Controlled hydrostatic pressure stress downregulates the expression of ribosomal genes in preimplantation embryos: a possible protection mechanism?
I. Bock A B , H. Raveh-Amit B , E. Losonczi C , A. C. Carstea B , A. Feher B , K. Mashayekhi B , S. Matyas D , A. Dinnyes A B and C. Pribenszky C E
+ Author Affiliations
- Author Affiliations
A Molecular Animal Biotechnology Laboratory, Szent Istvan University, Pater Karoly u. 1. 2100 Godollo, Hungary.
B Biotalentum Ltd., Aulich Lajos u. 26. 2100 Godollo, Hungary.
C Department of Animal Breeding and Genetics, Faculty of Veterinary Science, Szent Istvan University, Istvan u. 2. 1078 Budapest, Hungary.
D Laboratory of Embryology, Kaali Institute, Istenhegyi ut 54/A. 1125 Budapest, Hungary.
E Corresponding author. Email: pribenszky.csaba@aotk.szie.hu
Reproduction, Fertility and Development 28(6) 776-784 https://doi.org/10.1071/RD14346
Submitted: 1 April 2014 Accepted: 25 September 2014 Published: 3 December 2014
Abstract
The efficiency of various assisted reproductive techniques can be improved by preconditioning the gametes and embryos with sublethal hydrostatic pressure treatment. However, the underlying molecular mechanism responsible for this protective effect remains unknown and requires further investigation. Here, we studied the effect of optimised hydrostatic pressure treatment on the global gene expression of mouse oocytes after embryonic genome activation. Based on a gene expression microarray analysis, a significant effect of treatment was observed in 4-cell embryos derived from treated oocytes, revealing a transcriptional footprint of hydrostatic pressure-affected genes. Functional analysis identified numerous genes involved in protein synthesis that were downregulated in 4-cell embryos in response to hydrostatic pressure treatment, suggesting that regulation of translation has a major role in optimised hydrostatic pressure-induced stress tolerance. We present a comprehensive microarray analysis and further delineate a potential mechanism responsible for the protective effect of hydrostatic pressure treatment.
Additional keywords: microarray, tolerance, transcription, translation.
References
Aksu, D. A., Agca, C., Aksu, S., Bagis, H., Akkoc, T., Caputcu, A. T., Arat, S., Taskin, A. C., Kizil, S. H., Karasahin, T., Akyol, N., Satilmis, M., Sagirkaya, H., Ustuner, B., Nur, Z., and Agca, Y. (2012). Gene expression profiles of vitrified in vitro- and in vivo-derived bovine blastocysts. Mol. Reprod. Dev. 79, 613–625.| Gene expression profiles of vitrified in vitro- and in vivo-derived bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyksbzE&md5=1940b88f2946e8b427e1f63712e70cb1CAS |
Alpas, H., Lee, J., Bozoglu, F., and Kaletunc, G. (2003). Evaluation of high hydrostatic pressure sensitivity of Staphylococcus aureus and Escherichia coli 157:H7 by differential scanning calorimetry. Int. J. Food Microbiol. 87, 229–237.
| Evaluation of high hydrostatic pressure sensitivity of Staphylococcus aureus and Escherichia coli 157:H7 by differential scanning calorimetry.Crossref | GoogleScholarGoogle Scholar | 14527795PubMed |
Bachvarova, R., and De Leon, V. (1980). Polyadenylated RNA of mouse ova and loss of maternal RNA in early development. Dev. Biol. 74, 1–8.
| Polyadenylated RNA of mouse ova and loss of maternal RNA in early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXht1Gkurs%3D&md5=943f083a4853422932bbf3d05cdbdf4fCAS | 7350004PubMed |
Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289–300.
Bock, I., Losonczi, E., Mamo, S., Polgar, Z., Harnos, A., Dinnyes, A., and Pribenszky, C. (2010). Stress tolerance and transcriptional response in mouse embryos treated with high hydrostatic pressure to enhance cryotolerance. Cryo Letters 31, 401–412.
| 21042655PubMed |
Bogliolo, L., Ariu, F., Leoni, G., Uccheddu, S., and Bebbere, D. (2011). High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts. Reprod. Fertil. Dev. 23, 809–817.
| High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 21791182PubMed |
Bolton, V. N., Oades, P. J., and Johnson, M. H. (1984). The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J. Embryol. Exp. Morphol. 79, 139–163.
| 1:CAS:528:DyaL2cXlvVyrtr0%3D&md5=e4d55e36f5524fdb15307626c01dde49CAS | 6716041PubMed |
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
| The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=78315fac3e32033dbd8014eacd0b3e3eCAS | 19246619PubMed |
Callesen, H. (2010). Challenge testing of gametes to enhance their viability. Reprod. Fertil. Dev. 22, 40–46.
| Challenge testing of gametes to enhance their viability.Crossref | GoogleScholarGoogle Scholar | 20003844PubMed |
Cascio, S. M., and Wassarman, P. M. (1982). Program of early development in the mammal: post-transcriptional control of a class of proteins synthesized by mouse oocytes and early embryos. Dev. Biol. 89, 397–408.
| Program of early development in the mammal: post-transcriptional control of a class of proteins synthesized by mouse oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xms1aktw%3D%3D&md5=2f96be1af06263713f1552aa1568f899CAS | 7199001PubMed |
Chatot, C. L., Ziomek, C. A., Bavister, B. D., Lewis, J. L., and Torres, I. (1989). An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fertil. 86, 679–688.
| An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1Mzkt1emtA%3D%3D&md5=3dc2db4458005aee9570f8ac1d449254CAS | 2760894PubMed |
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3.
| DAVID: Database for Annotation, Visualization, and Integrated Discovery.Crossref | GoogleScholarGoogle Scholar | 12734009PubMed |
Gross, M., Lehle, K., Jaenicke, R., and Nierhaus, K. H. (1993). Pressure-induced dissociation of ribosomes and elongation cycle intermediates. Stabilizing conditions and identification of the most sensitive functional state. Eur. J. Biochem. 218, 463–468.
| Pressure-induced dissociation of ribosomes and elongation cycle intermediates. Stabilizing conditions and identification of the most sensitive functional state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1Gru7Y%3D&md5=65a76ddec2d73708d7d6f452a4b71d2cCAS | 8269935PubMed |
Gross, M., and Jaenicke, R. (1990). Pressure-induced dissociation of tight couple ribosomes. FEBS Lett. 267, 239–241.
| Pressure-induced dissociation of tight couple ribosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltFWht7Y%3D&md5=c0509eadd2cef476feb2124cc178cc6dCAS | 2199216PubMed |
Hellemans, J., and Vandesompele, J. (2011). Quantitative PCR data analysis: unlocking the secret to successful results. In ‘PCR Troubleshooting and Optimization: The Essential Guide’. (Eds S. Kennedy and N. Oswald.) pp. 139–150. (Caister Academic Press: Norwich, UK.)
Huang, S. Y., Pribenszky, C., Kuo, Y. H., Teng, S. H., Chen, Y. H., Chung, M. T., and Chiu, Y. F. (2009a). Hydrostatic pressure pre-treatment affects the protein profile of boar sperm before and after freezing–thawing. Anim. Reprod. Sci. 112, 136–149.
| Hydrostatic pressure pre-treatment affects the protein profile of boar sperm before and after freezing–thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWktLY%3D&md5=d3d73c65024b36b2a6363cba5a13ced6CAS | 18538515PubMed |
Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009b). Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4, 44–57.
| Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCkurnI&md5=b7e7568816f0cdaa4dd979e4d66b59c8CAS |
Iwahashi, H., Kaul, S. C., Obuchi, K., and Komatsu, Y. (1991). Induction of barotolerance by heat shock treatment in yeast. FEMS Microbiol. Lett. 64, 325–328.
| Induction of barotolerance by heat shock treatment in yeast.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzlslCmsA%3D%3D&md5=baa55ae1c197d3ffd4a79a442d415a1cCAS | 1884989PubMed |
Jarrell, V. L., Day, B. N., and Prather, R. S. (1991). The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis. Biol. Reprod. 44, 62–68.
| The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvFCrsw%3D%3D&md5=e90452da1bb93a9aac10c1ffb0145a45CAS | 2015352PubMed |
Kuretake, S., Kimura, Y., Hoshi, K., and Yanagimachi, R. (1996). Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789–795.
| Fertilization and development of mouse oocytes injected with isolated sperm heads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xls1Gkt7c%3D&md5=34487050e504be55ba5f5af6ea463686CAS | 8879491PubMed |
Leese, H. J. (2012). Metabolism of the preimplantation embryo: 40 years on. Reproduction 143, 417–427.
| Metabolism of the preimplantation embryo: 40 years on.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2ns7k%3D&md5=de57c32d788c33cecd35da9db2f078f9CAS | 22408180PubMed |
Leese, H. J., Baumann, C. G., Brison, D. R., McEvoy, T. G., and Sturmey, R. G. (2008). Metabolism of the viable mammalian embryo: quietness revisited. Mol. Hum. Reprod. 14, 667–672.
| Metabolism of the viable mammalian embryo: quietness revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gsA%3D%3D&md5=52d5be34b4c6a7764b63edc11d07cb99CAS | 19019836PubMed |
Li, L., Zheng, P., and Dean, J. (2010). Maternal control of early mouse development. Development 137, 859–870.
| Maternal control of early mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1Kjs7k%3D&md5=aaabe8177838be8e17af4d450220e4fcCAS | 20179092PubMed |
Lin, L., Kragh, P. M., Purup, S., Kuwayama, M., Du, Y., Zhang, X., Yang, H., Bolund, L., Callesen, H., and Vajta, G. (2009). Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes. Reprod. Fertil. Dev. 21, 338–344.
| Osmotic stress induced by sodium chloride, sucrose or trehalose improves cryotolerance and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVensb8%3D&md5=411c6ad51552e1f5fa6c1166d2ecd34eCAS | 19210925PubMed |
Lin, L., Luo, Y., Sørensen, P., Prætorius, H., Vajta, G., Callesen, H., Pribenszky, C., Bolund, L., and Kristensen, T. N. (2014). Effects of high hydrostatic pressure on genomic expression profiling of porcine parthenogenetic activated and cloned embryos. Reprod. Fertil. Dev. 26, 469–484.
| Effects of high hydrostatic pressure on genomic expression profiling of porcine parthenogenetic activated and cloned embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlelsbk%3D&md5=8f9ce5b547bc49dac0c3e575e6c3efc9CAS | 24618454PubMed |
Lu, B., Li, Q., Liu, W. Y., and Ruan, K. C. (1997). Effects of hydrostatic pressure on the activity of rat ribosome and cell-free translation system. Biochem. Mol. Biol. Int. 43, 499–506.
| Effects of hydrostatic pressure on the activity of rat ribosome and cell-free translation system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnt1CqtrY%3D&md5=afd633690417d79d31bda82f6d884ae1CAS | 9352067PubMed |
Mackey, B., and Mañas, P. (2008). Inactivation of Escherichia coli by high pressure. In ‘High Pressure Microbiology’. (Eds C. Michiels, D. H. Bartlett and A. Aertsen.) pp. 53–85. (ASM Press: Washington, DC.)
Mamo, S., Gal, A. B., Bodo, S., and Dinnyes, A. (2007). Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro. BMC Dev. Biol. 7, 14.
| Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 17341302PubMed |
Morey, J. S., Ryan, J. C., and Van Dolah, F. M. (2006). Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol. Proced. Online 8, 175–193.
| Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCmsbvE&md5=6307e45f451f9f991ef5c25b826e0b74CAS | 17242735PubMed |
Morley, S. J., and Naegele, S. (2002). Phosphorylation of eukaryotic initiation factor (eIF) 4E is not required for de novo protein synthesis following recovery from hypertonic stress in human kidney cells. J. Biol. Chem. 277, 32 855–32 859.
| Phosphorylation of eukaryotic initiation factor (eIF) 4E is not required for de novo protein synthesis following recovery from hypertonic stress in human kidney cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1SmtLo%3D&md5=b01047e9892d7d3a197041f1baea43daCAS |
Nakao, A., Yoshihama, M., and Kenmochi, N. (2004). RPG: the Ribosomal Protein Gene database. Nucleic Acids Res. 32, D168–D170.
| RPG: the Ribosomal Protein Gene database.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSrtbfP&md5=3b9ab870be2018d63547027a43cdd0d1CAS | 14681386PubMed |
Niven, G. W., Miles, C. A., and Mackey, B. M. (1999). The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry. Microbiology 145, 419–425.
| The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFChtro%3D&md5=3d6225ed9a27023fc5ea23ca79ace037CAS | 10075424PubMed |
Palhano, F. L., Orlando, M. T., and Fernandes, P. M. (2004). Induction of baroresistance by hydrogen peroxide, ethanol and cold-shock in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 233, 139–145.
| Induction of baroresistance by hydrogen peroxide, ethanol and cold-shock in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisVKltr0%3D&md5=f98d7c66dfb72fcb9a0851053383f7c8CAS | 15043880PubMed |
Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
| Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar | 11972351PubMed |
Pribenszky, C., and Vajta, G. (2011). Cells under pressure: how sublethal hydrostatic pressure stress treatment increases gametes’ and embryos’ performance? Reprod. Fertil. Dev. 23, 48–55.
| Cells under pressure: how sublethal hydrostatic pressure stress treatment increases gametes’ and embryos’ performance?Crossref | GoogleScholarGoogle Scholar | 21366980PubMed |
Pribenszky, C., Molnar, M., Cseh, S., and Solti, L. (2005). Improving post-thaw survival of cryopreserved mouse blastocysts by hydrostatic pressure challenge. Anim. Reprod. Sci. 87, 143–150.
| Improving post-thaw survival of cryopreserved mouse blastocysts by hydrostatic pressure challenge.Crossref | GoogleScholarGoogle Scholar | 15885447PubMed |
Pribenszky, C., Vajta, G., Molnar, M., Du, Y., Lin, L., Bolund, L., and Yovich, J. (2010). Stress for stress tolerance? A fundamentally new approach in mammalian embryology. Biol. Reprod. 83, 690–697.
| Stress for stress tolerance? A fundamentally new approach in mammalian embryology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGlsrfL&md5=994ecb883d80fba436aa0e86bde7b243CAS | 20554920PubMed |
Pribenszky, C., Lin, L., Du, Y., Losonczi, E., Dinnyes, A., and Vajta, G. (2012). Controlled stress improves oocyte performance-cell preconditioning in assisted reproduction. Reprod. Domest. Anim. 47, 197–206.
| Controlled stress improves oocyte performance-cell preconditioning in assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 22827371PubMed |
Rainer, J., Sanchez-Cabo, F., Stocker, G., Sturn, A., and Trajanoski, Z. (2006). CARMAweb: comprehensive R- and Bioconductor-based web service for microarray data analysis. Nucleic Acids Res. 34, W498–W503.
| CARMAweb: comprehensive R- and Bioconductor-based web service for microarray data analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1yisbw%3D&md5=6b3c6db9beeb409e25727659f797b351CAS | 16845058PubMed |
Rozen, S., and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386.
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=c0a04cc2da37ce24293e88ef86ddb8e7CAS | 10547847PubMed |
San Martín, M. F., Barbosa-Cánovas, G. V., and Swanson, B. G. (2002). Food processing by high hydrostatic pressure. Crit. Rev. Food Sci. Nutr. 42, 627–645.
| Food processing by high hydrostatic pressure.Crossref | GoogleScholarGoogle Scholar | 12487422PubMed |
Schulz, E., Lüdemann, H. D., and Jaenicke, R. (1976). High pressure equilibrium studies on the dissociation–association of E. coli ribosomes. FEBS Lett. 64, 40–43.
| High pressure equilibrium studies on the dissociation–association of E. coli ribosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XktVWgtrk%3D&md5=09cd68f446aeb40763fabe0658d8330cCAS | 773700PubMed |
Siqueira Filho, E., Caixeta, E. S., Pribenszky, C., Molnar, M., Horvath, A., Harnos, A., Franco, M. M., and Rumpf, R. (2011). Vitrification of bovine blastocysts pretreated with sublethal hydrostatic pressure stress: evaluation of post-thaw in vitro development and gene expression. Reprod. Fertil. Dev. 23, 585–590.
| Vitrification of bovine blastocysts pretreated with sublethal hydrostatic pressure stress: evaluation of post-thaw in vitro development and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFKnsLg%3D&md5=b2d59c276b6951c472ab199ade3d3d54CAS | 21557925PubMed |
Stokes, P. J., Hawkhead, J. A., Fawthrop, R. K., Picton, H. M., Sharma, V., Leese, H. J., and Houghton, F. D. (2007). Metabolism of human embryos following cryopreservation: implications for the safety and selection of embryos for transfer in clinical IVF. Hum. Reprod. 22, 829–835.
| Metabolism of human embryos following cryopreservation: implications for the safety and selection of embryos for transfer in clinical IVF.Crossref | GoogleScholarGoogle Scholar | 17138583PubMed |
Sutovsky, P., and Schatten, G. (2000). Paternal contributions to the mammalian zygote: fertilization after sperm–egg fusion. Int. Rev. Cytol. 195, 1–65.
| Paternal contributions to the mammalian zygote: fertilization after sperm–egg fusion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVehu74%3D&md5=fb232992cd0f9296eec0eb05d30dbadaCAS | 10603574PubMed |
Vandaele, L., Thys, M., Bijttebier, J., Van Langendonckt, A., Donnay, I., Maes, D., Meyer, E., and Van Soom, A. (2010). Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development. Reproduction 139, 505–511.
| Short-term exposure to hydrogen peroxide during oocyte maturation improves bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtV2lsb8%3D&md5=bb71329792a43a5967613e707b16376eCAS | 19939885PubMed |
Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437–440.
| The economics of ribosome biosynthesis in yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvVKmtA%3D%3D&md5=1e215aea26c21a446422159584fde15eCAS | 10542411PubMed |
Warner, J. R., Vilardell, J., and Sohn, J. H. (2001). Economics of ribosome biosynthesis. Cold Spring Harb. Symp. Quant. Biol. 66, 567–574.
| Economics of ribosome biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFyktLs%3D&md5=2a65d53b4d82d8a5a4671d0e13688401CAS | 12762058PubMed |
Wemekamp-Kamphuis, H. H., Karatzas, A. K., Wouters, J. A., and Abee, T. (2002). Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Appl. Environ. Microbiol. 68, 456–463.
| Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtV2gtbc%3D&md5=ad8fc11b8d2267af4468985c8f2ee358CAS | 11823178PubMed |
Whitworth, K. M., Agca, C., Kim, J. G., Patel, R. V., Springer, G. K., Bivens, N. J., Forrester, L. J., Mathialagan, N., Green, J. A., and Prather, R. S. (2005). Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biol. Reprod. 72, 1437–1451.
| Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFGqsbg%3D&md5=37bb870e394d5e22b294e6d2e84a5ccbCAS | 15703372PubMed |
Wiese, A. G., Pacifici, R. E., and Davies, K. J. (1995). Transient adaptation to oxidative stress in mammalian cells. Arch. Biochem. Biophys. 318, 231–240.
| Transient adaptation to oxidative stress in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltVShsbo%3D&md5=1faf88ff1ba3d7401b23c648df2553c6CAS | 7726566PubMed |
Wool, I. G. (1979). The structure and function of eukaryotic ribosomes. Annu. Rev. Biochem. 48, 719–754.
| The structure and function of eukaryotic ribosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltVers7k%3D&md5=531c3b7e58aab5efdf21ce35e2a7f2f1CAS | 382996PubMed |
Zuker, M. (2003). mFOLD web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406–3415.
| mFOLD web server for nucleic acid folding and hybridization prediction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVWisr8%3D&md5=0c12a546725f6c8ed64e575bfbd108b2CAS | 12824337PubMed |
