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• W2005693586 abstract "To investigate the role of the nerve growth factor (NGF) in the endometriosis-associated innervation in the development of endometriosis-associated symptoms, 41 peritoneal fluid samples (PF) from patients with surgically and histologically proven endometriosis and 20 PF from patients with other gynecologic conditions were analyzed with Western blot and a novel in vitro model using dorsal root ganglia (DRG) to show neuronal outgrowth; endometrial cells also were analyzed. The results suggest that the PF of endometriosis patients and endometriotic lesions have neurotropic properties, because the Western blot analysis and the cell culture stainings showed NGF expression, and the neurite outgrowth of DRG treated with PF of patients with endometriosis was significantly higher than when treated with PF of patients without endometriosis. Furthermore, blocking NGF with both anti-NGF and K252a leads to a significant decrease in neurite outgrowth. To investigate the role of the nerve growth factor (NGF) in the endometriosis-associated innervation in the development of endometriosis-associated symptoms, 41 peritoneal fluid samples (PF) from patients with surgically and histologically proven endometriosis and 20 PF from patients with other gynecologic conditions were analyzed with Western blot and a novel in vitro model using dorsal root ganglia (DRG) to show neuronal outgrowth; endometrial cells also were analyzed. The results suggest that the PF of endometriosis patients and endometriotic lesions have neurotropic properties, because the Western blot analysis and the cell culture stainings showed NGF expression, and the neurite outgrowth of DRG treated with PF of patients with endometriosis was significantly higher than when treated with PF of patients without endometriosis. Furthermore, blocking NGF with both anti-NGF and K252a leads to a significant decrease in neurite outgrowth. Endometriosis is a benign estrogen-dependent inflammatory disease, characterized by the presence of endometrial-like tissue outside the uterine cavity. The main symptoms of endometriosis are dysmenorrhea, chronic pelvic pain, dyspareunia, dyschezia, dysuria, and infertility. It seems that the expression of pain-mediating substances, such as prostaglandins, histamines, kinins, and interleukins, in endometriotic implants are involved in the activation of peritoneal nociceptors and in pain mediation (1Vercellini P. Trespidi L. de Giorgi O. Cortesi I. Parazzini F. Crosignani P.G. Endometriosis and pelvic pain: relation to disease stage and localization.Fertil Steril. 1996; 65: 299-304Abstract Full Text PDF PubMed Google Scholar, 2Vernon M.W. Beard J.S. Graves K. Wilson E.A. Classification of endometriotic implants by morphologic appearance and capacity to synthesize prostaglandin F.Fertil Steril. 1986; 46: 801-806Abstract Full Text PDF PubMed Google Scholar, 3Muzii L. Marana R. Pedulla S. Catalano G.F. Mancuso S. Correlation between endometriosis-associated dysmenorrhea and the presence of typical or atypical lesions.Fertil Steril. 1997; 68: 19-22Abstract Full Text PDF PubMed Scopus (71) Google Scholar). However, the pathophysiology of the peritoneal endometriosis-related pelvic pain is still not well understood. There is evidence that endometriosis may be related to neurotropic events, because neurotropins such as nerve growth factor (NGF) and neurotropin-3 (NT-3) are expressed in endometriotic implants (4Mechsner S. Schwarz J. Thode J. Loddenkemper C. Salomon D.S. Ebert A.D. Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions.Fertil Steril. 2007; 88: 581-587Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar, 5Anaf V. Simon P. el Nakadi I. Fayt I. Simonart T. Buxant F. et al.Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis.Hum Reprod. 2002; 17: 1895-1900Crossref PubMed Scopus (245) Google Scholar). The presence of growth-associated protein (GAP) 43 in endometriosis-associated nerve fibers and the colocalization of these nerve fibers with immature blood vessels have also been shown, suggesting that endometriosis-associated nerve fibres are formed anew (4Mechsner S. Schwarz J. Thode J. Loddenkemper C. Salomon D.S. Ebert A.D. Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions.Fertil Steril. 2007; 88: 581-587Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar). However, the neurotropic events in endometriosis have, to our knowledge, not been studied well. To understand the role of neurotropic substances in endometriosis, we investigated the NGF expression in peritoneal fluid (PF) from women with endometriosis using an in vitro neuronal growth assay. Peritoneal fluid was obtained from 41 patients undergoing diagnostic laparoscopy for symptomatic endometriosis. All of the patients were surgically and histologically diagnosed with peritoneal endometriosis at revised American Society for Reproductive Medicine stages I to IV (I = 12; II = 11; III = 8; and IV = 10) (6American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: 1996.Fertil Steril. 1997; 67: 817-821Abstract Full Text PDF PubMed Scopus (2202) Google Scholar). The mean age was 37.12 ± 9.2 years. Twenty-seven women had regular menstrual cycles and no hormonal treatment. Twelve women were in the secretory and 15 in the proliferative phase. Fourteen patients were on hormonal treatment at the time of surgery. Patients having undergone laparoscopy for other benign gynecologic conditions (uterine fibroids or myomata) were used as a control group (n = 20). Endometriotic biopsies (peritoneal lesions = 2, endometriotic cysts = 5) for the cell culture experiments were collected from patients with regular menstrual cycles in the proliferative phase with a mean age of 35 ± 5.7 years. Each of the patients gave consent for these biopsies, and the study was approved by the Institutional Review Board. Cell cultures were prepared from endometriotic tissues (endometriotic cysts = 5; peritoneal lesions = 2). Cultured endometriotic cells were plated onto glass coverslips, fixed with 4% paraformaldehyde, and stained with the polyclonal rabbit anti-NGF antibody and monoclonal mouse antivimentin antibody for stromal cell, or monoclonal mouse anti-cytokeratin antibody for epithelial cell characterization. Peritoneal fluid from endometriosis patients (n = 10) and from patients without endometriosis (n = 5) was prepared for Western blot analysis. The protein extracts were immunostained with anti-NGF mouse monoclonal antibody, rabbit antimouse peroxidase antibody, and enhanced chemiluminescence. Mononuclear cell factor 7 (MCF 7) lysates were used as positive control samples. Valo specific-pathogen free (SPF) eggs were incubated for 9 days. The embryonal dorsal root ganglia (DRG) were dissected and incubated in 8-well chamber slides with various media as follows:Dulbecco modified Eagle medium (DMEM; negative control).DMEM + 10 ng/mL NGF-2.5 S (positive control).PF from women with endometriosis (50% PF + 50% DMEM without and with 20 ng/mL anti-NGF and 200 nmol/L K252a).PF from women without endometriosis (50% PF + 50% DMEM). The area occupied by the neurites was established using a subjective score after taking pictures of the ganglia. These ratings were 0 for no neurite outgrowth, 1 for only a few isolated neurites, 2 if the neurites grew to more than one-fourth of the ganglia body size, and 3 for more than one-half of the ganglia body size (7Finas D. Huszar M. Agic A. Dogan S. Kiefel H. Riedle S. et al.L1 cell adhesion molecule (L1CAM) as a pathogenetic factor in endometriosis.Hum Reprod. 2008; 23: 1053-1062Crossref PubMed Scopus (33) Google Scholar). Each fluid was tested at least three times and the average score was recorded. After 48 hours, the ganglia were fixed with 4% paraformaldehyde, permeabilized with 0.2% Triton X-100 and stained with the monoclonal mouse antineurofilament (anti-NF) antibody or with monoclonal mouse anti–GAP 43. Ganglia were then incubated with rhodamine red–conjugated antibody. Fluorescence was detected with a radiophoto microscope. Endometriotic primary cells, double stained with NGF and vimentin or cytokeratin (Fig. 1A ) were NGF positive and therefore considered to be expressing NGF. We performed Western blot analyses of PF from patients with and without endometriosis. Anti-NGF antibodies were used to investigate NGF expression in the PF. We were able to detect a 27-kDa specific band in the PF from women with and without endometriosis. The NGF expression seemed to be much stronger in women with endometriosis (Fig. 1B). The neuronal growth assay was used to investigate neurotropic properties of endometriosis. The interplay of DRG with the PF of patients with and without endometriosis was analyzed. PF consists of the secretion of the surface cells, including endometriotic cells in patients with endometriosis. Ganglia incubated with PF from women with endometriosis showed neurite growth (P<.001) similar to that of the positive control (P>.05; Fig. 1C). DMEM medium alone showed no neurite outgrowth. The PF from patients without endometriosis only induced marginal neurite outgrowth (P<.01; Fig. 1C). A significant increase in the area occupied by neurites of ganglia treated with PF from women with endometriosis could be observed when compared with both the negative control (P<.001) and women without endometriosis (P<.01; Fig. 1C). We could not find any difference in the neurite outgrowth between patients undergoing hormone therapy and those not under therapy. Moreover, the outgrowth was seen to be independent of the cyclic phase (data not shown). Ganglia were NF and GAP 43 positive with immunofluorescence (Fig. 1D), demonstrating newly grown nerve fibers. Ganglia from patients without endometriosis also showed a positive, but weaker, signal (data not shown). The negative control showed no staining. We inhibited NGF with two potent NGF inhibitors (anti-NGF and K252a).The neurite outgrowth of ganglia treated with PF from women with endometriosis was significantly inhibited with both (P<.001; Fig. 1E). In this study we provide, to the best of our knowledge, the first description of neurotropic properties in endometriosis. Our investigation revealed the expression of NGF in endometriotic stromal and epithelial cells. We observed significantly stronger neurite outgrowths in patients with endometriosis. The neuronal growth assay showed significant outgrowth, and the inhibition confirmed that this outgrowth may be due to NGF. A close morphologic connection between peritoneal sensory nerves fibers and endometriotic implants has already been shown with immunohistochemistry. Furthermore, peritoneal endometriotic lesions have been shown to express neurotrophic factors such as NGF and NT-3 (4Mechsner S. Schwarz J. Thode J. Loddenkemper C. Salomon D.S. Ebert A.D. Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions.Fertil Steril. 2007; 88: 581-587Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar), suggesting the involvement of endometriosis in neurotropic events. Also, neurotropic events due to endometriosis have been shown in a rat model for endometriosis (8Berkley K.J. Dmitrieva N. Curtis K.S. Papka R.E. Innervation of ectopic endometrium in a rat model of endometriosis.Proc Natl Acad Sci U S A. 2004; 101: 11094-11098Crossref PubMed Scopus (181) Google Scholar). This animal model shows the outgrowth of several sensory, cholinergic and sympathetic nerve fibres in ectopic uterine tissue. It has also been reported that neurite outgrowth in endometrial tissue seems to be induced by the neural cell adhesion molecule (7Finas D. Huszar M. Agic A. Dogan S. Kiefel H. Riedle S. et al.L1 cell adhesion molecule (L1CAM) as a pathogenetic factor in endometriosis.Hum Reprod. 2008; 23: 1053-1062Crossref PubMed Scopus (33) Google Scholar). As has been shown, NGF produces an outgrowth of neurites from ganglia (7Finas D. Huszar M. Agic A. Dogan S. Kiefel H. Riedle S. et al.L1 cell adhesion molecule (L1CAM) as a pathogenetic factor in endometriosis.Hum Reprod. 2008; 23: 1053-1062Crossref PubMed Scopus (33) Google Scholar, 9Bilsland J. Rigby M. Young L. Harper S. A rapid method for semi-quantitative analysis of neurite outgrowth from chick DRG explants using image analysis.J Neurosci Methods. 1999; 92: 75-85Crossref PubMed Scopus (69) Google Scholar, 10Snider W.D. Silos-Santiago I. Dorsal root ganglia neurons require functional neurotrophin receptors for survival during development.Philos Trans R Soc Lond B Biol Sci. 1996; 351: 395-403Crossref PubMed Scopus (82) Google Scholar, 11Jones M.G. Munson J.B. Thompson S.W. A role for nerve growth factor in sympathetic sprouting in rat dorsal root ganglia.Pain. 1999; 79: 21-29Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar) and neural cell lines (12Hashimoto S. K-252a, a potent protein kinase inhibitor, blocks nerve growth factor–induced neurite outgrowth and changes in the phosphorylation of proteins in PC12h cells.J Cell Biol. 1988; 107: 1531-1539Crossref PubMed Scopus (94) Google Scholar, 13Matrone C. di Luzio A. Meli G. d’Aguanno S. Severini C. Ciotti M.T. et al.Activation of the amyloidogenic route by NGF deprivation induces apoptotic death in PC12 cells.J Alzheimers Dis. 2008; 13: 81-96PubMed Google Scholar, 14Greene L.A. Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.Proc Natl Acad Sci U S A. 1976; 73: 2424-2428Crossref PubMed Scopus (4800) Google Scholar, 15Nakayama T. Asami S. Ono S. Miura M. Hayasaka M. Yoshida Y. et al.Effect of cell differentiation for neuroblastoma by vitamin K analogs.Jpn J Clin Oncol. 2009; 39: 251-259Crossref PubMed Scopus (8) Google Scholar, 16Kimpinski K. Mearow K. Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase.J Neurosci Res. 2001; 63: 486-499Crossref PubMed Scopus (92) Google Scholar). We used DRG as an in vitro model for neuronal outgrowth. As has been described previously, this system has become an established method to study nerve outgrowth in other diseases (7Finas D. Huszar M. Agic A. Dogan S. Kiefel H. Riedle S. et al.L1 cell adhesion molecule (L1CAM) as a pathogenetic factor in endometriosis.Hum Reprod. 2008; 23: 1053-1062Crossref PubMed Scopus (33) Google Scholar, 17Ayala G.E. Wheeler T.M. Shine H.D. Schmelz M. Frolov A. Chakraborty S. et al.In vitro dorsal root ganglia and human prostate cell line interaction: redefining perineural invasion in prostate cancer.Prostate. 2001; 49: 213-223Crossref PubMed Scopus (161) Google Scholar, 18Gil Z Cavel O Kelly K Brader P Rein A Gao SP et al.Paracrine regulation of pancreatic cancer cell invasion by peripheral nerves.J Natl Cancer Inst. 2010; 102: 107-118Crossref PubMed Scopus (162) Google Scholar). Because it has been shown that NGF may play an important role in innervation in endometriosis (4Mechsner S. Schwarz J. Thode J. Loddenkemper C. Salomon D.S. Ebert A.D. Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions.Fertil Steril. 2007; 88: 581-587Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar), we wanted to prove this hypothesis. Also, Bersinger et al. (19Bersinger N.A. Brodbeck M.H. Jahns B. Mueller M.D. Effect of peritoneal fluid from endometriosis patients on neuroblastoma cells in culture.Gynecol Endocrinol. 2009; 25: 707-712Crossref PubMed Scopus (2) Google Scholar) demonstrated proliferation of neuronal cell lines incubated in PF from women with endometriosis, suggesting the presence of NGF. As far as we know, we are the first to demonstrate, using the neuronal growth assay, the presence of NGF in PF of women with endometriosis, because the ganglia reveal strong neurite outgrowth after treatment with the PF from women with endometriosis. There were only marginal neurite outgrowth after treating ganglia with PF from women without endometriosis, and this growth could be explained by the fact that all of these fluids were from women with other gynecological disease and not from healthy women. Nevertheless, the neurite outgrowth was significantly stronger in patients with endometriosis compared with patients without endometriosis. Our results reinforce the hypothesis that neurotropic events are strongly related to endometriosis. Neurite outgrowth does not seem to be influenced by hormonal treatment of the patients; the cycle phase also appears to be uninvolved in this outgrowth. The stained ganglia were NF and GAP 43 positive, indicating a new growth of the nerves, because GAP 43 stands for the development of nerves as well as its regeneration (4Mechsner S. Schwarz J. Thode J. Loddenkemper C. Salomon D.S. Ebert A.D. Growth-associated protein 43–positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions.Fertil Steril. 2007; 88: 581-587Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar, 20Ferretti A. Boschi E. Stefani A. Spiga S. Romanelli M. Lemmi M. et al.Angiogenesis and nerve regeneration in a model of human skin equivalent transplant.Life Sci. 2003; 73: 1985-1994Crossref PubMed Scopus (36) Google Scholar). To verify that the neurite outgrowth shown in the DRG after treatment with PF from women with endometriosis was an effect due to NGF and not to other neurotropic factors, such as NT-3, NT-4, or brain-derived neurotropic factor (BDNF) (21Bennett D.L. Neurotrophic factors: important regulators of nociceptive function.Neuroscientist. 2001; 7: 13-17Crossref PubMed Scopus (126) Google Scholar), we intentionally inhibited NGF with two different NGF inhibitors; anti-NGF and K252a. Anti-NGF binds to NGF, blocking the TrkA receptor binding site. The inhibition of NGF with anti-NGF prevents inflammatory hyperalgesia in different inflammatory models (22Abdiche Y.N. Malashock D.S. Pons J. Probing the binding mechanism and affinity of tanezumab, a recombinant humanized anti-NGF monoclonal antibody, using a repertoire of biosensors.Protein Sci. 2008; 17: 1326-1335Crossref PubMed Scopus (120) Google Scholar, 23Lecht S. Arien-Zakay H. Kohan M. Lelkes P.I. Lazarovici P. Angiostatic effects of K252a, a Trk inhibitor, in murine brain capillary endothelial cells.Mol Cell Biochem. 2010; 339: 201-213Crossref PubMed Scopus (17) Google Scholar). K252a blocks the NGF-mediated changes in the phosphorylation of proteins and neurite outgrowth in PC12 cells (12Hashimoto S. K-252a, a potent protein kinase inhibitor, blocks nerve growth factor–induced neurite outgrowth and changes in the phosphorylation of proteins in PC12h cells.J Cell Biol. 1988; 107: 1531-1539Crossref PubMed Scopus (94) Google Scholar, 23Lecht S. Arien-Zakay H. Kohan M. Lelkes P.I. Lazarovici P. Angiostatic effects of K252a, a Trk inhibitor, in murine brain capillary endothelial cells.Mol Cell Biochem. 2010; 339: 201-213Crossref PubMed Scopus (17) Google Scholar). In the present study, we showed that both of these NGF inhibitors blocked neurite outgrowth in DRG. However, we found only a reduction of the neurite outgrowth and not a total lack, suggesting the presence of other nerve growth factors in endometriosis. Our results suggest that NGF is an important neurotropic factor for the mediation of nerve growth and innervation in peritoneal endometriosis. Future studies are needed to demonstrate whether or not its antibody can be helpful in the treatment of endometriosis. Further investigations will have to be carried out to clarify the influence of NGF in pain generation of endometriosis-related symptoms. The authors thank Dr. F. Sacher (Bayer Schering Pharma) for helpful discussions and Ms. C Rüster for her excellent technical assistance." @default.
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• W2005693586 title "Overexpression of nerve growth factor in peritoneal fluid from women with endometriosis may promote neurite outgrowth in endometriotic lesions" @default.
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