against the development of cardiovascular changes associated with monocrotaline pulmonary hypertension in rats,” British Journal of Pharmacology, vol. 110, no. 2, pp. 719–723, 1993. View at Publisher · View at Google Scholar · View at Scopus
  89. I. Kovaleva, M. M. Artem'eva, O. S. Medvedev, and N. A. Medvedeva, “Chronic administration of estradiol to ovariectomized female Wistar rats causes development of hypoxic pulmonary hypertension,” Eksperimental'naia I Klinicheskaia Farmakologiia, vol. 76, no. 5, pp. 7–9, 2013. View at Google Scholar
  90. I. Kovaleva, M. M. Artem'eva, O. S. Medvedev, and N. A. Medvedeva, “Chronic administration of estrogen receptors antagonist reduces degree of hypoxia-induced pulmonary hypertension caused by chronic injections of estrogen in ovariectomised female Wistar rats,” Eksperimental'naia I Klinicheskaia Farmakologiia, vol. 76, no. 7, pp. 15–18, 2013. View at Google Scholar
  91. M. M. Artem'eva, Y. O. Kovaleva, O. S. Medvedev, and N. A. Medvedeva, “Effect of chronic administration of estradiol on responsiveness of isolated systemic and pulmonary blood vessels from ovariectomized Wistar rats with hypoxic pulmonary hypertension,” Bulletin of Experimental Biology and Medicine, vol. 159, no. 4, pp. 427–430, 2015. View at Publisher · View at Google Scholar · View at Scopus
  92. K. Abe, M. Toba, A. Alzoubi et al., “Formation of plexiform lesions in experimental severe pulmonary arterial hypertension,” Circulation, vol. 121, no. 25, pp. 2747–2754, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Dean, M. Nilsen, L. Loughlin, I. P. Salt, and M. R. MacLean, “Metformin reverses development of pulmonary hypertension via aromatase inhibition,” Hypertension, vol. 68, no. 2, pp. 446–454, 2016. View at Publisher · View at Google Scholar · View at Scopus
  94. A. L. Frump, K. N. Goss, A. Vayl et al., “Estradiol improves right ventricular function in rats with severe angioproliferative pulmonary hypertension: effects of endogenous and exogenous sex hormones,” American Journal of Physiology. Lung Cellular and Molecular Physiology, vol. 308, no. 9, pp. L873–L890, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. Y. Dempsie, N. A. MacRitchie, K. White et al., “Dexfenfluramine and the oestrogen-metabolizing enzyme CYP1B1 in the development of pulmonary arterial hypertension,” Cardiovascular Research, vol. 99, no. 1, pp. 24–34, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Dempsie, M. Nilsen, K. White et al., “Development of pulmonary arterial hypertension in mice over-expressing S100A4/Mts1 is specific to females,” vol. 12, no. 1, pp. 159–Respir Res, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. K. White, Y. Dempsie, M. Nilsen, A. F. Wright, L. Loughlin, and M. R. Maclean, “The serotonin transporter, gender, and 17beta oestradiol in the development of pulmonary arterial hypertension,” Cardiovascular Research, vol. 90, no. 2, pp. 373–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. L. J. Rubin, “Primary pulmonary hypertension,” The New England Journal of Medicine, vol. 336, no. 2, pp. 111–117, 1997. View at Publisher · View at Google Scholar · View at Scopus
  99. B. Meyrick and L. Reid, “Hypoxia-induced structural changes in the media and adventitia of the rat hilar pulmonary artery and their regression,” The American Journal of Pathology, vol. 100, no. 1, pp. 151–178, 1980. View at Google Scholar
  100. M. Rabinovitch, T. Bothwell, B. N. Hayakawa et al., “Pulmonary artery endothelial abnormalities in patients with congenital heart defects and pulmonary hypertension. A correlation of light with scanning electron microscopy and transmission electron microscopy,” Laboratory Investigation, vol. 55, no. 6, pp. 632–653, 1986. View at Google Scholar
  101. R. W. Kobs, N. E. Muvarak, J. C. Eickhoff, and N. C. Chesler, “Linked mechanical and biological aspects of remodeling in mouse pulmonary arteries with hypoxia-induced hypertension,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 288, no. 3, pp. H1209–H1217, 2005. View at Publisher · View at Google Scholar · View at Scopus
  102. O. Pak, A. Aldashev, D. Welsh, and A. Peacock, “The effects of hypoxia on the cells of the pulmonary vasculature,” The European Respiratory Journal, vol. 30, no. 2, pp. 364–372, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. K. R. Stenmark, K. A. Fagan, and M. G. Frid, “Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms,” Circulation Research, vol. 99, no. 7, pp. 675–691, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. R. M. Tuder, B. Groves, D. B. Badesch, and N. F. Voelkel, “Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension,” The American Journal of Pathology, vol. 144, no. 2, pp. 275–285, 1994. View at Google Scholar
  105. C. D. Cool, J. S. Stewart, P. Werahera et al., “Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers. Evidence for a dynamic and heterogeneous process of pulmonary endothelial cell growth,” The American Journal of Pathology, vol. 155, no. 2, pp. 411–419, 1999. View at Publisher · View at Google Scholar
  106. S. P. Tofovic, X. Zhang, H. Zhu, E. K. Jackson, O. Rafikova, and G. Petrusevska, “2-Ethoxyestradiol is antimitogenic and attenuates monocrotaline-induced pulmonary hypertension and vascular remodeling,” Vascular Pharmacology, vol. 48, no. 4–6, pp. 174–183, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. O. Rafikova, R. Rafikov, M. L. Meadows, A. Kangath, D. Jonigk, and S. M. Black, “The sexual dimorphism associated with pulmonary hypertension corresponds to a fibrotic phenotype,” Pulmonary Circulation, vol. 5, no. 1, pp. 184–197, 2015. View at Publisher · View at Google Scholar
  108. E. Stacher, B. B. Graham, J. M. Hunt et al., “Modern age pathology of pulmonary arterial hypertension,” American Journal of Respiratory and Critical Care Medicine, vol. 186, no. 3, pp. 261–272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. G. H. Sasaki, C. Y. Pang, and J. L. Wittliff, “Pathogenesis and treatment of infant skin strawberry hemangiomas: clinical and in vitro studies of hormonal effects,” Plastic and Reconstructive Surgery, vol. 73, no. 3, pp. 359–370, 1984. View at Publisher · View at Google Scholar
  110. M. E. Kleinman, M. R. Greives, S. S. Churgin et al., “Hypoxia-induced mediators of stem/progenitor cell trafficking are increased in children with hemangioma,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 12, pp. 2664–2670, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. R. W. Hallowell, R. M. Reed, M. Fraig, M. R. Horton, and R. E. Girgis, “Severe pulmonary hypertension in idiopathic nonspecific interstitial pneumonia,” Pulmonary Circulation, vol. 2, no. 1, pp. 101–106, 2012. View at Publisher · View at Google Scholar
  112. M. Rabinovitch, “Molecular pathogenesis of pulmonary arterial hypertension,” The Journal of Clinical Investigation, vol. 118, no. 7, pp. 2372–2379, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. A. M. Rojiani and K. Dorovini-Zis, “Glomeruloid vascular structures in glioblastoma multiforme: an immunohistochemical and ultrastructural study,” Journal of Neurosurgery, vol. 85, no. 6, pp. 1078–1084, 1996. View at Publisher · View at Google Scholar
  114. F. Tanaka, H. Oyanagi, K. Takenaka et al., “Glomeruloid microvascular proliferation is superior to intratumoral microvessel density as a prognostic marker in non-small cell lung cancer,” Cancer Research, vol. 63, no. 20, pp. 6791–6794, 2003. View at Google Scholar
  115. G. E. D'Alonzo, R. J. Barst, S. M. Ayres et al., “Survival in patients with primary pulmonary hypertension. Results from a national prospective registry,” Annals of Internal Medicine, vol. 115, no. 5, pp. 343–349, 1991. View at Publisher · View at Google Scholar
  116. R. D. Machado, O. Eickelberg, C. G. Elliott et al., “Genetics and genomics of pulmonary arterial hypertension,” Journal of the American College of Cardiology, vol. 54, supplement 1, pp. S32–S42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  118. Q. Felty, S. Sakao, and N. F. Voelkel, “Pulmonary arterial hypertension: a stem cell hypothesis,” in Lung Stem Cells in the Epithelium and Vasculature, A. Firth and J. X. J. Yuan, Eds., pp. 289–306, Springer International Publishing, Switzerland, 2015. View at Google Scholar
  119. Q. Felty and D. Roy, “Potential use of J774A.1 macrophage cells to biomonitor estrogenic activity in non-estrogen dependent tissue,” In Vitro Cellular & Developmental Biology, vol. 38, p. 13, 2002. View at Google Scholar
  120. D. Roy and Q. Cai, “Estrogen, immunoactivation, gene damage, and development of breast, endometrial, ovarian, prostate, and testicular cancers,” Recent Results Development Steroid Biochemistry and Molecular Biology, vol. 3, pp. 1–32, 2002. View at Google Scholar
  121. K. White, A. K. Johansen, M. Nilsen et al., “Activity of the estrogen-metabolizing enzyme cytochrome P450 1B1 influences the development of pulmonary arterial hypertension,” Circulation, vol. 126, no. 9, pp. 1087–1098, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. C. Federici, K. M. Drake, C. M. Rigelsky et al., “Increased mutagen sensitivity and DNA damage in pulmonary arterial hypertension,” American Journal of Respiratory and Critical Care Medicine, vol. 192, no. 192, pp. 219–228, 2015. View at Publisher · View at Google Scholar · View at Scopus
  123. J. K. Das and Q. Felty, “PCB153-induced overexpression of ID3 contributes to the development of microvascular lesions,” PloS One, vol. 9, no. 8, article e104159, 2014. View at Publisher · View at Google Scholar · View at Scopus
  124. A. K. Johansen, A. Dean, I. Morecroft et al., “The serotonin transporter promotes a pathological estrogen metabolic pathway in pulmonary hypertension via cytochrome P450 1B1,” Pulmonary Circulation, vol. 6, no. 1, pp. 82–92, 2016. View at Publisher · View at Google Scholar · View at Scopus
  125. D. C. Marquez-Garban, H. W. Chen, L. Goodglick, M. C. Fishbein, and R. J. Pietras, “Targeting aromatase and estrogen signaling in human non-small cell lung cancer,” Annals of the new York Academy of Sciences, vol. 1155, no. 1, pp. 194–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  126. J. Yu, A. Astrinidis, S. Howard, and E. P. Henske, “Estradiol and tamoxifen stimulate LAM-associated angiomyolipoma cell growth and activate both genomic and nongenomic signaling pathways,” American Journal of Physiology. Lung Cellular and Molecular Physiology, vol. 286, no. 4, pp. L694–L700, 2004. View at Publisher · View at Google Scholar
  127. K. E. Roberts, M. B. Fallon, M. J. Krowka et al., “Genetic risk factors for portopulmonary hypertension in patients with advanced liver disease,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 9, pp. 835–842, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. S. Catalano, R. Malivindi, C. Giordano et al., “Farnesoid X receptor, through the binding with steroidogenic factor 1-responsive element, inhibits aromatase expression in tumor Leydig cells,” The Journal of Biological Chemistry, vol. 285, no. 8, pp. 5581–5593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. L. Vignozzi, A. Morelli, I. Cellai et al., “Cardiopulmonary protective effects of the selective FXR agonist obeticholic acid in the rat model of monocrotaline-induced pulmonary hypertension,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 165, Part B, pp. 277–292, 2017. View at Publisher · View at Google Scholar
  130. P. Comeglio, S. Filippi, E. Sarchielli et al., “Anti-fibrotic effects of chronic treatment with the selective FXR agonist obeticholic acid in the bleomycin-induced rat model of pulmonary fibrosis,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 168, pp. 26–37, 2017. View at Publisher · View at Google Scholar
  131. R. K. Hopper, J. A. Moonen, I. Diebold et al., “In pulmonary arterial hypertension, reduced BMPR2 promotes endothelial-to-mesenchymal transition via HMGA1 and its target slug,” Circulation, vol. 133, no. 18, pp. 1783–1794, 2016. View at Publisher · View at Google Scholar · View at Scopus