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The effects of mutations on pericentromeric localization of shugoshin

Yıl 2022, Cilt: 24 Sayı: 2, 869 - 877, 08.07.2022

Öz

Elucidating the effects of mutations on protein-protein interactions can be useful for detecting damaged biological functions like chromosome segregations, because cellular structure and functions are mainly built on concerted interactions of proteins. Shugoshin (Sgo1) is one of those proteins that has many roles in correct chromosome segregation during mitosis and meiosis. One of the important aspects about Sgo1, to function properly, is the fact that it has to be on the chromosomal region surrounding the centromere (the pericentromere). However, some mutations can directly or indirectly affect the localization of Sgo1 and result in chromosomal instability which is known as the occasional gain/loss of chromosomes resulting in aneuploidy, cancer and other diseases. Therefore, this review focuses on the mutations that affect the pericentromeric localization of Sgo1.

Teşekkür

This work is produced from a part of PhD thesis of Begumhan Yilmaz Kardas. Authors would like to thank Adele Marston for introducing authors to this research area and the Scientific and Technological Research Council of Turkey (TUBITAK) for the scholarships provided to Begumhan Yilmaz Kardas.

Kaynakça

  • Husi, H., Nmda receptors, neural pathways, and protein interaction databases, International Review of Neurobiology, 61, 49-77, (2004).
  • Richards, A. L., Eckhardt, M. and Krogan, N. J., Mass spectrometry‐based protein–protein interaction networks for the study of human diseases, Molecular Systems Biology, 17, 1, (2021).
  • Hsieh, Y.-Y. P., Makrantoni, V., Robertson, D., Marston, A. L. and Murray, A. W., Evolutionary repair: Changes in multiple functional modules allow meiotic cohesin to support mitosis, PLoS Biology, 18, 3, e3000635, (2020).
  • Wenzel, E. S. and Singh, A. T. K., Cell-cycle checkpoints and aneuploidy on the path to cancer, In Vivo, 32, 1, 1-5, (2018).
  • Marston, A. L., Shugoshins: Tension-sensitive pericentromeric adaptors safeguarding chromosome segregation, Molecular and Cellular Biology, 35, 4, 634-648, (2015).
  • Kumar, R. and Agarwal, M., Shugoshin: From the perspective of clinical disorders, BioChem, 1, 2, 51-59, (2021).
  • Yao, Y. and Dai, W., Shugoshins function as a guardian for chromosomal stability in nuclear division, Cell Cycle, 11, 14, 2631-2642, (2012).
  • Hoevenaar, W. H. M. et al., Degree and site of chromosomal instability define its oncogenic potential, Nature Communications, 11, 1, (2020).
  • Kovalchuk, I., Cancer and genomic instability in Genome stability, 495-519, (2021).
  • Sugiyama, T. et al., Microsatellite frameshift variants in sgo1 of gastric cancer are not always associated with msi status, Journal of Clinical Pathology, (2020).
  • Iwaizumi, M. et al., Human sgo1 downregulation leads to chromosomal instability in colorectal cancer, Gut, 58, 2, 249-260, (2009).
  • Yamada, H. Y. et al., Haploinsufficiency of sgo1 results in deregulated centrosome dynamics, enhanced chromosomal instability and colon tumorigenesis, Cell Cycle, 11, 3, 479-488, (2012).
  • Matsuura, S. et al., Sgol1 variant b induces abnormal mitosis and resistance to taxane in non-small cell lung cancers, Scientific Reports, 3, 1, (2013).
  • Wang, L.-H., Yen, C.-J., Li, T.-N., Elowe, S., Wang, W.-C. and Wang, L. H.-C., Sgo1 is a potential therapeutic target for hepatocellular carcinoma, Oncotarget, 6, 4, 2023-2033, (2015).
  • Faridi, R. et al., Mutations ofsgo2andcldn14collectively cause coincidental perrault syndrome, Clinical Genetics, 91, 2, 328-332, (2017).
  • Domínguez-Ruiz, M. et al., Perrault syndrome with neurological features in a compound heterozygote for two twnk mutations: Overlap of twnk-related recessive disorders, Journal of Translational Medicine, 17, 1, (2019).
  • Kennedy, S. R., Loeb, L. A. and Herr, A. J., Somatic mutations in aging, cancer and neurodegeneration, Mechanisms of Ageing and Development, 133, 4, 118-126, (2012).
  • Chow, H.-M. and Herrup, K., Genomic integrity and the ageing brain, Nature Reviews Neuroscience, 16, 11, 672-684, (2015).
  • Vijg, J., Dong, X., Milholland, B. and Zhang, L., Genome instability: A conserved mechanism of ageing?, Essays in Biochemistry, 61, 3, 305-315, (2017).
  • Helbling-Leclerc, A., Garcin, C. and Rosselli, F., Beyond DNA repair and chromosome instability—fanconi anaemia as a cellular senescence-associated syndrome, Cell Death & Differentiation, 28, 4, 1159-1173, (2021).
  • Iourov, I. Y., Vorsanova, S. G., Liehr, T., Kolotii, A. D. and Yurov, Y. B., Increased chromosome instability dramatically disrupts neural genome integrity and mediates cerebellar degeneration in the ataxia-telangiectasia brain, Human Molecular Genetics, 18, 14, 2656-2669, (2009).
  • Iourov, I. Y., Yurov, Y. B., Vorsanova, S. G. and Kutsev, S. I., Chromosome instability, aging and brain diseases, Cells, 10, 5, 1256, (2021).
  • Verzijlbergen, K. F. et al., Shugoshin biases chromosomes for biorientation through condensin recruitment to the pericentromere, eLife, 3, e01374-e01374, (2014).
  • Nerusheva, O. O., Galander, S., Fernius, J., Kelly, D. and Marston, A. L., Tension-dependent removal of pericentromeric shugoshin is an indicator of sister chromosome biorientation, Genes and Development, 28, 12, 1291-1309, (2014).
  • Smurova, K. and De Wulf, P., Centromere and pericentromere transcription: Roles and regulation ... In sickness and in health, Frontiers in Genetics, 9, 674, (2018).
  • Duro, E. and Marston, A. L., From equator to pole: Splitting chromosomes in mitosis and meiosis, Genes and Development, 29, 2, 109-122, (2015).
  • Fernius, J., Nerusheva, O. O., Galander, S., Alves, F. d. L., Rappsilber, J. and Marston, A. L., Cohesin-dependent association of scc2/4 with the centromere initiates pericentromeric cohesion establishment, Current Biology, 23, 7, 599-606, (2013).
  • Uhlmann, F. and Nasmyth, K., Cohesion between sister chromatids must be established during DNA replication, Current Biology, 8, 20, 1095-1102, (1998).
  • Ng, T. M., Waples, W. G., Lavoie, B. D. and Biggins, S., Pericentromeric sister chromatid cohesion promotes kinetochore biorientation, Molecular Biology of the Cell, 20, 3818-3827, (2009).
  • Ribeiro, S. A. et al., Condensin regulates the stiffness of vertebrate centromeres, Molecular Biology of the Cell, 20, 9, 2371-2380, (2009).
  • Stephens, A. D., Haase, J., Vicci, L., Taylor, R. M. and Bloom, K., Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring, Journal of Cell Biology, 193, 7, 1167-1180, (2011).
  • Stephens, A. D. et al., Pericentric chromatin loops function as a nonlinear spring in mitotic force balance, Journal of Cell Biology, 200, 6, 757-772, (2013).
  • Yong-Gonzalez, V., Wang, B. D., Butylin, P., Ouspenski, I. and Strunnikov, A., Condensin function at centromere chromatin facilitates proper kinetochore tension and ensures correct mitotic segregation of sister chromatids, Genes to Cells, 12, 9, 1075-1090, (2007).
  • Jaqaman, K. et al., Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases, Journal of Cell Biology, 188, 5, 665-679, (2010).
  • Marston, A. L., Chromosome segregation in budding yeast: Sister chromatid cohesion and related mechanisms, Genetics, 196, 1, 31-63, (2014).
  • Eshleman, H. D. and Morgan, D. O., Sgo1 recruits pp2a to chromosomes to ensure sister chromatid bi-orientation during mitosis, Journal of Cell Science, 2014, 127, 4974-4983, (2014).
  • Peplowska, K., Wallek, A. U. and Storchova, Z., Sgo1 regulates both condensin and ipl1/aurora b to promote chromosome biorientation, PLOS Genetics, 10, 6, (2014).
  • Rabitsch, K. P., Gregan, J., Schleiffer, A., Javerzat, J.-P., Eisenhaber, F. and Nasmyth, K., Two fission yeast homologs of drosophila mei-s332 are required for chromosome segregation during meiosis i and ii, Current Biology, 14, 4, 287-301, (2004).
  • Tang, Z., Shu, H., Qi, W., Mahmood, N. A., Mumby, M. C. and Yu, H., Pp2a is required for centromeric localization of sgo1 and proper chromosome segregation, Developmental Cell, 10, 5, 575-585, (2006).
  • Xu, Z., Cetin, B., Anger, M., Cho, U. S., Helmhart, W. and Xu, W., Structure and function of the pp2a-shugoshin interaction, Molecular Cell, 35, 4, 426-441, (2009).
  • Kawashima, S. A., Yamagishi, Y., Honda, T., Lshiguro, K. I. and Watanabe, Y., Phosphorylation of h2a by bub1 prevents chromosomal instability through localizing shugoshin, Science, 327, 5962, 172-177, (2010).
  • Yahya, G. et al., Phospho-regulation of the shugoshin - condensin interaction at the centromere in budding yeast, PLOS Genetics, 16, 8, e1008569, (2020).
  • Indjeian, V. B., Stern, B. M. and Murray, A. W., The centromeric protein sgo1 is required to sense lack of tension on mitotic chromosomes, Science, 307, 5706, 130-133, (2005).
  • Kim, T. et al., Kinetochores accelerate or delay apc/c activation by directing cdc20 to opposing fates, Genes and Development, 31, 11, 1089-1094, (2017).
  • Levine, M. S. and Holland, A. J., The impact of mitotic errors on cell proliferation and tumorigenesis, Genes & Development, 32, 9-10, 620-638, (2018).
  • Garcia-Gimenez, J. L., Garces, C., Roma-Mateo, C. and Pallardo, F. V., Oxidative stress-mediated alterations in histone post-translational modifications, Free Radical Biology and Medicine, 170, 6-18, (2021).
  • Schmitz, M. L., Higgins, J. M. G. and Seibert, M., Priming chromatin for segregation: Functional roles of mitotic histone modifications, Cell Cycle, 19, 6, 625-641, (2020).
  • Singh, D., Nishi, K., Khambata, K. and Balasinor, N. H., Introduction to epigenetics: Basic concepts and advancements in the field in Tollefsbol, T., Epigenetics and reproductive health, Elsevier, 25-44, United Kingdom, (2020).
  • Ishiguro, T., Tanabe, K., Kobayashi, Y., Mizumoto, S., Kanai, M. and Kawashima, S. A., Malonylation of histone h2a at lysine 119 inhibits bub1-dependent h2a phosphorylation and chromosomal localization of shugoshin proteins, Scientific Reports, 8, 1, 1-10, (2018).
  • Tyagi, M., Imam, N., Verma, K. and Patel, A. K., Chromatin remodelers: We are the drivers!!, Nucleus, 7, 4, 388-404, (2016).
  • Min, S., Kim, K., Kim, S.-G., Cho, H. and Lee, Y., Chromatin-remodeling factor, rsf1, controls p53-mediated transcription in apoptosis upon DNA strand breaks, Cell Death & Disease, 9, 11, (2018).
  • Lee, H.-S. et al., The chromatin remodeler rsf1 controls centromeric histone modifications to coordinate chromosome segregation, Nature Communications, 9, 1, 3848-3848, (2018).
  • Cai, G., Yang, Q. and Sun, W., Rsf1 in cancer: Interactions and functions, Cancer Cell International, 21, 1, (2021).
  • Hargreaves, D. C. and Crabtree, G. R., Atp-dependent chromatin remodeling: Genetics, genomics and mechanisms, Cell Research, 21, 3, 396-420, (2011).
  • Hormozdiari, F. et al., The effect of insertions and deletions on wirings in protein-protein interaction networks: A large-scale study, Journal of Computational Biology, 16, 2, 159-167, (2009).
  • Wang, X., Gene mutation‐based and specific therapies in precision medicine, Journal of Cellular and Molecular Medicine, 20, 4, 577-580, (2016).

Mutasyonların şugoşinin perisentromerik lokalizasyonu üzerindeki etkileri

Yıl 2022, Cilt: 24 Sayı: 2, 869 - 877, 08.07.2022

Öz

Mutasyonların protein-protein etkileşimleri üzerindeki etkilerinin aydınlatılması, kromozom segregasyonları gibi biyolojik fonksiyonlardaki hasarlarn tespiti için faydalı olabilir, çünkü hücresel yapı ve fonksiyonlar esas olarak proteinlerin uyumlu etkileşimleri üzerine kuruludur. Shugoshin (Sgo1), mitoz ve mayoz bölünme sırasında doğru kromozom ayrımında birçok rolü olan proteinlerden biridir. Sgo1'in düzgün çalışması için gerekli olan faktörlerden biri, bu proteinin sentromeri çevreleyen (perisentromer) kromozomal bölgede bulunması gerekliliğidir. Bununla birlikte, bazı mutasyonlar Sgo1'in lokalizasyonunu doğrudan veya dolaylı olarak etkileyebilir ve anöploidi, kanser ve diğer hastalıklarla sonuçlanabilen kromozom kazanımı/kaybı olarak bilinen kromozomal kararsızlığa neden olabilir. Bu nedenle, bu makale Sgo1'in perisentromerik lokalizasyonunu etkileyen mutasyonlara odaklanmaktadır.

Kaynakça

  • Husi, H., Nmda receptors, neural pathways, and protein interaction databases, International Review of Neurobiology, 61, 49-77, (2004).
  • Richards, A. L., Eckhardt, M. and Krogan, N. J., Mass spectrometry‐based protein–protein interaction networks for the study of human diseases, Molecular Systems Biology, 17, 1, (2021).
  • Hsieh, Y.-Y. P., Makrantoni, V., Robertson, D., Marston, A. L. and Murray, A. W., Evolutionary repair: Changes in multiple functional modules allow meiotic cohesin to support mitosis, PLoS Biology, 18, 3, e3000635, (2020).
  • Wenzel, E. S. and Singh, A. T. K., Cell-cycle checkpoints and aneuploidy on the path to cancer, In Vivo, 32, 1, 1-5, (2018).
  • Marston, A. L., Shugoshins: Tension-sensitive pericentromeric adaptors safeguarding chromosome segregation, Molecular and Cellular Biology, 35, 4, 634-648, (2015).
  • Kumar, R. and Agarwal, M., Shugoshin: From the perspective of clinical disorders, BioChem, 1, 2, 51-59, (2021).
  • Yao, Y. and Dai, W., Shugoshins function as a guardian for chromosomal stability in nuclear division, Cell Cycle, 11, 14, 2631-2642, (2012).
  • Hoevenaar, W. H. M. et al., Degree and site of chromosomal instability define its oncogenic potential, Nature Communications, 11, 1, (2020).
  • Kovalchuk, I., Cancer and genomic instability in Genome stability, 495-519, (2021).
  • Sugiyama, T. et al., Microsatellite frameshift variants in sgo1 of gastric cancer are not always associated with msi status, Journal of Clinical Pathology, (2020).
  • Iwaizumi, M. et al., Human sgo1 downregulation leads to chromosomal instability in colorectal cancer, Gut, 58, 2, 249-260, (2009).
  • Yamada, H. Y. et al., Haploinsufficiency of sgo1 results in deregulated centrosome dynamics, enhanced chromosomal instability and colon tumorigenesis, Cell Cycle, 11, 3, 479-488, (2012).
  • Matsuura, S. et al., Sgol1 variant b induces abnormal mitosis and resistance to taxane in non-small cell lung cancers, Scientific Reports, 3, 1, (2013).
  • Wang, L.-H., Yen, C.-J., Li, T.-N., Elowe, S., Wang, W.-C. and Wang, L. H.-C., Sgo1 is a potential therapeutic target for hepatocellular carcinoma, Oncotarget, 6, 4, 2023-2033, (2015).
  • Faridi, R. et al., Mutations ofsgo2andcldn14collectively cause coincidental perrault syndrome, Clinical Genetics, 91, 2, 328-332, (2017).
  • Domínguez-Ruiz, M. et al., Perrault syndrome with neurological features in a compound heterozygote for two twnk mutations: Overlap of twnk-related recessive disorders, Journal of Translational Medicine, 17, 1, (2019).
  • Kennedy, S. R., Loeb, L. A. and Herr, A. J., Somatic mutations in aging, cancer and neurodegeneration, Mechanisms of Ageing and Development, 133, 4, 118-126, (2012).
  • Chow, H.-M. and Herrup, K., Genomic integrity and the ageing brain, Nature Reviews Neuroscience, 16, 11, 672-684, (2015).
  • Vijg, J., Dong, X., Milholland, B. and Zhang, L., Genome instability: A conserved mechanism of ageing?, Essays in Biochemistry, 61, 3, 305-315, (2017).
  • Helbling-Leclerc, A., Garcin, C. and Rosselli, F., Beyond DNA repair and chromosome instability—fanconi anaemia as a cellular senescence-associated syndrome, Cell Death & Differentiation, 28, 4, 1159-1173, (2021).
  • Iourov, I. Y., Vorsanova, S. G., Liehr, T., Kolotii, A. D. and Yurov, Y. B., Increased chromosome instability dramatically disrupts neural genome integrity and mediates cerebellar degeneration in the ataxia-telangiectasia brain, Human Molecular Genetics, 18, 14, 2656-2669, (2009).
  • Iourov, I. Y., Yurov, Y. B., Vorsanova, S. G. and Kutsev, S. I., Chromosome instability, aging and brain diseases, Cells, 10, 5, 1256, (2021).
  • Verzijlbergen, K. F. et al., Shugoshin biases chromosomes for biorientation through condensin recruitment to the pericentromere, eLife, 3, e01374-e01374, (2014).
  • Nerusheva, O. O., Galander, S., Fernius, J., Kelly, D. and Marston, A. L., Tension-dependent removal of pericentromeric shugoshin is an indicator of sister chromosome biorientation, Genes and Development, 28, 12, 1291-1309, (2014).
  • Smurova, K. and De Wulf, P., Centromere and pericentromere transcription: Roles and regulation ... In sickness and in health, Frontiers in Genetics, 9, 674, (2018).
  • Duro, E. and Marston, A. L., From equator to pole: Splitting chromosomes in mitosis and meiosis, Genes and Development, 29, 2, 109-122, (2015).
  • Fernius, J., Nerusheva, O. O., Galander, S., Alves, F. d. L., Rappsilber, J. and Marston, A. L., Cohesin-dependent association of scc2/4 with the centromere initiates pericentromeric cohesion establishment, Current Biology, 23, 7, 599-606, (2013).
  • Uhlmann, F. and Nasmyth, K., Cohesion between sister chromatids must be established during DNA replication, Current Biology, 8, 20, 1095-1102, (1998).
  • Ng, T. M., Waples, W. G., Lavoie, B. D. and Biggins, S., Pericentromeric sister chromatid cohesion promotes kinetochore biorientation, Molecular Biology of the Cell, 20, 3818-3827, (2009).
  • Ribeiro, S. A. et al., Condensin regulates the stiffness of vertebrate centromeres, Molecular Biology of the Cell, 20, 9, 2371-2380, (2009).
  • Stephens, A. D., Haase, J., Vicci, L., Taylor, R. M. and Bloom, K., Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring, Journal of Cell Biology, 193, 7, 1167-1180, (2011).
  • Stephens, A. D. et al., Pericentric chromatin loops function as a nonlinear spring in mitotic force balance, Journal of Cell Biology, 200, 6, 757-772, (2013).
  • Yong-Gonzalez, V., Wang, B. D., Butylin, P., Ouspenski, I. and Strunnikov, A., Condensin function at centromere chromatin facilitates proper kinetochore tension and ensures correct mitotic segregation of sister chromatids, Genes to Cells, 12, 9, 1075-1090, (2007).
  • Jaqaman, K. et al., Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases, Journal of Cell Biology, 188, 5, 665-679, (2010).
  • Marston, A. L., Chromosome segregation in budding yeast: Sister chromatid cohesion and related mechanisms, Genetics, 196, 1, 31-63, (2014).
  • Eshleman, H. D. and Morgan, D. O., Sgo1 recruits pp2a to chromosomes to ensure sister chromatid bi-orientation during mitosis, Journal of Cell Science, 2014, 127, 4974-4983, (2014).
  • Peplowska, K., Wallek, A. U. and Storchova, Z., Sgo1 regulates both condensin and ipl1/aurora b to promote chromosome biorientation, PLOS Genetics, 10, 6, (2014).
  • Rabitsch, K. P., Gregan, J., Schleiffer, A., Javerzat, J.-P., Eisenhaber, F. and Nasmyth, K., Two fission yeast homologs of drosophila mei-s332 are required for chromosome segregation during meiosis i and ii, Current Biology, 14, 4, 287-301, (2004).
  • Tang, Z., Shu, H., Qi, W., Mahmood, N. A., Mumby, M. C. and Yu, H., Pp2a is required for centromeric localization of sgo1 and proper chromosome segregation, Developmental Cell, 10, 5, 575-585, (2006).
  • Xu, Z., Cetin, B., Anger, M., Cho, U. S., Helmhart, W. and Xu, W., Structure and function of the pp2a-shugoshin interaction, Molecular Cell, 35, 4, 426-441, (2009).
  • Kawashima, S. A., Yamagishi, Y., Honda, T., Lshiguro, K. I. and Watanabe, Y., Phosphorylation of h2a by bub1 prevents chromosomal instability through localizing shugoshin, Science, 327, 5962, 172-177, (2010).
  • Yahya, G. et al., Phospho-regulation of the shugoshin - condensin interaction at the centromere in budding yeast, PLOS Genetics, 16, 8, e1008569, (2020).
  • Indjeian, V. B., Stern, B. M. and Murray, A. W., The centromeric protein sgo1 is required to sense lack of tension on mitotic chromosomes, Science, 307, 5706, 130-133, (2005).
  • Kim, T. et al., Kinetochores accelerate or delay apc/c activation by directing cdc20 to opposing fates, Genes and Development, 31, 11, 1089-1094, (2017).
  • Levine, M. S. and Holland, A. J., The impact of mitotic errors on cell proliferation and tumorigenesis, Genes & Development, 32, 9-10, 620-638, (2018).
  • Garcia-Gimenez, J. L., Garces, C., Roma-Mateo, C. and Pallardo, F. V., Oxidative stress-mediated alterations in histone post-translational modifications, Free Radical Biology and Medicine, 170, 6-18, (2021).
  • Schmitz, M. L., Higgins, J. M. G. and Seibert, M., Priming chromatin for segregation: Functional roles of mitotic histone modifications, Cell Cycle, 19, 6, 625-641, (2020).
  • Singh, D., Nishi, K., Khambata, K. and Balasinor, N. H., Introduction to epigenetics: Basic concepts and advancements in the field in Tollefsbol, T., Epigenetics and reproductive health, Elsevier, 25-44, United Kingdom, (2020).
  • Ishiguro, T., Tanabe, K., Kobayashi, Y., Mizumoto, S., Kanai, M. and Kawashima, S. A., Malonylation of histone h2a at lysine 119 inhibits bub1-dependent h2a phosphorylation and chromosomal localization of shugoshin proteins, Scientific Reports, 8, 1, 1-10, (2018).
  • Tyagi, M., Imam, N., Verma, K. and Patel, A. K., Chromatin remodelers: We are the drivers!!, Nucleus, 7, 4, 388-404, (2016).
  • Min, S., Kim, K., Kim, S.-G., Cho, H. and Lee, Y., Chromatin-remodeling factor, rsf1, controls p53-mediated transcription in apoptosis upon DNA strand breaks, Cell Death & Disease, 9, 11, (2018).
  • Lee, H.-S. et al., The chromatin remodeler rsf1 controls centromeric histone modifications to coordinate chromosome segregation, Nature Communications, 9, 1, 3848-3848, (2018).
  • Cai, G., Yang, Q. and Sun, W., Rsf1 in cancer: Interactions and functions, Cancer Cell International, 21, 1, (2021).
  • Hargreaves, D. C. and Crabtree, G. R., Atp-dependent chromatin remodeling: Genetics, genomics and mechanisms, Cell Research, 21, 3, 396-420, (2011).
  • Hormozdiari, F. et al., The effect of insertions and deletions on wirings in protein-protein interaction networks: A large-scale study, Journal of Computational Biology, 16, 2, 159-167, (2009).
  • Wang, X., Gene mutation‐based and specific therapies in precision medicine, Journal of Cellular and Molecular Medicine, 20, 4, 577-580, (2016).
Toplam 56 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm Derleme Makalesi
Yazarlar

Begumhan Yılmaz Kardas 0000-0002-8446-1116

Serap Doğan 0000-0001-5684-3662

Yayımlanma Tarihi 8 Temmuz 2022
Gönderilme Tarihi 7 Nisan 2022
Yayımlandığı Sayı Yıl 2022 Cilt: 24 Sayı: 2

Kaynak Göster

APA Yılmaz Kardas, B., & Doğan, S. (2022). The effects of mutations on pericentromeric localization of shugoshin. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 24(2), 869-877.
AMA Yılmaz Kardas B, Doğan S. The effects of mutations on pericentromeric localization of shugoshin. BAUN Fen. Bil. Enst. Dergisi. Temmuz 2022;24(2):869-877.
Chicago Yılmaz Kardas, Begumhan, ve Serap Doğan. “The Effects of Mutations on Pericentromeric Localization of Shugoshin”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 24, sy. 2 (Temmuz 2022): 869-77.
EndNote Yılmaz Kardas B, Doğan S (01 Temmuz 2022) The effects of mutations on pericentromeric localization of shugoshin. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 24 2 869–877.
IEEE B. Yılmaz Kardas ve S. Doğan, “The effects of mutations on pericentromeric localization of shugoshin”, BAUN Fen. Bil. Enst. Dergisi, c. 24, sy. 2, ss. 869–877, 2022.
ISNAD Yılmaz Kardas, Begumhan - Doğan, Serap. “The Effects of Mutations on Pericentromeric Localization of Shugoshin”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 24/2 (Temmuz 2022), 869-877.
JAMA Yılmaz Kardas B, Doğan S. The effects of mutations on pericentromeric localization of shugoshin. BAUN Fen. Bil. Enst. Dergisi. 2022;24:869–877.
MLA Yılmaz Kardas, Begumhan ve Serap Doğan. “The Effects of Mutations on Pericentromeric Localization of Shugoshin”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi, c. 24, sy. 2, 2022, ss. 869-77.
Vancouver Yılmaz Kardas B, Doğan S. The effects of mutations on pericentromeric localization of shugoshin. BAUN Fen. Bil. Enst. Dergisi. 2022;24(2):869-77.