Endometriosis and oxidative stress?

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1 Endometriosis and oxidative stress? Pietro Santulli MD, PhD Université Paris Descartes, Sorbonne Paris Cité, Faculté de médecine, AP-HP, Cochin Saint Vincent de Paul, Department of Gynecology Obstetrics II and Reproductive Medicine, Paris, France Inserm, Unité de recherche U1016 équipe Pr Batteux, Institut Cochin, Paris, France

2 Presentation outline Pathogenesis of inflammation Clinical consequences: Pain and infertility Oxidative stress Targeted treatments of endometriosis

3 Implantation theory of endometriosis Adenomyosis SUP OMA DIE SUP, superficial lesion; OMA, endometrioma; DIE, deep infiltrating endometriosis

4 Cycle of pathogenesis in endometriosis Adhesion Ectopic implantation Invasion Angiogenesis Proliferation Glands Stroma Steroidogenesis Kobayashi H et al. Arch Gynecol Obstet 2014; 289(1):

5 Mechanisms of pathogenesis in endometriosis Altered immune functions Attenuated progesterone action Adhesion Invasion Excess oxidative stress Ectopic implantation Angiogenesis Proliferation Neuroangiogenesis Glands Stroma Steroidogenesis Chronic inflammatory response ++++ Adapted from Kobayashi H et al. Arch Gynecol Obstet 2014; 289(1):

6 Molecular pathways involved in endometriosis + VEGF Angiogenesis MMP INSL3 Adhesion-Migration PGE 2 PTGER + PTGS2 + Inflammation Cholesterol STAR + NR5A1 Estradiol CYP11A1 CYP17 Steroidogenesis + Proliferation Androstenedione CYP19A1 Estrone VEGF, vascular endothelial growth factor; PGE 2, prostaglandin E 2 ; PTGS2, prostaglandin-endoperoxide synthase 2; PTGER, prostaglandin E receptor; MMP, matrix metalloproteinase; INSL3, insulin-like 3; STAR, steroidogenic acute regulatory protein; CYP, cytochrome P; NR, nuclear receptor. Adapted from Bulun SE. N Engl J Med 2009; 360(3):

7 Molecular pathways involved in endometriosis + VEGF Angiogenesis MMP INSL3 Adhesion-Migration PGE 2 PTGER + PTGS2 + Inflammation Cholesterol STAR + NR5A1 Estradiol CYP11A1 CYP17 Steroidogenesis + Proliferation Androstenedione CYP19A1 Estrone VEGF, vascular endothelial growth factor; PGE 2, prostaglandin E 2 ; PTGS2, prostaglandin-endoperoxide synthase 2; PTGER, prostaglandin E receptor; MMP, matrix metalloproteinase; INSL3, insulin-like 3; STAR, steroidogenic acute regulatory protein; CYP, cytochrome P; NR, nuclear receptor. Adapted from Bulun SE. N Engl J Med 2009; 360(3):

8 Inflammatory response pathway leads to tissue injury and chronic pain Inflammation Regurgitation! Iron ê CXCL 10 ê IL-19,22! NF- Kβ Oxidative stress Decreased anti-inflammatory factors Increased pro-inflammatory factors é é é é é TNF-α IL-1β IL-6,8,33 Rantes PGs Pelvic Pain Tissue injury Neuroangiogenesis é PGs Excessive sensory innervation é NGF IL, interleukin; TNF, tumor necrosis factor; PG, prostaglandin; CXCL, chemokine; NGF, nerve growth factor; NF-Kβ, nuclear factor kappa beta.

9 Inflammatory response can contribute to infertility Pelvic cavity: Proliferation of macrophages Phagocytic dysfunction Release of proinflammatory factors Uterus: Increased synthesis of prostaglandin & altered receptivity Production of estrogens in situ and resistance to progestogen Ovaries: Decreased ovarian response Altered oocyte quality? Iron overload (proinflammatory factors) de Ziegler D et al. Lancet 2010; 376(9742):

10 Inflammation in endometriosis: Molecular intermediates and pathways Sphingosines PTGS2 Adhesion Invasion Inflammation Angiogenesis Proliferation Oxidative Stress Steroidogenesis MAPK pathway PTGS2, prostaglandin-endoperoxide synthase 2

11 Inflammation in endometriosis: Molecular intermediates and pathways Sphingosines PTGS2 Adhesion Invasion Inflammation Angiogenesis Proliferation Oxidative Stress Steroidogenesis MAPK pathway PTGS2, prostaglandin-endoperoxide synthase 2

12 Inflammatory response is linked to an altered balance of oxidative stress Anti-Oxidants Persistent inflammation Pro-Oxidants IL, interleukin; CXCL, chemokine; GSH, glutathione; NADPH, nicotinamide adenine dinucleotide phosphate-oxidase; AOPP, advanced oxidation protein products; PGs, prostaglandins.

13 Oxidative stress is increased in endometriosis, especially in DIE Oxidative stress is increased further in intestinal DIE N=36 N=28 N=85 N=55 N=31 N=64 N=150 DIE, deep infiltrating endometriosis; SUP, superficial lesion; OMA, endometrioma; AOPP, advanced oxidation protein products. Santulli P et al. Hum Reprod 2015; 30(1):

14 Increased oxidative stress correlates with increased cellular proliferation Endometrioma 1 Superoxide Anion (O 2 --) Hydrogen Peroxide (H 2 O 2 ) Deep infiltrating endometriosis 2 Superoxide Anion (O 2 --) Hydrogen Peroxide (H 2 O 2 ) Epithelial Ce, control endometrial Ee, eutopic endometrial De, deep infiltrating endometriotic Stromal Cs, control endometrial Es, eutopic endometrial Ds, deep infiltrating endometriotic 1. Ngô C et al. Am J Pathol 2009; 175(1): Leconte M et al. Am J Pathol 2011; 179(2):

15 Increased oxidative stress correlates with increased cellular proliferation: Link to MAPK pathway Proliferation ERK perk Controls Eutopic Ectopic NAC H 2 O 2 Production Proliferation Level of untreated cells Level of untreated cells NAC Optic Density perk/erk NAC, N-acetyl-cysteine; ERK, Extracellular signal-regulated kinases; perk, phosphorylated-erk. Ngô C et al. Am J Pathol 2009; 175(1):

16 Inflammation in endometriosis: Molecular intermediates and pathways Sphingosines PTGS2 Adhesion Invasion Inflammation Angiogenesis Proliferation Oxidative Stress Steroidogenesis MAPK pathway PTGS2, prostaglandin-endoperoxide synthase 2

17 MAPK pathway links increased oxidative stress and inflammatory response in endometriosis S1P PDGFR VEGFR IL-33R NADPH oxidase ROS GSH MAPK pathway Angiogenesis Transcriptional regulation Cell proliferation IL, interleukin; NADPH, nicotinamide adenine dinucleotide phosphate-oxidase; GSH, glutathione; PDGFR, platelet-derived growth factor receptors; VEGFR, vascular endothelial growth factor receptor; ROS, reactive oxidative species. Ngô C et al. J Pathol 2010; 222(2): Santulli P et al. Fertil Steril 2012; 97(4): Santulli P et al. Hum Reprod 2012; 27(7):

18 Endometriosis and MAPK Vemurafenib - braf

19 Endometriosis and MAPK Sorafenib raf1- braf - tkr

20 Endometriosis and inflammation Targeting MAP Kinase pathway 2015

21 Future trends Targeting inflammation in endometriosis: MAPK LOCAL SYSTEMIC

22 Future trends Targeting inflammation in endometriosis: MAPK MAPK à " " New non hormonal targeted tretments of endometriosis

23 Conclusions Endometriosis is an Enigmatic Heterogeneous Neurologic Inflammatory disease New treatments could target inflammation and oxidative stress pathways

24 Gynecology Surgical unit: C Chapron, B Borghese, L Marcellin, P Santulli, H Foulot, MC Lafay-Pillet, A Bourret, G Pierre, MC Lamau, P Marzouk, F Decuypere, L Campin Medical unit: A Gompel, G Plu-Bureau, L Maitrot; J Hugon Reproductive endocrinology unit: P Santulli, V Gayet, M Bourdon, C Maignien, F Kefelian, S Eskenazi, S Douard, B Boquet, A Marszalek, A Fubini Intestinal surgery B Dousset, S Gaujoux, M Leconte Radiology AE Millischer, L Maitrot Laboratory: Genetic D Vaiman, F Mondon, S Barbaux Laboratory: Imunulogy F Batteux, S Chouzenoux, C Nicco, C Chéreau, B Weill Laboratory: Reproducive biology JP Wolf, C Patrat, K Pocate, V Lange, JM Kuntzman, C Chalas Statistical unit F Goffinet, PY Ancel A Gompel, Professor and Head, Medical Gynecological unit, P Santulli, Doctor and Head, Reproductive ART and Infertility unit, C Chapron, Professor and Chair, Gynecology Obstetrics II and Reproductive Medicine

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Dr Pietro Santulli. Inserm, Unité de recherche U1016 équipe Pr F. Batteux, Institut Cochin, Paris, France

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