Vasculogenesis: A new piece of the endometriosis puzzle
Abstract
BACKGROUND; Endometriosis is a complex disease with a multifactorial pathogenesis, which is crucially dependent on the development of new blood vessels. Based on the current literature, the present review highlights the fact that the neovascularization of endometriotic lesions is not only driven by angiogenesis, but also involves de novo formation of microvessels from circulating endothelial progenitor cells (EPCs). This process, termed post-natal vasculogenesis, is a characteristic of various pathogenic conditions, such as tumour growth and atherosclerosis, and typically comprises the activation, mobilization and recruitment of bone marrow-derived EPCs to the sites of tissue hypoxia. METHODS ; Literature searches were performed in PubMed, MEDLINE and ISI Web of Knowledge for publications focusing on vasculogenesis in the endometrium and endometriotic lesions. RESULTS ; Recent studies indicate that up to 37% of the microvascular endothelium of ectopic endometrial tissue originates from EPCs, partly controlled by the stromal-cell-derived factor-1/chemokine receptor type 4 axis. Accordingly, blockade of EPC recruitment effectively inhibits the formation of microvascular networks in developing endometriotic lesions, indicating that vasculogenesis represents an integral part of the pathogenesis of endometriosis. CONCLUSIONS ; The involvement of vasculogenesis in endometriosis may offer the exciting opportunity for the future establishment of novel diagnostic and therapeutic strategies for this frequent gynaecological disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The formation of new vessels is a necessary condition for the development of ectopic endometrium, especially in the peritoneal microenvironment.
“The formation of new vessels is a necessary condition for the development of the ectopic endometrium, especially in the peritoneal microenvironment.”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [81]
There is increasing evidence that vasculogenesis plays a role in blood vessel formation during growth of endometriotic lesions.
“There is increasing evidence that vasculogenesis plays a role in blood vessel formation during growth of endometriotic lesions.91,92”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [91]
Cites
Isolation of Putative Progenitor Endothelial Cells for Angiogenesis
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., & Isner, J. M. (1997) · Science · doi:10.1126/science.275.5302.964 · Cited by 8,725 · see citing works
Risau, W. (1997) · Nature · doi:10.1038/386671a0 · Cited by 5,727 · see citing works
Mechanisms of angiogenesis and arteriogenesis
Carmeliet, P. (2000) · Nature Medicine · doi:10.1038/74651 · Cited by 4,146 · see citing works
Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., & Isner, J. M. (1999) · Circulation Research · doi:10.1161/01.res.85.3.221 · Cited by 3,249 · see citing works
Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1
Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., & Gurtner, G. C. (2004) · Nature Medicine · doi:10.1038/nm1075 · Cited by 2,600 · see citing works
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
Circulating endothelial progenitor cells and cardiovascular outcomes
Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., Böhm, M., & Nickenig, G. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa043814 · Cited by 2,048 · see citing works
Giudice, L. C. (2010) · New England Journal of Medicine · doi:10.1056/nejmcp1000274 · Cited by 1,924 · see citing works
Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., Crystal, R. G., Besmer, P., Lyden, D. C., Moore, M. A. S., et al. (2002) · Cell · doi:10.1016/s0092-8674(02)00754-7 · Cited by 1,744 · see citing works
Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration
Rafii, S., & Lyden, D. C. (2003) · Nature Medicine · doi:10.1038/nm0603-702 · Cited by 1,572 · see citing works
Vascular Endothelial Growth Factor
Ferrara, N. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.179663 · Cited by 1,283 · see citing works
Hur, J., Yoon, C., Kim, H.-S., Choi, J., Kang, H., Hwang, K.-K., Oh, B., Lee, M. M., & Park, Y.-B. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000114236.77009.06 · Cited by 1,205 · see citing works
Sata, M., Saiura, A., Kunisato, A., Tojo, A., Okada, S., Tokuhisa, T., Hirai, H., Makuuchi, M., Hirata, Y., & Nagai, R. (2002) · Nature Medicine · doi:10.1038/nm0402-403 · Cited by 1,149 · see citing works
(1984) · PubMed · Cited by 997 · see citing works
Laufs, U., Werner, N., Link, A., Endres, M., Waßmann, S., Jürgens, K., Miche, E., Böhm, M., & Nickenig, G. (2003) · Circulation · doi:10.1161/01.cir.0000109141.48980.37 · Cited by 858 · see citing works
Clonogenicity of Human Endometrial Epithelial and Stromal Cells1
Chan, R. W. S., Schwab, K. E., & Gargett, C. E. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024109 · Cited by 653 · see citing works
Kalka, C., Masuda, H., Takahashi, T., Gordon, R., Tepper, O. M., Gravereaux, E. C., Pieczek, A., Iwaguro, H., Hayashi, S.-I., Isner, J. M., et al. (2000) · Circulation Research · doi:10.1161/01.res.86.12.1198 · Cited by 564 · see citing works
Endothelial progenitor cells for postnatal vasculogenesis
Asahara, T., & Kawamoto, A. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00330.2003 · Cited by 524 · see citing works
Endometrial cells derived from donor stem cells in bone marrow transplant recipients
Taylor, H. S. (2004) · JAMA · doi:10.1001/jama.292.1.81 · Cited by 510 · see citing works
Contribution of bone marrow–derived endothelial cells to human tumor vasculature
Peters, B. A., Diaz, L. A., Polyák, K., Meszler, L., Romans, K., Guinan, E. C., Antin, J. H., Myerson, D., Hamilton, S. R., Vogelstein, B., et al. (2005) · Nature Medicine · doi:10.1038/nm1200 · Cited by 481 · see citing works
Vascular repair by endothelial progenitor cells
Zampetaki, A., Kirton, J. P., & Xu, Q. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn081 · Cited by 472 · see citing works
Strehlow, K., Werner, N., Berweiler, J., Link, A., Dirnagl, U., Priller, J., Laufs, K., Ghaeni, L., Milošević, M., Böhm, M., et al. (2003) · Circulation · doi:10.1161/01.cir.0000077911.81151.30 · Cited by 454 · see citing works
Contribution of Bone Marrow-Derived Stem Cells to Endometrium and Endometriosis
Du, H., & Taylor, H. S. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0828 · Cited by 449 · cited 2× · see citing works
“…marrow-derived EPCs CD31+/VEGFR+/CD45–/GFP Bratincsák et al. (2007) Murine endometrium Bone marrow-derived haematopoietic stem cells CD45+, GFP Du and Taylor (2007) Murine endometrium, murine endometriotic lesions Bone marrow-derived stem cells Y chromosome in females, lacZ Ikoma et al.…”
BackgroundPeripheral biomarkers of endometriosis: a systematic review
May, K. E., Conduit-Hulbert, S. A., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq009 · Cited by 418 · see citing works
Intussusceptive angiogenesis: Its emergence, its characteristics, and its significance
Burri, P. H., Hlushchuk, R., & Djonov, V. (2004) · Developmental Dynamics · doi:10.1002/dvdy.20184 · Cited by 416 · see citing works
Iwakura, A., Luedemann, C., Shastry, S., Hanley, A., Kearney, M., Aikawa, R., Isner, J. M., Asahara, T., & Losordo, D. W. (2003) · Circulation · doi:10.1161/01.cir.0000106906.56972.83 · Cited by 414 · see citing works
Uterine stem cells: What is the evidence?
Gargett, C. E. (2007) · Human Reproduction Update · doi:10.1093/humupd/dml045 · Cited by 373 · see citing works
<i>Stem Cells and the Pathogenesis of Endometriosis</i>
Sasson, I. E., & Taylor, H. S. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1434.014 · Cited by 371 · see citing works
The Relation of Endometriosis to Menstrual Characteristics, Smoking, and Exercise
Cramer, D. W. (1986) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1986.03370140102032 · Cited by 367 · see citing works
Adult stem cells in the endometrium
Gargett, C. E., & Masuda, H. (2010) · Molecular Human Reproduction · doi:10.1093/molehr/gaq061 · Cited by 361 · see citing works
Homing to Hypoxia: HIF-1 as a Mediator of Progenitor Cell Recruitment to Injured Tissue
Ceradini, D. J., & Gurtner, G. C. (2005) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2005.02.002 · Cited by 324 · see citing works
Masuda, H., Matsuzaki, Y., Hiratsu, E., Ono, M., Nagashima, T., Kajitani, T., Arase, T., Oda, H., Uchida, H., Asada, H., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010387 · Cited by 303 · see citing works
Morphometric study of the stromal vascularization in peritoneal endometriosis
Nisolle, M., Casanas‐Roux, F., Anaf, V., Mine, J.-M., & Donnez, J. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55823-3 · Cited by 289 · see citing works
Vascular endothelial growth factor and endometriotic angiogenesis
McLaren, J. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.45 · Cited by 269 · see citing works
Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling
Makanya, A. N., Hlushchuk, R., & Djonov, V. (2009) · Angiogenesis · doi:10.1007/s10456-009-9129-5 · Cited by 243 · see citing works
Vajkoczy, P., Blum, S., Lamparter, M., Mailhammer, R., Erber, R., Engelhardt, B., Vestweber, D., & Hatzopoulos, A. K. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021659 · Cited by 212 · see citing works
Genetic heterogeneity of angiogenesis in mice
Rohan, R. M., Fernandez-Perez, A., Udagawa, T., Yuan, J., & D’Amato, R. J. (2000) · The FASEB Journal · doi:10.1096/fasebj.14.7.871 · Cited by 211 · see citing works
Circulating endothelial progenitor cells in multiple myeloma: implications and significance
Zhang, H. (2004) · Blood · doi:10.1182/blood-2004-06-2101 · Cited by 204 · see citing works
Mechanistic and Therapeutic Implications of Angiogenesis in Endometriosis
Taylor, R. N., Yu, J., Torres, P. B., Schickedanz, A. C., Park, J. K., Mueller, M. D., & Sidell, N. (2008) · Reproductive Sciences · doi:10.1177/1933719108324893 · Cited by 195 · see citing works
Oxidative stress and endometriosis
Jackson, L. W., Schisterman, E. F., Dey-Rao, R., Browne, R. W., & Armstrong, D. (2005) · Human Reproduction · doi:10.1093/humrep/dei001 · Cited by 192 · see citing works
Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation
Demir, R., Yaba, A., & Huppertz, B. (2009) · Acta Histochemica · doi:10.1016/j.acthis.2009.04.004 · Cited by 191 · see citing works
Vascular development in endometriosis
Groothuis, P. G., Nap, A. W., Winterhager, E., & Grümmer, R. (2005) · Angiogenesis · doi:10.1007/s10456-005-9005-x · Cited by 183 · see citing works
Laschke, M. W., & Menger, M. D. (2007) · Human Reproduction Update · doi:10.1093/humupd/dmm006 · Cited by 177 · see citing works
Self-citationMasuda, H., Kalka, C., Takahashi, T., Yoshida, M., Wada, M., Kobori, M., Itoh, R., Iwaguro, H., Eguchi, M., Iwami, Y., et al. (2007) · Circulation Research · doi:10.1161/circresaha.106.144006 · Cited by 170 · see citing works
Laschke, M. W., Elitzsch, A., Vollmar, B., Vajkoczy, P., & Menger, M. (2005) · Human Reproduction · doi:10.1093/humrep/dei308 · Cited by 168 · see citing works
Self-citationBecker, C. M., Rohwer, N., Funakoshi, T., Cramer, T., Bernhardt, W., Birsner, A. E., Folkman, J., & D’Amato, R. J. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.061244 · Cited by 167 · see citing works
Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis
González-Ramos, R., Donnez, J., Defrère, S., Leclercq, I. A., Squifflet, J. P., Lousse, J., & Langendonckt, A. V. (2007) · Molecular Human Reproduction · doi:10.1093/molehr/gam033 · Cited by 154 · see citing works
Estrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153 · cited 1× · see citing works
“Considering the fact that endometriosis is an E2-dependent disease (Rizner, 2009), these findings imply that hormonally regulated EPC mobilization may also play a crucial role in endometriosis (Fig.”
BackgroundRegulation of endothelial progenitor cell homing after arterial injury
Hristov, M., Zernecke, A., Liehn, E. A., & Weber, C. (2007) · Thrombosis and Haemostasis · doi:10.1160/th07-03-0181 · Cited by 151 · see citing works
Mobilization of endothelial progenitor cells in fracture healing and distraction osteogenesis
Lee, D. Y., Cho, T., Kim, J. A., et al. (2008) · Bone · doi:10.1016/j.bone.2008.01.007 · Cited by 151 · see citing works
Circulating endothelial/skeletal progenitor cells for bone regeneration and healing
Matsumoto, T., Kuroda, R., Mifune, Y., Kawamoto, A., Shoji, T., Miwa, M., Asahara, T., & Kurosaka, M. (2008) · Bone · doi:10.1016/j.bone.2008.05.001 · Cited by 148 · see citing works
Mints, M., Jansson, M., Sadeghi, B., Westgren, M., Uzunel, M., Hassan, M., & Palmblad, J. E. W. (2007) · Human Reproduction · doi:10.1093/humrep/dem342 · Cited by 146 · see citing works
Endothelial Progenitor Cells for Vasculogenesis
Murasawa, S., & Asahara, T. (2005) · Physiology · doi:10.1152/physiol.00033.2004 · Cited by 144 · see citing works
Ikoma, T., Kyo, S., Maida, Y., Ozaki, S., Takakura, M., Nakao, S., & Inoue, M. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.07.026 · Cited by 137 · see citing works
Anti-angiogenic effects of green tea catechin on an experimental endometriosis mouse model.
Xu, H., Lui, W. T., Chu, C., Ng, P., Wang, C.-C., & Rogers, M. S. (2008) · Human Reproduction · doi:10.1093/humrep/den417 · Cited by 134 · see citing works
Foubert, P., Silvestre, J., Souttou, B., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci28338 · Cited by 134 · see citing works
Pathogenesis of endometriosis: The role of defective ‘immunosurveillance’
Christodoulakos, G., Augoulea, A., Lambrinoudaki, I., Sioulas, V., & Creatsas, G. (2007) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625180701387266 · Cited by 133 · see citing works
Shi, Q., Wu, M. H.-D., Hayashida, N., Wechezak, A. R., Clowes, A. W., & Sauvage, L. R. (1994) · Journal of Vascular Surgery · doi:10.1016/0741-5214(94)90279-8 · Cited by 132 · see citing works
Xavier, P., Belo, L., Beires, J., Rebelo, I., Martinez-de-Oliveira, J., Lunet, N., & Barros, H. (2006) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-005-0080-4 · Cited by 130 · see citing works
Endothelial precursors in vascular repair
Kirton, J. P., & Xu, Q. (2010) · Microvascular Research · doi:10.1016/j.mvr.2010.02.009 · Cited by 130 · see citing works
The role of the oxidative-stress in the endometriosis-related infertility
Augoulea, A., Mastorakos, G., Lambrinoudaki, I., Christodoulakos, G., & Creatsas, G. (2009) · Gynecological Endocrinology · doi:10.1080/09513590802485012 · Cited by 129 · see citing works
Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis
Meola, J., Silva, J. C. R. E., Dentillo, D. B., Silva, W. A., Veiga-Castelli, L. C., Bernardes, L. Â. D. S., Ferriani, R. A., de Paz, C. C. P., Giuliatti, S., & Martelli, L. R. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.058 · Cited by 120 · see citing works
CD45-Positive Blood Cells Give Rise to Uterine Epithelial Cells in Mice
Bratincsák, A., Brownstein, M., Cassiani‐Ingoni, R., Pastorino, S., Szalayova, I., Tóth, Z., Key, S., Németh, K., Pickel, J. M., & Mezey, É. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0301 · Cited by 118 · see citing works
Immunological aspects of endometriosis
Vinatier, D. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.371 · Cited by 113 · see citing works
The impact of progenitor cells in atherosclerosis
Xu, Q. (2006) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio0396 · Cited by 109 · see citing works
Laschke, M. W., Elitzsch, A., Scheuer, C., Vollmar, B., & Menger, M. D. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.068 · Cited by 100 · see citing works
Self-citationLaschke, M. W., Schwender, C., Scheuer, C., Vollmar, B., & Menger, M. D. (2008) · Human Reproduction · doi:10.1093/humrep/den245 · Cited by 98 · see citing works
Self-citationMatalliotakis, I., Goumenou, A. G., Koumantakis, G. E., Neonaki, M., Koumantakis, E., Dionyssopoulou, E., Athanassakis, I., & Vassiliadis, S. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(02)00216-3 · Cited by 96 · see citing works
Lev, E. I., Estrov, Z. E., Aboulfatova, K., et al. (2006) · Thrombosis and Haemostasis · doi:10.1160/th06-05-0250 · Cited by 85 · see citing works
A Novel Noninvasive Model of Endometriosis for Monitoring the Efficacy of Antiangiogenic Therapy
Becker, C. M., Wright, R. D., Satchi‐Fainaro, R., Funakoshi, T., Folkman, J., Kung, A. L., & D’Amato, R. J. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.051133 · Cited by 84 · see citing works
New Insights in Vascular Development: Vasculogenesis and Endothelial Progenitor Cells
Käßmeyer, S., Plendl, J., Custodis, P., et al. (2009) · Anatomia Histologia Embryologia · doi:10.1111/j.1439-0264.2008.00894.x · Cited by 84 · see citing works
Circulating Endothelial Progenitor Cells Are Up-Regulated in a Mouse Model of Endometriosis
Becker, C. M., Beaudry, P., Funakoshi, T., Benny, O., Zaslavsky, A., Zurakowski, D., Folkman, J., D'Amato, R. J., & Ryeom, S. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2010.12.037 · Cited by 81 · see citing works
Silverman, M. D., Haas, C. S., Rad, A. M., Arbab, A. S., & Koch, A. E. (2007) · Arthritis & Rheumatism · doi:10.1002/art.22706 · Cited by 79 · see citing works
Akt Is a Key Modulator of Endothelial Progenitor Cell Trafficking in Ischemic Muscle
Hur, J., Yoon, C., Lee, C., Kim, T., Oh, I., Park, K. W., Kim, J., Lee, H., Kang, H., Chae, I., et al. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0385 · Cited by 76 · see citing works
(2008) · PubMed · Cited by 74 · see citing works
Endothelial Progenitor Cells Contribute to the Vascularization of Endometriotic Lesions
Laschke, M. W., Giebels, C., Nickels, R. M., Scheuer, C., & Menger, M. D. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2010.11.037 · Cited by 72 · see citing works
Self-citationLaschke, M. W., Elitzsch, A., Scheuer, C., Holstein, J. H., Vollmar, B., & Menger, M. D. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706857 · Cited by 70 · see citing works
Self-citationKatayama, H., Katayama, T., Uematsu, K., Hiratsuka, M., Kiyomura, M., Shimizu, Y., Sugita, A., & Ito, M. (2010) · Human Reproduction · doi:10.1093/humrep/deq241 · Cited by 68 · see citing works
Endothelial progenitor cells correlate with lesion volume and growth in acute stroke
Bogoslovsky, T., Chaudhry, A., Latour, L., et al. (2010) · Neurology · doi:10.1212/wnl.0b013e318200d741 · Cited by 66 · see citing works
Antiangiogenic and vascular-disrupting agents in endometriosis: pitfalls and promises
Langendonckt, A. V., Donnez, J., Defrère, S., Dunselman, G. A. J., & Groothuis, P. G. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan019 · Cited by 66 · see citing works
Zhang, C.-J. (2010) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2010.552 · Cited by 64 · see citing works
Clinical Presentation and Diagnosis of Endometriosis
Galle, P. C. (1989) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(21)00136-4 · Cited by 61 · see citing works
Hematopoietic stem cells and endothelial cell precursors express Tie-2, CD31 and CD45
Shaw, J. P., Basch, R. S., & Shamamian, P. E. (2003) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2003.10.003 · Cited by 60 · see citing works
Hudelist, G., Keckstein, J., Czerwenka, K. F., Lass, H., Walter, I., Auer, M., Wieser, F., Wenzl, R. J., Kubista, E., & Singer, C. F. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.06.014 · Cited by 57 · see citing works
High-Resolution Ultrasound Imaging
Laschke, M. W., Körbel, C., Rudzitis‐Auth, J., Gashaw, I., Reinhardt, M., Hauff, P., Zollner, T. M., & Menger, M. D. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090617 · Cited by 56 · see citing works
Self-citationDuan, H., Cheng, L., Sun, X., et al. (2006) · Thrombosis and Haemostasis · doi:10.1160/th06-04-0199 · Cited by 54 · see citing works
The Role of Endothelial Progenitor Cells in Tumour Vasculogenesis
Ding, Y.-T., Kumar, S., & Yu, D. (2008) · Pathobiology · doi:10.1159/000151706 · Cited by 49 · see citing works
In vivo analysis of angiogenesis in endometriosis-like lesions by intravital fluorescence microscopy
Laschke, M. W., Elitzsch, A., Vollmar, B., & Menger, M. D. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.05.010 · Cited by 49 · see citing works
Self-citationFontaine, V., Filipe, C., Werner, N., Gourdy, P., Billon, A., Garmy-Susini, B. H., Brouchet, L., Bayard, F., Prats, H., Doetschman, T., et al. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.060260 · Cited by 49 · see citing works
Identification of E-selectin as a Novel Target for the Regulation of Postnatal Neovascularization
Liu, Z., Tian, R., An, W., Zhuge, Y., Li, Y., Shao, H., Habib, B., Livingstone, A. S., & Velazquez, O. C. (2010) · Annals of Surgery · doi:10.1097/sla.0b013e3181f5a079 · Cited by 45 · see citing works
Cigarette smoke inhibits recruitment of bone-marrow-derived stem cells to the uterus
Zhou, Y., Gan, Y., & Taylor, H. S. (2010) · Reproductive Toxicology · doi:10.1016/j.reprotox.2010.10.007 · Cited by 45 · see citing works
Antiangiogenic therapies in endometriosis
Ferrero, S., Ragni, N., & Remorgida, V. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706860 · Cited by 44 · see citing works
Bolego, C., Rossoni, G., Fadini, G. P., Vegeto, E., Pinna, C., Albiero, M., Boscaro, E., Agostini, C., Avogaro, A., Gaion, R. M., et al. (2010) · The FASEB Journal · doi:10.1096/fj.09-139220 · Cited by 43 · see citing works
Elevated levels of fibroblast growth factor-2 in serum from women with endometriosis
Бурлев, В. А., Larsson, A. O., & Olovsson, M. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.08.064 · Cited by 36 · see citing works
Körbel, C., Menger, M. D., & Laschke, M. W. (2010) · Human Reproduction · doi:10.1093/humrep/deq201 · Cited by 34 · see citing works
Self-citationEndothelial lineage cell as a vehicle for systemic delivery of cancer gene therapy
Dudek, A. Z. (2010) · Translational research · doi:10.1016/j.trsl.2010.07.003 · Cited by 32 · see citing works
Engineering blood vessels using stem cells: innovative approaches to treat vascular disorders
Kusuma, S., & Gerecht, S. (2010) · Expert Review of Cardiovascular Therapy · doi:10.1586/erc.10.121 · Cited by 31 · see citing works
Clinical Potential of Adult Vascular Progenitor Cells
Kumar, A. H. S., & Caplice, N. (2010) · Arteriosclerosis, Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.198895 · Cited by 27 · see citing works
Circulating endothelial cells as biomarkers of prostate cancer
Georgiou, H. D., Namdarian, B., Corcoran, N. M., Costello, A. J., & Hovens, C. M. (2008) · Nature Clinical Practice Urology · doi:10.1038/ncpuro1188 · Cited by 23 · see citing works
Histological and Electron-Microscopy Studies on Endometriosis
Schweppe, K.-W. (2008) · Hormone Research · doi:10.1159/000181321 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pathogenesis and pathophysiology of endometriosis
Burney, R. O., & Giudice, L. C. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.029 · Cited by 1,590 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
Theories on the pathogenesis of endometriosis
Sourial, S., Tempest, N., & Hapangama, D. K. (2014) · International Journal of Reproductive Medicine · doi:10.1155/2014/179515 · Cited by 418 · see citing works
Peripheral changes in endometriosis-associated pain
Morotti, M., Vincent, K., Brawn, J., Zondervan, K. T., & Becker, C. M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu021 · Cited by 198 · see citing works
Rogers, P. A. W., D’Hooghe, T. M., Fazleabas, A., Giudice, L. C., Montgomery, G. W., Petraglia, F., & Taylor, R. N. (2013) · Reproductive Sciences · doi:10.1177/1933719113477495 · Cited by 154 · see citing works
Chiang, H.-J., Lan, K.-C., Yang, Y.-H., Chiang, J. Y., Kung, F.-T., Huang, F.-J., Lin, Y.-J., Su, Y.-T., & Sung, P.-H. (2021) · Journal of the Formosan Medical Association · doi:10.1016/j.jfma.2020.10.005 · Cited by 42 · see citing works
Integrative analysis reveals regulatory programs in endometriosis
Yang, H., Kang, K., Cheng, C., Mamillapalli, R., & Taylor, H. S. (2015) · Reproductive Sciences · doi:10.1177/1933719115592709 · Cited by 39 · see citing works
Serum YKL-40 levels as a novel marker of inflammation in patients with endometriosis
Ural, Ü. M., Tekin, Y. B., Cüre, M. C., & Şahin, F. K. Ş. (2015) · Clinical and Experimental Obstetrics & Gynecology · doi:10.12891/ceog1882.2015 · Cited by 12 · see citing works
- Authors
- Laschke, M. W., Giebels, C., & Menger, M. D.
- Affiliations
- Saarland University (DE)
- Corresponding author
- Laschke, M.W.
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-05-17
- Volume
- 17
- Issue
- 5
- Pages
- 628-636
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W2146493861
- Cited by
- 136
- References
- 100
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 7 · 2023: 5 · 2022: 5 · 2021: 5 · 2020: 13 · 2019: 10 · 2018: 8 · 2017: 7 · 2016: 16 · 2015: 11 · 2014: 13 · 2013: 13 · 2012: 12
- FWCI
- 1.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- endometriosis, vasculogenesis, endothelial progenitor cells, angiogenesis, neovascularization, endometriotic lesions, CXCL12, bone marrow-derived cells, tissue hypoxia, microvascular endothelium
- MeSH terms
- Cell Movement, Endometriosis, Female, Humans, Neovascularization, Pathologic, Stem Cells, Endothelial Cells, Microvessels
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review