Helicase SUV3, polynucleotide phosphorylase, and mitochondrial polyadenylation polymerase form a transient complex to modulate mitochondrial mRNA polyadenylated tail lengths in response to energetic changes

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 16727-16735

  Wang, Dennis Ding Hwa ^a,c   Guo, Xuning Emily ^a   Modrek, Aram Sandaldjian ^a,d   Chen, Chi Fen ^a   Chen, Phang Lang ^a   Lee, Wen Hwa ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DIMERS; EXPERIMENTS; MAMMALS; PURIFICATION; RNA;

C-TERMINAL REGIONS; ELECTRON TRANSPORT CHAIN; INORGANIC PHOSPHATES; MITOCHONDRIAL MATRIX; POLYNUCLEOTIDE PHOSPHORYLASE; RNA BINDING DOMAINS; SELECTIVE INHIBITION; TRANSIENT COMPLEXES;

BINDING ENERGY;

HELICASE; MESSENGER RNA; MITOCHONDRIAL POLYADENYLATION POLYMERASE; PHOSPHATE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN SUV3; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; GENETIC PARAMETERS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MRNA POLYADENYLATED TAIL LENGTH; MOLECULAR WEIGHT; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RESPIRATORY CHAIN;

BIOENERGETICS; MITOCHONDRIA; MITOCHONDRIAL MRNA POLY(A) TAILS; MTPAP; PNPASE; POLYADENYLATION; RNA HELICASE; RNA PROCESSING; SUV3;

BINDING SITES; DEAD-BOX RNA HELICASES; DNA-DIRECTED RNA POLYMERASES; ENERGY METABOLISM; EXORIBONUCLEASES; HEK293 CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PHOSPHATES; POLYADENYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RNA, MESSENGER;

EID: 84902436539     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.536540     Document Type: Article

References (52)

1. Carpousis, A. J., Leroy, A., Vanzo, N., and Khemici, V. (2001) Escherichia coli RNA degradosome. Methods Enzymol. 342, 333-345 (Pubitemid 32911954)
2. Coburn, G. A., Miao, X., Briant, D. J., and Mackie, G. A. (1999) Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase. Genes Dev. 13, 2594-2603 (Pubitemid 29489650)
3. Hajnsdorf, E., Steier, O., Coscoy, L., Teysset, L., and Régnier, P. (1994) Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcripts of Escherichia coli: stabilizing function of RNase II and evidence for efficient degradation in an ams pnp rnb mutant. EMBO J. 13, 3368-3377
4. Yehudai-Resheff, S., Hirsh, M., and Schuster, G. (2001) Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 21, 5408-5416 (Pubitemid 32702445)
5. Dreyfus, M., and Régnier, P. (2002) The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell 111, 611-613 (Pubitemid 35441243)
6. Manley, J. L., and Proudfoot, N. J. (1994) RNA 3′ ends: formation and function, meeting review. Genes Dev. 8, 259-264 (Pubitemid 24065968)
7. Colgan, D. F., and Manley, J. L. (1997) Mechanism and regulation of mRNA polyadenylation. Genes Dev. 11, 2755-2766 (Pubitemid 27481677)
8. Ojala, D., Montoya, J., and Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470-474 (Pubitemid 11159076)
9. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J., Staden, R., and Young, I. G. (1981) Sequence and organization of the human mitochondrial genome. Nature 290, 457-465 (Pubitemid 11159074)
10. Yokobori, S., and Pääbo, S. (1997) Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNA(Tyr). J. Mol. Biol. 265, 95-99 (Pubitemid 27110647)
11. Tomita, K., Ueda, T., and Watanabe, K. (1996) RNA editing in the acceptor stem of squid mitochondrial tRNA(Tyr). Nucleic Acids Res. 24, 4987-4991
12. Jacob, S. T., and Schindler, D. G. (1972) Polyriboadenylate polymerase solubilized from rat liver mitochondria. Biochem. Biophys. Res. Commun. 48, 126-134
13. Chujo, T., Ohira, T., Sakaguchi, Y., Goshima, N., Nomura, N., Nagao, A., and Suzuki, T. (2012) LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res. 40, 8033-8047
14. Nagaike, T., Suzuki, T., Katoh, T., and Ueda, T. (2005) Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochon-dria- specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 280, 19721-19727 (Pubitemid 41379497)
15. Tomecki, R., Dmochowska, A., Gewartowski, K., Dziembowski, A., and Stepien, P. P. (2004) Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res. 32, 6001-6014 (Pubitemid 40073995)
16. Bai, Y., Srivastava, S. K., Chang, J. H., Manley, J. L., and Tong, L. (2011) Structural basis for dimerization and activity of human PAPD1, a noncanonical poly(A) polymerase. Mol Cell 41, 311-320
17. Nagao, A., Hino-Shigi, N., and Suzuki, T. (2008) Measuring mRNA decay in human mitochondria. Methods Enzymol. 447, 489-499
18. Borowski, L. S., Szczesny, R. J., Brzezniak, L. K., and Stepien, P. P. (2010) RNA turnover in human mitochondria: more questions than answers? Biochim. Biophys. Acta 1797, 1066-1070
19. Xu, F., and Cohen, S. N. (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374, 180-183
20. Carpousis, A. J., Van Houwe, G., Ehretsmann, C., and Krisch, H. M. (1994) Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76, 889-900 (Pubitemid 24085326)
21. Carpousis, A. J. (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61, 71-87
22. Portnoy, V., Palnizky, G., Yehudai-Resheff, S., Glaser, F., and Schuster, G. (2008) Analysis of the human polynucleotide phosphorylase (PNPase) reveals differences in RNA binding and response to phosphate compared to its bacterial and chloroplast counterparts. RNA 14, 297-309 (Pubitemid 351171590)
23. Mohanty, B. K., and Kushner, S. R. (2000) Polynucleotide phosphorylase functions both as a 3′ → 5′ exonuclease and a poly(A) polymerase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 97, 11966-11971
24. Wang, G., Chen, H. W., Oktay, Y., Zhang, J., Allen, E. L., Smith, G. M., Fan, K. C., Hong, J. S., French, S. W., McCaffery, J. M., Lightowlers, R. N., Morse, H. C., 3rd, Koehler, C. M., and Teitell, M. A. (2010) PNPase regulates RNA import into mitochondria. Cell 142, 456-467
25. Chen, H. W., Rainey, R. N., Balatoni, C. E., Dawson, D. W., Troke, J. J., Wasiak, S., Hong, J. S., McBride, H. M., Koehler, C. M., Teitell, M. A., and French, S. W. (2006) Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol. Cell. Biol. 26, 8475-8487 (Pubitemid 44748580)
26. Sarkar, D., and Fisher, P. B. (2006) Human polynucleotide phosphorylase (hPNPase old-35): an RNA degradation enzyme with pleiotrophic biological effects. Cell Cycle 5, 1080-1084 (Pubitemid 43765303)
27. Das, S. K., Bhutia, S. K., Sokhi, U. K., Dash, R., Azab, B., Sarkar, D., and Fisher, P. B. (2011) Human polynucleotide phosphorylase (hPNPase(old- 35)): an evolutionary conserved gene with an expanding repertoire ofRNA degradation functions. Oncogene 30, 1733-1743
28. Shu, Z., Vijayakumar, S., Chen, C. F., Chen, P. L., and Lee, W. H. (2004) Purified human SUV3p exhibits multiple-substrate unwinding activity upon conformational change. Biochemistry 43, 4781-4790 (Pubitemid 38509099)
29. Wang, D. D., Shu, Z., Lieser, S. A., Chen, P. L., and Lee, W. H. (2009) Human mitochondrial SUV3 and polynucleotide phosphorylase form a 330-kDa heteropentamer to cooperatively degrade double-stranded RNA with a 3′-to-5′ directionality. J. Biol. Chem. 284, 20812-20821
30. Khidr, L., Wu, G., Davila, A., Procaccio, V., Wallace, D., and Lee, W. H. (2008) Role of SUV3 helicase in maintaining mitochondrial homeostasis in human cells. J. Biol. Chem. 283, 27064-27073
31. Guo, X. E., Chen, C. F., Wang, D. D., Modrek, A. S., Phan, V. H., Lee, W. H., and Chen, P. L. (2011) Uncoupling the roles of the SUV3 helicase in maintenance of mitochondrial genome stability and RNA degradation. J. Biol. Chem. 286, 38783-38794
32. Margossian, S. P., Li, H., Zassenhaus, H. P., and Butow, R. A. (1996) The DExH box protein Suv3p is a component of a yeast mitochondrial 3′-to-5′ exoribonuclease that suppresses group I intron toxicity. Cell 84, 199-209
33. Smith, A. L., Friedman, D. B., Yu, H., Carnahan, R. H., and Reynolds, A. B. (2011) ReCLIP (reversible cross-link immunoprecipitation): an efficient method for interrogation of labile protein complexes. PLoS One 6, e16206
34. Slomovic, S., Laufer, D., Geiger, D., and Schuster, G. (2005) Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell. Biol. 25, 6427-6435 (Pubitemid 41023219)
35. Palmieri, F. (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch. 447, 689-709
36. Thiaudiere, E., Gallis, J. L., Dufour, S., Rousse, N., and Canioni, P. (1993) Compartmentation of inorganic phosphate in perfused rat liver. Can cytosol be distinguished from mitochondria by 31P NMR? FEBS Lett. 330, 231-235 (Pubitemid 23265138)
37. Vidal, G., Gallis, J. L., Dufour, S., and Canioni, P. (1997) NMR studies of inorganic phosphate compartmentation in the isolated rat liver during acidic perfusion. Arch. Biochem. Biophys. 337, 317-325 (Pubitemid 27198197)
38. Chen, H. W., Koehler, C. M., and Teitell, M. A. (2007) Human polynucleotide phosphorylase: location matters. Trends Cell Biol. 17, 600-608 (Pubitemid 350138435)
39. Jedrzejczak, R., Wang, J., Dauter, M., Szczesny, R. J., Stepien, P. P., and Dauter, Z. (2011) Human Suv3 protein reveals unique features among SF2 helicases. Acta Crystallogr. D Biol. Crystallogr. 67, 988-996
40. Temperley, R. J., Wydro, M., Lightowlers, R. N., and Chrzanowska- Lightowlers, Z. M. (2010) Human mitochondrial mRNAs-like members of all families, similar but different. Biochim. Biophys. Acta 1797, 1081-1085
41. Borowski, L. S., Dziembowski, A., Hejnowicz, M. S., Stepien, P. P., and Szczesny, R. J. (2013) Human mitochondrial RNA decay mediated by PNPase-hSuv3 complex takes place in distinct foci. Nucleic Acids Res. 41, 1223-1240
42. Bogenhagen, D. F., Rousseau, D., and Burke, S. (2008) The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 283, 3665-3675
43. Rhee, H. W., Zou, P., Udeshi, N. D., Martell, J. D., Mootha, V. K., Carr, S. A., and Ting, A. Y. (2013) Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339, 1328-1331
44. Poulsen, J. B., Andersen, K. R., Kjær, K. H., Durand, F., Faou, P., Vestergaard, A. L., Talbo, G. H., Hoogenraad, N., Brodersen, D. E., Justesen, J., and Martensen, P. M. (2011) Human 2′-phosphodiesterase localizes to the mitochondrial matrix with a putative function in mitochondrial RNA turnover. Nucleic Acids Res. 39, 3754-3770
45. Rorbach, J., Nicholls, T. J., and Minczuk, M. (2011) PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Nucleic Acids Res. 39, 7750-7763
46. Cao, G. J., and Sarkar, N. (1992) Identification of the gene for an Escherichia coli poly(A) polymerase. Proc. Natl. Acad. Sci. U.S.A. 89, 10380 -10384
47. Lin-Chao, S., Chiou, N. T., and Schuster, G. (2007) The PNPase, exosome and RNA helicases as the building components of evolutionarily-conserved RNA degradation machines. J. Biomed. Sci. 14, 523-532 (Pubitemid 47063488)
48. Bollenbach, T. J., Schuster, G., and Stern, D. B. (2004) Cooperation of endo- and exoribonucleases in chloroplast mRNA turnover. Prog. Nucleic Acid Res. Mol. Biol. 78, 305-337 (Pubitemid 39752483)
49. Slomovic, S., and Schuster, G. (2008) Stable PNPase RNAi silencing: its effect on the processing and adenylation of human mitochondrial RNA. RNA 14, 310-323 (Pubitemid 351171591)
50. Crosby, A. H., Patel, H., Chioza, B. A., Proukakis, C., Gurtz, K., Patton, M. A., Sharifi, R., Harlalka, G., Simpson, M. A., Dick, K., Reed, J. A., Al- Memar, A., Chrzanowska-Lightowlers, Z. M., Cross, H. E., and Lightowlers, R. N. (2010) Defective mitochondrial mRNA maturation is associated with spastic ataxia. Am. J. Hum. Genet. 87, 655-660
51. Temperley, R. J., Seneca, S. H., Tonska, K., Bartnik, E., Bindoff, L. A., Lightowlers, R. N., and Chrzanowska-Lightowlers, Z. M. (2003) Investigation of a pathogenic mtDNA microdeletion reveals a translation-dependent deadenylation decay pathway in human mitochondria. Hum. Mol. Genet. 12, 2341-2348 (Pubitemid 37160878)
52. Wydro, M., Bobrowicz, A., Temperley, R. J., Lightowlers, R. N., and Chrzanowska- Lightowlers, Z. M. (2010) Targeting of the cytosolic poly(A) binding protein PABPC1 to mitochondria causes mitochondrial translation inhibition. Nucleic Acids Res. 38, 3732-3742