Sensory nerve-derived neuropeptides accelerate the development and fibrogenesis of endometriosis
Open accessAbstract
STUDY QUESTION: Do sensory nerves play any role in the development of endometriosis? SUMMARY ANSWER: Sensory nerves participate in all major steps (epithelial-mesenchymal transition (EMT), fibroblast-to-myofibroblast transdifferentiation (FMT) and smooth muscle metaplasia (SMM)) in the development and fibrogenesis of endometriotic lesions. WHAT IS KNOWN ALREADY: Endometriotic lesions are known to be hyperinnervated due to neurogenesis resulting from neutrophins secreted by endometriotic lesions and possibly platelets. These neutrophins seem to preferentially favour production of sensory neurons at the expense of sympathetic neurons. STUDY DESIGN, SIZE, DURATION: Three independent, yet complementary, prospective, randomized mouse experimentations were conducted. A total of 143 female Balb/C mice and 24 female immunodeficient nude Balb/C mice were used. The mice were sacrificed 2 or 4 weeks after the induction of endometriosis. PARTICIPANTS/MATERIALS, SETTING, METHODS: In Experiment 1, 21 mice were randomly divided into three groups of equal size for sympathetic denervation, sensory denervation and controls. Denervation was carried out chemically. In Experiment 2, 24 nude mice were randomly divided into three equal-sized groups: the BEFORE and AFTER groups that respectively received surgical denervation 3 days before or after the induction of endometriosis by subcutaneous grafting of human endometriotic tissues, and the Control group that received a sham surgery without denervation 3 days before induction. For Experiments 1 and 2, all mice were sacrificed two weeks after induction of endometriosis. In Experiment 3, substance P (SP) and aprepitant, a potent and selective neurokinin 1 receptor (NK1R) antagonist, were used to activate and inhibit the NK1R signalling pathway, respectively. A total of 32 mice were randomly divided into four groups of equal sizes: control (CTL), SP, Before-Induction and After-Induction. One day before the induction of endometriosis, mice in CTL, SP and Before-Induction groups were infused with sterile saline, SP and aprepitant, respectively, via Alzet osmotic pumps. Two weeks after the induction, the After-induction group was infused with aprepitant in similar fashion. All mice were sacrificed four weeks after the induction of endometriosis. In all three experiments, the bodyweight and hotplate latency were evaluated before induction and sacrifice. In addition, all lesions were excised, weighed and processed for quantification and immunohistochemistry analysis of markers for EMT, FMT and SMM, and the extent of fibrosis was evaluated by Masson trichrome staining. MAIN RESULTS AND THE ROLE OF CHANCE: In Experiment 1, chemical denervation of sympathetic and sensory nerves reduced the lesion weight by 43.2% (±23.1%) and 68.7% (±20.3%), respectively, as compared with controls. In particular, sensory denervation led to significantly greater reduction in lesion weight than sympathetic denervation. Sensory denervation also resulted in significantly improved hyperalgesia as compared with controls. In contrast, sympathetic denervation yielded only transient improvement in hyperalgesia. Both sympathetic and sensory denervation resulted in lower immunoreactivity against markers of proliferation and fibrosis, especially sensory denervation.In Experiment 2, surgical denervation before or after induction of endometriosis also decelerated the development of endometriosis, as manifested by significantly reduced lesion weight and extent of lesional fibrosis, along with improved hyperalgesia.In Experiment 3, NK1R activation by SP infusion accelerated lesional development, as evidenced by significantly increased lesional weight, more thorough progression of EMT, FMT, SMM, exaggerated lesional fibrosis and deteriorated hyperalgesia. In contrast, NK1R antagonism decelerated lesional development and improved hyperalgesia. LARGE SCALE DATA: N/A. LIMITATIONS, REASONS FOR CAUTION: This study is limited by the use of histologic and immunohistochemistry analyses only and the lack of molecular data. WIDER IMPLICATIONS OF THE FINDINGS: Since sensory nerves are known to be important in wound healing and fibrogenesis, our findings also give more credence to the notion that endometriotic lesions are wounds undergoing repeated tissue injury and repair. As such, sensory nerves or the NK1R signalling pathway in particular may be potential targets for intervention. STUDY FUNDING/COMPETING INTEREST(S): This research was supported by Grants 81471434 (SWG), 81530040 (SWG), 81771553 (SWG), 81671436 (XSL) and 81871144 (XSL) from the National Natural Science Foundation of China and an Excellence in Centres of Clinical Medicine grant (2017ZZ01016) from the Science and Technology Commission of Shanghai Municipality. None of the authors have anything to disclose.
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Many non-endometriotic cells in the lesional microenvironment, such as platelets, macrophages, and nerve fibers, are actively involved in facilitating lesional development.
“many non-endometriotic cells in the lesional microenvironment, such as platelets21,23, macrophages19,24, and now nerve fibers25,26, are actively involved in facilitating lesional development.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [25]
Regardless of subtypes, all endometriotic lesions appear to undergo identical molecular processes such as EMT, FMT, SMM, and fibrogenesis, even in adenomyotic lesions.
“regardless of subtypes, all endometriotic lesions appear to undergo identical molecular processes such as epithelial-mesenchymal transition (EMT), fibroblast-to-myofibroblast transdifferentiation (FMT), smooth muscle metaplasia (SMM), and fibrogenesis25,26,53, even in adenomyotic lesions81,82.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [25]
Antagonism of neurokinin 1 receptor (NK1R), the SP receptor, significantly reduced lesional fibrosis.
“the antagonism of neurokinin 1 receptor (NK1R), the SP receptor, also achieved the same effect35.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [35]
Chemical denervation of sensory nerves in mouse models resulted in significantly less lesional fibrosis than denervation of sympathetic nerves.
“we found, via mouse models, that chemical denervation of sensory nerves resulted in significantly less lesional fibrosis than denervation of sympathetic nerves35.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [35]
Surgical denervation of sensory nerves significantly reduced lesional fibrosis.
“surgical denervation of sensory nerves significantly reduced lesional fibrosis”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [35]
Sensory nerve fibers play a potent facilitatory role in expediting the development and fibrogenesis of endometriotic lesions.
“These data, taken together with our in vivo data35 in conjunction with the successful establishment of a mouse DE model of by infusion of SP and CGRP in addition to i.p. endometrium injection45 provide an additional strong piece of evidence that sensory nerve fibers play a potent facilitatory role in expediting the development and fibrogenesis of endometriotic lesions.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [35]
Sensory nerve-derived neuropeptides accelerate lesional fibrogenesis through similar processes.
“In this and our in vivo studies35, we have shown that sensory nerve-derived neuropeptides also accelerate lesional fibrogenesis through similar processes.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [35]
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Cassidy, M., Sheldon, H., Gainsbury, M. L., Gillespie, E., Kosaka, H., Heydrick, S., & Stucchi, A. (2014) · Journal of Surgical Research · doi:10.1016/j.jss.2014.04.030 · Cited by 19 · see citing works
Nanji, A. A., Liong, E. C., Xiao, J., et al. (2012) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01838.x · Cited by 17 · see citing works
Endometriosis-Derived Thromboxane A2 Induces Neurite Outgrowth
Yan, D., Liu, X., & Guo, S.-W. (2017) · Reproductive Sciences · doi:10.1177/1933719116670037 · Cited by 17 · see citing works
Self-citationSubstance P–Neurokinin-1 receptor interaction upregulates monocyte tissue factor
Khan, M. M., Douglas, S. D., & Benton, T. D. (2011) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2011.10.012 · Cited by 16 · see citing works
Migrating action potential complex: unmasked by 6-hydroxydopamine
Mathias, J. R., Clench, M. H., Davis, R. H., et al. (1985) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1985.249.3.g416 · Cited by 14 · see citing works
The neurokinin 1 receptor: a potential new target for anti-platelet therapy?
Jones, S., & Gibbins, J. M. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.01.004 · Cited by 12 · see citing works
Yamaguchi, R., Yamamoto, T., Sakamoto, A., Ishimaru, Y., 楢原, 真., Sugiuchi, H., & Yamaguchi, Y. (2016) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2016.01.006 · Cited by 11 · see citing works
Wang, K. Y., Lu, D., Zhang, B., et al. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000452561 · Cited by 11 · see citing works
Tweaking the gain on platelet regulation: The tachykinin connection
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Flagged first, then by citations
Research works printed but not linked: 1
- Long Q, Liu X, Guo SW. Surgery accelerates the development of endo- metriosis in mouse. Am J Obstet Gynecol 2016;215:320.e1-320.e15.
Cited by
Sorted by citations
Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96 · see citing works
Self-citationYan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · see citing works
Self-citationQi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
Self-citationQi, Q.-M., Guo, S.-W., & Liu, X.-S. (2019) · Reproductive and Developmental Medicine · doi:10.4103/2096-2924.262390 · Cited by 15 · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citation
- Authors
- Liu, X., Yan, D., & Guo, S.-W.
- Affiliations
- Fudan University (CN)
- Corresponding author
- Guo, Sun-Wei
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-01-28
- Volume
- 34
- Issue
- 3
- Pages
- 452-468
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2912583275
- Cited by
- 51
- References
- 92
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 6 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 6
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation of China (81471434, 81530040, 81771553, 81671436, 81871144)
- Excellence in Centers of Clinical Medicine grant (2017ZZ01016)
- Science and Technology Commission of Shanghai Municipality
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, sensory nerves, neuropeptides, sensory denervation, sympathetic denervation, epithelial-mesenchymal transition, fibroblast-to-myofibroblast transdifferentiation, substance P, neurokinin-1 receptor, aprepitant, hyperinnervation
- MeSH terms
- Animals, Blood Platelets, Cell Differentiation, Denervation, Endometriosis, Female, Fibroblasts, Humans, Hyperalgesia, Mice, Inbred BALB C, Mice, Nude, Muscle, Smooth, Neuropeptides, Random Allocation, Sensory Receptor Cells, Signal Transduction, Receptors, Neurokinin-1, Myoblasts, Cell Proliferation, Mice
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.
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