Combinatorial optimization of CRISPR/Cas9 expression enables precision genome engineering in the methylotrophic yeast Pichia pastoris

Ahmad, 2014, Protein expression in Pichia pastoris: recent achievements and perspectives for heterologous protein production, Appl. Microbiol. Biotechnol., 98, 5301, 10.1007/s00253-014-5732-5 Barnes, 2001, Non-homologous end joining as a mechanism of DNA repair, Curr. Biol., 11, R455, 10.1016/S0960-9822(01)00279-2 Bill, 2014, Playing catch-up with Escherichia coli: Using yeast to increase success rates in recombinant protein production experiments, Front. Microbiol., 5, 1, 10.3389/fmicb.2014.00085 Caldecott, 2008, Single-strand break repair and genetic disease, Nat. Rev. Genet., 9, 619, 10.1038/nrg2380 Carvalho, 2010, Expanding the ku70 toolbox for filamentous fungi: establishment of complementation vectors and recipient strains for advanced gene analyses, Appl. Microbiol. Biotechnol., 87, 1463, 10.1007/s00253-010-2588-1 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 DiCarlo, 2013, Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems, Nucleic Acids Res., 41, 4336, 10.1093/nar/gkt135 Dieci, 2007, The expanding RNA polymerase III transcriptome, Trends Genet., 23, 614, 10.1016/j.tig.2007.09.001 Doudna, 2002, The chemical repertoire of natural ribozymes, Nature, 418, 222, 10.1038/418222a Ferre-D’Amare, 1998, Crystal structure of a hepatitis delta virus ribozyme, Nature, 395, 567, 10.1038/26912 Fu, 2014, Improving CRISPR-Cas nuclease specificity using truncated guide RNAs, Nat. Biotechnol., 32, 279, 10.1038/nbt.2808 Gaj, 2013, ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering, Trends Biotechnol., 31, 397, 10.1016/j.tibtech.2013.04.004 Gantz, 2015, The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations, Science, 348, 442, 10.1126/science.aaa5945 Gao, 2014, Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing, J. Integr. Plant Biol., 56, 343, 10.1111/jipb.12152 Gasiunas, 2013, RNA-dependent DNA endonuclease Cas9 of the CRISPR system: holy grail of genome editing?, Trends Microbiol., 21, 562, 10.1016/j.tim.2013.09.001 Gasser, 2013, Pichia pastoris: protein production host and model organism for biomedical research, Futur. Microbiol., 8, 191, 10.2217/fmb.12.133 Geier, 2015, Compact multi-enzyme pathways in P. pastoris, Chem. Commun., 51, 1643, 10.1039/C4CC08502G Gilbert, 2013, CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes, Cell, 154, 442, 10.1016/j.cell.2013.06.044 Harju, 2004, Rapid isolation of yeast genomic DNA: Bust n’ Grab, BMC Biotechnol., 21, 4 Higgins, 1998, 10.1385/0896034216 Hobl, 2013, Bacteriophage T7 RNA polymerase-based expression in Pichia pastoris, Protein Expr. Purif., 92, 100, 10.1016/j.pep.2013.09.004 Jacobs, 2014, Implementation of the CRISPR-Cas9 system in fission yeast, Nat. Commun., 5, 5344, 10.1038/ncomms6344 Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 Kim, 2014, A guide to genome engineering with programmable nucleases, Nat. Rev. Genet., 15, 321, 10.1038/nrg3686 Krainer, 2013, Knockout of an endogenous mannosyltransferase increases the homogeneity of glycoproteins produced in Pichia pastoris, Sci. Rep., 3, 3279, 10.1038/srep03279 Leão-Helder, 2003, Transcriptional down-regulation of peroxisome numbers affects selective peroxisome degradation in Hansenula polymorpha, J. Biol. Chem., 278, 40749, 10.1074/jbc.M304029200 Lewis, 1997, The role of the cap structure in RNA processing and nuclear export, Eur. J. Biochem., 247, 461, 10.1111/j.1432-1033.1997.00461.x Li, 2007, Expression of recombinant proteins in Pichia pastoris, Appl. Biochem. Biotechnol., 142, 105, 10.1007/s12010-007-0003-x Lin-Cereghino, 2005, Condensed protocol for competent cell preparation and transformation of the methylotrophic yeast Pichia pastoris, Biotechniques, 38, 44, 10.2144/05381BM04 Lin-Cereghino, 2006, Mxr1p, a key regulator of the methanol utilization pathway and peroxisomal genes in Pichia pastoris, Mol. Cell. Biol., 26, 883, 10.1128/MCB.26.3.883-897.2006 Mali, 2013, RNA-guided human genome engineering via cas9, Science, 339, 823, 10.1126/science.1232033 Näätsaari, 2012, Deletion of the Pichia pastoris KU70 homologue facilitates platform strain generation for gene expression and synthetic biology, PLoS One, 7, e39720, 10.1371/journal.pone.0039720 Nagalakshmi, 2008, The transcriptional landscape of the yeast genome defined by RNA sequencing, Science, 320, 1344, 10.1126/science.1158441 Nelson, 1989, Context affects nuclear protein localization in Saccharomyces cerevisiae, Mol. Cell. Biol., 9, 384, 10.1128/MCB.9.2.384 Nett, 2003, Cloning and disruption of the PpURA5 gene and construction of a set of integration vectors for the stable genetic modification of Pichia pastoris, Yeast, 20, 1279, 10.1002/yea.1049 Pley, 1994, Three-dimensional structure of a hammerhead ribozyme, Nature, 372, 68, 10.1038/372068a0 Rouet, 1994, Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease, Mol. Cell. Biol., 14, 8096, 10.1128/MCB.14.12.8096 Ryan, 2014, Selection of chromosomal DNA libraries using a multiplex CRISPR system in Saccharomyces cerevisiae, Elife, 3, 10.7554/eLife.03703 Sahu, 2014, Trm1p, a Zn(II) 2Cys6-type transcription factor, is essential for the transcriptional activation of genes of methanol utilization pathway, in Pichia pastoris, Biochem. Biophys. Res. Commun., 451, 158, 10.1016/j.bbrc.2014.07.094 Sander, 2014, CRISPR-Cas systems for editing, regulating and targeting genomes, Nat. Biotechnol., 32, 347, 10.1038/nbt.2842 Shen, 2014, Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects, Nat. Methods, 11, 399, 10.1038/nmeth.2857 Smih, 1995, Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells, Nucleic Acids Res., 23, 5012, 10.1093/nar/23.24.5012 Storici, 2003, Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast, Proc. Natl. Acad. Sci. U. S. A., 100, 14994, 10.1073/pnas.2036296100 Tsai, 2014, Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing, Nat. Biotechnol., 32, 569, 10.1038/nbt.2908 Vogl, 2013, Regulation of Pichia pastoris promoters and its consequences for protein production, N. Biotechnol., 30, 385, 10.1016/j.nbt.2012.11.010 Vogl, T., Kickenweiz, T., Sturmberger, L., Glieder, A., 2014. Bidirectional Promoters, United States Patent Application 20150011407, filing date; 07/07/2014/European patent application EP14175932 which was filed in 2014. Vogl, 2015, Restriction site free cloning (RSFC) plasmid family for seamless, sequence independent cloning in Pichia pastoris, Microb. Cell Fact., 14, 103, 10.1186/s12934-015-0293-6 Waterham, 1997, Isolation of the Pichia pastoris glyceraldehyde-3-phosphate dehydrogenase gene and regulation and use of its promoter, Gene, 186, 37, 10.1016/S0378-1119(96)00675-0 Weis, 2004, Reliable high-throughput screening with Pichia pastoris by limiting yeast cell death phenomena, FEMS Yeast Res., 5, 179, 10.1016/j.femsyr.2004.06.016 Weninger, 2015, A toolbox of endogenous and heterologous nuclear localization sequences for the methylotrophic yeast Pichia pastoris, FEMS Yeast Res., 15, fov082, 10.1093/femsyr/fov082 Weninger, A., Killinger, M., Vogl, T., 2015. Key Methods for Synthetic Biology: Genome Engineering and DNA Assembly, in: Glieder, A., Kubicek, C.P., Mattanovich, D., Wiltschi, B., Sauer, M. (Eds.), Synthetic Biology. pp. 101–141., 10.1007/978-90-481-2678-1 Wilusz, 2001, The cap-to-tail guide to mRNA turnover, Nat. Rev. Mol. Cell. Biol., 2, 237, 10.1038/35067025