{"entryType":"UniProtKB reviewed (Swiss-Prot)","primaryAccession":"G5EDT1","uniProtkbId":"LIN35_CAEEL","entryAudit":{"firstPublicDate":"2017-07-05","lastAnnotationUpdateDate":"2026-09-02","lastSequenceUpdateDate":"2011-12-14","entryVersion":106,"sequenceVersion":1},"annotationScore":5.0,"organism":{"scientificName":"Caenorhabditis elegans","taxonId":6239,"evidences":[{"evidenceCode":"ECO:0000312","source":"Proteomes","id":"UP000001940"}],"lineage":["Eukaryota","Metazoa","Ecdysozoa","Nematoda","Chromadorea","Rhabditida","Rhabditina","Rhabditomorpha","Rhabditoidea","Rhabditidae","Peloderinae","Caenorhabditis"]},"proteinExistence":"1: Evidence at protein level","proteinDescription":{"recommendedName":{"fullName":{"evidences":[{"evidenceCode":"ECO:0000305"}],"value":"Retinoblastoma-like protein homolog lin-35"}},"alternativeNames":[{"fullName":{"evidences":[{"evidenceCode":"ECO:0000312","source":"WormBase","id":"C32F10.2"}],"value":"Abnormal cell lineage protein 35"}},{"fullName":{"evidences":[{"evidenceCode":"ECO:0000305"}],"value":"Synthetic multivulva protein lin-35"}}]},"genes":[{"geneName":{"evidences":[{"evidenceCode":"ECO:0000312","source":"WormBase","id":"C32F10.2"}],"value":"lin-35"},"orfNames":[{"evidences":[{"evidenceCode":"ECO:0000312","source":"WormBase","id":"C32F10.2"}],"value":"C32F10.2"}]}],"comments":[{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"11684669"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"11850412"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"12062054"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"12783801"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15196946"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15280233"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15328017"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15621535"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15649460"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"16287966"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"16624904"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17070797"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17075059"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17237514"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17417969"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17466069"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17881492"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"18437219"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"19521497"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"22542970"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"23347407"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"23664972"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"24214340"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"24752899"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"26100681"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"27104746"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"9875852"},{"evidenceCode":"ECO:0000305","source":"PubMed","id":"15315757"},{"evidenceCode":"ECO:0000305","source":"PubMed","id":"16507136"},{"evidenceCode":"ECO:0000305","source":"PubMed","id":"24715729"}],"value":"Key regulator of cell division which acts as a transcriptional repressor and negatively regulates cell cycle progression in its active unphosphorylated form, but allows cell cycle progression when phosphorylated (PubMed:11684669, PubMed:12062054, PubMed:16287966, PubMed:17466069, PubMed:25562820). When unphosphorylated and in its active form, interacts with E2F transcription factors such as efl-1 to repress their transcriptional activity and negatively regulate the progression through the G1 phase of the cell cycle during postembryonic development (PubMed:11684669, PubMed:12062054, PubMed:15238519, PubMed:17466069, PubMed:25562820). May furthermore act with cell cycle regulator cki-1 to negatively regulate cell cycle progression (PubMed:11684669). Acts redundantly with lin-53, fzr-1 and lin-23 to control cell cycle progression by regulating the expression of G1 phase cyclins (PubMed:11850412, PubMed:25562820). In particular, negatively regulates the expression of the cyclin E homolog cye-1, which is essential for the G1/S phase transition (PubMed:16287966, PubMed:17466069). Regulates cell division in the intestinal lineage, repressing the expression of genes such as cdc-25.2, which are required for intestinal cells to transition from the karyokinesis cell cycle (also known as nuclear division) to endoreplication, a specific growth pathway in the intestinal epithelium required for feeding and gut development in growing larvae during the L1 stage molt (PubMed:17466069, PubMed:27104746). Its role as a transcriptional repressor in the regulation of intestinal cell division during postembryonic development is most likely in complex with an E2F cell cycle regulatory transcription factor efl-1 and its binding partner the synthetic multivulva class B protein dpl-1 (PubMed:17466069). Synthetic multivulva (synMuv) class B protein (PubMed:11850412, PubMed:9875852). SynMuv proteins are required to repress the induction of vulval development by Ras signaling and probably act by forming the multiprotein DRM complex that represses transcription (PubMed:17075059, PubMed:9875852). Together with synMuv class B protein lin-53, and redundantly with synMuv class A protein lin-15A, represses transcription to control vulval development, most likely through antagonization of the Ras-signaling pathway in the major hypodermal syncytium hyp7 (PubMed:15621535, PubMed:16624904, PubMed:26100681, PubMed:9875852). Acts redundantly with the transcriptional corepressor spr-1 and the zinc finger protein zfp-2 to play a role in vulval morphogenesis, promote germline proliferation and somatic gonad development (PubMed:17070797, PubMed:17417969). Acts redundantly with ubc-18 in the regulation of pharyngeal morphogenesis during embryonic development by negatively regulating the expression of proteins such as sup-35 (PubMed:12783801, PubMed:19521497, PubMed:24214340). Functions with the SWI/SNF complex and proteins such as pha-1 to regulate larval development (PubMed:15196946, PubMed:15280233). Functions redundantly with xnp-1 to regulate somatic gonad development (PubMed:15328017, PubMed:15649460). Acts redundantly with slr-2 to regulate the expression of intestinal genes required for nutrient utilization (PubMed:18437219, PubMed:22542970). Regulates transcription in response to starvation (PubMed:23664972). Furthermore, in response to starvation, promotes germ cell programmed cell death by negatively regulating the expression of the anti-apoptotic protein ced-9 (PubMed:17881492, PubMed:24752899). Conversely, in conjunction with mcd-1, efl-1 and the synthetic multivulva class B proteins dpl-1, lin-37 and lin-52, may also regulate transcription to promote programmed cell death independently of ced-1, ced-8 and ced-9 cell death pathways (PubMed:17237514). Directly involved in heterochromatin formation by maintaining overall chromatin structure and, in particular, that of constitutive heterochromatin by stabilizing histone methylation (PubMed:23347407). In particular, negatively regulates the expression of mes-4, a histone methyltransferase that controls the expression of germline specific genes (PubMed:23347407). May play a role in double strand break formation during meiosis (PubMed:15315757). May suppress sensitivity to RNAi (PubMed:16507136, PubMed:17417969). May play a role in the response to endoplasmic reticulum (ER) stress (PubMed:24715729)"}],"commentType":"FUNCTION"},{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"11463372"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"16020796"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17075059"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"9875852"}],"value":"Component of the DRM complex, at least composed of lin-9, lin-35, lin-37, lin-52, lin-53, lin-54, dpl-1 and efl-1 (PubMed:17075059). Interacts with lin-53 (PubMed:9875852). Interacts (via C-terminus) with dpl-1 (via C-terminus) and efl-1 (via C-terminus) (PubMed:11463372). Interacts (via C-terminus) with lin-8 (PubMed:16020796)"}],"commentType":"SUBUNIT"},{"commentType":"INTERACTION","interactions":[{"interactantOne":{"uniProtKBAccession":"G5EDT1","intActId":"EBI-321470"},"interactantTwo":{"uniProtKBAccession":"Q22703","geneName":"dpl-1","intActId":"EBI-324825"},"numberOfExperiments":2,"organismDiffer":false}]},{"commentType":"SUBCELLULAR LOCATION","note":{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"}],"value":"Expressed in dividing cells, but decreased expression after cell cycle exit"}]},"subcellularLocations":[{"location":{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15621535"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"23347407"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"9875852"}],"value":"Nucleus","id":"SL-0191"}}]},{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15621535"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"9875852"}],"value":"Expressed in embryos and newly hatched L1 larvae (PubMed:9875852). In older larvae and adults expressed in P(3-8).p vulval precursor cells and its descendents (PubMed:9875852). Expressed in the major hypodermal syncytium hyp7 during the L3 stage of larval development (PubMed:15621535)"}],"commentType":"DEVELOPMENTAL STAGE"},{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"}],"value":"Phosphorylated by the cyclin dependent kinase cdk-4. Phosphorylation inhibits the transcriptional repressor activity of lin-35 and allows for progression through the G1 phase of the cell cycle during postembryonic development"}],"commentType":"PTM"},{"texts":[{"evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"11684669"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15196946"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15280233"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15328017"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"15649460"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"16507136"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"16624904"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17070797"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17237514"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17417969"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"17466069"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"18437219"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"22542970"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"24715729"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"26100681"},{"evidenceCode":"ECO:0000269","source":"PubMed","id":"27650246"}],"value":"Viable, but with a reduced fertility and brood size (PubMed:11684669, PubMed:15280233, PubMed:15328017, PubMed:17417969). Low penetrance defects including reduced integrity of the proximal gonad, a low percentage of endomitotic oocytes, distal tip cell migration defects and abnormalities in vulval morphology (PubMed:17417969). Some studies demonstrate aberrant intestinal nuclear divisions, with increased intestinal nuclei in growing larvae (PubMed:17466069). In addition there is increased sensitivity to RNA-induced gene silencing by RNAi (PubMed:16507136, PubMed:17417969). RNAi-mediated knockdown results in increased survival in response to ER stress inducer tunicamycin as compared to wild-type animals (PubMed:24715729). RNAi-mediated knockdown results in larval arrest at 25 degrees Celsius in an xpn-1 mutant background (PubMed:15649460). RNAi-mediated knockdown in a ced-1 mutant background results in reduced somatic cell apoptosis (PubMed:27650246). Double knockout with the synthetic multivulva class B protein lin-15A results in a multiple vulva (Muv) phenotype (PubMed:16624904, PubMed:26100681). Double knockout with either cdk-4 or cyd-1 rescues the cell cycle progression defect in the single cdk-4 and cyd-1 mutants (PubMed:11684669, PubMed:25562820). Double knockout with xnp-1 results in 43% embryonic lethality (PubMed:15328017). Surviving animals develop slowly, are small, sterile and display male and female gonad developmental defects characterized by shorter gonadal arms, fewer germ cells, an everted vulva phenotype, and failed formation of sheath and spermathecal cells (PubMed:15328017). Double knockout with spr-1 or zfp-2 results in defects in growth, vulval morphogenesis, somatic gonad development and fertility (PubMed:17070797, PubMed:17417969). Double knockout with the programmed cell death regulator mcd-1 results in 100% lethality during the L1 stage of larval development (PubMed:17237514). Programmed cell death defect in a ced-3 n2427 mutant background (PubMed:17237514). Knockout with RNAi-mediated knockdown of psa-1, ham-3, swsn-2.2, swsn-3 or swsn-6 (components of the SWI/SNF complex) results in larval arrest during larval development (PubMed:15280233). Knockout with RNAi-mediated knockdown of pha-1 (developmental protein), snfc-5 or swsn-8 (additional SWI/SNF complex components) results in sterility and/or a protruding vulva phenotype (PubMed:15196946, PubMed:15280233). Double knockout with slr-2 results in early larval arrest due to mis-regulation of intestinal specific gene expression, which results in starvation-induced growth arrest (PubMed:18437219, PubMed:22542970)"}],"commentType":"DISRUPTION PHENOTYPE"},{"texts":[{"evidences":[{"evidenceCode":"ECO:0000305"}],"value":"Belongs to the retinoblastoma protein (RB) family"}],"commentType":"SIMILARITY"}],"features":[{"type":"Chain","location":{"start":{"value":1,"modifier":"EXACT"},"end":{"value":961,"modifier":"EXACT"}},"description":"Retinoblastoma-like protein homolog lin-35","evidences":[{"evidenceCode":"ECO:0000305"}],"featureId":"PRO_0000441023"},{"type":"Region","location":{"start":{"value":1,"modifier":"EXACT"},"end":{"value":43,"modifier":"EXACT"}},"description":"Disordered","evidences":[{"evidenceCode":"ECO:0000256","source":"SAM","id":"MobiDB-lite"}]},{"type":"Region","location":{"start":{"value":55,"modifier":"EXACT"},"end":{"value":129,"modifier":"EXACT"}},"description":"Disordered","evidences":[{"evidenceCode":"ECO:0000256","source":"SAM","id":"MobiDB-lite"}]},{"type":"Compositional bias","location":{"start":{"value":68,"modifier":"EXACT"},"end":{"value":81,"modifier":"EXACT"}},"description":"Polar residues","evidences":[{"evidenceCode":"ECO:0000256","source":"SAM","id":"MobiDB-lite"}]},{"type":"Compositional bias","location":{"start":{"value":107,"modifier":"EXACT"},"end":{"value":119,"modifier":"EXACT"}},"description":"Acidic residues","evidences":[{"evidenceCode":"ECO:0000256","source":"SAM","id":"MobiDB-lite"}]},{"type":"Modified residue","location":{"start":{"value":714,"modifier":"EXACT"},"end":{"value":714,"modifier":"EXACT"}},"description":"Phosphoserine; by CDK4","evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"}]},{"type":"Modified residue","location":{"start":{"value":719,"modifier":"EXACT"},"end":{"value":719,"modifier":"EXACT"}},"description":"Phosphothreonine; by CDK4","evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"25562820"}]},{"type":"Mutagenesis","location":{"start":{"value":151,"modifier":"EXACT"},"end":{"value":961,"modifier":"EXACT"}},"description":"In n745; on a ubc-18 mutant background, 4% of larvae display a Pun (pharyngeal unattached) phenotype, whereby the pharynx fails to elongate and form an attachment to the anterior alimentary opening or buccal cavity.","evidences":[{"evidenceCode":"ECO:0000269","source":"PubMed","id":"12783801"}],"alternativeSequence":{}}],"keywords":[{"id":"KW-0131","category":"Biological process","name":"Cell cycle"},{"id":"KW-0238","category":"Molecular function","name":"DNA-binding"},{"id":"KW-0539","category":"Cellular component","name":"Nucleus"},{"id":"KW-0597","category":"PTM","name":"Phosphoprotein"},{"id":"KW-1185","category":"Technical term","name":"Reference proteome"},{"id":"KW-0678","category":"Molecular function","name":"Repressor"},{"id":"KW-0804","category":"Biological process","name":"Transcription"},{"id":"KW-0805","category":"Biological process","name":"Transcription regulation"}],"references":[{"referenceNumber":1,"citation":{"id":"9875852","citationType":"journal article","authors":["Lu X.","Horvitz H.R."],"citationCrossReferences":[{"database":"PubMed","id":"9875852"},{"database":"DOI","id":"10.1016/s0092-8674(00)81722-5"}],"title":"lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48.","publicationDate":"1998","journal":"Cell","firstPage":"981","lastPage":"991","volume":"95"},"referencePositions":["NUCLEOTIDE SEQUENCE [MRNA]","FUNCTION","INTERACTION WITH LIN-53","SUBCELLULAR LOCATION","DEVELOPMENTAL STAGE"],"evidences":[{"evidenceCode":"ECO:0000312","source":"EMBL","id":"AAD05570.1"}]},{"referenceNumber":2,"citation":{"id":"9851916","citationType":"journal article","authoringGroup":["The C. elegans sequencing consortium"],"citationCrossReferences":[{"database":"PubMed","id":"9851916"},{"database":"DOI","id":"10.1126/science.282.5396.2012"}],"title":"Genome sequence of the nematode C. elegans: a platform for investigating biology.","publicationDate":"1998","journal":"Science","firstPage":"2012","lastPage":"2018","volume":"282"},"referencePositions":["NUCLEOTIDE SEQUENCE [LARGE SCALE GENOMIC DNA]"],"referenceComments":[{"evidences":[{"evidenceCode":"ECO:0000312","source":"Proteomes","id":"UP000001940"}],"value":"Bristol N2","type":"STRAIN"}],"evidences":[{"evidenceCode":"ECO:0000312","source":"Proteomes","id":"UP000001940"}]},{"referenceNumber":3,"citation":{"id":"11684669","citationType":"journal article","authors":["Boxem M.","van den Heuvel S."],"citationCrossReferences":[{"database":"PubMed","id":"11684669"},{"database":"DOI","id":"10.1242/dev.128.21.4349"}],"title":"lin-35 Rb and cki-1 Cip/Kip cooperate in developmental regulation of G1 progression in C. elegans.","publicationDate":"2001","journal":"Development","firstPage":"4349","lastPage":"4359","volume":"128"},"referencePositions":["FUNCTION","DISRUPTION PHENOTYPE"],"evidences":[{"evidenceCode":"ECO:0000305"}]},{"referenceNumber":4,"citation":{"id":"11463372","citationType":"journal article","authors":["Ceol C.J.","Horvitz H.R."],"citationCrossReferences":[{"database":"PubMed","id":"11463372"},{"database":"DOI","id":"10.1016/s1097-2765(01)00194-0"}],"title":"dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C.elegans vulval development.","publicationDate":"2001","journal":"Mol. 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