Woolford Laboratory  

Department of Biological Sciences l Carnegie Mellon University


Biedka S, Micic J, Wilson D, Brown H, Diorio-Toth L, Woolford JL Jr. Hierarchical recruitment of ribosomal proteins and assembly factors remodels nucleolar pre-60S ribosomes. J Cell Biol. 2018 Jul 2;217(7):2503-2518. doi: 10.1083/jcb.201711037.

Biedka S, Wu S, LaPeruta AJ, Gao N, Woolford JL Jr. (2017) Insights into remodeling events during eukaryotic large ribosomal subunit assembly provided by high resolution cryo-EM structures. RNA Biol. 2017 Oct 3;14(10):1306-1313.

Konikkat, S., Biedka, S., Woolford, J.L. Jr.  (2017). The assembly factor Erb1 functions in multiple remodeling events during 60S ribosomal subunit assembly in S. cerevisiae.  Nucleic Acids Research  45: 4853-4865.

Wu S, Tan D, Woolford JL Jr, Dong MQ, Gao N. (2017). Atomic modeling of the ITS2 ribosome assembly subcomplex from Cryo-EM together with mass spectrometry-identified protein-protein crosslinks. Protein Sci. 26:103-112.

Liu,Z., Gutierrez-Varga,C., Wei, J., Grassucci,R.A., Ramesh,M., Espina,N., Sun,M., Tutuncuoglu,B., Madison-Antenucci,S., Woolford, J.L.Jr., Tong, L., and Frank, J. (2016). Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit. Proceedings of the National Academy of Sciences, USA 113:12174-12179.

Ma, C., Wu,S., Li,N., Chen,Y., Yan,K., Li,Z., Zheng,L., Lei,J. Woolford,J.L.Jr. , and Gao,N. (2017) Structural snapshot of cytoplasmic pre-60S ribosomal particles bound with Nmd3, Lsg1, Tif6, and Reh1. Nature Structural and Molecular Biology. 24: 214-220.

Konikkat, S. and Woolford,J.L.Jr. (2017). Principles of 60S Ribosomal Subunit Assembly Emerging from Recent Studies In Yeast. Biochemical Journal. 474: 195-214.

Tutuncuoglu B, Jakovljevic J, Wu S, Gao N, Woolford JL Jr. (2016) The n-terminal extension of yeast ribosomal protein L8 is involved in two major remodeling events during late nuclear stages of 605 ribosomal subunit assembly. RNA. 22: 1386-1399.

Ramesh M, Woolford JL Jr. (2016) Eukaryote-specific rRNA expansion segments function in ribosome biogenesis. RNA. 2016 Jun 17 22: 1153-1162.

Shan Wu, Beril Tutuncuoglu, Kaige Yan, Hailey Brown, Yixiao Zhang, Dan Tan, Michael Gamalinda, Yi Yuan, Zhifei Li, Jelena Jakovljevic, Chengying Ma, Jianlin Lei, Meng-Qiu Dong, John L. Woolford Jr & Ning Gao. (2016) Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature. 534: 133-137.

Kormuth KA, Woolford JL Jr, Armitage BA. (2016) Homologous PNA Hybridization to Noncanonical DNA G-Quadruplexes. Biochemistry. Biochemistry. 2016 Mar 29;55(12):1749-57.

Talkish J, Biedka S, Jakovljevic J, Zhang J, Tang L, Strahler JR, Andrews PC, Maddock JR, Woolford JL Jr. (2016)Disruption of ribosome assembly in yeast blocks cotranscriptional pre-rRNA processing and affects the global hierarchy of ribosome biogenesis. RNA. 2016 Jun;22(6):852-66.

Gamalinda M, Woolford JL Jr. (2015) Paradigms of ribosome synthesis: Lessons learned from ribosomal proteins. Translation. 3:1 e975018-1–e975018-11.

de la Cruz J, Karbstein K, Woolford JL Jr. (2015) Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annual Reviews of Biochemistry. 84: 92-129.

Gamalinda M, Woolford JL Jr. (2014) Deletion of L4 domains reveals insights into the importance of ribosomal protein extensions in eukaryotic ribosome assembly. RNA. 20(11) 1725-31.

Talkish J, May G, Lin Y, Woolford JL Jr, McManus CJ. (2014) Mod-seq: high-throughput sequencing for chemical probing of RNA structure. RNA. 20(5):713-20.

Talkish J, Campbell IW, Sahasranaman A, Jakovljevic J, Woolford JL Jr. (2014) Ribosome assembly factors Pwp1 and Nop12 are important for folding of 5.8S rRNA during ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol. 34(10):1863-77.

Gamalinda M, Ohmayer U, Jakovljevic J, Kumcuoglu B, Woolford J, Mbom B, Lin L, Woolford JL Jr. (2014) A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains. Genes Dev. 28(2):198-210.

Woolford, J.L., Jr. and Baserga, S. (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195: 643-681.

Dembowski, J.A., Ramesh, M., McManus, C. J., and Woolford, J.L. Jr. (2013) Identification of the binding site of Rlp7 on assembling 60S ribosomal subunits in Saccharomyces cerevisiae. RNA 19:1639-1647.

Ohmayer, U., Gamalinda, M., Sauert,M., Ossowski,J., Poll,G., Linnemann,J., Hierlmeier,T., Perez-Fernandez,J., Kumcuoglu,B., Leger-Silvestre, I., Faubladier,M., Griesenbeck,M. Woolford,J.L.Jr., Tschochner,H., and Milkereit,P. (2013) Assembly characteristics of large subunit ribosomal proteins in S. cerevisiae. PLOS One 8:e68412.

Sahasranaman, A., and Woolford, J.L. Jr. (2013) "Ribosome Assembly" in Encyclopedia of Biological Chemistry, 2nd edition (Lennarz, W.J. and Lane, M.D. eds.) Elsevier, Inc

Dembowski, J.A., Kuo,B., and Woolford,J.L. Jr. (2013) Has1 regulates consecutive maturation and processing steps for assembly of 60S ribosomal subunits. Nucleic Acids Research 41:7889-7904.

Curtis,R.E., Kim,S., Woolford,J.L.Jr., Xu,W., and Xing,E.P. (2013) Structured association analysis leads to insight into Saccharomyces cerevisiae gene regulation by finding multiple contributing eQTL hotspots associated with functional gene modules. BMC Genomics 14: 196.

Gamalinda, M., Jakovljevic, J., Talkish, J., Babiano, R., de la Cruz, J., and Woolford, J.L., Jr. (2013) Yeast polypeptide exit tunnel ribosomal proteins L17, L35, and L37 are necessary to recruit late-assembling factors required for 27SB pre-rRNA processing. Nucleic Acids Research 41:1965-1983.

Jakovljevic, J., Ohmayer, U., Gamalinda, M., Talkish, J., Alexander, L., Linneman, J., Milkereit, P., and Woolford, J.L., Jr. (2012) Ribosomal proteins L7 and L8 function in concert with six A3 assembly factors to propagate assembly of domains I and II of 25S rRNA in yeast ribosomal subunits. RNA 10:1805-1822.

Talkish, J., Zhang, J., Jakovljevic, J., Horsey, E.W., and Woolford, J.L. Jr. (2012) Hierarchical recruitment into nascent ribosomes of assembly factors required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Research 40: 8646-8661.

Babiano, R., Gamalinda, M., Woolford, J.L., Jr., and de la Cruz, J. (2012) Saccharomyces cerevisiae ribosomal protein L26 is not essential for ribosome assembly and function. Molecular and Cellular Biology 32:3228-3241.

Shimoji,K.*, Jakovljevic, J.*, Tsuchihashi, K., Umeki, Y., Wan, K., Kawasaki, S., Talkish, J., Woolford, J.L., Jr., and Mizuta, K. (2012) Ebp2 and Brx1 function cooperatively in 60S ribosomal subunit assembly in Saccharomyces cerevisiae. Nucleic Acids Research 40:4574-4588. *equal contributors.

Bartoli K, Jakovljevic J, Woolford Jr JL, Saunders W. (2011) Kinesin molecular motor Eg5 functions during the elongation phase of polypeptide synthesis. Molecular Biology of the Cell 22(18): 34240-30. Epub 2011 Jul 27.

Sahasranaman A, Dembowski J, Strahler J, Andrews P, Maddock J and Woolford Jr JL. (2011) Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. EMBO J 30(19):4020-32.

Sahasranaman A and Woolford Jr JL. (2012) Ribsome Assembly in Encyclopedia of Biological Chemistry (in press).

Poll G, Braun T, Jakovljevic J, Neueder A, Jakob S, Woolford Jr JL, Tschochner H, Milkereit P. (2009) rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLOS One 4: e8249.

Talkish J and Woolford Jr JL. (2009) The Rea1 tadpole loses its tail. Cell 138: 832-834.

Staley J and Woolford Jr JL. (2009) Assembly of ribosomes and spliceosomes:complex ribonucleoprotein machines. Current Opinion in Cell Biology 21:109-118.

Qui H, Eifert J, Wacheul L, Thiry M, Berger A, Jakovljevic J, Woolford Jr JL, Corbett A, Lafontaine DLJ, Terns RM, Terns MP. (2008) Identification of Genes That Function In the Biogenesis and Localization of Small Nucleolar RNAs in Saccharomyces cerevisiae. Molecular and Cellular Biology 28:3686-3699.

Tang L, Sahasranaman A, Jakovljevic J, Schleifman E, Woolford Jr JL. (2008) Interactions among Ytm1, Erb1, and Nop7 Required for Assembly of the Nop7-Subcomplex in Yeast Preribosomes. Molecular Biology of the Cell 19: 2844-2856.

Zhang J, Harnpicharnchai P, Jakovljevic J, Tang L, Guo Y, Oeffinger M, Rout MP, Hiley SL, Hughes T, Woolford Jr JL. (2007) Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes and Development 21: 2580-2592.

Miles,TD, Jakovljevic, J, Horsey, E, Harnpicharnchai, P, Tang, L, and Woolford, JL, Jr. (2005) Ytm1,Nop7,and Erb1 Form a Complex Necessary for Maturation of 66S Preribosomes. Molecular and Cellular Biology 25: 10419-10432.

Jakovljevic J, Antunez de Mayolo P, Miles TD, Nguyen TM-L, Leger-Silvestre, I, Gas N, Woolford, JL Jr. (2004) The carboxyl-terminal extension of yeast ribosomal protein S14 is necessary for maturation of 43S preribosomes. Molecular Cell 14: 331-342.

Horsey EW, Jakovljevic J, Miles TD, Harnpicharnchai P, Woolford JL Jr. (2004) Role of the Yeast Rrp1 Protein in the dynamics of pre-ribosome maturation. RNA 10: 813-827.

Farach-Colton M, Huang Y, Woolford JL Jr. (2004) Discovering temporal relations in molecular pathways using protein-protein interactions. RECOMB Proceedings of International Conference on Computational Molecular Biology.

Antunez de Mayolo P, Woolford JL Jr. (2003) Interactions of yeast ribosomal protein S14 with RNA. Journal of Molecular Biology 333:697-709.

Woolford JL Jr. (2003) Ribosome Assembly. IN Encyclopedia of Biological Chemistry. (Lennarz, W. J. and Lane, M.D. eds.).

Woolford JL Jr. (2003) Chaperoning Ribosome Assembly. Molecular Cell 10: 8-10.

Adams CA, Jakovljevic J, Roman J, Harnpicharnchai P, Woolford JL Jr. (2002) Saccharomyces cerevisiae Nucleolar Protein Nop7p is Necessary for Biogenesis of 60S Ribosomal Subunits. RNA 8: 150-165.

Harnpicharnchai P, Jakovljevic J, Horsey E, Miles T, Roman J, Rout M, Meagher D, Imai B, Guo Y, Brame C, Shabanowitz J, Hunt DF, Woolford JL Jr. (2001) Composition and Functional Characterization of Yeast 66S Ribosome Assembly Intermediates. Molecular Cell 8: 505-515.

Fewell SW, Woolford JL Jr. (1999) Ribosomal Protein S14 of Saccharomyces cerevisiae Regulates Its Expression by Binding to RPS14B pre-mRNA and to 18S rRNA. Molecular and Cellular Biology 19: 826-834.

Sun C, Woolford JL Jr. (1997) The Yeast Nucleolar Protein Nop4p Contains Four RNA Recognition Motifs Necessary for Ribosome Biogenesis. Journal of Biological Chemistry 272: 25345-25352.

Anthony JG, Weidenhammer EM, Woolford JL Jr. (1997) The Yeast Prp3 Protein is a U4/U6 snRNP Protein Necessary for Integrity of the U4/U6 snRNP and the U4/U6. U5 tri-snRNP. RNA 3: 1143-1152.

Weidenhammer EM, Ruiz-Noriega M, Woolford JL Jr. (1997) Prp31p Promotes the Association of the U4/U6. U5 tri-snRNP with Pre-spliceosomes to Form Spliceosomes in Saccharomyces cerevisiae. Molecular and Cellular Biology 17: 3580-3588.

Maddock JR, Roy J, Woolford JL Jr. (1996) Six Novel Genes Necessary for Pre-mRNA Splicing in Saccharomyces cerevisiae. Nucleic Acids Research 24: 1037-1044.

Weidenhammer EM, Singh M, Woolford JL Jr. (1996) The PRP31 Gene Encodes a Novel Protein Required for Pre-mRNA Splicing in Saccharomyces cerevisiae. Nucleic Acids Research 24: 1164-1170.

Li Z, Paulovich AG, Woolford JL Jr. (1995) Feedback Inhibition of the Yeast Ribosomal Protein Gene CRY2 Is Mediated by the Nucleotide Sequence and Secondary Structure of CRY2 Pre-mRNA. Molecular and Cellular Biology 15: 6454-6464.

Roy J, Kim K, Maddock JR, Anthony JG, Woolford JL Jr. (1995) The Final Stages of Spliceosome Maturation Require Spp2p That Interacts With the DEAH Box Protein Prp2p and Promotes Step 1 of Splicing. RNA 1: 375-390.

Roy J, Zheng B, Rymond B, Woolford JL Jr. (1994) Structurally Related but Functionally Distinct Yeast SmD Core Small Nuclear Ribonucleoprotein Particle Proteins. Molecular and Cellular Biology 15: 445-455.

Maddock JR, Weidenhammer E, Adams C, Lunz R, Woolford JL Jr. (1994) Extragenic Suppressors of Saccharomyces cerevisiae prp4 Mutations Identify a Negative Regulator of PRP Genes. Genetics 136: 833-847.

Sun C, Woolford JL Jr. (1994) The Yeast NOP4 Gene Product Is an Essential Nucleolar Protein Required for Pre-rRNA Processing and Accumulation of 60S Ribosomal Subunits. EMBO J. 13: 3127-3135.

Ripmaster T, Vaughn G, Woolford JL Jr. (1993) DRS1 to DRS7, Novel Genes Required for Ribosome Assembly and Function in Saccharomyces cerevisiae. Molecular and Cellular Biology 13: 7901-7912.

Paulovich AG, Thompson JR, Larkin JC, Li Z, Woolford JL Jr. (1993) Molecular Genetics of Cryptopleurine Resistance in Saccharomyces cerevisiae: Expression of a Ribosomal Protein Gene Family. Genetics 135: 719-730.

Deshmukh M, Tsay Y-F, Paulovich AG, Woolford JL Jr. (1993) Yeast Ribosomal Protein L1 Is Required for the Stability of Newly Synthesized 5S rRNA and the Assembly of 60S Ribosomal Subunits. Molecular and Cellular Biology 13: 2835-2845.

Ripmaster T, Vaughn G, Woolford JL Jr. (1992) A Putative ATP-Dependent RNA Helicase Involved in Saccharomyces cerevisiae Ribosome Assembly. Proceedings of the National Academy of Sciences of the United States of America 89: 11131-11135.


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