A genetic interactome of the let-7 microRNA in C. elegans

Developmental Biology

Volumn 401, Issue 2, 2015, Pages 276-286

  Rausch, Magdalene ^a,b   Ecsedi, Matyas ^a,b   Bartake, Hrishikesh ^a,b,c   Müllner, Almuth ^a,d   Großhans, Helge ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

C. elegans; CDC 25.2; CDK 1; Cell cycle; Col 19; Condensin; Condensin II complex; Developmental timing; Differentiation; Heterochronic; Hypodermis; Let 7; LIN 29; MicroRNA; MiRNA regulation; MiRNA target; NCC 1; Vulva

Indexed keywords

CONDENSIN; CONDENSIN II COMPLEX; CYCLIN DEPENDENT KINASE 1; LET 7 MICRORNA; MICRORNA; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CAENORHABDITIS ELEGANS PROTEIN; DNA BINDING PROTEIN; LET-7 MICRORNA, C ELEGANS; LIN-29 PROTEIN, C ELEGANS; MULTIPROTEIN COMPLEX; TRANSCRIPTION FACTOR;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE IDENTIFICATION; GENE INTERACTION; GENE SILENCING; GENE TARGETING; GENETIC REGULATION; GENOME ANALYSIS; MICROARRAY ANALYSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SUPPRESSOR GENE; ANIMAL; BIOSYNTHESIS; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MORPHOGENESIS;

CAENORHABDITIS ELEGANS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CDC2 PROTEIN KINASE; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICRORNAS; MULTIPROTEIN COMPLEXES; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

EID: 84929283834     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.02.013     Document Type: Article

References (57)

1. Abe S., Nagasaka K., Hirayama Y., Kozuka-Hata H., Oyama M., Aoyagi Y., Obuse C., Hirota T. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev. 2011, 25:863-874.
2. Abrahante J.E., Daul A.L., Li M., Volk M.L., Tennessen J.M., Miller E.A., Rougvie A.E. The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev. Cell 2003, 4:625-637.
3. Abrahante J.E., Miller E.A., Rougvie A.E. Identification of heterochronic mutants in Caenorhabditis elegans. Temporal misexpression of a collagen: green fluorescent protein fusion gene. Genetics 1998, 149:1335-1351.
4. Ambros V., Horvitz H.R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 1984, 226:409-416.
5. Aspöck G., Kagoshima H., Niklaus G., Bürglin T.R. Caenorhabditis elegans has scores of hedgehog-related genes: sequence and expression analysis. Genome Res. 1999, 9:909-923.
6. Bagga S., Bracht J., Hunter S., Massirer K., Holtz J., Eachus R., Pasquinelli A.E. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563.
7. Beanan M.J., Strome S. Characterization of a germ-line proliferation mutation in C. elegans. Development 1992, 116:755-766.
8. Boxem M., Srinivasan D.G., van den Heuvel S. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 1999, 126:2227-2239.
9. Büssing I., Slack F.J., Großhans H. let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med. 2008, 14:400-409.
10. Büssing I., Yang J.S., Lai E.C., Großhans H. The nuclear export receptor XPO-1 supports primary miRNA processing in C. elegans and Drosophila. EMBO J. 2010, 29:1830-1839.
11. Csankovszki G., Collette K., Spahl K., Carey J., Snyder M., Petty E., Patel U., Tabuchi T., Liu H., McLeod I., Thompson J., Sarkeshik A., Yates J., Meyer B.J., Hagstrom K. Three distinct condensin complexes control C. elegans chromosome dynamics. Curr. Biol. 2009, 19:9-19.
12. Ding X.C., Großhans H. Repression of C. elegans microRNA targets at the initiation level of translation requires GW182 proteins. EMBO J. 2009, 28:213-222.
13. Ding X.C., Slack F.J., Großhans H. The let-7 microRNA interfaces extensively with the translation machinery to regulate cell differentiation. Cell Cycle 2008, 7:3083-3090.
14. Ecsedi M., Rausch M., Großhans H. The let-7 microRNA directs vulval development through a single target. Dev. Cell 2015, 32:335-344.
15. Edgar R., Domrachev M., Lash A.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
16. Frokjaer-Jensen C., Davis M.W., Hopkins C.E., Newman B.J., Thummel J.M., Olesen S.P., Grunnet M., Jorgensen E.M. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 2008, 40:1375-1383.
17. Großhans H., Johnson T., Reinert K.L., Gerstein M., Slack F.J. The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev. Cell 2005, 8:321-330.
18. Hagstrom K.A., Holmes V.F., Cozzarelli N.R., Meyer B.J. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 2002, 16:729-742.
19. Harris D.T., Horvitz H.R. MAB-10/NAB acts with LIN-29/EGR to regulate terminal differentiation and the transition from larva to adult in C. elegans. Development 2011, 138:4051-4062.
20. Hendriks G.J., Gaidatzis D., Aeschimann F., Großhans H. Extensive oscillatory gene expression during C. elegans larval development. Mol. Cell 2014, 53:380-392.
21. Hong Y., Roy R., Ambros V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 1998, 125:3585-3597.
22. Hunter S.E., Finnegan E.F., Zisoulis D.G., Lovci M.T., Melnik-Martinez K.V., Yeo G.W., Pasquinelli A.E. Functional genomic analysis of the let-7 regulatory network in Caenorhabditis elegans. PLoS Genet. 2013, 9:e1003353.
23. Johnson C.D., Esquela-Kerscher A., Stefani G., Byrom M., Kelnar K., Ovcharenko D., Wilson M., Wang X., Shelton J., Shingara J., Chin L., Brown D., Slack F.J. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 2007, 67:7713-7722.
24. Johnson S.M., Großhans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
25. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
26. Kim J., Kawasaki I., Shim Y.H. cdc-25.2, a C. elegans ortholog of cdc25, is required to promote oocyte maturation. J. Cell Sci. 2010, 123:993-1000.
27. Kim J.K., Gabel H.W., Kamath R.S., Tewari M., Pasquinelli A., Rual J.F., Kennedy S., Dybbs M., Bertin N., Kaplan J.M., Vidal M., Ruvkun G. Functional genomic analysis of RNA interference in C. elegans. Science 2005, 308:1164-1167.
28. Koh K., Rothman J.H. ELT-5 and ELT-6 are required continuously to regulate epidermal seam cell differentiation and cell fusion in C. elegans. Development 2001, 128:2867-2880.
29. Kranz A.L., Jiao C.Y., Winterkorn L.H., Albritton S.E., Kramer M., Ercan S. Genome-wide analysis of condensin binding in Caenorhabditis elegans. Genome Biol. 2013, 14:R112.
30. Lee Y.S., Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 2007, 21:1025-1030.
31. Lin S.Y., Johnson S.M., Abraham M., Vella M.C., Pasquinelli A., Gamberi C., Gottlieb E., Slack F.J. The C elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell 2003, 4:639-650.
32. Liu Z., Kirch S., Ambros V. The Caenorhabditis elegans heterochronic gene pathway controls stage-specific transcription of collagen genes. Development 1995, 121:2471-2478.
33. Melton C., Judson R.L., Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010, 463:621-626.
34. Mori H., Palmer R.E., Sternberg P.W. The identification of a Caenorhabditis elegans homolog of p34cdc2 kinase. Mol. Gen. Genet. 1994, 245:781-786.
35. Ouyang B., Wang Y., Wei D. Caenorhabditis elegans contains structural homologs of human prk and plk. DNA Seq. 1999, 10:109-113.
36. Parry D.H., Xu J., Ruvkun G. A whole-genome RNAi Screen for C. elegans miRNA pathway genes. Curr. Biol. 2007, 17:2013-2022.
37. Pasquinelli A.E., Reinhart B.J., Slack F., Martindale M.Q., Kuroda M.I., Maller B., Hayward D.C., Ball E.E., Degnan B., Muller P., Spring J., Srinivasan A., Fishman M., Finnerty J., Corbo J., Levine M., Leahy P., Davidson E., Ruvkun G. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
38. Podbilewicz B., White J.G. Cell fusions in the developing epithelial of C. elegans. Dev. Biol. 1994, 161:408-424.
39. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
40. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
41. Rougvie A.E., Ambros V. The heterochronic gene lin-29 encodes a zinc finger protein that controls a terminal differentiation event in Caenorhabditis elegans. Development 1995, 121:2491-2500.
42. Roush S., Slack F.J. The let-7 family of microRNAs. Trends Cell. Biol. 2008, 18:505-516.
43. Rual J.F., Ceron J., Koreth J., Hao T., Nicot A.S., Hirozane-Kishikawa T., Vandenhaute J., Orkin S.H., Hill D.E., van den Heuvel S., Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 2004, 14:2162-2168.
44. Rybak A., Fuchs H., Smirnova L., Brandt C., Pohl E.E., Nitsch R., Wulczyn F.G. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 2008, 10:987-993.
45. Sampson V.B., Rong N.H., Han J., Yang Q., Aris V., Soteropoulos P., Petrelli N.J., Dunn S.P., Krueger L.J. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res. 2007, 67:9762-9770.
46. Santamaria D., Barriere C., Cerqueira A., Hunt S., Tardy C., Newton K., Caceres J.F., Dubus P., Malumbres M., Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 2007, 448:811-815.
47. Shirayama M., Seth M., Lee H.C., Gu W., Ishidate T., Conte D., Mello C.C. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 2012, 150:65-77.
48. Singh R.N., Sulston J.E. Some Observations On Moulting in Caenorhabditis Elegans. Nematologica 1978, 24:63-71.
49. Slack F.J., Basson M., Liu Z., Ambros V., Horvitz H.R., Ruvkun G. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 2000, 5:659-669.
50. Stear J.H., Roth M.B. Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes Dev. 2002, 16:1498-1508.
51. Sulston J.E., Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 1977, 56:110-156.
52. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
53. Takamizawa J., Konishi H., Yanagisawa K., Tomida S., Osada H., Endoh H., Harano T., Yatabe Y., Nagino M., Nimura Y., Mitsudomi T., Takahashi T. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004, 64:3753-3756.
54. Timmons L., Court D.L., Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263:103-112.
55. Vella M.C., Choi E.Y., Lin S.Y., Reinert K., Slack F.J. The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3'UTR. Genes Dev. 2004, 18:132-137.
56. Worringer K.A., Rand T.A., Hayashi Y., Sami S., Takahashi K., Tanabe K., Narita M., Srivastava D., Yamanaka S. The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes. Cell Stem Cell 2014, 14:40-52.
57. Zisoulis D.G., Lovci M.T., Wilbert M.L., Hutt K.R., Liang T.Y., Pasquinelli A.E., Yeo G.W. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 2010, 17:173-179.