A shared role for RBF1 and dCAP-D3 in the regulation of transcription with consequences for innate immunity

PLoS Genetics

Volumn 8, Issue 4, 2012, Pages

  Longworth, Michelle S ^a   Walker, James A ^b,c   Anderssen, Endre ^b   Moon, Nam Sung ^d   Gladden, Andrew ^e   Heck, Margarete M S ^f   Ramaswamy, Sridhar ^b   Dyson, Nicholas J ^b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONDENSIN; CONDENSIN DCAP D3; PROTEIN RBF1; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; ANTIMICROBIAL CATIONIC PEPTIDE; ATTACIN A PROTEIN, DROSOPHILA; ATTACIN B PROTEIN, DROSOPHILA; ATTACIN-A PROTEIN, DROSOPHILA; ATTACIN-B PROTEIN, DROSOPHILA; CAP D3 PROTEIN, DROSOPHILA; CAP-D3 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; RBF1 PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL PEPTIDE GENE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL INFECTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FAT BODY; FEMALE; GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; IMMUNOREACTIVITY; INNATE IMMUNITY; LIFE CYCLE; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; SURVIVAL RATE; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; METABOLISM; MULTIGENE FAMILY; PATHOGENICITY; PHAGOCYTOSIS; POLYTENE CHROMOSOME;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FAT BODY; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; MULTIGENE FAMILY; ORGAN SPECIFICITY; PHAGOCYTOSIS; POLYTENE CHROMOSOME; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84860577638     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002618     Document Type: Article

References (85)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Sherr CJ, McCormick F, (2002) The RB and p53 pathways in cancer. Cancer Cell 2: 103-112.
3. Trimarchi JM, Lees JA, (2002) Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3: 11-20.
4. Thomas DM, Carty SA, Piscopo DM, Lee JS, Wang WF, et al. (2001) The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell 8: 303-316.
5. Schneider J, Gu W, Zhu L, Mahdavi V, Nadal-Ginard B, (1994) Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells 10.1126/science.8197461. Science 264: 1467-1471.
6. Novitch B, Mulligan G, Jacks T, Lassar A, (1996) Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle 10.1083/jcb.135.2.441. J Cell Biol 135: 441-456.
7. Zacksenhaus E, Jiang Z, Chung D, Marth JD, Phillips RA, et al. (1996) pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev 10: 3051-3064.
8. Nicolay BN, Bayarmagnai B, Moon NS, Benevolenskaya EV, Frolov MV, (2010) Combined inactivation of pRB and hippo pathways induces dedifferentiation in the Drosophila retina. PLoS Genet 6: e1000918 doi:10.1371/journal.pgen.1000918.
9. Longworth MS, Dyson NJ, (2010) pRb, a local chromatin organizer with global possibilities. Chromosoma 119: 1-11.
10. Isaac CE, Francis SM, Martens AL, Julian LM, Seifried LA, et al. (2006) The retinoblastoma protein regulates pericentric heterochromatin. Mol Cell Biol 26: 3659-3671.
11. Longworth MS, Herr A, Ji JY, Dyson NJ, (2008) RBF1 promotes chromatin condensation through a conserved interaction with the Condensin II protein dCAP-D3. Genes Dev 22: 1011-1024.
12. Manning AL, Longworth MS, Dyson NJ, (2010) Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev 24: 1364-1376.
13. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J, (2006) Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 16: 333-344.
14. Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, et al. (2003) Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115: 109-121.
15. Steffensen S, Coelho PA, Cobbe N, Vass S, Costa M, et al. (2001) A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr Biol 11: 295-307.
16. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM, (2004) Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 117: 6435-6445.
17. Bazett-Jones DP, Kimura K, Hirano T, (2002) Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 9: 1183-1190.
18. Strick TR, Kawaguchi T, Hirano T, (2004) Real-time detection of single-molecule DNA compaction by condensin I. Curr Biol 14: 874-880.
19. Ono T, Fang Y, Spector DL, Hirano T, (2004) Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 15: 3296-3308.
20. Kimura K, Cuvier O, Hirano T, (2001) Chromosome condensation by a human condensin complex in Xenopus egg extracts. J Biol Chem 276: 5417-5420.
21. Gosling KM, Makaroff LE, Theodoratos A, Kim YH, Whittle B, et al. (2007) A mutation in a chromosome condensin II subunit, kleisin beta, specifically disrupts T cell development. Proc Natl Acad Sci U S A 104: 12445-12450.
22. Xu Y, Leung CG, Lee DC, Kennedy BK, Crispino JD, (2006) MTB, the murine homolog of condensin II subunit CAP-G2, represses transcription and promotes erythroid cell differentiation. Leukemia 20: 1261-1269.
23. Cobbe N, Savvidou E, Heck MM, (2006) Diverse mitotic and interphase functions of condensins in Drosophila. Genetics 172: 991-1008.
24. Dej KJ, Ahn C, Orr-Weaver TL, (2004) Mutations in the Drosophila condensin subunit dCAP-G: defining the role of condensin for chromosome condensation in mitosis and gene expression in interphase. Genetics 168: 895-906.
25. Lemaitre B, Hoffmann J, (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
26. Dimova DK, Stevaux O, Frolov MV, Dyson NJ, (2003) Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 17: 2308-2320.
27. Kwon SY, Xiao H, Glover BP, Tjian R, Wu C, et al. (2008) The nucleosome remodeling factor (NURF) regulates genes involved in Drosophila innate immunity. Dev Biol 316: 538-547.
28. Meister M, (2004) Blood cells of Drosophila: cell lineages and role in host defence. Curr Opin Immunol 16: 10-15.
29. Kurucz E, Markus R, Zsamboki J, Folkl-Medzihradszky K, Darula Z, et al. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr Biol 17: 649-654.
30. Lebestky T, Chang T, Hartenstein V, Banerjee U, (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288: 146-149.
31. Alfonso TB, Jones BW, (2002) gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev Biol 248: 369-383.
32. Lanot R, Zachary D, Holder F, Meister M, (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230: 243-257.
33. Elrod-Erickson M, Mishra S, Schneider D, (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10: 781-784.
34. Nappi AJ, Ottaviani E, (2000) Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22: 469-480.
35. Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, et al. (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7: 335-350.
36. Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, et al. (2005) Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6: R94.
37. Uvell H, Engstrom Y, (2007) A multilayered defense against infection: combinatorial control of insect immune genes. Trends Genet 23: 342-349.
38. Brennan CA, Anderson KV, (2004) Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 22: 457-483.
39. Imler JL, Bulet P, (2005) Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy 86: 1-21.
40. DiAngelo JR, Birnbaum MJ, (2009) Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol Cell Biol 29: 6341-6352.
41. Aggarwal K, Silverman N, (2008) Positive and negative regulation of the Drosophila immune response. BMB Rep 41: 267-277.
42. Ferrandon D, Imler JL, Hetru C, Hoffmann JA, (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7: 862-874.
43. Senger K, Harris K, Levine M, (2006) GATA factors participate in tissue-specific immune responses in Drosophila larvae. Proc Natl Acad Sci U S A 103: 15957-15962.
44. Tanji T, Yun EY, Ip YT, (2010) Heterodimers of NF-kappaB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila. Proc Natl Acad Sci U S A 107: 14715-14720.
45. Meister M, Braun A, Kappler C, Reichhart JM, Hoffmann JA, (1994) Insect immunity. A transgenic analysis in Drosophila defines several functional domains in the diptericin promoter. Embo J 13: 5958-5966.
46. Georgel P, Meister M, Kappler C, Lemaitre B, Reichhart JM, et al. (1993) Insect immunity: the diptericin promoter contains multiple functional regulatory sequences homologous to mammalian acute-phase response elements. Biochem Biophys Res Commun 197: 508-517.
47. Kappler C, Meister M, Lagueux M, Gateff E, Hoffmann JA, et al. (1993) Insect immunity. Two 17 bp repeats nesting a kappa B-related sequence confer inducibility to the diptericin gene and bind a polypeptide in bacteria-challenged Drosophila. Embo J 12: 1561-1568.
48. Valanne S, Myllymaki H, Kallio J, Schmid MR, Kleino A, et al. (2010) Genome-wide RNA interference in Drosophila cells identifies G protein-coupled receptor kinase 2 as a conserved regulator of NF-kappaB signaling. J Immunol 184: 6188-6198.
49. Meng X, Khanuja BS, Ip YT, (1999) Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev 13: 792-797.
50. Kaneko T, Silverman N, (2005) Bacterial recognition and signalling by the Drosophila IMD pathway. Cell Microbiol 7: 461-469.
51. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, et al. (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123: 335-346.
52. Ayres JS, Freitag N, Schneider DS, (2008) Identification of Drosophila mutants altering defense of and endurance to Listeria monocytogenes infection. Genetics 178: 1807-1815.
53. Ayres JS, Schneider DS, (2008) A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol 6: e305 doi:10.1371/journal.pbio.0060305.
54. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS, (2006) Akt and FOXO dysregulation contribute to infection-induced wasting in Drosophila. Curr Biol 16: 1977-1985.
55. Schneider DS, Ayres JS, (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889-895.
56. Korenjak M, Taylor-Harding B, Binne UK, Satterlee JS, Stevaux O, et al. (2004) Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119: 181-193.
57. Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, et al. (2004) Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18: 2929-2940.
58. Diamond G, Beckloff N, Weinberg A, Kisich KO, (2009) The roles of antimicrobial peptides in innate host defense. Curr Pharm Des 15: 2377-2392.
59. Kimura K, Hirano T, (2000) Dual roles of the 11S regulatory subcomplex in condensin functions. Proc Natl Acad Sci U S A 97: 11972-11977.
60. Hartl TA, Smith HF, Bosco G, (2008) Chromosome alignment and transvection are antagonized by condensin II. Science 322: 1384-1387.
61. Petersen UM, Kadalayil L, Rehorn KP, Hoshizaki DK, Reuter R, et al. (1999) Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif. Embo J 18: 4013-4022.
62. Hirano T, (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311-322.
63. Nasmyth K, Haering CH, (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595-648.
64. Hirano T, (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360: 507-514.
65. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, et al. (2009) Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 5: e1000739 doi:10.1371/journal.pgen.1000739.
66. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
67. Ferrandon D, Jung AC, Criqui M, Lemaitre B, Uttenweiler-Joseph S, et al. (1998) A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. Embo J 17: 1217-1227.
68. Ryu JH, Nam KB, Oh CT, Nam HJ, Kim SH, et al. (2004) The homeobox gene Caudal regulates constitutive local expression of antimicrobial peptide genes in Drosophila epithelia. Mol Cell Biol 24: 172-185.
69. Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart JM, et al. (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13: 737-748.
70. Kim M, Lee JH, Lee SY, Kim E, Chung J, (2006) Caspar, a suppressor of antibacterial immunity in Drosophila. Proc Natl Acad Sci U S A 103: 16358-16363.
71. Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, et al. (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319: 777-782.
72. Gobert V, Gottar M, Matskevich AA, Rutschmann S, Royet J, et al. (2003) Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302: 2126-2130.
73. Pili-Floury S, Leulier F, Takahashi K, Saigo K, Samain E, et al. (2004) In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against Gram-positive bacterial infection in Drosophila adults. J Biol Chem 279: 12848-12853.
74. Bergman P, Johansson L, Asp V, Plant L, Gudmundsson GH, et al. (2005) Neisseria gonorrhoeae downregulates expression of the human antimicrobial peptide LL-37. Cell Microbiol 7: 1009-1017.
75. Chakraborty K, Ghosh S, Koley H, Mukhopadhyay AK, Ramamurthy T, et al. (2008) Bacterial exotoxins downregulate cathelicidin (hCAP-18/LL-37) and human beta-defensin 1 (HBD-1) expression in the intestinal epithelial cells. Cell Microbiol 10: 2520-2537.
76. Sperandio B, Regnault B, Guo J, Zhang Z, Stanley SL Jr, et al. (2008) Virulent Shigella flexneri subverts the host innate immune response through manipulation of antimicrobial peptide gene expression. J Exp Med 205: 1121-1132.
77. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, et al. (2005) Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci U S A 102: 18129-18134.
78. Markey MP, Bergseid J, Bosco EE, Stengel K, Xu H, et al. (2007) Loss of the retinoblastoma tumor suppressor: differential action on transcriptional programs related to cell cycle control and immune function. Oncogene 26: 6307-6318.
79. Zurawski DV, Mumy KL, Faherty CS, McCormick BA, Maurelli AT, (2009) Shigella flexneri type III secretion system effectors OspB and OspF target the nucleus to downregulate the host inflammatory response via interactions with retinoblastoma protein. Mol Microbiol 71: 350-368.
80. Tsichritzis T, Gaentzsch PC, Kosmidis S, Brown AE, Skoulakis EM, et al. (2007) A Drosophila ortholog of the human cylindromatosis tumor suppressor gene regulates triglyceride content and antibacterial defense. Development 134: 2605-2614.
81. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
82. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
83. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series 57: 289-300.
84. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37: D555-559.
85. Romeo Y, Lemaitre B, (2008) Drosophila immunity: methods for monitoring the activity of Toll and Imd signaling pathways. Methods Mol Biol 415: 379-394.