SLI-1 Cbl Inhibits the Engulfment of Apoptotic Cells in C. elegans through a Ligase-Independent Function
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{"title"=>"SLI-1 Cbl Inhibits the Engulfment of Apoptotic Cells in C. elegans through a Ligase-Independent Function", "type"=>"journal", "authors"=>[{"first_name"=>"Courtney", "last_name"=>"Anderson", "scopus_author_id"=>"55548340400"}, {"first_name"=>"Shan", "last_name"=>"Zhou", "scopus_author_id"=>"55547487700"}, {"first_name"=>"Emma", "last_name"=>"Sawin", "scopus_author_id"=>"55547987800"}, {"first_name"=>"H. Robert", "last_name"=>"Horvitz", "scopus_author_id"=>"7007006983"}, {"first_name"=>"Michael E.", "last_name"=>"Hurwitz", "scopus_author_id"=>"55939550800"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-84872013502", "sgr"=>"84872013502", "pui"=>"368067363", "issn"=>"15537390", "isbn"=>"10.1371/journal.pgen.1003115", "pmid"=>"23271977", "doi"=>"10.1371/journal.pgen.1003115"}, "id"=>"bedb3493-7cd9-3872-8a31-cd0f1d1a23d0", "abstract"=>"The engulfment of apoptotic cells is required for normal metazoan development and tissue remodeling. In Caenorhabditis elegans, two parallel and partially redundant conserved pathways act in cell-corpse engulfment. One pathway, which includes the small GTPase CED-10 Rac and the cytoskeletal regulator ABI-1, acts to rearrange the cytoskeleton of the engulfing cell. The CED-10 Rac pathway is also required for proper migration of the distal tip cells (DTCs) during the development of the C. elegans gonad. The second pathway includes the receptor tyrosine kinase CED-1 and might recruit membranes to extend the surface of the engulfing cell. Cbl, the mammalian homolog of the C. elegans E3 ubiquitin ligase and adaptor protein SLI-1, interacts with Rac and Abi2 and modulates the actin cytoskeleton, suggesting it might act in engulfment. Our genetic studies indicate that SLI-1 inhibits apoptotic cell engulfment and DTC migration independently of the CED-10 Rac and CED-1 pathways. We found that the RING finger domain of SLI-1 is not essential to rescue the effects of SLI-1 deletion on cell migration, suggesting that its role in this process is ubiquitin ligase-independent. We propose that SLI-1 opposes the engulfment of apoptotic cells via a previously unidentified pathway.", "link"=>"http://www.mendeley.com/research/sli1-cbl-inhibits-engulfment-apoptotic-cells-c-elegans-through-ligaseindependent-function", "reader_count"=>12, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2}, "reader_count_by_subject_area"=>{"Mathematics"=>1, "Agricultural and Biological Sciences"=>9, "Medicine and Dentistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Computer Science"=>{"Computer Science"=>1}, "Mathematics"=>{"Mathematics"=>1}}, "reader_count_by_country"=>{"United States"=>2}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/525786"], "description"=>"<p>Third larval stage (L3) worms were anaesthetized and viewed using DIC microscopy. The numbers of extra cell nuclei in the anterior pharynges were counted.</p>a<p>These strains contained <i>nIs96</i> [<i>lin-11p::gfp</i>] V.</p>", "links"=>[], "tags"=>["mutation", "programmed"], "article_id"=>196283, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.t002", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_sli_1_mutation_and_programmed_cell_death_/196283", "title"=>"<i>sli-1</i> mutation and programmed cell death.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-13 01:44:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/525486"], "description"=>"<p>(A) The heads of <i>ced-1(e1735)</i> L1 animals with or without the <i>sli-1(sy143)</i> mutation and with or without treatment with <i>abi-1</i> feeding RNAi were scored for engulfment defects using DIC microscopy. The mean ± standard deviation (s.d.) is indicated within each bar. Error bars are sd. <i>p</i> values derived using Student's t test are shown. At least 15 animals were analyzed for each genotype. (B) The heads of <i>ced-5(n1812)</i> L1 animals with or without the <i>sli-1(sy143)</i> and/or <i>abi-1(tm494)</i> mutations were scored as in (A). At least 15 animals were analyzed for each genotype. (C) The gonads of <i>ced-5(n1812)</i> young adult worms with and without mutations in <i>sli-1(sy143)</i> and/or <i>abi-1(tm494)</i> were scored for morphology using DIC microscopy. More than 80 gonad arms were scored for all genotypes. <i>p</i> values derived using Fisher's exact test are shown.</p>", "links"=>[], "tags"=>["suppresses", "engulfment", "dtc", "defects", "loss-of-function"], "article_id"=>195977, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g006", "stats"=>{"downloads"=>3, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Loss_of_sli_1_function_suppresses_engulfment_and_DTC_migration_defects_in_an_abi_1_loss_of_function_mutant_/195977", "title"=>"Loss of <i>sli-1</i> function suppresses engulfment and DTC migration defects in an <i>abi-1</i> loss-of-function mutant.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:39:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/525318"], "description"=>"<p>The gonads of young adult animals mutant for an engulfment gene with or without <i>sli-1</i> mutation were observed and scored for morphology using DIC microscopy. Scoring was as described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003115#s4\" target=\"_blank\">Materials and Methods</a>. Percentages of abnormal gonad arms are shown. More than 80 gonad arms were scored for all genotypes. <i>p</i> values derived using Fisher's exact test are shown.</p>", "links"=>[], "tags"=>["mutation", "suppresses", "dtc", "defects", "caused", "ced-10", "rac", "pathway"], "article_id"=>195796, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_sli_1_mutation_suppresses_the_DTC_migration_defects_caused_by_all_CED_10_Rac_pathway_gene_mutations_/195796", "title"=>"<i>sli-1</i> mutation suppresses the DTC migration defects caused by all CED-10 Rac pathway gene mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:36:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/525865"], "description"=>"<p>First larval stage (L1) worms were anaesthetized and viewed using DIC microscopy. The numbers of cell corpses in the heads were counted. s.d., standard deviation. <i>p-</i>Values refer to comparisons between the double mutant and accompanying triple mutant strains.</p>", "links"=>[], "tags"=>["suppression", "engulfment"], "article_id"=>196359, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.t004", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Losses_of_sli_1_and_abl_1_enhance_each_other_s_suppression_of_some_engulfment_gene_defects_/196359", "title"=>"Losses of <i>sli-1</i> and <i>abl-1</i> enhance each other's suppression of some engulfment gene defects.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-13 01:45:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/525592"], "description"=>"<p>A <i>let-60</i> Ras gain-of-function mutation does not affect apoptotic cell engulfment.</p>", "links"=>[], "tags"=>["ras", "gain-of-function", "mutation", "apoptotic"], "article_id"=>196084, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g007", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_let_60_Ras_gain_of_function_mutation_does_not_affect_apoptotic_cell_engulfment_/196084", "title"=>"A <i>let-60</i> Ras gain-of-function mutation does not affect apoptotic cell engulfment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:41:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/525097"], "description"=>"<p>(A) The number and time of appearance of apoptotic cell corpses that occurred from the first cell death to the comma stage were recorded at 3-min intervals in wild-type and <i>sli-1(sy143)</i> animals using time-lapse DIC microscopy (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003115#s4\" target=\"_blank\">Materials and Methods</a>). Mean numbers of corpses at each time point were calculated from three embryos for both wild-type and <i>sli-1(sy143)</i> animals. Statistical analysis was by the Wilcoxon rank-sum test. The curves are similar (<i>p</i>>0.05). (B) The duration of cell-corpse visibility is similar in wild-type and <i>sli-1(sy143)</i> embryos. The percentage of cell corpses visible for a given period was recorded. The duration of appearance of all cell corpses recorded from three wild-type (n = 159 cell corpses) and three <i>sli-1(sy143)</i> (n = 154) embryos was analyzed. Statistical analysis was by the Wilcoxon rank-sum test. The curves are similar (p>0.5). (C) The morphology of cell corpses in wild-type and <i>sli-1(sy143)</i> embryos are similar. Arrowheads, apoptotic corpses. Embryos were at similar stages of development, approximately six minutes prior to the comma stage. Bar = 5 microns.</p>", "links"=>[], "tags"=>["deaths", "morphology"], "article_id"=>195590, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_sli_1_does_not_affect_the_timing_of_deaths_or_morphology_of_cell_corpses_/195590", "title"=>"<i>sli-1</i> does not affect the timing of deaths or morphology of cell corpses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:33:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/525666"], "description"=>"<p>(A) Truncation minigene <i>sli-1</i> constructs used in this study. Red lines represent proline-rich areas. L, conserved linker domain between the TKB domain (composed of the 4H, EF hand and SH2 domains) and the RING finger. (B) The gonads of <i>ced-10(n1993); sli-1(sy143)</i> young adult animals with or without transgenic arrays containing the genes shown in (A) were scored for abnormal morphology after heat shock. 200 gonad arms in two independent strains were analyzed per genotype. <i>p</i> values derived using Fisher's exact test are shown.</p>", "links"=>[], "tags"=>["tkb"], "article_id"=>196163, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_TKB_domain_of_sli_1_is_required_for_its_cell_migration_function_/196163", "title"=>"The TKB domain of <i>sli-1</i> is required for its cell migration function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:42:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/525753"], "description"=>"<p><i>ced-10(n1993); sli-1(sy143)</i> embryos containing the transgenes indicated above were heat shocked at 33°C for 1 hour and then allowed to recover for 3–3.5 hours at 20°<i>C.</i> The numbers of cell corpses in the heads of anaesthetized first larval stage (L1) worms were counted using DIC microscopy within 0.5 h of hatching. The number of persistent corpses was determined from two independent transgenic lines for each transgene except for P<i><sub>hsp</sub>sli-1ΔRING</i> (see text for explanation). s.d., standard deviation.</p>", "links"=>[], "tags"=>["reverses", "engulfment"], "article_id"=>196244, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.t003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_sli_1_reverses_the_effect_of_sli_1_sy143_on_engulfment_in_ced_10_n1993_sli_1_sy143_animals_/196244", "title"=>"Overexpression of <i>sli-1</i> reverses the effect of <i>sli-1(sy143)</i> on engulfment in <i>ced-10(n1993); sli-1(sy143)</i> animals.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-13 01:44:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/525412"], "description"=>"<p>The gonads of <i>ced-5(n1812)</i> and <i>ced-10(n1993)</i> young adult worms with and without mutations in <i>abl-1(ok171)</i> and/or <i>sli-1(n3538)</i> were scored for morphology using DIC microscopy. More than 80 gonad arms were scored for all genotypes. <i>p</i> values derived using Fisher's exact test are shown.</p>", "links"=>[], "tags"=>["suppression", "engulfment", "dtc"], "article_id"=>195906, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Losses_of_sli_1_and_abl_1_enhance_each_other_s_suppression_of_some_engulfment_gene_DTC_defects_/195906", "title"=>"Losses of <i>sli-1</i> and <i>abl-1</i> enhance each other's suppression of some engulfment gene DTC defects.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:38:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/525201"], "description"=>"<p>SLI-1::GFP was expressed under the control of its own promoter in an extrachromosomal array. (A) Images of morphologically normal animals expressing the SLI-1::GFP transgene. i, iii and v show fluorescence images and ii, iv and vi show accompanying DIC images (i–iv, embryos; v–vi, L4 larvae). Arrowheads in i–iv indicate positions of unengulfed cell corpses. In image iii corpses are not visible. Arrowheads in v and vi indicate the DTC. (B) Images of morphologically abnormal embryos expressing the SLI-1::GFP transgene. i, iii and v show fluorescence images and ii, iv and vi show accompanying DIC images. Arrowheads indicate positions of unengulfed cell corpses. Bar = 5 microns.</p>", "links"=>[], "tags"=>["genetics and genomics", "developmental biology", "Biochemistry"], "article_id"=>195696, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_pattern_of_SLI_1_GFP_under_control_of_the_sli_1_promoter_/195696", "title"=>"Expression pattern of SLI-1::GFP under control of the <i>sli-1</i> promoter.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:34:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/525825"], "description"=>"<p>First larval stage (L1) worms were anaesthetized and viewed using DIC microscopy. The numbers of cell corpses in the heads were counted. s.d., standard deviation.</p>", "links"=>[], "tags"=>["mutations", "suppress", "engulfment", "defects", "caused"], "article_id"=>196313, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.t001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_sli_1_mutations_suppress_the_engulfment_defects_caused_by_engulfment_ced_gene_mutations_/196313", "title"=>"<i>sli-1</i> mutations suppress the engulfment defects caused by engulfment <i>ced</i> gene mutations.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-13 01:45:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/283552", "https://ndownloader.figshare.com/files/283604"], "description"=>"<div><p>The engulfment of apoptotic cells is required for normal metazoan development and tissue remodeling. In <em>Caenorhabditis elegans</em>, two parallel and partially redundant conserved pathways act in cell-corpse engulfment. One pathway, which includes the small GTPase CED-10 Rac and the cytoskeletal regulator ABI-1, acts to rearrange the cytoskeleton of the engulfing cell. The CED-10 Rac pathway is also required for proper migration of the distal tip cells (DTCs) during the development of the <em>C. elegans</em> gonad. The second pathway includes the receptor tyrosine kinase CED-1 and might recruit membranes to extend the surface of the engulfing cell. Cbl, the mammalian homolog of the <em>C. elegans</em> E3 ubiquitin ligase and adaptor protein SLI-1, interacts with Rac and Abi2 and modulates the actin cytoskeleton, suggesting it might act in engulfment. Our genetic studies indicate that SLI-1 inhibits apoptotic cell engulfment and DTC migration independently of the CED-10 Rac and CED-1 pathways. We found that the RING finger domain of SLI-1 is not essential to rescue the effects of SLI-1 deletion on cell migration, suggesting that its role in this process is ubiquitin ligase-independent. We propose that SLI-1 opposes the engulfment of apoptotic cells via a previously unidentified pathway.</p> </div>", "links"=>[], "tags"=>["sli-1", "cbl", "inhibits", "engulfment", "apoptotic", "cells", "ligase-independent", "function"], "article_id"=>115909, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003115.s001", "https://dx.doi.org/10.1371/journal.pgen.1003115.s002"], "stats"=>{"downloads"=>5, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/SLI_1_Cbl_Inhibits_the_Engulfment_of_Apoptotic_Cells_in_C_elegans_through_a_Ligase_Independent_Function__/115909", "title"=>"SLI-1 Cbl Inhibits the Engulfment of Apoptotic Cells in <em>C. elegans</em> through a Ligase-Independent Function", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-12-13 01:38:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/525027"], "description"=>"<p>Proteins of the CED-10 Rac pathway are labeled in yellow. Proteins of the CED-1 pathway are labeled in green. <i>C. elegans</i> protein names are indicated above and their mammalian homologs below. The Wave Regulatory Complex (WRC) contains ABI-1, GEX-2, GEX-3, WVE-1 and NUO-3. The dashed arrow from CED-6 to CED-10 indicates that CED-1, CED-6 and CED-7 might also signal through CED-10 <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003115#pgen.1003115-Kinchen1\" target=\"_blank\">[6]</a>. The CED-1 pathway is required for engulfment only, whereas the CED-10 Rac pathway is required for both engulfment and DTC migration.</p>", "links"=>[], "tags"=>["molecular", "pathways", "engulfment", "apoptotic"], "article_id"=>195519, "categories"=>["Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Courtney Anderson", "Shan Zhou", "Emma Sawin", "H. Robert Horvitz", "Michael E. Hurwitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003115.g001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Core_molecular_pathways_required_for_the_engulfment_of_apoptotic_cells_/195519", "title"=>"Core molecular pathways required for the engulfment of apoptotic cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-13 01:31:59"}

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Relative Metric

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