Missense mutation in the second RNA binding domain reveals a role for prkra (PACT/RAX) during skull development

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Dickerman, Benjamin K ^a,b   White, Christine L ^a   Chevalier, Claire ^c   Nalesso, Valérie ^c   Charles, Cyril ^d   Fouchécourt, Sophie ^e   Guillou, Florian ^e   Viriot, Laurent ^d   Sen, Ganes C ^a,b   Hérault, Yann ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c INSTITUT CLINIQUE DE LA SOURIS   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; MESSENGER RNA; MUTANT PROTEIN; PROTEIN ACTIVATOR OF PROTEIN KINASE R; PROTEIN KINASE R ASSOCIATED PROTEIN X; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; PRKRA PROTEIN, MOUSE; RNA;

ALLELE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; EAR MALFORMATION; FEMALE; FEMALE GENITAL TRACT MALFORMATION; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; GENETIC TRANSCRIPTION; GROWTH DISORDER; HISTOPATHOLOGY; HUMAN CELL; MALE; MICROTIA; MISSENSE MUTATION; MOUSE; MUTAGENESIS; NONHUMAN; OVARY; PHENOTYPE; PRKRA GENE; PROTEIN RNA BINDING; PROTEIN STABILITY; SKULL DEVELOPMENT; STEADY STATE; AMINO ACID SEQUENCE; ANIMAL; BODY WEIGHT; BRAIN; CHEMISTRY; ENZYME ACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RECESSIVE GENE; SKULL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BODY WEIGHT; BRAIN; DNA MUTATIONAL ANALYSIS; ENZYME ACTIVATION; GENES, RECESSIVE; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RNA; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA-BINDING PROTEINS; SKULL; STRESS, PHYSIOLOGICAL;

EID: 83355168951     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028537     Document Type: Article

References (40)

1. Patel RC, Sen GC, (1998) PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J 17: 4379-4390.
2. Ito T, Yang M, May WS, (1999) RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J Biol Chem 274: 15427-15432.
3. Ruvolo PP, Gao F, Blalock WL, Deng X, May WS, (2001) Ceramide regulates protein synthesis by a novel mechanism involving the cellular PKR activator RAX. J Biol Chem 276: 11754-11758.
4. Patel CV, Handy I, Goldsmith T, Patel RC, (2000) PACT, a stress-modulated cellular activator of interferon-induced double-stranded RNA-activated protein kinase, PKR. J Biol Chem 275: 37993-37998.
5. Gilbert SJ, Duance VC, Mason DJ, (2002) Tumour necrosis factor alpha up-regulates protein kinase R (PKR)-activating protein (PACT) and increases phosphorylation of PKR and eukaryotic initiation factor 2-alpha in articular chondrocytes. Biochem Soc Trans 30: 886-889.
6. Chen G, Ma C, Bower KA, Ke Z, Luo J, (2006) Interaction between RAX and PKR modulates the effect of ethanol on protein synthesis and survival of neurons. J Biol Chem 281: 15909-15915.
7. Peters GA, Hartmann R, Qin J, Sen GC, (2001) Modular structure of PACT: distinct domains for binding and activating PKR. Mol Cell Biol 21: 1908-1920.
8. Bennett RL, Blalock WL, Abtahi DM, Pan Y, Moyer SA, et al. (2006) RAX, the PKR activator, sensitizes cells to inflammatory cytokines, serum withdrawal, chemotherapy, and viral infection. Blood 108: 821-829.
9. Lee ES, Yoon CH, Kim YS, Bae YS, (2007) The double-strand RNA-dependent protein kinase PKR plays a significant role in a sustained ER stress-induced apoptosis. FEBS Lett 581: 4325-4332.
10. Singh M, Fowlkes V, Handy I, Patel CV, Patel RC, (2009) Essential role of PACT-mediated PKR activation in tunicamycin-induced apoptosis. J Mol Biol 385: 457-468.
11. Chong KL, Feng L, Schappert K, Meurs E, Donahue TF, et al. (1992) Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. Embo J 11: 1553-1562.
12. Hershey JW, (1989) Protein phosphorylation controls translation rates. J Biol Chem 264: 20823-20826.
13. Kozak CA, Gatignol A, Graham K, Jeang KT, McBride OW, (1995) Genetic mapping in human and mouse of the locus encoding TRBP, a protein that binds the TAR region of the human immunodeficiency virus (HIV-1). Genomics 25: 66-72.
14. Park H, Davies MV, Langland JO, Chang HW, Nam YS, et al. (1994) TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc Natl Acad Sci U S A 91: 4713-4717.
15. Lee K, Fajardo MA, Braun RE, (1996) A testis cytoplasmic RNA-binding protein that has the properties of a translational repressor. Mol Cell Biol 16: 3023-3034.
16. Gupta V, Huang X, Patel RC, (2003) The carboxy-terminal, M3 motifs of PACT and TRBP have opposite effects on PKR activity. Virology 315: 283-291.
17. Laraki G, Clerzius G, Daher A, Melendez-Pena C, Daniels S, et al. (2008) Interactions between the double-stranded RNA-binding proteins TRBP and PACT define the Medipal domain that mediates protein-protein interactions. RNA Biol 5: 92-103.
18. Peters GA, Li S, Sen GC, (2006) Phosphorylation of specific serine residues in the PKR activation domain of PACT is essential for its ability to mediate apoptosis. J Biol Chem 281: 35129-35136.
19. Bennett RL, Blalock WL, May WS, (2004) Serine 18 phosphorylation of RAX, the PKR activator, is required for PKR activation and consequent translation inhibition. J Biol Chem 279: 42687-42693.
20. Daher A, Laraki G, Singh M, Melendez-Pena CE, Bannwarth S, et al. (2009) TRBP control of PACT-induced phosphorylation of protein kinase R is reversed by stress. Mol Cell Biol 29: 254-265.
21. Singh M, Castillo D, Patel CV, Patel RC, (2011) Stress-induced phosphorylation of PACT reduces its interaction with TRBP and leads to PKR activation. Biochemistry 50: 4550-4560.
22. Li S, Peters GA, Ding K, Zhang X, Qin J, et al. (2006) Molecular basis for PKR activation by PACT or dsRNA. Proc Natl Acad Sci U S A 103: 10005-10010.
23. Huang X, Hutchins B, Patel RC, (2002) The C-terminal, third conserved motif of the protein activator PACT plays an essential role in the activation of double-stranded-RNA-dependent protein kinase (PKR). Biochem J 366: 175-186.
24. Yang YL, Reis LF, Pavlovic J, Aguzzi A, Schafer R, et al. (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J 14: 6095-6106.
25. Rowe TM, Rizzi M, Hirose K, Peters GA, Sen GC, (2006) A role of the double-stranded RNA-binding protein PACT in mouse ear development and hearing. Proc Natl Acad Sci U S A 103: 5823-5828.
26. Peters GA, Seachrist DD, Keri RA, Sen GC, (2009) The double-stranded RNA-binding protein, PACT, is required for postnatal anterior pituitary proliferation. Proc Natl Acad Sci U S A 106: 10696-10701.
27. Lee Y, Hur I, Park SY, Kim YK, Suh MR, et al. (2006) The role of PACT in the RNA silencing pathway. EMBO J 25: 522-532.
28. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, et al. (2003) Dicer is essential for mouse development. Nat Genet 35: 215-217.
29. Otsuka M, Zheng M, Hayashi M, Lee JD, Yoshino O, et al. (2008) Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J Clin Invest 118: 1944-1954.
30. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, et al. (2009) Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326: 250-259.
31. Camargos S, Scholz S, Simon-Sanchez J, Paisan-Ruiz C, Lewis P, et al. (2008) DYT16, a novel young-onset dystonia-parkinsonism disorder: identification of a segregating mutation in the stress-response protein PRKRA. Lancet Neurol 7: 207-215.
32. Seibler P, Djarmati A, Langpap B, Hagenah J, Schmidt A, et al. (2008) A heterozygous frameshift mutation in PRKRA (DYT16) associated with generalised dystonia in a German patient. Lancet Neurol 7: 380-381.
33. Hrabe de Angelis MH, Flaswinkel H, Fuchs H, Rathkolb B, Soewarto D, et al. (2000) Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat Genet 25: 444-447.
34. Besson V, Nalesso V, Herpin A, Bizot JC, Messaddeq N, et al. (2005) Training and aging modulate the loss-of-balance phenotype observed in a new ENU-induced allele of Otopetrin1. Biol Cell 97: 787-798.
35. Magnol L, Chevallier MC, Nalesso V, Retif S, Fuchs H, et al. (2007) KIT is required for hepatic function during mouse post-natal development. BMC Dev Biol 7: 81.
36. Bennett RL, Blalock WL, Choi EJ, Lee YJ, Zhang Y, et al. (2008) RAX is required for fly neuronal development and mouse embryogenesis. Mech Dev 125: 777-785.
37. Kok KH, Ng MH, Ching YP, Jin DY, (2007) Human TRBP and PACT directly interact with each other and associate with dicer to facilitate the production of small interfering RNA. J Biol Chem 282: 17649-17657.
38. Zehir A, Hua LL, Maska EL, Morikawa Y, Cserjesi P, (2010) Dicer is required for survival of differentiating neural crest cells. Dev Biol 340: 459-467.
39. Hallgrimsson B, Dorval CJ, Zelditch ML, German RZ, (2004) Craniofacial variability and morphological integration in mice susceptible to cleft lip and palate. J Anat 205: 501-517.
40. Peters GA, Khoo D, Mohr I, Sen GC, (2002) Inhibition of PACT-mediated activation of PKR by the herpes simplex virus type 1 Us11 protein. J Virol 76: 11054-11064.