Scar matrix drives Piezo1 mediated stromal inflammation leading to placenta accreta spectrum.
Female
Pregnancy
Humans
Placenta Accreta
/ metabolism
Cicatrix
/ metabolism
Ion Channels
/ metabolism
Animals
Inflammation
/ metabolism
Trophoblasts
/ metabolism
Decidua
/ pathology
Mice
NF-kappa B
/ metabolism
Cesarean Section
/ adverse effects
Protein Kinase C
/ metabolism
Interleukin-8
/ metabolism
Uterus
/ pathology
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 Sep 2024
27 Sep 2024
Historique:
received:
31
01
2023
accepted:
03
09
2024
medline:
28
9
2024
pubmed:
28
9
2024
entrez:
27
9
2024
Statut:
epublish
Résumé
Scar tissue formation is a hallmark of wound repair in adults and can chronically affect tissue architecture and function. To understand the general phenomena, we sought to explore scar-driven imbalance in tissue homeostasis caused by a common, and standardized surgical procedure, the uterine scar due to cesarean surgery. Deep uterine scar is associated with a rapidly increasing condition in pregnant women, placenta accreta spectrum (PAS), characterized by aggressive trophoblast invasion into the uterus, frequently necessitating hysterectomy at parturition. We created a model of uterine scar, recapitulating PAS-like invasive phenotype, showing that scar matrix activates mechanosensitive ion channel, Piezo1, through glycolysis-fueled cellular contraction. Piezo1 activation increases intracellular calcium activity and Protein kinase C activation, leading to NF-κB nuclear translocation, and MafG stabilization. This inflammatory transformation of decidua leads to production of IL-8 and G-CSF, chemotactically recruiting invading trophoblasts towards scar, initiating PAS. Our study demonstrates aberrant mechanics of scar disturbs stroma-epithelia homeostasis in placentation, with implications in cancer dissemination.
Identifiants
pubmed: 39333481
doi: 10.1038/s41467-024-52351-0
pii: 10.1038/s41467-024-52351-0
doi:
Substances chimiques
Ion Channels
0
PIEZO1 protein, human
0
NF-kappa B
0
Protein Kinase C
EC 2.7.11.13
Interleukin-8
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8379Subventions
Organisme : U.S. Department of Health & Human Services | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD)
ID : 1R01HD112424
Organisme : U.S. Department of Health & Human Services | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD)
ID : 1K99HD105973
Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)
ID : 5R37CA248161
Informations de copyright
© 2024. The Author(s).
Références
Gurtner, G. C., Werner, S., Barrandon, Y. & Longaker, M. T. Wound repair and regeneration. Nature 453, 314–321 (2008).
doi: 10.1038/nature07039
Rodrigues, M., Kosaric, N., Bonham, C. A. & Gurtner, G. C. Wound healing: a cellular perspective. Physiol. Rev. 99, 665–706 (2019).
doi: 10.1152/physrev.00067.2017
Xue, M. & Jackson, C. J. Extracellular matrix reorganization during wound healing and its impact on abnormal scarring. Adv. Wound Care 4, 119–136 (2015).
doi: 10.1089/wound.2013.0485
Moretti, L., Stalfort, J., Barker, T. H. & Abebayehu, D. The interplay of fibroblasts, the extracellular matrix, and inflammation in scar formation. J. Biol. Chem. 298, 101530 (2022).
doi: 10.1016/j.jbc.2021.101530
Eming, S. A., Martin, P. & Tomic-Canic, M. Wound repair and regeneration: mechanisms, signaling, and translation. Sci. Transl. Med. 6, 265sr6–265sr6 (2014).
pmcid: 4973620
doi: 10.1126/scitranslmed.3009337
Sarrazy, V., Billet, F., Micallef, L., Coulomb, B. & Desmoulière, A. Mechanisms of pathological scarring: Role of myofibroblasts and current developments. Wound Repair Regen. 19, s10–s15 (2011).
doi: 10.1111/j.1524-475X.2011.00708.x
Gauglitz, G. G., Korting, H. C., Pavicic, T., Ruzicka, T. & Jeschke, M. G. Hypertrophic scarring and keloids: pathomechanisms and current and emerging treatment strategies. Mol. Med. 17, 113–125 (2011).
doi: 10.2119/molmed.2009.00153
Profyris, C., Tziotzios, C. & Do Vale, I. Cutaneous scarring: pathophysiology, molecular mechanisms, and scar reduction therapeutics: Part I. The molecular basis of scar formation. J. Am. Acad. Dermatol. 66, 1–10 (2012).
doi: 10.1016/j.jaad.2011.05.055
Bartels, H. C., Postle, J. D., Downey, P. & Brennan, D. J. Placenta accreta spectrum: a review of pathology, molecular biology, and biomarkers. Dis. Markers 2018, 1507674 (2018).
pmcid: 6051104
doi: 10.1155/2018/1507674
American College of Obstetricians and Gynecologists & Society for Maternal-Fetal Medicine. Obstetric care consensus No. 7: placenta accreta spectrum. Obstet. Gynecol. 132, e259–e275 (2018).
Badr, D. A., Al Hassan, J., Salem Wehbe, G. & Ramadan, M. K. Uterine body placenta accreta spectrum: a detailed literature review. Placenta 95, 44–52 (2020).
doi: 10.1016/j.placenta.2020.04.005
Rosen, T. Placenta accreta and cesarean scar pregnancy: overlooked costs of the rising cesarean section rate. Clin. Perinatol. 35, 519–529 (2008).
doi: 10.1016/j.clp.2008.07.003
Clark, S. L., Koonings, P. P. & Phelan, J. P. Placenta previa/accreta and prior cesarean section. Obstet. Gynecol. 66, 89–92 (1985).
Morlando, M. et al. Placenta accreta: incidence and risk factors in an area with a particularly high rate of cesarean section. Acta Obstet. Gynecol. Scand. 92, 457–460 (2013).
doi: 10.1111/aogs.12080
Garmi, G. & Salim, R. Epidemiology, etiology, diagnosis, and management of placenta accreta. Obstet. Gynecol. Int. 2012, e873929 (2012).
doi: 10.1155/2012/873929
Betran, A. P., Ye, J., Moller, A.-B., Souza, J. P. & Zhang, J. Trends and projections of caesarean section rates: global and regional estimates. BMJ Glob. Health 6, e005671 (2021).
pmcid: 8208001
doi: 10.1136/bmjgh-2021-005671
Boerma, T. et al. Global epidemiology of use of and disparities in caesarean sections. Lancet 392, 1341–1348 (2018).
doi: 10.1016/S0140-6736(18)31928-7
Jauniaux, E., Chantraine, F., Silver, R. M. & Langhoff-Roos, J., & for the FIGO placenta accreta diagnosis and management expert consensus panel FIGO consensus guidelines on placenta accreta spectrum disorders: epidemiology. Int. J. Gynecol. Obstet. 140, 265–273 (2018).
doi: 10.1002/ijgo.12407
Jauniaux, E., Grønbeck, L., Bunce, C., Langhoff-Roos, J. & Collins, S. L. Epidemiology of placenta previa accreta: a systematic review and meta-analysis. BMJ Open 9, e031193 (2019).
pmcid: 6858111
doi: 10.1136/bmjopen-2019-031193
Jauniaux, E., Silver, R. M. & Matsubara, S. The new world of placenta accreta spectrum disorders. Int. J. Gynecol. Obstet. 140, 259–260 (2018).
doi: 10.1002/ijgo.12433
Hecht, J. L. et al. Classification and reporting guidelines for the pathology diagnosis of placenta accreta spectrum (PAS) disorders: recommendations from an expert panel. Mod. Pathol. 33, 2382–2396 (2020).
doi: 10.1038/s41379-020-0569-1
Mogos, M. F., Salemi, J. L., Ashley, M., Whiteman, V. E. & Salihu, H. M. Recent trends in placenta accreta in the United States and its impact on maternal-fetal morbidity and healthcare-associated costs, 1998-20. J. Matern-Fetal Neonatal Med. 29, 1077–1082 (2016).
doi: 10.3109/14767058.2015.1034103
Jauniaux, E., Collins, S. & Burton, G. J. Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging. Am. J. Obstet. Gynecol. 218, 75–87 (2018).
doi: 10.1016/j.ajog.2017.05.067
Kshitiz et al. Evolution of placental invasion and cancer metastasis are causally linked. Nat. Ecol. Evol. 3, 1743–1753 (2019).
doi: 10.1038/s41559-019-1046-4
Wagner, G. P., Kshitiz, Dighe, A. & Levchenko, A. The coevolution of placentation and cancer. Annu. Rev. Anim. Biosci. 10, 259–279 (2022).
doi: 10.1146/annurev-animal-020420-031544
Pollheimer, J., Vondra, S., Baltayeva, J., Beristain, A. G. & Knöfler, M. Regulation of placental extravillous trophoblasts by the maternal uterine environment. Front. Immunol. 9, 2597 (2018).
Soares, M. J., Varberg, K. M. & Iqbal, K. Hemochorial placentation: development, function, and adaptations. Biol. Reprod. 99, 196–211 (2018).
pmcid: 6044390
doi: 10.1093/biolre/ioy049
Bączkowska, M. et al. Molecular changes on maternal–fetal interface in placental abruption—a systematic review. Int. J. Mol. Sci. 22, 6612 (2021).
pmcid: 8235312
doi: 10.3390/ijms22126612
Higuchi, A. et al. Histopathological evaluation of cesarean scar defect in women with cesarean scar syndrome. Reprod. Med. Biol. 21, e12431 (2022).
doi: 10.1002/rmb2.12431
Morris, H. Surgical pathology of the lower uterine segment caesarean section scar: is the scar a source of clinical symptoms? Int. J. Gynecol. Pathol. 14, 16–20 (1995).
doi: 10.1097/00004347-199501000-00004
Donnez, O., Donnez, J., Orellana, R. & Dolmans, M.-M. Gynecological and obstetrical outcomes after laparoscopic repair of a cesarean scar defect in a series of 38 women. Fertil. Steril. 107, 289–296 (2017).
doi: 10.1016/j.fertnstert.2016.09.033
Sandall, J. et al. Short-term and long-term effects of caesarean section on the health of women and children. Lancet 392, 1349–1357 (2018).
doi: 10.1016/S0140-6736(18)31930-5
Timor-Tritsch, I. E. et al. Cesarean scar pregnancy is a precursor of morbidly adherent placenta. Ultrasound Obstet. Gynecol. 44, 346–353 (2014).
doi: 10.1002/uog.13426
Ewies, A. A. A. & Zanetto, U. Caesarean section scar causes myometrial hypertrophy with subsequent heavy menstrual flow and dysmenorrhoea. Med. Hypotheses 108, 54–56 (2017).
doi: 10.1016/j.mehy.2017.08.006
Sahai, E. et al. A framework for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer 20, 174–186 (2020).
pmcid: 7046529
doi: 10.1038/s41568-019-0238-1
Ping, Q. et al. Cancer-associated fibroblasts: overview, progress, challenges, and directions. Cancer Gene Ther. 28, 984–999 (2021).
doi: 10.1038/s41417-021-00318-4
Labernadie, A. et al. A mechanically active heterotypic E-cadherin/N-cadherin adhesion enables fibroblasts to drive cancer cell invasion. Nat. Cell Biol. 19, 224–237 (2017).
pmcid: 5831988
doi: 10.1038/ncb3478
Nadiarnykh, O., LaComb, R. B., Brewer, M. A. & Campagnola, P. J. Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy. BMC Cancer 10, 94 (2010).
pmcid: 2841668
doi: 10.1186/1471-2407-10-94
di Pasquo, E. et al. Evaluation of the uterine scar stiffness in women with previous Cesarean section by ultrasound elastography: A cohort study. Clin. Imaging 64, 53–56 (2020).
doi: 10.1016/j.clinimag.2020.03.006
Wildman, D. E. et al. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203–3208 (2006).
pmcid: 1413940
doi: 10.1073/pnas.0511344103
Afzal, J. et al. Paracrine HB-EGF signaling reduce enhanced contractile and energetic state of activated decidual fibroblasts by rebalancing SRF-MRTF-TCF transcriptional axis. Front. Cell Dev. Biol. 10, 927631 (2022).
pmcid: 9485834
doi: 10.3389/fcell.2022.927631
Suhail, Y. et al. Tracing the cis-regulatory changes underlying the endometrial control of placental invasion. Proc. Natl Acad. Sci. USA 119, e2111256119 (2022).
pmcid: 8832988
doi: 10.1073/pnas.2111256119
Clark, A. G. & Vignjevic, D. M. Modes of cancer cell invasion and the role of the microenvironment. Curr. Opin. Cell Biol. 36, 13–22 (2015).
doi: 10.1016/j.ceb.2015.06.004
Pickup, M. W., Mouw, J. K. & Weaver, V. M. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 15, 1243–1253 (2014).
pmcid: 4264927
doi: 10.15252/embr.201439246
De Wever, O. & Mareel, M. Role of tissue stroma in cancer cell invasion. J. Pathol. 200, 429–447 (2003).
doi: 10.1002/path.1398
Kim, D. J. et al. Suppression of TGFβ-mediated conversion of endothelial cells and fibroblasts into cancer associated (myo)fibroblasts via HDAC inhibition. Br. J. Cancer 118, 1359–1368 (2018).
pmcid: 5959903
doi: 10.1038/s41416-018-0072-3
Tuo, Z. et al. RUNX1 is a promising prognostic biomarker and related to immune infiltrates of cancer-associated fibroblasts in human cancers. BMC Cancer 22, 523 (2022).
pmcid: 9088136
doi: 10.1186/s12885-022-09632-y
Kang, J. I. et al. p62-Induced cancer-associated fibroblast activation via the Nrf2-ATF6 pathway promotes lung tumorigenesis. Cancers 13, 864 (2021).
pmcid: 7922306
doi: 10.3390/cancers13040864
Liu, S., Suhail, Y., Novin, A., Perpetua, L. & Kshitiz. Metastatic transition of pancreatic ductal cell adenocarcinoma is accompanied by the emergence of pro-invasive cancer-associated fibroblasts. Cancers 14, 2197 (2022).
pmcid: 9104173
doi: 10.3390/cancers14092197
Afshar, Y. et al. Placenta accreta spectrum disorder at single-cell resolution: a loss of boundary limits in the decidua and endothelium. Am. J. Obstet. Gynecol. 29, S0002-9378(23)00729-9 (2024)
Jovanović, M., Stefanoska, I., Radojcić, L. & Vićovac, L. Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP)2 and MMP9 and integrins alpha5 and beta1. Reproduction 139, 789–798 (2010).
doi: 10.1530/REP-09-0341
Ding, J. et al. M2 macrophage-derived G-CSF promotes trophoblasts EMT, invasion and migration via activating PI3K/Akt/Erk1/2 pathway to mediate normal pregnancy. J. Cell. Mol. Med. 25, 2136–2147 (2021).
pmcid: 7882967
doi: 10.1111/jcmm.16191
Kefauver, J. M., Ward, A. B. & Patapoutian, A. Discoveries in structure and physiology of mechanically activated ion channels. Nature 587, 567–576 (2020).
pmcid: 8477435
doi: 10.1038/s41586-020-2933-1
Murthy, S. E., Dubin, A. E. & Patapoutian, A. Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat. Rev. Mol. Cell Biol. 18, 771–783 (2017).
doi: 10.1038/nrm.2017.92
Lewis, A. H. & Grandl, J. Mechanical sensitivity of Piezo1 ion channels can be tuned by cellular membrane tension. eLife 4, e12088 (2015).
pmcid: 4718726
doi: 10.7554/eLife.12088
Ridone, P. et al. Disruption of membrane cholesterol organization impairs the activity of PIEZO1 channel clusters. J. Gen. Physiol. 152, e201912515 (2020).
pmcid: 7398139
doi: 10.1085/jgp.201912515
Viatour, P., Merville, M.-P., Bours, V. & Chariot, A. Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30, 43–52 (2005).
doi: 10.1016/j.tibs.2004.11.009
Christian, F., Smith, E. L. & Carmody, R. J. The regulation of NF-κB subunits by phosphorylation. Cells 5, 12 (2016).
pmcid: 4810097
doi: 10.3390/cells5010012
Vento-Tormo, R. et al. Single-cell reconstruction of the early maternal–fetal interface in humans. Nature 563, 347–353 (2018).
pmcid: 7612850
doi: 10.1038/s41586-018-0698-6
Arutyunyan, A. et al. Spatial multiomics map of trophoblast development in early pregnancy. Nature 616, 143–151 (2023).
pmcid: 10076224
doi: 10.1038/s41586-023-05869-0
Afzal, J. et al. Cardiac ultrastructure inspired matrix induces advanced metabolic and functional maturation of differentiated human cardiomyocytes. Cell Rep. 40, 111146 (2022).
doi: 10.1016/j.celrep.2022.111146
Munevar, S., Wang, Y. & Dembo, M. Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80, 1744–1757 (2001).
pmcid: 1301364
doi: 10.1016/S0006-3495(01)76145-0
Shi, L., Pan, H., Liu, Z., Xie, J. & Han, W. Roles of PFKFB3 in cancer. Signal Transduct. Target. Ther. 2, 1–10 (2017).
Wang, Y., Qu, C., Liu, T. & Wang, C. PFKFB3 inhibitors as potential anticancer agents: Mechanisms of action, current developments, and structure-activity relationships. Eur. J. Med. Chem. 203, 112612 (2020).
doi: 10.1016/j.ejmech.2020.112612
Park, J. S. et al. Mechanical regulation of glycolysis via cytoskeleton architecture. Nature 578, 621–626 (2020).
pmcid: 7210009
doi: 10.1038/s41586-020-1998-1
Lilienbaum, A. & Israël, A. From calcium to NF-κB signaling pathways in neurons. Mol. Cell. Biol. 23, 2680–2698 (2003).
pmcid: 152563
doi: 10.1128/MCB.23.8.2680-2698.2003
Massrieh, W. et al. Regulation of the MAFF transcription factor by proinflammatory cytokines in myometrial cells1. Biol. Reprod. 74, 699–705 (2006).
doi: 10.1095/biolreprod.105.045450
Wheeler, M. A. et al. MAFG-driven astrocytes promote CNS inflammation. Nature 578, 593–599 (2020).
pmcid: 8049843
doi: 10.1038/s41586-020-1999-0
Richardson, R. J. Parallels between vertebrate cardiac and cutaneous wound healing and regeneration. Npj Regen. Med. 3, 1–9 (2018).
doi: 10.1038/s41536-018-0059-y
Holmes, J. W., Laksman, Z. & Gepstein, L. Making better scar: emerging approaches for modifying mechanical and electrical properties following infarction and ablation. Prog. Biophys. Mol. Biol. 120, 134–148 (2016).
doi: 10.1016/j.pbiomolbio.2015.11.002
Otsuka, I. Cutaneous metastasis after surgery, injury, lymphadenopathy, and peritonitis: possible mechanisms. Int. J. Mol. Sci. 20, 3286 (2019).
pmcid: 6651228
doi: 10.3390/ijms20133286
Bobba, R. K., Holly, J. S., Loy, T. & Perry, M. C. Scar carcinoma of the lung: a historical perspective. Clin. Lung Cancer 12, 148–154 (2011).
doi: 10.1016/j.cllc.2011.03.011
Chiriac, A. E. et al. Malignant degeneration of scars. Cancer Manag. Res. 12, 10297–10302 (2020).
pmcid: 7585506
doi: 10.2147/CMAR.S274470
Lu, Y.-Y. et al. Risk of cancer development in patients with keloids. Sci. Rep. 11, 9390 (2021).
pmcid: 8087779
doi: 10.1038/s41598-021-88789-1
Chaturvedi, G., Gupta, A. K., Das, S., Gohil, A. J. & Lamba, S. Marjolin ulcer: an observational epidemiological study from a Tertiary Care Centre in India. Ann. Plast. Surg. 83, 518 (2019).
doi: 10.1097/SAP.0000000000001995
Bazaliński, D., Przybek-Mita, J., Barańska, B. & Więch, P. Marjolin’s ulcer in chronic wounds – review of available literature. Contemp. Oncol. 21, 197–202 (2017).
McNally, L. et al. Up-regulated cytotrophoblast DOCK4 contributes to over-invasion in placenta accreta spectrum. Proc. Natl Acad. Sci. USA 117, 15852–15861 (2020).
pmcid: 7355036
doi: 10.1073/pnas.1920776117
Duzyj, C. et al. Extravillous trophoblast invasion in placenta accreta is associated with differential local expression of angiogenic and growth factors: a cross-sectional study. BJOG 125, 1441–1448 (2018).
doi: 10.1111/1471-0528.15176
Solis, A. G. et al. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity. Nature 573, 69–74 (2019).
pmcid: 6939392
doi: 10.1038/s41586-019-1485-8
Harman, I., Costello, A., Ganong, B., Bell, R. M. & Handwerger, S. Activation of protein kinase C inhibits synthesis and release of decidual prolactin. Am. J. Physiol. 251, E172–E177 (1986).
Trushin, S. A. et al. Protein kinase Cα (PKCα) acts upstream of PKCθ to activate IκB kinase and NF-κB in T lymphocytes. Mol. Cell. Biol. 23, 7068–7081 (2003).
pmcid: 193945
doi: 10.1128/MCB.23.19.7068-7081.2003
Katsuoka, F. & Yamamoto, M. Small Maf proteins (MafF, MafG, MafK): history, structure and function. Gene 586, 197–205 (2016).
pmcid: 4911266
doi: 10.1016/j.gene.2016.03.058
Fang, M., Ou, J., Hutchinson, L. & Green, M. R. The BRAF oncoprotein functions through the transcriptional repressor MAFG to mediate the CpG island methylator phenotype. Mol. Cell 55, 904–915 (2014).
pmcid: 4170521
doi: 10.1016/j.molcel.2014.08.010
Kirk, D. et al. Normal human endometrium in cell culture. I. Separation and characterization of epithelial and stromal components in vitro. In Vitro 14, 651–662 (1978).
doi: 10.1007/BF02616162
Kolberg, L., Raudvere, U., Kuzmin, I., Vilo, J. & Peterson, H. gprofiler2 – an R package for gene list functional enrichment analysis and namespace conversion toolset g:Profiler. F1000Research 9, ELIXIR–709 (2020).
pmcid: 7859841
doi: 10.12688/f1000research.24956.2
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. 102, 15545–15550 (2005).
pmcid: 1239896
doi: 10.1073/pnas.0506580102
Ge, S. X., Jung, D. & Yao, R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36, 2628–2629 (2020).
doi: 10.1093/bioinformatics/btz931
Kanehisa, M., Furumichi, M., Sato, Y., Ishiguro-Watanabe, M. & Tanabe, M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res. 49, D545–D551 (2021).
doi: 10.1093/nar/gkaa970
Kuleshov, M. V. et al. KEA3: improved kinase enrichment analysis via data integration. Nucleic Acids Res. 49, W304–W316 (2021).
pmcid: 8265130
doi: 10.1093/nar/gkab359
Colin-York, H., Eggeling, C. & Fritzsche, M. Dissection of mechanical force in living cells by super-resolved traction force microscopy. Nat. Protoc. 12, 783–796 (2017).
doi: 10.1038/nprot.2017.009
Bauer, A. et al. pyTFM: A tool for traction force and monolayer stress microscopy. PLOS Comput. Biol. 17, e1008364 (2021).
pmcid: 8248623
doi: 10.1371/journal.pcbi.1008364