Stathmin Regulates Keratinocyte Proliferation and Migration during Cutaneous Regeneration
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{"title"=>"Stathmin Regulates Keratinocyte Proliferation and Migration during Cutaneous Regeneration", "type"=>"journal", "authors"=>[{"first_name"=>"Sabrina", "last_name"=>"Schmitt", "scopus_author_id"=>"24067793300"}, {"first_name"=>"Kai", "last_name"=>"Safferling", "scopus_author_id"=>"36993997100"}, {"first_name"=>"Kathi", "last_name"=>"Westphal", "scopus_author_id"=>"36599622500"}, {"first_name"=>"Manuel", "last_name"=>"Hrabowski", "scopus_author_id"=>"35760992100"}, {"first_name"=>"Ute", "last_name"=>"Müller", "scopus_author_id"=>"57197008292"}, {"first_name"=>"Peter", "last_name"=>"Angel", "scopus_author_id"=>"7005408632"}, {"first_name"=>"Lars", "last_name"=>"Wiechert", "scopus_author_id"=>"55330040000"}, {"first_name"=>"Volker", "last_name"=>"Ehemann", "scopus_author_id"=>"6701822243"}, {"first_name"=>"Benedikt", "last_name"=>"Müller", "scopus_author_id"=>"55878951600"}, {"first_name"=>"Stefan", "last_name"=>"Holland-Cunz", "scopus_author_id"=>"6603552176"}, {"first_name"=>"Damian", "last_name"=>"Stichel", "scopus_author_id"=>"55855859500"}, {"first_name"=>"Nathalie", "last_name"=>"Harder", "scopus_author_id"=>"23009067000"}, {"first_name"=>"Karl", "last_name"=>"Rohr", "scopus_author_id"=>"55332030200"}, {"first_name"=>"Günter", "last_name"=>"Germann", "scopus_author_id"=>"23768068200"}, {"first_name"=>"Franziska", "last_name"=>"Matthäus", "scopus_author_id"=>"24169231300"}, {"first_name"=>"Peter", "last_name"=>"Schirmacher", "scopus_author_id"=>"7005272237"}, {"first_name"=>"Niels", "last_name"=>"Grabe", "scopus_author_id"=>"23018837200"}, {"first_name"=>"Kai", "last_name"=>"Breuhahn", "scopus_author_id"=>"6603321273"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"369822320", "doi"=>"10.1371/journal.pone.0075075", "isbn"=>"1932-6203", "pmid"=>"24066165", "issn"=>"19326203", "scopus"=>"2-s2.0-84884191572", "sgr"=>"84884191572"}, "id"=>"f4baaea0-2a4a-373c-8d38-80da5c1d516e", "abstract"=>"Cutaneous regeneration utilizes paracrine feedback mechanisms to fine-tune the regulation of epidermal keratinocyte proliferation and migration. However, it is unknown how fibroblast-derived hepatocyte growth factor (HGF) affects these mutually exclusive processes in distinct cell populations. We here show that HGF stimulates the expression and phosphorylation of the microtubule-destabilizing factor stathmin in primary human keratinocytes. Quantitative single cell- and cell population-based analyses revealed that basal stathmin levels are important for the migratory ability of keratinocytes in vitro; however, its expression is moderately induced in the migration tongue of mouse skin or organotypic multi-layered keratinocyte 3D cultures after full-thickness wounding. In contrast, clearly elevated stathmin expression is detectable in hyperproliferative epidermal areas. In vitro, stathmin silencing significantly reduced keratinocyte proliferation. Automated quantitative and time-resolved analyses in organotypic cocultures demonstrated a high correlation between Stathmin/phospho-Stathmin and Ki67 positivity in epidermal regions with proliferative activity. Thus, activation of stathmin may stimulate keratinocyte proliferation, while basal stathmin levels are sufficient for keratinocyte migration during cutaneous regeneration.", "link"=>"http://www.mendeley.com/research/stathmin-regulates-keratinocyte-proliferation-migration-during-cutaneous-regeneration", "reader_count"=>20, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>6, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Computer Science"=>1, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Kazakhstan"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1206388"], "description"=>"<p>(A) High-power magnification of hair follicle in unwounded mouse skin after Stathmin staining. Black bordered arrows: Stathmin-positive interfollicular keratinocytes; black arrows: keratinocytes surrounding the papilla; arrowheads: cells encircling the sebaceous gland. (B) Exemplary pictures for Stathmin- and H&E overview staining in unwounded and wounded mouse skin at different time-points after wounding (day 1, 3, and 15 post-wounding). Black bordered arrows: migration tongue; black arrows: keratinocytes after reepithelialization; arrowheads: epidermal keratinocytes with high Stathmin positivity. (C) Stathmin staining of OTC samples consisting of primary human keratinocytes and fibroblasts after including 8 µm punches (2 independent sets of samples were analyzed). Black bordered arrows: migration tongue; black arrows: keratinocytes after reepithelialization; arrowheads: epidermal keratinocytes with high Stathmin positivity.</p>", "links"=>[], "tags"=>["stathmin"], "article_id"=>800940, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g003", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differential_Stathmin_expression_in_skin_in_wound_healing_/800940", "title"=>"Differential Stathmin expression in skin in wound healing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206396"], "description"=>"<p>(A) Immunofluorescence Ki67/phospho-Stathmin double staining of OTC wound healing sections. Representative wound edges were shown for 1, 2, 4 and 7 days after punching. For days 2 and 4, Ki67/phospho-Stathmin double positive keratinocytes are highlighted. (B) Percentages of Ki67/phospho-Stathmin positive cells are shown. Note, that regions D/D' and/or E/E' are not detectable due to incomplete wound closure at very early time points. (C) Summarized results of automated quantitative analysis of Ki67 and phospho-Stathmin positivity in keratinocytes of the basal epidermal layer are depicted.</p>", "links"=>[], "tags"=>["phospho-stathmin", "correlate", "keratinocyte", "proliferation", "otc", "healing"], "article_id"=>800948, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_phospho_Stathmin_levels_correlate_with_keratinocyte_proliferation_in_an_OTC_wound_healing_model_/800948", "title"=>"Increased phospho-Stathmin levels correlate with keratinocyte proliferation in an OTC wound healing model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206390"], "description"=>"<p>(A) DNA incorporation assay (SYBR-green assay) after siRNA-mediated inhibition of Stathmin in keratinocytes (final concentration: 20 nM). Nonsense siRNA served as negative controls and was used for statistical comparison (#). Data are shown as mean + SEM (n=3). (B) Keratinocyte viability assay (MTT assay) after siRNA-mediated inhibition of Stathmin (final concentration: 20 nM). Nonsense siRNA served as negative controls and was used for statistical comparison (#). Data are shown as mean + SEM (n=3). (C) Mitotic events of individual keratinocytes were automatically detected after Stathmin or c-Met inhibition based on morphological features. (D) FACS cell cycle analysis. The number of S-phase keratinocytes is indicated. Statistical test: Mann-Whitney U, p*<0.05, p**<0.01, p***<0.001.</p>", "links"=>[], "tags"=>["stathmin", "keratinocyte"], "article_id"=>800942, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g004", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_Stathmin_levels_support_keratinocyte_proliferation_/800942", "title"=>"Increased Stathmin levels support keratinocyte proliferation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206399", "https://ndownloader.figshare.com/files/1206400", "https://ndownloader.figshare.com/files/1206401", "https://ndownloader.figshare.com/files/1206402", "https://ndownloader.figshare.com/files/1206403"], "description"=>"<div><p>Cutaneous regeneration utilizes paracrine feedback mechanisms to fine-tune the regulation of epidermal keratinocyte proliferation and migration. However, it is unknown how fibroblast-derived hepatocyte growth factor (HGF) affects these mutually exclusive processes in distinct cell populations. We here show that HGF stimulates the expression and phosphorylation of the microtubule-destabilizing factor stathmin in primary human keratinocytes. Quantitative single cell- and cell population-based analyses revealed that basal stathmin levels are important for the migratory ability of keratinocytes <i>in vitro</i>; however, its expression is moderately induced in the migration tongue of mouse skin or organotypic multi-layered keratinocyte 3D cultures after full-thickness wounding. In contrast, clearly elevated stathmin expression is detectable in hyperproliferative epidermal areas. <i>In vitro</i>, stathmin silencing significantly reduced keratinocyte proliferation. Automated quantitative and time-resolved analyses in organotypic cocultures demonstrated a high correlation between Stathmin/phospho-Stathmin and Ki67 positivity in epidermal regions with proliferative activity. Thus, activation of stathmin may stimulate keratinocyte proliferation, while basal stathmin levels are sufficient for keratinocyte migration during cutaneous regeneration.</p> </div>", "links"=>[], "tags"=>["regulates", "keratinocyte", "proliferation", "cutaneous"], "article_id"=>800951, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0075075.s001", "https://dx.doi.org/10.1371/journal.pone.0075075.s002", "https://dx.doi.org/10.1371/journal.pone.0075075.s003", "https://dx.doi.org/10.1371/journal.pone.0075075.s004", "https://dx.doi.org/10.1371/journal.pone.0075075.s005"], "stats"=>{"downloads"=>27, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stathmin_Regulates_Keratinocyte_Proliferation_and_Migration_during_Cutaneous_Regeneration_/800951", "title"=>"Stathmin Regulates Keratinocyte Proliferation and Migration during Cutaneous Regeneration", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206377"], "description"=>"<p>(A) Manual tracking of individual primary keratinocyte velocity by time-lapse microscopy. Values represent means +/- SEM (n>10). Statistical test: Mann-Whitney U, p*<0.05. # - Nonsense siRNA-transfected cells were used for statistical comparison. (B) Cell trajectories of keratinocytes after centering all starting points to 0,0 (upper panel). Angle statistics depicting distribution of angles during keratinocyte runs (Rose plot). Diameter shows time, while perimeter indicates the angle of cell migration (lower panel). (C) Kinographs showing the cell density (left) and speed profiles (right) during the gap filling process of migrating keratinocytes. Profiles are color-coded and depict all frames (y-axis represents time, x-axis represents cell position). Cell densities are computed in relation to the position across the gap. Color-coding (density): red - high density, blue - low density. Color-coding (speed): red - high speed, blue - low speed. (D) 2D-migration assay of confluent keratinocytes in a 500 µm gap. Migratory ability was documented using time-lapse microscopy. Relative gap closure was exemplarily calculated and relative cell-free areas are depicted for 24 time-points (1: open gap; 0: closed gap). Representative pictures for each biological sample after 24 hours are shown. Migration front is indicated (white line). All experiments have been performed at least two times showing similar results.</p>", "links"=>[], "tags"=>["stathmin", "supports", "keratinocyte"], "article_id"=>800933, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Basal_Stathmin_supports_keratinocyte_migration_/800933", "title"=>"Basal Stathmin supports keratinocyte migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206373"], "description"=>"<p>(A) Real-time PCR kinetics of Stathmin mRNA expression for 8 hours after administration of HGF (20 ng/ml). For each time-point the ratio of stimulated to untreated primary human keratinocytes was calculated. Data are shown as mean +/- SEM (n=3) and were normalized to transcript levels of untreated cells. (B) Scheme depicting the two major signaling pathways activated by HGF. Chemical inhibitors Akti-1/2 (5 µM) and GW5074 (2 µM) were utilized for selective inhibition of PI3K/AKT- and Ras/Raf/MAPK-pathways. Stathmin transcript levels of keratinocytes were analyzed 1h after stimulation with HGF (20 ng/ml) and administration of both substances for 15 and 30 min, respectively. Data are shown as mean +/- SEM (n=3). (C) Quantitative western immunoblotting analysis of Stathmin and phospho-Stathmin in keratinocytes after stimulation with HGF and administration of Akti-1/2 or GW5074. Total AKT and ERK1/2 as well as phospho-AKT (pAKT) and phospho-ERK1/2 (pERK1/2) served as controls for successful HGF stimulation and pathway inhibition. Numbers indicate quantitative densitometric values of phospho-Stathmin and total Stathmin levels compared to untreated cells. (D) Influence of c-Met inhibition on total Stathmin levels and its phosphorylation status using a receptor-specific inhibitor. Primary keratinocytes were treated with the c-Met inhibitor (PHA-665752, 0.5µM). Numbers indicate quantitative densitometric values of phospho-Stathmin and total Stathmin. (E) Stathmin and c-Met protein expression in keratinocytes after siRNA-mediated inhibition of Stathmin and c-Met after 48 hours (final concentration: 20 nM). Two independent nonsense siRNAs served as negative controls. Different parts of one gel are shown (dividing lines). For all western immunoblots, actin served as loading control.</p>", "links"=>[], "tags"=>["activation", "stathmin"], "article_id"=>800929, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g001", "stats"=>{"downloads"=>3, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bimodal_activation_of_Stathmin_via_HGF_c_Met_signaling_/800929", "title"=>"Bimodal activation of Stathmin via HGF/c-Met signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/1206394"], "description"=>"<p>(A) Schematic display of sample segmentation for automated analysis of OTC wound specimens. Segmentation in 10 areas was defined using HE-staining, while quantitative evaluation was performed using consecutive sections after Ki67/Stathmin double staining. Opposite areas were pooled (A/A’, B/B’, C/C’, D/D’, E/E’) to increase the cell number suitable for statistical analysis. (B) Ki67 and Stathmin double staining of OTC wound healing sections. Exemplary wound edges were shown for 0 (immediately after wounding), 1, 4, and 6 days after punching. (C) Percentage of Stathmin (left) and Ki67 (right) positive cells in different regions of the OTC specimens at indicated time-points. Please note that the regions E/E' (for day 1) and D/D’; E/E’ (for day 0) are not detectable due to incomplete wound closure at early time points. (D) Exemplarily, Ki67/Stathmin double staining is shown. Results of automated quantitative analysis of Ki67 and Stathmin positivity in keratinocytes of the basal epidermal layer are depicted. Black arrows: Ki67-negative/Stathmin-positive cells; White arrows: Ki67/Stathmin-positive cells. Dashed line in bar graph indicates the mathematical regression for the whole experimental time-course. Two independent time-courses were analyzed showing similar results.</p>", "links"=>[], "tags"=>["stathmin", "correlate", "keratinocyte", "proliferating", "otc", "healing"], "article_id"=>800946, "categories"=>["Biological Sciences"], "users"=>["Sabrina Schmitt", "Kai Safferling", "Kathi Westphal", "Manuel Hrabowski", "Ute Müller", "Peter Angel", "Lars Wiechert", "Volker Ehemann", "Benedikt Müller", "Stefan Holland-Cunz", "Damian Stichel", "Nathalie Harder", "Karl Rohr", "Günter Germann", "Franziska Matthäus", "Peter Schirmacher", "Niels Grabe", "Kai Breuhahn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0075075.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_Stathmin_levels_correlate_with_keratinocyte_proliferating_in_an_OTC_wound_healing_model_/800946", "title"=>"Increased Stathmin levels correlate with keratinocyte proliferating in an OTC wound healing model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-09-16 03:16:38"}

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Relative Metric

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