The role of iron in the pathogenesis of endometriosis

Gynecological Endocrinology

Volumn 25, Issue 1, 2009, Pages 39-52

  Kobayashi, Hiroshi ^a   Yamada, Yoshihiko ^a   Kanayama, Seiji ^a   Furukawa, Naoto ^a   Noguchi, Taketoshi ^a   Haruta, Shoji ^a   Yoshida, Shozo ^a   Sakata, Mariko ^a   Sado, Toshiyuki ^a   Oi, Hidekazu ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Endometriosis; Heme; Iron; Oxidative stress

Indexed keywords

3 AMINOPICOLINALDEHYDE THIOSEMICARBAZONE; CALGRANULIN A; CHEMOKINE; CYCLIN DEPENDENT KINASE; CYCLINE; DEFERASIROX; DEFERIPRONE; DEFEROXAMINE; ESTROGEN RECEPTOR; GROWTH FACTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HEME; HEPATOCYTE NUCLEAR FACTOR 1BETA; HISTONE DEACETYLASE; IRON; IRON CHELATING AGENT; LEUKOTRIENE B4 RECEPTOR; LIPOCALIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PROGESTERONE RECEPTOR; RANTES; RAZOXANE; SCATTER FACTOR RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TRANSCRIPTION FACTOR; UNINDEXED DRUG;

CELL DAMAGE; DETOXIFICATION; DNA DAMAGE; ENDOMETRIOSIS; ENERGY METABOLISM; FEMALE; FIBROSIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE TARGETING; GENOME ANALYSIS; GENOMICS; HEMOLYSIS; HUMAN; INFLAMMATION; IRON OVERLOAD; LIPID PEROXIDATION; LYMPHOKINE ACTIVATED KILLER CELL; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL;

ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEME; HUMANS; IRON; OVARIAN DISEASES;

EID: 60749132542     PISSN: 09513590     EISSN: 14730766     Source Type: Journal    
DOI: 10.1080/09513590802366204     Document Type: Review

References (141)

1. Giudice LC, Tazuke SI, Swiersz L. Status of current research on endometriosis. J Reprod Med 1998;43(Suppl 3):252-262.
2. Nap AW, Groothuis PG, Demir AY, Evers JL, Dunselman GA. Pathogenesis of endometriosis. Best Pract Res Clin Obstet Gynaecol 2004;18:233-244.
3. Templeton DM, Liu Y. Genetic regulation of cell function in response to iron overload or chelation. Biochim Biophys Acta 2003;1619:113-124.
4. Johansson S, Berg L, Hall H, Höglund P. NK cells: elusive players in autoimmunity. Trends Immunol 2005;26:613-618.
5. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, Nezhat CR, Lessey BA, Giudice LC. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007;148:3814-3826.
6. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
7. Dearn S, Rahman M, Lewis A, Ahmed Z, Eggo MC, Ahmed A. Activation of platelet-activating factor (PAF) receptor stimulates nitric oxide (NO) release via protein kinase C-α in HEC-1B human endometrial epithelial cell line. Mol Med 2000;6:37-49.
8. Eyster KM, Boles AL, Brannian JD, Hansen KA. DNA microarray analysis of gene expression markers of endometriosis. Fertil Steril 2002;77:38-42.
9. Lebovic DI, Baldocchi RA, Mueller MD, Taylor RN. Altered expression of a cell-cycle suppressor gene, Tob-1, in endometriotic cells by cDNA array analyses. Fertil Steril 2002;78:849-854.
10. Arimoto T, Katagiri T, Oda K, Tsunoda T, Yasugi T, Osuga Y, Yoshikawa H, Nishii O, Yano T, Taketani Y, et al. Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol 2003;22:551-560.
11. Matsuzaki S, Canis M, Vaurs-Barriere C, Pouly JL, Boespflug-Tanguy O, Penault-Llorca F, Dechelotte P, Dastugue B, Okamura K, Mage G. DNA microarray analysis of gene expression profiles in deep endometriosis using laser capture microdissection. Mol Hum Reprod 2004;10:719-728.
12. Smith SK. Study of the profile of gene expression in the endometrium. J Gynecol Obstet Biol Reprod 2004;33:3S15-3S18.
13. Fan Y, Chen BL, Ma XD, Su MQ. Detection of expression of endometriosis-related cytokine and their receptor genes by cDNA microarray technique. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2005;21:489-492.
14. Matsuzaki S, Canis M, Pouly JL, Dechelotte P, Okamura K, Mage G. The macrophage stimulating protein/RON system: a potential novel target for prevention and treatment of endometriosis. Mol Hum Reprod 2005;11:345-349.
15. Matsuzaki S, Canis M, Vaurs-Barriere C, Boespflug-Tanguy O, Dastugue B, Mage G. DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection. Fertil Steril 2005;84(Suppl 2):1180-1190.
16. Kato N, Sasou S, Motoyama T. Expression of hepatocyte nuclear factor-1β (HNF-1β) in clear cell tumors and endometriosis of the ovary. Mod Pathol 2006;19:83-89.
17. Wu Y, Kajdacsy-Balla A, Strawn E, Basir Z, Halverson G, Jailwala P, Wang Y, Wang X, Ghosh S, Guo SW. Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 2006;147:232-246.
18. Gaetje R, Holtrich U, Engels K, Kourtis K, Cikrit E, Kissler S, Rody A, Karn T, Kaufmann M. Expression of membrane-type 5 matrix metalloproteinase in human endometrium and endometriosis. Gynecol Endocrinol 2007;23:567-573.
19. Wren JD, Wu Y, Guo SW. A system-wide analysis of differentially expressed genes in ectopic and eutopic endometrium. Hum Reprod 2007;22:2093-2102.
20. Goumenou A, Panayiotides I, Mahutte NG, Matalliotakis I, Fragouli Y, Arici A. Immunohistochemical expression of p53, MDM2, and p21Waf1 oncoproteins in endometriomas but not adenomyosis. J Soc Gynecol Investig 2005;12:263-266.
21. Fauvet R, Poncelet C, Hugol D, Lavaur A, Feldmann G, Daraï E. Expression of apoptosis-related proteins in endometriomas and benign and malignant ovarian tumours. Virchows Arch 2003;443:38-43.
22. Matsuzaki S, Canis M, Murakami T, Dechelotte P, Bruhat MA, Okamura K. Expression of the cyclin-dependent kinase inhibitor p27Kip1 in eutopic endometrium and peritoneal endometriosis. Fertil Steril 2001;75:956-960.
23. Lembessis P, Milingos S, Michalas S, Milingos D, Creatsas G, Sourla A, Koutsilieris M. Urokinase-type plasminogen activator and insulin-like growth factor-binding protein 3 mRNA expression in endometriotic lesions and eutopic endometrium: implications for the pathophysiology of endometriosis. Ann N Y Acad Sci 2003;997:223-228.
24. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Miura S, Sekine I, Ishimaru T. Peritoneal fluid and serum levels of hepatocyte growth factor may predict the activity of endometriosis. Acta Obstet Gynecol Scand 2006;85:458-466.
25. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Sekine I, Matsuyama T, Ishimaru T. Interleukin-6- and tumour necrosis factor α-mediated expression of hepatocyte growth factor by stromal cells and its involvement in the growth of endometriosis. Hum Reprod 2005;20:2715-2723.
26. Yoshida S, Harada T, Mitsunari M, Iwabe T, Sakamoto Y, Tsukihara S, Iba Y, Horie S, Terakawa N. Hepatocyte growth factor/Met system promotes endometrial and endometriotic stromal cell invasion via autocrine and paracrine pathways. J Clin Endocrinol Metab 2004;89:823-832.
27. Pritts EA, Zhao D, Ricke E, Waite L, Taylor RN. PPAR-γ decreases endometrial stromal cell transcription and translation of RANTES in vitro. J Clin Endocrinol Metab 2002;87:1841-1844.
28. Corton CH, Anderson SP, Stauber A. Central role of peroxisome proliferator-activated receptors in the actions of peroxisome proliferators. Annu Rev Pharmacol Toxicol 2000;40:491-518.
29. Hornung D, Waite LL, Ricke EA, Bentzien F, Wallweiner D, Taylor RN. Nuclear peroxisome proliferator-activated receptors have opposing effects on monocyte chemotaxis in endometriosis. J Clin Endocrinol Metab 2001;86:3108-3114.
30. Aytan H, Caliskan AC, Demirturk F, Aytan P, Koseoglu DR. Peroxisome proliferator-activated receptor-γ agonist rosiglitazone reduces the size of experimental endometriosis in the rat model. Aust N Z J Obstet Gynaecol 2007;47:321-325.
31. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997;389:349-352.
32. Wu Y, Starzinski-Powitz A, Guo SW. Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reprod Sci 2007;14:374-382.
33. Murphy AA, Santanam N, Parthasarathy S. Endometriosis: a disease of oxidative stress? Semin Reprod Endocrinol 1998;16:263-273.
34. Yoshino O, Osuga Y, Hirota Y, Koga K, Hirata T, Harada M, Morimoto C, Yano T, Nishii O, Tsutsumi O, Taketani Y. Possible pathophysiological roles of mitogen-activated protein kinases (MAPKs) in endometriosis. Am J Reprod Immunol 2004;52:306-311.
35. Schneider H, Rudd CE. CD28 and Grb-2 (but not Gads or Grap) cooperate with Vav1 in the activation of NFAT/AP-1. Biochem Biophys Res Commun 2008;369:616-621.
36. Konno R, Fujiwara H, Netsu S, Odagiri K, Shimane M, Nomura H, Suzuki M. Gene expression profiling of the rat endometriosis model. Am J Reprod Immunol 2007;58:330-343.
37. Yankee TM, Solow SA, Draves KD, Clark EA. Expression of the Grb2-related protein of the lymphoid system in B cell subsets enhances B cell antigen receptor signaling through mitogen-activated protein kinase pathways. J Immunol 2003;170:349-355.
38. Hever A, Roth RB, Hevezi P, Marin ME, Acosta JA, Acosta H, Rojas J, Herrera R, Grigoriadis D, White E, et al. Human endometriosis is associated with plasma cells and overexpression of B lymphocyte stimulator. Proc Natl Acad Sci U S A 2007;104:12451-12456.
39. Ulukus M, Arici A. Immunology of endometriosis. Minerva Ginecol 2005;57:237-248.
40. Abe Y, Van Eden M, Gatanaga M, Wang FI, Brightbill HD, Granger GA, Gatanaga T. The role of lymphotoxin in the IL-2-driven differentiation of human lymphokine-activated T-killer (T-LAK) cells in vitro. Lymphokine Cytokine Res 1993;12:279-284.
41. Abe Y, Matsumoto S, Kito K, Ueda N. Cloning and expression of a novel MAPKK-like protein kinase, lymphokine-activated killer T-cell-originated protein kinase, specifically expressed in the testis and activated lymphoid cells. J Biol Chem 2000;275:21525-21531.
42. Ishii S, Shimizu T. Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog Lipid Res 2000;39:41-82.
43. Brown SL, Jala VR, Raghuwanshi SK, Nasser MW, Haribabu B, Richardson RM. Activation and regulation of platelet-activating factor receptor: role of G(i) and G(q) in receptor-mediated chemotactic, cytotoxic, and cross-regulatory signals. J Immunol 2006;177:3242-3249.
44. Simoni J, Simoni G, Lox CD, McGunegle DE, Feola M. Cytokines and PAF release from human monocytes and macrophages: effect of hemoglobin and contaminants. Artif Cells Blood Substit Immobil Biotechnol 1994;22:525-534.
45. Kato N, Sasou S, Motoyama T. Expression of hepatocyte nuclear factor-1β (HNF-1β) in clear cell tumors and endometriosis of the ovary. Mod Pathol 2006;19:83-89.
46. Yamamoto S, Tsuda H, Aida S, Shimazaki H, Tamai S, Matsubara O. Immunohistochemical detection of hepatocyte nuclear factor 1β in ovarian and endometrial clear-cell adenocarcinomas and nonneoplastic endometrium. Hum Pathol 2007;38:1074-1080.
47. González-Ramos R, Donnez J, Defrère S, Leclercq I, Squifflet J, Lousse JC, Van Langendonckt A. Nuclear factor-κB is constitutively activated in peritoneal endometriosis. Mol Hum Reprod 2007;13:503-509.
48. Yamauchi N, Harada T, Taniguchi F, Yoshida S, Iwabe T, Terakawa N. Tumor necrosis factor-alpha induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-κB and mitogen-activated protein kinase pathways. Fertil Steril 2004;82(Suppl 3):1023-1028.
49. Wu MH, Chen KF, Lin SC, Lgu CW, Tsai SJ. Aberrant expression of leptin in human endometriotic stromal cells is induced by elevated levels of hypoxia inducible factor-1α. Am J Pathol 2007;170:590-598.
50. Gurates B, Bulun SE. Endometriosis: the ultimate hormonal disease. Semin Reprod Med 2003;21:125-134.
51. Taylor RN, Lebovic DI, Hornung D, Mueller MD. Endocrine and paracrine regulation of endometrial angiogenesis. Ann N Y Acad Sci 2001;943:109-121.
52. Hayrabedyan S, Kyurkchiev S, Kehayov I. FGF-1 and S100A13 possibly contribute to angiogenesis in endometriosis. J Reprod Immunol 2005;67:87-101.
53. Komiyama S, Aoki D, Komiyama M, Nozawa S. Local activation of TGF-β1 at endometriosis sites. J Reprod Med 2007;52:306-312.
54. Tamburro S, Canis M, Albuisson E, Dechelotte P, Darcha C, Mage G. Expression of transforming growth factor β1 in nerve fibers is related to dysmenorrhea and laparoscopic appearance of endometriotic implants. Fertil Steril 2003;80:1131-1136.
55. Schall TJ, Bacon K, Toy KJ, Goeddel DV. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 1990;347:669-671.
56. Bersinger NA, von Roten S, Wunder DM, Raio L, Dreher E, Mueller MD. PAPP-A and osteoprotegerin, together with interleukin-8 and RANTES, are elevated in the peritoneal fluid of women with endometriosis. Am J Obstet Gynecol 2006;195:103-108.
57. Lebovic DI, Chao VA, Taylor RN. Peritoneal macrophages induce RANTES (regulated on activation, normal T cell expressed and secreted) chemokine gene transcription in endometrial stromal cells. J Clin Endocrinol Metab 2004;89:1397-1401.
58. 1-microglobulin on T lymphocytes: inhibition of antigen-induced interleukin-2 production. Scand J Immunol 1998;48:1-7.
59. 1-microglobulin in normal and healed tissues and its effect on immunocompetent cells. Scand J Immunol 1999;50:289-295.
60. Subbarao K, Jala VR, Mathis S, Suttles J, Zacharias W, Ahamed J, Ali H, Tseng MT, Haribabu B. Role of leukotriene B4 receptors in the development of atherosclerosis: potential mechanisms. Arterioscler Thromb Vasc Biol 2004;24:369-375.
61. Yokomizo T, Kato K, Terawaki K, Izumi T, Shimizu T. A second leukotriene B-4 receptor, BLT2: a new therapeutic target in inflammation and immunological disorders. J Exp Med 2000;192:421-431.
62. Konno R, Fujiwara H, Suzuki M. Effectiveness of leukotriene receptor antagonists for dysmenorrhea of endometriosis. Fam Med 2004;36:8-9.
63. Ihara T, Uchiide I, Sugamata M. Light and electron microscopic evaluation of antileukotriene therapy for experimental rat endometriosis. Fertil Steril 2004;81(Suppl 1):819-823.
64. Osteen KG, Yeaman GR, Bruner-Tran KL. Matrix metalloproteinases and endometriosis. Semin Reprod Med 2003;21:155-164.
65. Zhou HE, Nothnick WB. The relevancy of the matrix metalloproteinase system to the pathophysiology of endometriosis. Front Biosci 2005;10:569-575.
66. Bruse C, Guan Y, Carlberg M, Carlström K, Bergqvist A. Basal release of urokinase plasminogen activator, plasminogen activator inhibitor-1, and soluble plasminogen activator receptor from separated and cultured endometriotic and endometrial stromal and epithelial cells. Fertil Steril 2005;83(Suppl 1):1155-1160.
67. Froelich CJ, Zhang X, Turbov J, Hudig D, Winkler U, Hanna WL. Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J Immunol 1993;151:7161-7171.
68. Fujimoto J, Ichigo S, Hori M, Tamaya T. Expression of E-cadherin, α- and β-catenin mRNAs in ovarian endometriosis. Eur J Obstet Gynecol Reprod Biol 1996;67:179-183.
69. Clarke CJ, Truong TG, Hannun YA. Role for neutral sphingomyelinase-2 in tumor necrosis factor α-stimulated expression of vascular cell adhesion molecule-1 (VCAM) and intercellular adhesion molecule-1 (ICAM) in lung epithelial cells: p38 MAPK is an upstream regulator of nSMase2. J Biol Chem 2007;282:1384-1396.
70. Pettersen CA, Adler KB. Airways inflammation and COPD: epithelial-neutrophil interactions. Chest 2002;121(Suppl 5):S142-S150.
71. Barrier BF, Sharpe-Timms KL. Expression of soluble adhesion molecules in sera of women with stage III and IV endometriosis. J Soc Gynecol Investig 2002;9:98-101.
72. Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, Mathieu C, D'Hooghe TM. Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril 2008;89:301-310.
73. Meinhardt U, Mullis PE. The aromatase cytochrome P-450 and its clinical impact. Horm Res 2002;57:145-152.
74. Barros RP, Machado UF, Warner M, Gustafsson JA. Muscle GLUT4 regulation by estrogen receptors ERβ and ERα. Proc Natl Acad Sci U S A 2006;103:1605-1608.
75. Slater M, Quagliotto G, Cooper M, Murphy CR. Endometriotic cells exhibit metaplastic change and oxidative DNA damage as well as decreased function, compared to normal endometrium. J Mol Histol 2005;36:257-263.
76. Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glö ssl J, Luschnig C, Adam G. Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 2003;278:47905-47914.
77. Gagne JF, Montminy V, Belanger P, Journault K, Gaucher G, Guillemette C. Common human UGT1A polymorphisms and the altered metabolism of irinotecan active metabolite 7-ethyl-10-hydroxycamptothecin (SN-38). Mol Pharmacol 2002;62:608-617.
78. Mann GE, Niehueser-Saran J, Watson A, Gao L, Ishii T, de Winter P, Siow RC. Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: implications for atherosclerosis and pre-eclampsia. Sheng Li Xue Bao 2007;59:117-127.
79. Pennington JD, Jacobs KM, Sun L, Bar-Sela G, Mishra M, Gius D. Thioredoxin and thioredoxin reductase as redox-sensitive molecular targets for cancer therapy. Curr Pharm Des 2007;13:3368-3377.
80. Thome J, Gsell W, Rösler M, Kornhuber J, Frölich L, Hashimoto E, Zielke B, Wiesbeck GA, Riederer P. Oxidative-stress associated parameters (lactoferrin, superoxide dismutases) in serum of patients with Alzheimer's disease. Life Sci 1997;60:13-19.
81. Walmer DK, Wrona MA, Hughes CL, Nelson KG. Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 1992;131:1458-1466.
82. Newsome AL, Johnson JP, Seipelt RL, Thompson MW. Apolactoferrin inhibits the catalytic domain of matrix metalloproteinase-2 by zinc chelation. Biochem Cell Biol 2007;85:563-572.
83. Madsen M, Møller HJ, Nielsen MJ, Jacobsen C, Graversen JH, van den Berg T, Moestrup SK. Molecular characterization of the haptoglobin.hemoglobin receptor CD163. Ligand binding properties of the scavenger receptor cysteine-rich domain region. J Biol Chem 2004;279:51561-51567.
84. Zuwała-Jagiełło J. Haemoglobin scavenger receptor: function in relation to disease. Acta Biochim Pol 2006;53:257-268.
85. Fornace AJ Jr. Mammalian genes induced by radiation; activation of genes associated with growth control. Annu Rev Genet 1992;26:507-526.
86. Jackson LW, Schisterman EF, Dey-Rao R, Browne R, Armstrong D. Oxidative stress and endometriosis. Hum Reprod 2005;20:2014-2020.
87. Sheikh MS, Fernandez-Salas E, Yu M, Hussain A, Dinman JD, Peltz SW, Huang Y, Fornace AJ Jr. Cloning and characterization of a human genotoxic and endoplasmic reticulum stress-inducible cDNA that encodes translation initiation factor 1(eIF1(A121/SUI1)). J Biol Chem 1999;274:16487-16493.
88. Zhao ZZ, Nyholt DR, Le L, Martin NG, James MR, Treloar SA, Montgomery GW. KRAS variation and risk of endometriosis. Mol Hum Reprod 2006;12:671-676.
89. Dinulescu DM, Ince TA, Quade BJ, Shafer SA, Crowley D, Jacks T. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 2005;11:63-70.
90. Martinez O, Goud B. Rab proteins. Biochim Biophys Acta 1998;1404:101-112.
91. Echard A, Jollivet F, Martinez O, Lacapère JJ, Rousselet A, Janoueix-Lerosey I, Goud B. Interaction of a Golgi-associated kinesin-like protein with Rab6. Science 1998;279:580-585.
92. Lee AS. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 2007;67:3496-3499.
93. Pan M, Cederbaum AI, Zhang YL, Ginsberg HN, Williams KJ, Fisher EA. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J Clin Invest 2004;113:1277-1287.
94. Courtois F, Suc I, Garofalo C, Ledoux M, Seidman E, Levy E. Iron-ascorbate alters the efficiency of Caco-2 cells to assemble and secrete lipoproteins. Am J Physiol Gastrointest Liver Physiol 2000;279:G12-G19.
95. Harada T, Iwabe T, Terakawa N. Role of cytokines in endometriosis. Fertil Steril 2001;76:1-10.
96. Pol O, Alameda F, Puig MM. Inflammation enhances μ-opioid receptor transcription and expression in mice intestine. Mol Pharmacol 2001;60:894-899.
97. Matsuzaki S, Canis M, Pouly JL, Botchorishvili R, Déchelotte PJ, Mage G. Both GnRH agonist and continuous oral progestin treatments reduce the expression of the tyrosine kinase receptor B and μ-opioid receptor in deep infiltrating endometriosis. Hum Reprod 2007;22:124-128.
98. Zurawski G, Benedik M, Kamb B, Araens J, Zurawski S, Lee F. Activation of mouse T-helper cells induces abundant proenkephalin mRNA synthesis. Science 1986;232:772-775.
99. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res 2008;68:1777-1785.
100. Kumar S, Bandyopadhyay U. Free heme toxicity and its detoxification systems in human. Toxicol Lett 2005;157:175-188.
101. Ferrándiz ML, Devesa I. Inducers of heme oxygenase-1. Curr Pharm Des 2008;14:473-486.
102. Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 2000;28:289-309.
103. Kato J, Kobune M, Ohkubo S, Fujikawa K, Tanaka M, Takimoto R, Takada K, Takahari D, Kawano Y, Kohgo Y, et al. Iron/IRP-1-dependent regulation of mRNA expression for transferrin receptor, DMT1 and ferritin during human erythroid differentiation. Exp Hematol 2007;35:879-887.
104. Yoshiki N, Kubota T, Aso T. Identification of heme oxygenase in human endometrium. J Clin Endocrinol Metab 2001;86:5033-5038.
105. Ryter SW, Si M, Lai CC, Su CY. Regulation of endothelial heme oxygenase activity during hypoxia is dependent on chelatable iron. Am J Physiol Heart Circ Physiol 2000;279:H2889-H2897.
106. Inguaggiato P, Gonzalez-Michaca L, Croatt AJ, Haggard JJ, Alam J, Nath KA. Cellular overexpression of heme oxygenase-1 up-regulates p21 and confers resistance to apoptosis. Kidney Int 2001;60:2181-2191.
107. Yamaguchi K, Mandai M, Toyokuni S, Hamanishi J, Higuchi T, Takakura K, Fujii S. Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res 2008;14:32-40.
108. Kim BH, Jun YC, Jin JK, Kim JI, Kim NH, Leibold EA, Connor JR, Choi EK, Carp RI, Kim YS. Alteration of iron regulatory proteins (IRP1 and IRP2) and ferritin in the brains of scrapie-infected mice. Neurosci Lett 2007;422:158-163.
109. Tacchini L, Fusar-Poli D, Bernelli-Zazzera A. Activation of transcription factors by drugs inducing oxidative stress in rat liver. Biochem Pharmacol 2002;63:139-148.
110. Pantopoulos K. Iron metabolism and the IRE/IRP regulatory system: an update. Ann N Y Acad Sci 2004;1012:1-13.
111. Le NT, Richardson DR. The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim Biophys Acta 2002;1603:31-46.
112. Kalyanaraman B. Iron signaling and oxidant damage. Cardiovasc Toxicol 2007;7:92-94.
113. Nappi AJ, Vass E. Iron, metalloenzymes and cytotoxic reactions. Cell Mol Biol (Noisy-le-grand) 2000;46:637-647.
114. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, Figdor CG. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 2003;55:551-571.
115. Liu Y, Popovich Z, Templeton DM. Global genomic approaches to the iron-regulated proteome. Ann Clin Lab Sci 2005;35:230-239.
116. Eisenstein RS. Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 2000;20:627-662.
117. Van Langendonckt A, Casanas-Roux F, Dolmans MM, Donnez J. Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 2002;77:561-570.
118. Fisher AE, Naughton DP. Therapeutic chelators for the twenty first century: new treatments for iron and copper mediated inflammatory and neurological disorders. Curr Drug Deliv 2005;2:261-268.
119. Burk RF, Hill KE. Regulation of selenoproteins. Annu Rev Nutr 1993;13:65-81.
120. Ursini F, Maiorino M, Brigelius FR, Aumann KD, Roveri A, Schomburg D, Flohe L. Diversity of glutathione peroxidases. Methods Enzymol 1995;252:38-53.
121. Szczepańska M, Koźlik J, Skrzypczak J, Mikołajczyk M. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 2003;79:1288-1293.
122. Alam J, Smith A. Receptor-mediated transport of heme by hemopexin regulates gene expression in mammalian cells. J Biol Chem 1989;264:17637-17640.
123. Alam J, Smith A. Heme-hemopexin-mediated induction of metallothionein gene expression. J Biol Chem 1992;267:16379-16384.
124. Wicherek L, Popiela TJ, Galazka K, Dutsch-Wicherek M, Opławski M, Basta A, Klimek M. Metallothionein and RCAS1 expression in comparison to immunological cells activity in endometriosis, endometrial adenocarcinoma and endometrium according to menstrual cycle changes. Gynecol Oncol 2005;99:622-630.
125. Srivastava S, Spite M, Trent JO, West MB, Ahmed Y, Bhatnagar A. Aldose reductase-catalyzed reduction of aldehyde phospholipids. J Biol Chem 2004;279:53395-53406.
126. Rossi M, Sharkey AM, Viganò P, Fiore G, Furlong R, Florio P, Ambrosini G, Smith SK, Petraglia F. Identification of genes regulated by interleukin-1β in human endometrial stromal cells. Reproduction 2005;130:721-729.
127. Marzullo L, Tosco A, Capone R, Andersen HS, Capasso A, Leone A. Identification of dietary copper- and iron-regulated genes in rat intestine. Gene 2004;338:225-233.
128. Cooper CE. Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 2002;27:33-39.
129. Hintze KJ, Theil EC. DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc Natl Acad Sci U S A 2005;102:15048-15052.
130. Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Eaton JW, Balla G. Heme, heme oxygenase and ferritin in vascular endothelial cell injury. Mol Nutr Food Res 2005;49:1030-1043.
131. Hintze KJ, Wald KA, Zeng H, Jeffery EH, Finley JW. Thioredoxin reductase in human hepatoma cells is transcriptionally regulated by sulforaphane and other electrophiles via an antioxidant response element. J Nutr 2003;133:2721-2727.
132. Iwasaki K, Mackenzie EL, Hailemariam K, Sakamoto K, Tsuji Y. Hemin-mediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells. Mol Cell Biol 2006;26:2845-2856.
133. Li XL, Xing QC, Dong B, Gao YY, Xing SS, Pang YZ, Jiang HF, Tang CS. Plasma level of mitochondrial coupling factor 6 increases in patients with type 2 diabetes mellitus. Int J Cardiol 2007;117:411-412.
134. Osanai T, Sasaki S, Kamada T, Fujiwara N, Nakano T, Tomita H, Matsunaga T, Magota K, Okumura K. Circulating coupling factor 6 in human hypertension: role of reactive oxygen species. J Hypertens 2003;21:2323-2328.
135. Smeitink JA, van den Heuvel LW, Koopman WJ, Nijtmans LG, Ugalde C, Willems PH. Cell biological consequences of mitochondrial NADH:ubiquinone oxidoreductase deficiency. Curr Neurovasc Res 2004;1:29-40.
136. Cheng J, Diaz Encarnacion MM, Warner GM, Gray CE, Nath KA, Grande JP. TGF-β1 stimulates monocyte chemoattractant protein-1 expression in mesangial cells through a phosphodiesterase isoenzyme 4-dependent process. Am J Physiol Cell Physiol 2005;289:C959-C970.
137. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008;214:199-210.
138. Hsieh YY, Chang CC, Tsai FJ, Peng CT, Yeh LS, Lin CC. Polymorphism for transforming growth factor β 1-509 (TGF-B1-509): association with endometriosis. Biochem Genet 2005;43:203-210.
139. Kontoghiorghes GJ, Efstathiou A, Ioannou-Loucaides S, Kolnagou A. Chelators controlling metal metabolism and toxicity pathways: applications in cancer prevention, diagnosis and treatment. Hemoglobin 2008;32:217-227.
140. Sã Chaud R, Dutreix C, Balez S, Pommier F, Dumortier T, Morisson S, Brun E. Relative bioavailability of deferasirox tablets administered without dispersion and dispersed in various drinks. Int J Clin Pharmacol Ther 2008;46:102-108.
141. Yang LP, Keam SJ, Keating GM. Deferasirox: a review of its use in the management of transfusional chronic iron overload. Drugs 2007;67:2211-2230.