دورية أكاديمية

Mechanochemical control of epidermal stem cell divisions by B-plexins.

التفاصيل البيبلوغرافية
العنوان: Mechanochemical control of epidermal stem cell divisions by B-plexins.
المؤلفون: Jiang C; Institute of Pharmacology, University of Marburg, Marburg, Germany.; Department of Pharmacology, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany., Javed A; Helsinki Institute of Life Science, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland., Kaiser L; Institute of Pharmacology, University of Marburg, Marburg, Germany., Nava MM; Helsinki Institute of Life Science, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland., Xu R; Institute of Pharmacology, University of Marburg, Marburg, Germany.; Department of Pharmacology, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany., Brandt DT; Institute of Pharmacology, University of Marburg, Marburg, Germany., Zhao D; Institute of Pharmacology, University of Marburg, Marburg, Germany., Mayer B; Biochemistry, Faculty of Chemistry, and Center for Synthetic Microbiology (synmikro), University of Marburg, Marburg, Germany., Fernández-Baldovinos J; Institute of Pharmacology, University of Marburg, Marburg, Germany., Zhou L; Institute of Pharmacology, University of Marburg, Marburg, Germany.; Department of Diabetes and Endocrinology, Affiliated Hospital of Southwest Medical University, Luzhou, China., Höß C; Institute of Pharmacology, University of Marburg, Marburg, Germany., Sawmynaden K; LifeArc, Stevenage, UK., Oleksy A; LifeArc, Stevenage, UK., Matthews D; LifeArc, Stevenage, UK., Weinstein LS; Metabolic Diseases Branch, NIDDK, NIH, Bethesda, USA., Hahn H; Institute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany., Gröne HJ; Institute of Pharmacology, University of Marburg, Marburg, Germany., Graumann PL; Biochemistry, Faculty of Chemistry, and Center for Synthetic Microbiology (synmikro), University of Marburg, Marburg, Germany., Niessen CM; Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany., Offermanns S; Department of Pharmacology, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany.; Medical Faculty, University of Frankfurt, Frankfurt, Germany., Wickström SA; Helsinki Institute of Life Science, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland.; Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany.; Wihuri Research Institute, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland.; Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.; Max-Planck-Institute for Biology of Ageing, Cologne, Germany., Worzfeld T; Institute of Pharmacology, University of Marburg, Marburg, Germany. worzfeld@uni-marburg.de.; Department of Pharmacology, Max-Planck-Institute for Heart and Lung Research, Bad Nauheim, Germany. worzfeld@uni-marburg.de.
المصدر: Nature communications [Nat Commun] 2021 Feb 26; Vol. 12 (1), pp. 1308. Date of Electronic Publication: 2021 Feb 26.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Cell Adhesion Molecules/*metabolism , Cell Division/*physiology , Epidermal Cells/*metabolism , Nerve Tissue Proteins/*metabolism , Receptors, Cell Surface/*metabolism , Stem Cells/*metabolism, Animals ; Carcinoma, Basal Cell/pathology ; Carrier Proteins/metabolism ; Cell Adhesion ; Cell Proliferation ; Embryonic Development/physiology ; Epithelial Cells/metabolism ; Epithelium/metabolism ; Female ; Intercellular Junctions ; Keratinocytes ; Mice ; Mitosis ; Morphogenesis ; Organogenesis
مستخلص: The precise spatiotemporal control of cell proliferation is key to the morphogenesis of epithelial tissues. Epithelial cell divisions lead to tissue crowding and local changes in force distribution, which in turn suppress the rate of cell divisions. However, the molecular mechanisms underlying this mechanical feedback are largely unclear. Here, we identify a critical requirement of B-plexin transmembrane receptors in the response to crowding-induced mechanical forces during embryonic skin development. Epidermal stem cells lacking B-plexins fail to sense mechanical compression, resulting in disinhibition of the transcriptional coactivator YAP, hyperproliferation, and tissue overgrowth. Mechanistically, we show that B-plexins mediate mechanoresponses to crowding through stabilization of adhesive cell junctions and lowering of cortical stiffness. Finally, we provide evidence that the B-plexin-dependent mechanochemical feedback is also pathophysiologically relevant to limit tumor growth in basal cell carcinoma, the most common type of skin cancer. Our data define a central role of B-plexins in mechanosensation to couple cell density and cell division in development and disease.
References: Ben Amar, M., Nassoy, P. & LeGoff, L. Physics of growing biological tissues: the complex cross-talk between cell activity, growth and resistance. Philos. Trans. A 377, 20180070 (2019). (PMID: 10.1098/rsta.2018.0070)
Irvine, K. D. & Shraiman, B. I. Mechanical control of growth: ideas, facts and challenges. Development 144, 4238–4248 (2017). (PMID: 29183937576963010.1242/dev.151902)
LeGoff, L. & Lecuit, T. Mechanical forces and growth in animal tissues. Cold Spring Harb. Perspect. Biol. 8, a019232 (2015). (PMID: 2626127910.1101/cshperspect.a019232)
Petridou, N. I. & Heisenberg, C. P. Tissue rheology in embryonic organization. EMBO J. 38, e102497 (2019). (PMID: 31512749679201210.15252/embj.2019102497)
Petridou, N. I., Spiro, Z. & Heisenberg, C. P. Multiscale force sensing in development. Nat. Cell Biol. 19, 581–588 (2017). (PMID: 2856105010.1038/ncb3524)
Hannezo, E. & Heisenberg, C. P. Mechanochemical feedback loops in development and disease. Cell 178, 12–25 (2019). (PMID: 3125191210.1016/j.cell.2019.05.052)
Godard, B. G. & Heisenberg, C. P. Cell division and tissue mechanics. Curr. Opin. Cell Biol. 60, 114–120 (2019). (PMID: 3128820610.1016/j.ceb.2019.05.007)
Wickstrom, S. A. & Niessen, C. M. Cell adhesion and mechanics as drivers of tissue organization and differentiation: local cues for large scale organization. Curr. Opin. Cell Biol. 54, 89–97 (2018). (PMID: 2986472110.1016/j.ceb.2018.05.003)
Chacon-Martinez, C. A., Koester, J. & Wickstrom, S. A. Signaling in the stem cell niche: regulating cell fate, function and plasticity. Development 145, dev165399 (2018). https://doi.org/10.1242/dev.165399 .
Biggs, L. C., Kim, C. S., Miroshnikova, Y. A. & Wickstrom, S. A. Mechanical forces in the skin: roles in tissue architecture, stability, and function. J. Investig. Dermatol. 140, 284–290 (2020).
Tamagnone, L. et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71–80 (1999). (PMID: 1052099510.1016/S0092-8674(00)80063-X)
Winberg, M. L. et al. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95, 903–916 (1998). (PMID: 987584510.1016/S0092-8674(00)81715-8)
Worzfeld, T. & Offermanns, S. Semaphorins and plexins as therapeutic targets. Nat. Rev. Drug Discov. 13, 603–621 (2014). (PMID: 2508228810.1038/nrd4337)
Gurrapu, S. & Tamagnone, L. Semaphorins as regulators of phenotypic plasticity and functional reprogramming of cancer cells. Trends Mol. Med. 25, 303–314 (2019). (PMID: 3082419710.1016/j.molmed.2019.01.010)
Nishide, M. & Kumanogoh, A. The role of semaphorins in immune responses and autoimmune rheumatic diseases. Nat. Rev. Rheumatol. 14, 19–31 (2018). (PMID: 2921312510.1038/nrrheum.2017.201)
Verlinden, L., Vanderschueren, D. & Verstuyf, A. Semaphorin signaling in bone. Mol. Cell. Endocrinol. 432, 66–74 (2016). (PMID: 2636529610.1016/j.mce.2015.09.009)
Mehta, V. et al. The guidance receptor plexin D1 is a mechanosensor in endothelial cells. Nature 578, 290–295 (2020). (PMID: 32025034702589010.1038/s41586-020-1979-4)
Miroshnikova, Y. A. et al. Adhesion forces and cortical tension couple cell proliferation and differentiation to drive epidermal stratification. Nat. Cell Biol. 20, 69–80 (2018). (PMID: 2923001610.1038/s41556-017-0005-z)
Zhang, H., Pasolli, H. A. & Fuchs, E. Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc. Natl Acad. Sci. USA 108, 2270–2275 (2011). (PMID: 2126281210.1073/pnas.1019603108)
Dekoninck, S. et al. Defining the design principles of skin epidermis postnatal growth. Cell 181, 604–620.e22 (2020).
Daviaud, N., Chen, K., Huang, Y., Friedel, R. H. & Zou, H. Impaired cortical neurogenesis in plexin-B1 and -B2 double deletion mutant. Dev. Neurobiol. 76, 882–899 (2016). (PMID: 2657959810.1002/dneu.22364)
Perala, N. et al. Sema4C-Plexin B2 signalling modulates ureteric branching in developing kidney. Differentiation 81, 81–91 (2011). (PMID: 2103593810.1016/j.diff.2010.10.001)
Xia, J. et al. Semaphorin-plexin signaling controls mitotic spindle orientation during epithelial morphogenesis and repair. Dev. Cell 33, 299–313 (2015). (PMID: 2589201210.1016/j.devcel.2015.02.001)
Hafner, M. et al. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 38, 176–181 (2004). (PMID: 1508351810.1002/gene.20016)
Blanpain, C., Lowry, W. E., Pasolli, H. A. & Fuchs, E. Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 20, 3022–3035 (2006). (PMID: 17079689162002010.1101/gad.1477606)
Zhao, B. et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747–2761 (2007). (PMID: 17974916204512910.1101/gad.1602907)
Aragona, M. et al. Mechanisms of stretch-mediated skin expansion at single-cell resolution. Nature 584, 268–273 (2020). (PMID: 32728211711604210.1038/s41586-020-2555-7)
Debaugnies, M. et al. YAP and TAZ are essential for basal and squamous cell carcinoma initiation. EMBO Rep. 19, e45809 (2018). https://doi.org/10.15252/embr.201845809 .
Elbediwy, A. et al. Integrin signalling regulates YAP and TAZ to control skin homeostasis. Development 143, 1674–1687 (2016). (PMID: 269891774874484)
Schlegelmilch, K. et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144, 782–795 (2011). (PMID: 21376238323719610.1016/j.cell.2011.02.031)
Totaro, A. et al. YAP/TAZ link cell mechanics to Notch signalling to control epidermal stem cell fate. Nat. Commun. 8, 15206 (2017). (PMID: 28513598544232110.1038/ncomms15206)
Niessen, C. M., Leckband, D. & Yap, A. S. Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol. Rev. 91, 691–731 (2011). (PMID: 21527735355681910.1152/physrev.00004.2010)
Mannaerts, I. et al. The Hippo pathway effector YAP controls mouse hepatic stellate cell activation. J. Hepatol. 63, 679–688 (2015). (PMID: 2590827010.1016/j.jhep.2015.04.011)
Gavini, J. et al. Verteporfin-induced lysosomal compartment dysregulation potentiates the effect of sorafenib in hepatocellular carcinoma. Cell Death Dis. 10, 749 (2019). (PMID: 31582741677651010.1038/s41419-019-1989-z)
Gurrapu, S. et al. Reverse signaling by semaphorin 4C elicits SMAD1/5- and ID1/3-dependent invasive reprogramming in cancer cells. Sci. Signal. 12, eaav2041 (2019). https://doi.org/10.1126/scisignal.aav2041 .
Sun, T. et al. A reverse signaling pathway downstream of Sema4A controls cell migration via Scrib. J. Cell Biol. 216, 199–215 (2017). (PMID: 28007914522360010.1083/jcb.201602002)
Ohta, K. et al. Plexin: a novel neuronal cell surface molecule that mediates cell adhesion via a homophilic binding mechanism in the presence of calcium ions. Neuron 14, 1189–1199 (1995). (PMID: 760563210.1016/0896-6273(95)90266-X)
Kim, N. G., Koh, E., Chen, X. & Gumbiner, B. M. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl Acad. Sci. USA 108, 11930–11935 (2011). (PMID: 2173013110.1073/pnas.1103345108)
Lecuit, T. & Yap, A. S. E-cadherin junctions as active mechanical integrators in tissue dynamics. Nat. Cell Biol. 17, 533–539 (2015). (PMID: 2592558210.1038/ncb3136)
Yap, A. S., Duszyc, K. & Viasnoff, V. Mechanosensing and mechanotransduction at cell–cell junctions. Cold Spring Harb. Perspect. Biol. 10, a028761 (2018). https://doi.org/10.1101/cshperspect.a028761 .
Vasioukhin, V., Bauer, C., Degenstein, L., Wise, B. & Fuchs, E. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin. Cell 104, 605–617 (2001). (PMID: 1123941610.1016/S0092-8674(01)00246-X)
Noethel, B. et al. Transition of responsive mechanosensitive elements from focal adhesions to adherens junctions on epithelial differentiation. Mol. Biol. Cell 29, 2317–2325 (2018). (PMID: 30044710624980510.1091/mbc.E17-06-0387)
Chugh, P. & Paluch, E. K. The actin cortex at a glance. J. Cell Sci. 131, jcs186254 (2018). https://doi.org/10.1242/jcs.186254 .
Engl, W., Arasi, B., Yap, L. L., Thiery, J. P. & Viasnoff, V. Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions. Nat. Cell Biol. 16, 587–594 (2014). (PMID: 2485900310.1038/ncb2973)
Kunda, P. & Baum, B. The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 19, 174–179 (2009). (PMID: 1928586910.1016/j.tcb.2009.01.006)
Cramer, L. P. & Mitchison, T. J. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Mol. Biol. Cell 8, 109–119 (1997). (PMID: 901759927606310.1091/mbc.8.1.109)
Thery, M. & Bornens, M. Get round and stiff for mitosis. HFSP J. 2, 65–71 (2008). (PMID: 19404473264557510.2976/1.2895661)
Luxenburg, C., Pasolli, H. A., Williams, S. E. & Fuchs, E. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 13, 203–214 (2011). (PMID: 21336301327833710.1038/ncb2163)
Barberis, D. et al. Plexin signaling hampers integrin-based adhesion, leading to Rho-kinase independent cell rounding, and inhibiting lamellipodia extension and cell motility. FASEB J. 18, 592–594 (2004). (PMID: 1473463310.1096/fj.03-0957fje)
McColl, B., Garg, R., Riou, P., Riento, K. & Ridley, A. J. Rnd3-induced cell rounding requires interaction with Plexin-B2. J. Cell Sci. 129, 4046–4056 (2016). (PMID: 276561115117210)
Carreno, S. et al. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J. Cell Biol. 180, 739–746 (2008). (PMID: 18283112226558310.1083/jcb.200709161)
Kunda, P., Pelling, A. E., Liu, T. & Baum, B. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91–101 (2008). (PMID: 1820773810.1016/j.cub.2007.12.051)
Kaji, N., Muramoto, A. & Mizuno, K. LIM kinase-mediated cofilin phosphorylation during mitosis is required for precise spindle positioning. J. Biol. Chem. 283, 4983–4992 (2008). (PMID: 1807911810.1074/jbc.M708644200)
Arbeille, E. et al. Cerebrospinal fluid-derived Semaphorin3B orients neuroepithelial cell divisions in the apicobasal axis. Nat. Commun. 6, 6366 (2015). (PMID: 2572151410.1038/ncomms7366)
Iglesias-Bartolome, R. et al. Inactivation of a Galpha(s)-PKA tumour suppressor pathway in skin stem cells initiates basal-cell carcinogenesis. Nat. Cell Biol. 17, 793–803 (2015). (PMID: 25961504444981510.1038/ncb3164)
Bonilla, X. et al. Genomic analysis identifies new drivers and progression pathways in skin basal cell carcinoma. Nat. Genet. 48, 398–406 (2016). (PMID: 2695009410.1038/ng.3525)
Connelly, J. T. et al. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat. Cell Biol. 12, 711–718 (2010). (PMID: 2058183810.1038/ncb2074)
Ellis, S. J. et al. Distinct modes of cell competition shape mammalian tissue morphogenesis. Nature 569, 497–502 (2019). (PMID: 31092920663857210.1038/s41586-019-1199-y)
Watt, F. M., Jordan, P. W. & O’Neill, C. H. Cell shape controls terminal differentiation of human epidermal keratinocytes. Proc. Natl Acad. Sci. USA 85, 5576–5580 (1988). (PMID: 245657210.1073/pnas.85.15.5576)
Mesa, K. R. et al. Homeostatic epidermal stem cell self-renewal is driven by local differentiation. Cell Stem Cell 23, 677–686 (2018). e674. (PMID: 30269903621470910.1016/j.stem.2018.09.005)
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011). (PMID: 10.1016/j.cell.2011.02.013)
Mendonsa, A. M., Na, T. Y. & Gumbiner, B. M. E-cadherin in contact inhibition and cancer. Oncogene 37, 4769–4780 (2018). (PMID: 29780167611909810.1038/s41388-018-0304-2)
Gomez Roman, J. J. et al. Plexin B1 is downregulated in renal cell carcinomas and modulates cell growth. Transl. Res. 151, 134–140 (2008). (PMID: 1827981210.1016/j.trsl.2007.12.003)
Argast, G. M. et al. Plexin B1 is repressed by oncogenic B-Raf signaling and functions as a tumor suppressor in melanoma cells. Oncogene 28, 2697–2709 (2009). (PMID: 19483722323849210.1038/onc.2009.133)
Stevens, L. et al. Plexin B1 suppresses c-Met in melanoma: a role for plexin B1 as a tumor-suppressor protein through regulation of c-Met. J. Investig. Dermatol. 130, 1636–1645 (2010). (PMID: 2016484310.1038/jid.2010.13)
Rody, A. et al. Loss of Plexin B1 is highly prognostic in low proliferating ER positive breast cancers—results of a large scale microarray analysis. Eur. J. Cancer 45, 405–413 (2009). (PMID: 1905466510.1016/j.ejca.2008.10.016)
Rody, A. et al. Poor outcome in estrogen receptor-positive breast cancers predicted by loss of plexin B1. Clin. Cancer Res. 13, 1115–1122 (2007). (PMID: 1731781910.1158/1078-0432.CCR-06-2433)
Worzfeld, T. et al. ErbB-2 signals through Plexin-B1 to promote breast cancer metastasis. J. Clin. Investig. 122, 1296–1305 (2012). (PMID: 2237804010.1172/JCI60568)
Ahammad, I. A comprehensive review of tumor proliferative and suppressive role of semaphorins and therapeutic approaches. Biophys. Rev. 12, 1233–1247 (2020). (PMID: 32577918757565410.1007/s12551-020-00709-1)
Neufeld, G. et al. The semaphorins and their receptors as modulators of tumor progression. Drug Resist. Update 29, 1–12 (2016). (PMID: 10.1016/j.drup.2016.08.001)
Alto, L. T. & Terman, J. R. Semaphorins and their signaling mechanisms. Methods Mol. Biol. 1493, 1–25 (2017). (PMID: 27787839553878710.1007/978-1-4939-6448-2_1)
Battistini, C. & Tamagnone, L. Transmembrane semaphorins, forward and reverse signaling: have a look both ways. Cell. Mol. Life Sci. 73, 1609–1622 (2016). (PMID: 2679484510.1007/s00018-016-2137-x)
Kong, Y. et al. Structural basis for plexin activation and regulation. Neuron 91, 548–560 (2016). (PMID: 27397516498055010.1016/j.neuron.2016.06.018)
Suzuki, K. et al. Structure of the plexin ectodomain bound by semaphorin-mimicking antibodies. PLoS ONE 11, e0156719 (2016). (PMID: 27258772489251210.1371/journal.pone.0156719)
Moehring, F., Mikesell, A. R., Sadler, K. E., Menzel, A. D. & Stucky, C. L. Piezo1 mediates keratinocyte mechanotransduction. Preprint at bioRxiv https://doi.org/10.1101/2020.07.19.211086 (2020).
Ranade, S. S. et al. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 516, 121–125 (2014). (PMID: 25471886438017210.1038/nature13980)
Woo, S. H. et al. Piezo2 is required for Merkel-cell mechanotransduction. Nature 509, 622–626 (2014). (PMID: 24717433403962210.1038/nature13251)
Rübsam, M. et al. E-cadherin integrates mechanotransduction and EGFR signaling to control junctional tissue polarization and tight junction positioning. Nat. Commun. 8, 1250 (2017). (PMID: 29093447566591310.1038/s41467-017-01170-7)
Benham-Pyle, B. W., Pruitt, B. L. & Nelson, W. J. Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and beta-catenin activation to drive cell cycle entry. Science 348, 1024–1027 (2015). (PMID: 26023140457284710.1126/science.aaa4559)
Wong, V. W. et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat. Med. 18, 148–152 (2011). (PMID: 22157678445750610.1038/nm.2574)
Yap, A. S., Gomez, G. A. & Parton, R. G. Adherens junctions revisualized: organizing cadherins as nanoassemblies. Dev. Cell 35, 12–20 (2015). (PMID: 2646094410.1016/j.devcel.2015.09.012)
Oinuma, I., Katoh, H. & Negishi, M. Semaphorin 4D/Plexin-B1-mediated R-Ras GAP activity inhibits cell migration by regulating beta(1) integrin activity. J. Cell Biol. 173, 601–613 (2006). (PMID: 16702230206386810.1083/jcb.200508204)
Douguet, D. & Honore, E. Mammalian mechanoelectrical transduction: structure and function of force-gated ion channels. Cell 179, 340–354 (2019). (PMID: 3158507810.1016/j.cell.2019.08.049)
Perala, N. M., Immonen, T. & Sariola, H. The expression of plexins during mouse embryogenesis. Gene Expr. Patterns 5, 355–362 (2005). (PMID: 1566164110.1016/j.modgep.2004.10.001)
Zielonka, M., Xia, J., Friedel, R. H., Offermanns, S. & Worzfeld, T. A systematic expression analysis implicates Plexin-B2 and its ligand Sema4C in the regulation of the vascular and endocrine system. Exp. Cell Res. 316, 2477–2486 (2010). (PMID: 2047830410.1016/j.yexcr.2010.05.007)
Deng, S. et al. Plexin-B2, but not Plexin-B1, critically modulates neuronal migration and patterning of the developing nervous system in vivo. J. Neurosci. 27, 6333–6347 (2007). (PMID: 17554007667215010.1523/JNEUROSCI.5381-06.2007)
Vasioukhin, V., Degenstein, L., Wise, B. & Fuchs, E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl Acad. Sci. USA 96, 8551–8556 (1999). (PMID: 1041191310.1073/pnas.96.15.8551)
Chen, M. et al. Increased glucose tolerance and reduced adiposity in the absence of fasting hypoglycemia in mice with liver-specific Gs alpha deficiency. J. Clin. Investig. 115, 3217–3227 (2005). (PMID: 1623996810.1172/JCI24196)
Uhmann, A. et al. The Hedgehog receptor Patched controls lymphoid lineage commitment. Blood 110, 1814–1823 (2007). (PMID: 1753601210.1182/blood-2007-02-075648)
Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. & Shibata, M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533–542 (2010). (PMID: 2045384910.1038/ncb2055)
Worzfeld, T. et al. Genetic dissection of plexin signaling in vivo. Proc. Natl Acad. Sci. USA 111, 2194–2199 (2014). (PMID: 2446981310.1073/pnas.1308418111)
Meerbrey, K. L. et al. The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Proc. Natl Acad. Sci. USA 108, 3665–3670 (2011). (PMID: 2130731010.1073/pnas.1019736108)
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). (PMID: 2274377210.1038/nmeth.2019)
Faust, U. et al. Cyclic stress at mHz frequencies aligns fibroblasts in direction of zero strain. PLoS ONE 6, e28963 (2011). (PMID: 22194961324170110.1371/journal.pone.0028963)
المشرفين على المادة: 0 (Carrier Proteins)
0 (Cell Adhesion Molecules)
0 (Nerve Tissue Proteins)
0 (PLXNB1 protein, human)
0 (PLXNB2 protein, human)
0 (Receptors, Cell Surface)
0 (plexin)
تواريخ الأحداث: Date Created: 20210227 Date Completed: 20210315 Latest Revision: 20230129
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC7910479
DOI: 10.1038/s41467-021-21513-9
PMID: 33637728
قاعدة البيانات: MEDLINE