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Hematogenous Dissemination of Mesenchymal Stem Cells From TISSUE‐SPECIFIC STEM CELLS Department of Obstetrics, Gyne‐ Hematogenous Dissemination of Mesenchy‐ cology & Reproductive Sciences, mal Stem Cells from Endometriosis Yale School of Medicine, New Ha‐ 1 ven, CT 06520; Department of 1 1 1 1 Obstetrics and Gynecology and FEI LI MYLES H. ALDERMAN III , AYA TAL , RAMANAIAH MAMILLAPALLI , 1 1 1 Reproductive Sciences, Yale School ALEXIS COOLIDGE , DEMETRA HUFNAGEL , ZHIHAO WANG , 1 1 1 of Medicine, New Haven, Connect‐ ELHAM NEISANI , STEPHANIE GIDICSIN , GRACIELA KRIKUN , 1 icut. HUGH S. TAYLOR Address all correspondence and requests for reprints to: Hugh S. Key words. Mesenchymal stem cells (MSCs) Stromal derived factor‐1 (SDF‐ Taylor, Department of Obstetrics, 1) Cellular proliferation Differentiation Gynecology and Reproductive Sci‐ ences, Yale School of Medicine, 333 Cedar Street, New Haven, CT, USA, 06520, Phone: 203‐785‐4001, ABSTRACT [email protected]. Received March 22, 2017; accept‐ Endometriosis is ectopic growth of endometrial tissue traditionally thought ed for publication January 19, to arise through retrograde menstruation. We aimed to determine if cells 2018; available online without sub‐ derived from endometriosis could enter vascular circulation and lead to scription through the open access hematogenous dissemination. Experimental endometriosis was estab‐ option. lished by transplanting endometrial tissue from DsRed+ mice into the peri‐ ©AlphaMed Press toneal cavity of DsRed‐ mice. Using flow cytometry, we identified DsRed+ 1066‐5099/2018/$30.00/0 cells in blood of animals with endometriosis. The circulating donor cells This article has been accepted for expressed CXCR4 and mesenchymal stem cell (MSC) biomarkers, but not publication and undergone full hematopoietic stem cell markers. Nearly all the circulating endometrial peer review but has not been stem cells originated from endometriosis rather than from the uterus. Cells through the copyediting, typeset‐ expressing DsRed, CXCR4 and MSCs markers were identified in the perito‐ ting, pagination and proofreading neal wall and surrounding vessels of recipient mice, contributing to both process which may lead to differ‐ endometriosis and angiogenesis. Cells originating in endometriosis lesions ences between this version and the migrated and implanted in lung tissue and displayed makers of differentia‐ Version of Record. Please cite this tion, indicating retained multipotency. In vitro these cells demonstrated article as doi: 10.1002/stem.2804 multipotency and were able to differentiate into adipogenic, osteogenic, and chondrogenic lineages. Endometriosis lesions also expressed high lev‐ els of CXCL12, the CXCR4 receptor ligand. Serum CXCL12 levels were great‐ er than in sham control mice. In humans with endometriosis, serum CXCL12 levels were significantly higher than controls, suggesting that the CXCL12/CXCR4 axis is operational in women with spontaneous endometri‐ osis as well. Stem cells, rather than differentiated cells from endometriosis, enter the circulation in response to CXCL12. We identify an endometriosis‐ derived stem cell population, a potential mechanism of dissemination of this disease and a potential target for treatment of endometriosis. STEM CELLS 2017; 00:000–000 SIGNIFICANCE STATEMENT Endometriosis is ectopic growth of endometrial tissue traditionally thought to arise through retrograde menstruation. We aimed to determine if stem cells in endometriosis lesions were present in the circulation thus propagat‐ ing the disease. We identified circulating endometrial stem cells originating from endometriosis rather than the uterus, providing a potential etiology for remote endometriosis lesions. A clear majority of cells in circulation from STEM CELLS 2017;00:00‐00 www.StemCells.com ©AlphaMed Press 2017 2 Hematogenous MSCs from Endometriosis endometriosis lesions express stem cell markers. Endometriosis derived mesenchymal stem cells contrib‐ mesenchymal stem cell markers ute to lesion angiogenesis and proliferation, and may provide a novel etiolo‐ and CXCR4, but not hematogenous gy for remote lesion propagation in humans. INTRODUCTION neal wall. In the endometriosis plus ovariectomy group (EMS+OVX group, n=10), each host underwent simulta‐ Endometriosis is a chronic, estrogen‐dependent condi‐ neous ovariectomy as well as endometriosis induction tion in which ectopic endometrial glands and stroma as described above. In control groups, sham surgeries are present outside the uterine cavity. Endometriosis were conducted either with (n=10) or without ovariec‐ has been estimated to affect approximately 10% of re‐ tomy (n=10), placing sutures in the peritoneal wall. An‐ productive‐age women, 25% to 50% of women with imals were treated with 1 mg/kg/day SQ of Meloxicam infertility, and up to 50% of women with pelvic pain as an analgesic for 72hrs post‐operatively. [1,2]. While endometriosis lesions are primarily located in the pelvis they have also been found in areas remote Flow Cytometry Analysis and Cell Sorting from the peritoneal cavity including pericardium, pleu‐ (FACS) of Circulating Ectopic Cells ra, lung parenchyma, liver, spine, and the brain [3,4]. FACS analysis was performed after surgeries at set in‐ The definitive pathogenesis of endometriosis re‐ tervals to determine the presence of donor DsRed‐ mains uncertain; the most commonly accepted mecha‐ positive cells in the peripheral blood. We collected nism is Sampson's theory of retrograde menstruation, 100μl of peripheral blood from each mouse by cheek whereby endometrial cells are shed through the fallopi‐ puncture into tubes pre‐treated with unfractionated an tubes into the peritoneal cavity [5]. While this theory heparin. Blood was kept on ice until processing, and red explains intraperitoneal endometriosis lesions, to ac‐ blood cells were lysed using ACK Lyse Solution (Life count for the presence of endometriosis at distant sites Technique, New York, USA), per the manufacturer's outside the pelvis it has been suggested that lymphatic directions. and hematogenous migration of endometrial tissue Flow cytometry was performed using a Beckman contributes to the pathogenesis of endometriosis [5,6]. Coulter MoFlo (Beckman Coulter, SanJose, CA) and ac‐ In previous studies we demonstrated in both humans quired data were analyzed with FLOWJO flow cytometry and a murine endometriosis model that bone marrow‐ analysis software v9.5 (Treestar, Ashland, OR) with derived mesenchymal stem cells contribute to the analysis gates designed to remove residual platelets and makeup of the eutopic endometrium and to endome‐ cellular debris. RFP‐positive cells were defined by set‐ triosis lesions, likely traveling through the circulatory ting gates to exclude any background DsRed signaling system [7,8]. found in control animals and IgG isotype staining. Be‐ Here we hypothesized that vascular metastasis of tween 500,000 and 1,000,000 events were counted in endometriosis‐derived mesenchymal stem cells may be each sample, and duplicate measurements were per‐ a source of new lesions and contribute to pre‐existing formed for each sample. DsRed positive cells were sort‐ distant endometriosis [9]. To investigate the potential ed into sterile PBS on ice for further qRT‐PCR and fluo‐ contribution of circulating ectopic endometrial‐derived rescent‐immunocytochemistry analysis. cells to the pathogenesis of endometriosis, we used an established mouse model of surgically induced endome‐ Fluorescent ‐Immunocytochemistry (FICC) triosis to identify and characterize circulating endome‐ Sorted cells were smeared on slides and fixed using 4% triosis derived cells. paraformaldehyde overnight and blocked with 5% BSA for two hours. Slides were incubated with primary anti‐ EXPERIMENTAL PROCEDURES body (1:200 diluted in PBS with 1% donkey serum) in a humidified chamber overnight at 4°C, followed by and Experimental murine endometriosis secondary antibodies for 1 h at 37 . Primary antibod‐ All murine experiments were approved by the Yale In‐ ies used included goat polyclonal DsRed (Santa Cruz stitutional Animal Care and Use Committee (IACUC, Biotechnology, sc‐33354, Dallas, TX), rabbit polyclonal 2014‐07113). The endometriosis mouse model was cre‐ anti‐CD140B (abcam, ab32570, Cambridge, UK), rat pol‐ ated using forty C57BL/6 female mice obtained from yclonal anti‐CD146 (abcam, ab75769), followed by don‐ Charles River Laboratories (Wilmington, MA) as tissue key‐anti‐goat secondary antibody AlexaFluor® 633 (Life recipients and ten DsRed mice [Tg(CAGDsRed* Technologies, A‐21082, Carlsbad, CA), donkey‐anti‐ MST)1Nagy/J (Jackson Laboratories, Bar Harbor) [10– rabbit secondary antibody AlexaFluor® 568 (Life Tech‐ 12]. In the endometriosis group (EMS group, n=10), nologies, A‐10012) and donkey anti‐rat secondary anti‐ each recipient animal received one DsRed donor uterus body AlexaFluor® 488 (Life Technologies, A‐21208) con‐ cut into three one‐centimeter segments. Each segment jugate for 1 h at 37 °C respectively. Vectashield/4, 6‐ was sutured into the peritoneum at separate sites so diamidino‐2‐phenylindole (DAPI, Vector laboratories, that the uterine serosa was in contact with the perito‐ Peterborough, UK) was added onto the cells before ob‐ www.StemCells.com ©AlphaMed Press 2017 3 Hematogenous MSCs from Endometriosis servation on a Zeiss LSM 710 Duo NLO/Multiphoton the peritoneum (4 in each side) of C57BL/6J females, Confocal Microscope (Zeiss Company, Germany). Nega‐ with the luminal side facing the peritoneum. Females tive and positive controls for DsRed consisted of smears were kept cycling
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