The dengue vector aedes aegypti contains a functional high mobility group box 1 (HMGB1) protein with a unique regulatory C-terminus

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Ribeiro, Fabio Schneider ^a   de Abreu da Silva, Isabel Caetano ^a   Carneiro, Vitor Coutinho ^a   Belgrano, Fabrício dos Santos ^a   Mohana Borges, Ronaldo ^a   de Andrade Rosa, Ivone ^a,b   Benchimol, Marlene ^b   Souza, Nathalia Rocha Quintino ^a   Mesquita, Rafael Dias ^a   Sorgine, Marcos Henrique Ferreira ^a   Gazos Lopes, Felipe ^a,d   Vicentino, Amanda Roberta Revoredo ^a   Wu, Wenjie ^c   de Moraes Maciel, Renata ^a   da Silva Neto, Mario Alberto Cardoso ^a   Fantappié, Marcelo Rosado ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSIDADE SANTA ÚRSULA   (Brazil)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; DNA; HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN KINASE C;

AEDES AEGYPTI; ALPHA HELIX; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CIRCULAR DICHROISM; CONTROLLED STUDY; DISEASE CARRIER; DNA SUPERCOILING; EMBRYO; FEMALE; MALE; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AEDES; AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEUS; CLONING, MOLECULAR; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; HMGB1 PROTEIN; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASE C;

AEDES AEGYPTI; DIPTERA; EUKARYOTA; YELLOW FEVER VIRUS GROUP;

EID: 84863621365     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040192     Document Type: Article

References (55)

1. Celona B, Weiner A, Di Felice F, Mancuso FM, Cesarini E, et al. (2011) Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol 9: e1001086.
2. Li B, Carey M, Workman JL, (2007) The role of chromatin during transcription. Cell 128: 707-719.
3. Groth A, Rocha W, Verreault A, Almouzni G, (2007) Chromatin challenges during DNA replication and repair. Cell 128: 721-733.
4. Thomas JO, Travers AA, (2001) HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem Sci 26: 167-174.
5. Stros M, (2010) HMGB proteins: interactions with DNA and chromatin. Biochim Biophys Acta 1799: 101-113.
6. Bianchi ME, Agresti A, (2005) HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 15: 496-506.
7. Boonyaratanakornkit V, Melvin V, Prendergast P, Altmann M, Ronfani L, et al. (1998) High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol Cell Biol 18: 4471-4487.
8. Roemer SC, Adelman J, Churchill ME, Edwards DP, (2008) Mechanism of high-mobility group protein B enhancement of progesterone receptor sequence-specific DNA binding. Nucleic Acids Res 36: 3655-3666.
9. Martin D, Daulny A, Decoville M, Locker D, (2003) Mutagenesis analysis of the interaction between the dorsal rel homology domain and HMG boxes of DSP1 protein. J Biochem 134: 583-589.
10. Stros M, Muselikova-Polanska E, Pospisilova S, Strauss F, (2004) High-affinity binding of tumor-suppressor protein p53 and HMGB1 to hemicatenated DNA loops. Biochemistry 43: 7215-7225.
11. Lotze MT, Tracey KJ, (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5: 331-342.
12. Bianchi ME, Manfredi AA, (2007) High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 220: 35-46.
13. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, et al. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22: 5551-5560.
14. Youn JH, Shin JS, (2006) Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol 177: 7889-7897.
15. Wisniewski JR, Schulze E, (1994) High affinity interaction of dipteran high mobility group (HMG) proteins 1 with DNA is modulated by COOH-terminal regions flanking the HMG box domain. J Biol Chem 269: 10713-10719.
16. Stott K, Watson M, Howe FS, Grossmann JG, Thomas JO, (2010) Tail-mediated collapse of HMGB1 is dynamic and occurs via differential binding of the acidic tail to the A and B domains. J Mol Biol 403: 706-722.
17. Pasheva E, Sarov M, Bidjekov K, Ugrinova I, Sarg B, et al. (2004) In vitro acetylation of HMGB-1 and-2 proteins by CBP: the role of the acidic tail. Biochemistry 43: 2935-2940.
18. Briquet S, Boschet C, Gissot M, Tissandie E, Sevilla E, et al. (2006) High-mobility-group box nuclear factors of Plasmodium falciparum. Eukaryot Cell 5: 672-682.
19. Abhyankar MM, Hochreiter AE, Hershey J, Evans C, Zhang Y, et al. (2008) Characterization of an Entamoeba histolytica high-mobility-group box protein induced during intestinal infection. Eukaryot Cell 7: 1565-1572.
20. Kiilerich B, Stemmer C, Merkle T, Launholt D, Gorr G, et al. (2008) Chromosomal high mobility group (HMG) proteins of the HMGB-type occurring in the moss Physcomitrella patens. Gene 407: 86-97.
21. de Oliveira FM, de Abreu da Silva IC, Rumjanek FD, Dias-Neto E, Guimaraes PE, et al. (2006) Cloning the genes and DNA binding properties of High Mobility Group B1 (HMGB1) proteins from the human blood flukes Schistosoma mansoni and Schistosoma japonicum. Gene 377: 33-45.
22. Thomsen MS, Franssen L, Launholt D, Fojan P, Grasser KD, (2004) Interactions of the basic N-terminal and the acidic C-terminal domains of the maize chromosomal HMGB1 protein. Biochemistry 43: 8029-8037.
23. Chen YH, Jia XT, Huang XD, Zhang S, Li M, et al. (2011) Two Litopenaeus vannamei HMGB proteins interact with transcription factors LvSTAT and LvDorsal to activate the promoter of white spot syndrome virus immediate-early gene ie1. Mol Immunol 48: 793-799.
24. Aleporou-Marinou V, Marinou H, Patargias T, (2003) A mini review of the high mobility group proteins of insects. Biochem Genet 41: 291-304.
25. Wisniewski JR, Schulze E, (1992) Insect proteins homologous to mammalian high mobility group protein 1. Characterization and DNA-binding properties. J Biol Chem 267: 17170-17177.
26. Wagner CR, Hamana K, Elgin SC, (1992) A high-mobility-group protein and its cDNAs from Drosophila melanogaster. Mol Cell Biol 12: 1915-1923.
27. Lehming N, Thanos D, Brickman JM, Ma J, Maniatis T, et al. (1994) An HMG-like protein that can switch a transcriptional activator to a repressor. Nature 371: 175-179.
28. Mosrin-Huaman C, Canaple L, Locker D, Decoville M, (1998) DSP1 gene of Drosophila melanogaster encodes an HMG-domain protein that plays multiple roles in development. Dev Genet 23: 324-334.
29. Salvaing J, Decoville M, Mouchel-Vielh E, Bussiere M, Daulny A, et al. (2006) Corto and DSP1 interact and bind to a maintenance element of the Scr Hox gene: understanding the role of Enhancers of trithorax and Polycomb. BMC Biol 4: 9.
30. Lamiable O, Rabhi M, Peronnet F, Locker D, Decoville M, (2010) Rm62, a DEAD-box RNA helicase, complexes with DSP1 in Drosophila embryos. Genesis 48: 244-253.
31. Muller S, Scaffidi P, Degryse B, Bonaldi T, Ronfani L, et al. (2001) New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 20: 4337-4340.
32. Stros M, Stokrova J, Thomas JO, (1994) DNA looping by the HMG-box domains of HMG1 and modulation of DNA binding by the acidic C-terminal domain. Nucleic Acids Res 22: 1044-1051.
33. Stros M, (1998) DNA bending by the chromosomal protein HMG1 and its high mobility group box domains. Effect of flanking sequences. J Biol Chem 273: 10355-10361.
34. Ward LD, (1985) Measurement of ligand binding to proteins by fluorescence spectroscopy. Methods Enzymol 117: 400-414.
35. Zhang X, Wheeler D, Tang Y, Guo L, Shapiro RA, et al. (2008) Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages. J Immunol 181: 5015-5023.
36. Oh YJ, Youn JH, Ji Y, Lee SE, Lim KJ, et al. (2009) HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism. J Immunol 182: 5800-5809.
37. de Abreu da Silva IC, Carneiro VC, Maciel Rde M, da Costa RF, Furtado DR, et al. (2011) CK2 phosphorylation of Schistosoma mansoni HMGB1 protein regulates its cellular traffic and secretion but not its DNA transactions. PLoS One 6: e23572.
38. Ner SS, Churchill ME, Searles MA, Travers AA, (1993) dHMG-Z, a second HMG-1-related protein in Drosophila melanogaster. Nucleic Acids Res 21: 4369-4371.
39. Lee KB, Thomas JO, (2000) The effect of the acidic tail on the DNA-binding properties of the HMG1,2 class of proteins: insights from tail switching and tail removal. J Mol Biol 304: 135-149.
40. Payet D, Travers A, (1997) The acidic tail of the high mobility group protein HMG-D modulates the structural selectivity of DNA binding. J Mol Biol 266: 66-75.
41. Wisniewski JR, Schulze E, Sapetto B, (1994) DNA binding and nuclear translocation of insect high-mobility-group- protein-1 (HMG1) proteins are inhibited by phosphorylation. Eur J Biochem 225: 687-693.
42. Paull TT, Haykinson MJ, Johnson RC, (1993) The nonspecific DNA-binding and-bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev 7: 1521-1534.
43. Lehming N, Le Saux A, Schuller J, Ptashne M, (1998) Chromatin components as part of a putative transcriptional repressing complex. Proc Natl Acad Sci U S A 95: 7322-7326.
44. Kirov NC, Lieberman PM, Rushlow C, (1996) The transcriptional corepressor DSP1 inhibits activated transcription by disrupting TFIIA-TBP complex formation. EMBO J 15: 7079-7087.
45. Raikhel AS, Kokoza VA, Zhu J, Martin D, Wang SF, et al. (2002) Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity. Insect Biochem Mol Biol 32: 1275-1286.
46. Hagedorn HH, (1989) Physiological roles of hemolymph Ecdysteroid in the adult insect. Koolman J, editor. New York: Thieme Medical Publishers.
47. Wang SF, Miura K, Miksicek RJ, Segraves WA, Raikhel AS, (1998) DNA binding and transactivation characteristics of the mosquito ecdysone receptor-Ultraspiracle complex. J Biol Chem 273: 27531-27540.
48. Seabra-Junior ES, Souza EM, Mesquita RD, (2011) FAT- Functional Analysis Tool. In: IFRJ, editors. editor. INPI. Brasil.
49. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
50. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
51. Thompson JD, Gibson TJ, Higgins DG, (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2 3.
52. Retief JD, (2000) Phylogenetic analysis using PHYLIP. Methods Mol Biol 132: 243-258.
53. Gentile C, Lima JB, Peixoto AA, (2005) Isolation of a fragment homologous to the rp49 constitutive gene of Drosophila in the Neotropical malaria vector Anopheles aquasalis (Diptera: Culicidae). Mem Inst Oswaldo Cruz 100: 545-547.
54. Pfaffl MW, Lange IG, Daxenberger A, Meyer HH, (2001) Tissue-specific expression pattern of estrogen receptors (ER): quantification of ER alpha and ER beta mRNA with real-time RT-PCR. APMIS 109: 345-355.
55. Stros M, Reich J, (1998) Formation of large nucleoprotein complexes upon binding of the high-mobility-group (HMG) box B-domain of HMG1 protein to supercoiled DNA. Eur J Biochem 251: 427-434.