Determining the minimal amount of DMSO necessary to stabilize the Angiomotin lipid binding domain
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Published:
Jun 13, 2024
Keywords:
Amot, ACCH domain, Nuclear Magnetic Resonance, Dynamic Scanning Fluorescence, DMSO
Main Article Content
Abstract
Angiomotins (Amots) are a family of adaptor proteins with important roles in cell growth, migration, and proliferation. The Amot coiled-coil homology (ACCH) domain, has a high affinity for non-phosphorylated phosphatidylinositol and mono-phosphorylated phosphatidylinositol. This provides specificity in the membrane association. This membrane specificity is linked with the targeting and recycling of the membrane protein in order to maintain normal cell phenotypes and function. Therefore, we endeavored to understand the protein function by studying the atomic structure of the protein. Our laboratory looked to determine the structure using nuclear magnetic resonance (NMR), which requires higher protein concentrations than those possible in our current buffered solutions. Based on literature reported on other proteins, DMSO can be used as a stabilizing agent up to 33-70% DMSO. Higher concentrations have led DMSO to become a denaturing agent. Therefore, this work shows our preliminary findings for the minimal amount of dimethyl sulfoxide (DMSO) needed to stabilize the domain at higher concentrations without disrupting its native structure. To that end, we determined DMSO related changes in protein structure seen as shifts in the melting temperature that is determined by dynamic scanning fluorescence measurements. As a result, we found that the ACCH domain is denatured in solutions >10% DMSO.
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Araya, F. (2024). Determining the minimal amount of DMSO necessary to stabilize the Angiomotin lipid binding domain. IU Journal of Undergraduate Research, 8(1). https://doi.org/10.14434/iujur.v8i1.31200
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Natural Sciences
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References
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6. Lv, M., Li, S., Luo, C., Zhang, X., Shen, Y., Sui, Y., et al. (2016). Angiomotin Promotes Renal Epithelial and Carcinoma Cell Proliferation by Retaining the Nuclear Yap. Oncotarget, 7(11), 12393-12403.
7. Jiang, W., Watkins, G., Douglas-Jones, A., Holmgren, L., & Mansel, R. (2006). Angiomotin and Angiomotin Like Proteins, Their Expression and Correlation with Angiogenesis and Clinical Outcome in Human Breast Cancer. BMC Cancer, 6(1), 16.
8. Zhang, H., & Fan, Q. (2015). Microrna-205 Inhibits the Proliferation and Invasion of Breast Cancer by Regulating Amot Expression. Oncology reports, 34(4), 2163-2170.
9. Ranahan, W. P., Han, Z., Smith-Kinnaman, W., Nabinger, S. C., Heller, B., Herbert, B.-S., et al. (2011). The Adaptor Protein Amot Promotes the Proliferation of Mammary Epithelial Cells Via the Prolonged Activation of the Extracellular Signal-Regulated Kinases. Cancer Research, 71(6), 2203-2211.
10. Ruan, W., Wang, P., Feng, S., Xue, Y., & Li, Y. (2016). Long Non-Coding Rna Small Nucleolar Rna Host Gene 12 (Snhg12) Promotes Cell Proliferation and Migration by Upregulating Angiomotin Gene Expression in Human Osteosarcoma Cells. [journal article]. Tumor Biology, 37(3), 4065-4073.
11. Ruan, W.-D., Wang, P., Feng, S., Xue, Y., & Zhang, B. (2016). Microrna-497 Inhibits Cell Proliferation, Migration, and Invasion by Targeting Amot in Human Osteosarcoma Cells. OncoTargets and therapy, 9, 303-313.
12. Albrecht, L. V., Green, K. J., & Dubash, A. D. (2016). Cadherins in Cancer. In S. T. Suzuki & S. Hirano (Eds.), The Cadherin Superfamily: Key Regulators of Animal Development and Physiology (pp. 363-397). Tokyo: Springer Japan.
13. Hakami, F., Darda, L., Stafford, P., Woll, P., Lambert, D. W., & Hunter, K. D. (2014). The Roles of Hoxd10 in the Development and Progression of Head and Neck Squamous Cell Carcinoma (Hnscc). [Genetics and Genomics]. Br J Cancer, 111(4), 807-816.
14. Yi, C., Shen, Z., Stemmer-Rachamimov, A., Dawany, N., Troutman, S., Showe, L. C., et al. (2013). The P130 Isoform of Angiomotin Is Required for Yap-Mediated Hepatic Epithelial Cell Proliferation and Tumorigenesis. Science signaling, 6(291), ra77-ra77.
15. Wang, Y., Justilien, V., Brennan, K. I., Jamieson, L., Murray, N. R., & Fields, A. P. (2017). Pkc[Iota] Regulates Nuclear Yap1 Localization and Ovarian Cancer Tumorigenesis. [Original Article]. Oncogene, 36(4), 534-545.
16. Hsu, Y. L., Hung, J. Y., Chou, S. H., Huang, M. S., Tsai, M. J., Lin, Y. S., et al. (2015). Angiomotin Decreases Lung Cancer Progression by Sequestering Oncogenic Yap/Taz and Decreasing Cyr61 Expression. [Original Article]. Oncogene, 34(31), 4056-4068.
17. Ellmark, P., Ingvarsson, J., Carlsson, A., Lundin, B. S., Wingren, C., & Borrebaeck, C. a. K. (2006). Identification of Protein Expression Signatures Associated with Helicobacter Pylori Infection and Gastric Adenocarcinoma Using Recombinant Antibody Microarrays. Molecular & Cellular Proteomics, 5(9), 1638-1646.
18. Aase, K., Ernkvist, M., Ebarasi, L., Jakobsson, L., Majumdar, A., Yi, C., et al. (2007). Angiomotin Regulates Endothelial Cell Migration During Embryonic Angiogenesis. Genes & Development, 21(16), 2055-2068.
19. Chan, S. W., Lim, C. J., Chong, Y. F., Pobbati, A. V., Huang, C., & Hong, W. (2011). Hippo Pathway-Independent Restriction of Taz and Yap by Angiomotin. The Journal of Biological Chemistry, 286(9), 7018-7026.
20. Ernkvist, M., Aase, K., Ukomadu, C., Wohlschlegel, J., Blackman, R., Veitonmäki, N., et al. (2006). P130-Angiomotin Associates to Actin and Controls Endothelial Cell Shape. FEBS Journal, 273(9), 2000-2011.
21. Hirate, Y., Hirahara, S., Inoue, K.-I., Suzuki, A., Alarcon, Vernadeth b., Akimoto, K., et al. (2013). Polarity-Dependent Distribution of Angiomotin Localizes Hippo Signaling in Preimplantation Embryos. Current Biology, 23(13), 1181-1194.
22. Hirate, Y., & Sasaki, H. (2014). The Role of Angiomotin Phosphorylation in the Hippo Pathway During Preimplantation Mouse Development. Tissue Barriers, 2(1), e28127.
23. Levchenko, T., Veitonmäki, N., Lundkvist, A., Gerhardt, H., Ming, Y., Berggren, K., et al. (2008). Therapeutic Antibodies Targeting Angiomotin Inhibit Angiogenesis in Vivo. The FASEB Journal, 22(3), 880-889.
24. Mana-Capelli, S., Paramasivam, M., Dutta, S., & Mccollum, D. (2014). Angiomotins Link F-Actin Architecture to Hippo Pathway Signaling. Molecular Biology of the Cell, 25(10), 1676-1685.
25. Ortiz, A., Lee, Y.-C., Yu, G., Liu, H.-C., Lin, S.-C., Bilen, M. A., et al. (2015). Angiomotin Is a Novel Component of Cadherin-11/Β-Catenin/P120 Complex and Is Critical for Cadherin-11-Mediated Cell Migration. The FASEB Journal, 29(3), 1080-1091.
26. Shimono, A., & Behringer, R. R. (2003). Angiomotin Regulates Visceral Endoderm Movements During Mouse Embryogenesis Current Biology, 13(7), 613-617
27. Sugihara-Mizuno, Y., Adachi, M., Kobayashi, Y., Hamazaki, Y., Nishimura, M., Imai, T., et al. (2007). Molecular Characterization of Angiomotin/Jeap Family Proteins: Interaction with Mupp1/Patj and Their Endogenous Properties. Genes to Cells, 12(4), 473-486.
28. Wang, W., Huang, J., & Chen, J. (2011). Angiomotin-Like Proteins Associate with and Negatively Regulate Yap1. Journal of Biological Chemistry, 286(6), 4364-4370.
29. Zhao, B., Li, L., Lu, Q., Wang, L. H., Liu, C.-Y., Lei, Q., et al. (2011). Angiomotin Is a Novel Hippo Pathway Component That Inhibits Yap Oncoprotein. Genes & Development, 25(1), 51-63.
30. Zheng, Y., Vertuani, S., Nyström, S., Audebert, S., Meijer, I., Tegnebratt, T., et al. (2009). Angiomotin-Like Protein 1 Controls Endothelial Polarity and Junction Stability During Sprouting Angiogenesis. Circulation Research, 105(3), 260-270.
31. Heller, B., Adu-Gyamfi, E., Smith-Kinnaman, W., Babbey, C., Vora, M., Xue, Y., et al. (2010). Amot Recognizes a Juxtanuclear Endocytic Recycling Compartment Via a Novel Lipid Binding Domain. Journal of Biological Chemistry, 285(16), 12308-12320.
32. Kimble-Hill, A. C., Petrache, H. I., Seifert, S., & Firestone, M. A. (2018). Reorganization of Ternary Lipid Mixtures of Non-Phosphorylated Phosphatidylinositol Interacting with Angiomotin. The Journal of Physical Chemistry B.
33. Hall, L. C., Donovan, E., Araya, M., Idowa, E., Jiminez-Segovia, I., Folck, A., et al. (2019). Identification of Specific Lysines and Arginines That Mediate Angiomotin Membrane Association. ACS Omega, 4(4), 6726-6736.
34. Sterling, H. J., Prell, J. S., Cassou, C. A., & Williams, E. R. (2011). Protein Conformation and Supercharging with Dmso from Aqueous Solution. Journal of the American Society for Mass Spectrometry, 22(7).
35. Ghosh, S., Chattoraj, S., Chowdhury, R., & Bhattacharyya, K. (2014). Structure and Dynamics of Lysozyme in Dmso–Water Binary Mixture: Fluorescence Correlation Spectroscopy. [10.1039/C4RA00719K]. RSC Advances, 4(28), 14378-14384.
36. Jackson, M., & Mantsch, H. H. (1991). Beware of Proteins in Dmso. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1078(2), 231-235.
37. Zhang, G., Babenko, V., Dzwolak, W., & Keiderling, T. A. (2015). Dimethyl Sulfoxide Induced Destabilization and Disassembly of Various Structural Variants of Insulin Fibrils Monitored by Vibrational Circular Dichroism. Biochemistry, 54(49), 7193-7202.
38. Arnau, J., Lauritzen, C., Petersen, G. E., & Pedersen, J. (2006). Current Strategies for the Use of Affinity Tags and Tag Removal for the Purification of Recombinant Proteins. Protein Expression and Purification, 48(1), 1-13.
39. Terpe, K. (2003). Overview of Tag Protein Fusions: From Molecular and Biochemical Fundamentals to Commercial Systems. Applied Microbiology and Biotechnology, 60(5), 523-533.
40. Niesen, F. H., Berglund, H., & Vedadi, M. (2007). The Use of Differential Scanning Fluorimetry to Detect Ligand Interactions That Promote Protein Stability. [10.1038/nprot.2007.321]. Nat. Protocols, 2(9), 2212-2221.
41. Steinberg, T. H., Lauber, W. M., Berggren, K., Kemper, C., Yue, S., & Patton, W. F. (2000). Fluorescence Detection of Proteins in Sodium Dodecyl Sulfate-Polyacrylamide Gels Using Environmentally Benign, Nonfixative, Saline Solution. ELECTROPHORESIS, 21(3), 497-508.
42. Maheshwari, A. S., & Archunan, G. (2013). Mutational Effect of Structural Parameters on Coiled-Coil Stability of Proteins. Proteomics Insights, 6, PRI.S10988.
43. Alexandrov, A. I., Mileni, M., Chien, E. Y. T., Hanson, M. A., & Stevens, R. C. (2008). Microscale Fluorescent Thermal Stability Assay for Membrane Proteins. Structure, 16(3), 351-359.
44. Yip, K. S., Stillman, T. J., Britton, K. L., Artymiuk, P. J., Baker, P. J., Sedelnikova, S. E., et al. (1995). The Structure of Pyrococcus Furiosus Glutamate Dehydrogenase Reveals a Key Role for Ion-Pair Networks in Maintaining Enzyme Stability at Extreme Temperatures. Structure, 3(11), 1147-1158.
45. Yip, K. S., Britton, K. L., Stillman, T. J., Lebbink, J., De Vos, W. M., Robb, F. T., et al. (1998). Insights into the Molecular Basis of Thermal Stability from the Analysis of Ion-Pair Networks in the Glutamate Dehydrogenase Family. Eur J Biochem, 255(2), 336-346.
46. Yu, Y., Monera, O. D., Hodges, R. S., & Privalov, P. L. (1996). Ion Pairs Significantly Stabilize Coiled-Coils in the Absence of Electrolyte. J Mol Biol, 255(3), 367-372.
47. Xu, C., Joss, L., Wang, C., Pechar, M., & Kopeček, J. (2002). The Influence of Fusion Sequences on the Thermal Stabilities of Coiled-Coil Proteins. Macromolecular Bioscience, 2(8), 395-401.
48. Vogt, G., & Argos, P. (1997). Protein Thermal Stability: Hydrogen Bonds or Internal Packing? Fold Des, 2(4), S40-46.
49. Arakawa, T., Kita, Y., & Timasheff, S. N. (2007). Protein Precipitation and Denaturation by Dimethyl Sulfoxide. Biophys Chem, 131(1-3), 62-70.
50. Voets, I. K., Cruz, W. A., Moitzi, C., Lindner, P., Arêas, E. P. G., & Schurtenberger, P. (2010). Dmso-Induced Denaturation of Hen Egg White Lysozyme. The Journal of Physical Chemistry B, 114(36), 11875-11883.
2. Siegel, R. L., Miller, K. D., & Jemal, A. (2017). Cancer Statistics, 2017. CA: A Cancer Journal for Clinicians, 67(1), 7-30.
3. Ernkvist, M., Birot, O., Sinha, I., Veitonmaki, N., Nyström, S., Aase, K., et al. (2008). Differential Roles of P80- and P130-Angiomotin in the Switch between Migration and Stabilization of Endothelial Cells. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1783(3), 429-437.
4. Aase, K., Ernkvist, M., Ebarasi, L., Jakobsson, L., Majumdar, A., Yi, C., et al. (2007). Angiomotin Regulates Endothelial Cell Migration During Embryonic Angiogenesis. Genes & Development, 21(16), 2055-2068.
5. Lv, M., Shen, Y., Yang, J., Li, S., Wang, B., Chen, Z., et al. (2017). Angiomotin Family Members: Oncogenes or Tumor Suppressors? International Journal of Biological Sciences, 13(6), 772-781.
6. Lv, M., Li, S., Luo, C., Zhang, X., Shen, Y., Sui, Y., et al. (2016). Angiomotin Promotes Renal Epithelial and Carcinoma Cell Proliferation by Retaining the Nuclear Yap. Oncotarget, 7(11), 12393-12403.
7. Jiang, W., Watkins, G., Douglas-Jones, A., Holmgren, L., & Mansel, R. (2006). Angiomotin and Angiomotin Like Proteins, Their Expression and Correlation with Angiogenesis and Clinical Outcome in Human Breast Cancer. BMC Cancer, 6(1), 16.
8. Zhang, H., & Fan, Q. (2015). Microrna-205 Inhibits the Proliferation and Invasion of Breast Cancer by Regulating Amot Expression. Oncology reports, 34(4), 2163-2170.
9. Ranahan, W. P., Han, Z., Smith-Kinnaman, W., Nabinger, S. C., Heller, B., Herbert, B.-S., et al. (2011). The Adaptor Protein Amot Promotes the Proliferation of Mammary Epithelial Cells Via the Prolonged Activation of the Extracellular Signal-Regulated Kinases. Cancer Research, 71(6), 2203-2211.
10. Ruan, W., Wang, P., Feng, S., Xue, Y., & Li, Y. (2016). Long Non-Coding Rna Small Nucleolar Rna Host Gene 12 (Snhg12) Promotes Cell Proliferation and Migration by Upregulating Angiomotin Gene Expression in Human Osteosarcoma Cells. [journal article]. Tumor Biology, 37(3), 4065-4073.
11. Ruan, W.-D., Wang, P., Feng, S., Xue, Y., & Zhang, B. (2016). Microrna-497 Inhibits Cell Proliferation, Migration, and Invasion by Targeting Amot in Human Osteosarcoma Cells. OncoTargets and therapy, 9, 303-313.
12. Albrecht, L. V., Green, K. J., & Dubash, A. D. (2016). Cadherins in Cancer. In S. T. Suzuki & S. Hirano (Eds.), The Cadherin Superfamily: Key Regulators of Animal Development and Physiology (pp. 363-397). Tokyo: Springer Japan.
13. Hakami, F., Darda, L., Stafford, P., Woll, P., Lambert, D. W., & Hunter, K. D. (2014). The Roles of Hoxd10 in the Development and Progression of Head and Neck Squamous Cell Carcinoma (Hnscc). [Genetics and Genomics]. Br J Cancer, 111(4), 807-816.
14. Yi, C., Shen, Z., Stemmer-Rachamimov, A., Dawany, N., Troutman, S., Showe, L. C., et al. (2013). The P130 Isoform of Angiomotin Is Required for Yap-Mediated Hepatic Epithelial Cell Proliferation and Tumorigenesis. Science signaling, 6(291), ra77-ra77.
15. Wang, Y., Justilien, V., Brennan, K. I., Jamieson, L., Murray, N. R., & Fields, A. P. (2017). Pkc[Iota] Regulates Nuclear Yap1 Localization and Ovarian Cancer Tumorigenesis. [Original Article]. Oncogene, 36(4), 534-545.
16. Hsu, Y. L., Hung, J. Y., Chou, S. H., Huang, M. S., Tsai, M. J., Lin, Y. S., et al. (2015). Angiomotin Decreases Lung Cancer Progression by Sequestering Oncogenic Yap/Taz and Decreasing Cyr61 Expression. [Original Article]. Oncogene, 34(31), 4056-4068.
17. Ellmark, P., Ingvarsson, J., Carlsson, A., Lundin, B. S., Wingren, C., & Borrebaeck, C. a. K. (2006). Identification of Protein Expression Signatures Associated with Helicobacter Pylori Infection and Gastric Adenocarcinoma Using Recombinant Antibody Microarrays. Molecular & Cellular Proteomics, 5(9), 1638-1646.
18. Aase, K., Ernkvist, M., Ebarasi, L., Jakobsson, L., Majumdar, A., Yi, C., et al. (2007). Angiomotin Regulates Endothelial Cell Migration During Embryonic Angiogenesis. Genes & Development, 21(16), 2055-2068.
19. Chan, S. W., Lim, C. J., Chong, Y. F., Pobbati, A. V., Huang, C., & Hong, W. (2011). Hippo Pathway-Independent Restriction of Taz and Yap by Angiomotin. The Journal of Biological Chemistry, 286(9), 7018-7026.
20. Ernkvist, M., Aase, K., Ukomadu, C., Wohlschlegel, J., Blackman, R., Veitonmäki, N., et al. (2006). P130-Angiomotin Associates to Actin and Controls Endothelial Cell Shape. FEBS Journal, 273(9), 2000-2011.
21. Hirate, Y., Hirahara, S., Inoue, K.-I., Suzuki, A., Alarcon, Vernadeth b., Akimoto, K., et al. (2013). Polarity-Dependent Distribution of Angiomotin Localizes Hippo Signaling in Preimplantation Embryos. Current Biology, 23(13), 1181-1194.
22. Hirate, Y., & Sasaki, H. (2014). The Role of Angiomotin Phosphorylation in the Hippo Pathway During Preimplantation Mouse Development. Tissue Barriers, 2(1), e28127.
23. Levchenko, T., Veitonmäki, N., Lundkvist, A., Gerhardt, H., Ming, Y., Berggren, K., et al. (2008). Therapeutic Antibodies Targeting Angiomotin Inhibit Angiogenesis in Vivo. The FASEB Journal, 22(3), 880-889.
24. Mana-Capelli, S., Paramasivam, M., Dutta, S., & Mccollum, D. (2014). Angiomotins Link F-Actin Architecture to Hippo Pathway Signaling. Molecular Biology of the Cell, 25(10), 1676-1685.
25. Ortiz, A., Lee, Y.-C., Yu, G., Liu, H.-C., Lin, S.-C., Bilen, M. A., et al. (2015). Angiomotin Is a Novel Component of Cadherin-11/Β-Catenin/P120 Complex and Is Critical for Cadherin-11-Mediated Cell Migration. The FASEB Journal, 29(3), 1080-1091.
26. Shimono, A., & Behringer, R. R. (2003). Angiomotin Regulates Visceral Endoderm Movements During Mouse Embryogenesis Current Biology, 13(7), 613-617
27. Sugihara-Mizuno, Y., Adachi, M., Kobayashi, Y., Hamazaki, Y., Nishimura, M., Imai, T., et al. (2007). Molecular Characterization of Angiomotin/Jeap Family Proteins: Interaction with Mupp1/Patj and Their Endogenous Properties. Genes to Cells, 12(4), 473-486.
28. Wang, W., Huang, J., & Chen, J. (2011). Angiomotin-Like Proteins Associate with and Negatively Regulate Yap1. Journal of Biological Chemistry, 286(6), 4364-4370.
29. Zhao, B., Li, L., Lu, Q., Wang, L. H., Liu, C.-Y., Lei, Q., et al. (2011). Angiomotin Is a Novel Hippo Pathway Component That Inhibits Yap Oncoprotein. Genes & Development, 25(1), 51-63.
30. Zheng, Y., Vertuani, S., Nyström, S., Audebert, S., Meijer, I., Tegnebratt, T., et al. (2009). Angiomotin-Like Protein 1 Controls Endothelial Polarity and Junction Stability During Sprouting Angiogenesis. Circulation Research, 105(3), 260-270.
31. Heller, B., Adu-Gyamfi, E., Smith-Kinnaman, W., Babbey, C., Vora, M., Xue, Y., et al. (2010). Amot Recognizes a Juxtanuclear Endocytic Recycling Compartment Via a Novel Lipid Binding Domain. Journal of Biological Chemistry, 285(16), 12308-12320.
32. Kimble-Hill, A. C., Petrache, H. I., Seifert, S., & Firestone, M. A. (2018). Reorganization of Ternary Lipid Mixtures of Non-Phosphorylated Phosphatidylinositol Interacting with Angiomotin. The Journal of Physical Chemistry B.
33. Hall, L. C., Donovan, E., Araya, M., Idowa, E., Jiminez-Segovia, I., Folck, A., et al. (2019). Identification of Specific Lysines and Arginines That Mediate Angiomotin Membrane Association. ACS Omega, 4(4), 6726-6736.
34. Sterling, H. J., Prell, J. S., Cassou, C. A., & Williams, E. R. (2011). Protein Conformation and Supercharging with Dmso from Aqueous Solution. Journal of the American Society for Mass Spectrometry, 22(7).
35. Ghosh, S., Chattoraj, S., Chowdhury, R., & Bhattacharyya, K. (2014). Structure and Dynamics of Lysozyme in Dmso–Water Binary Mixture: Fluorescence Correlation Spectroscopy. [10.1039/C4RA00719K]. RSC Advances, 4(28), 14378-14384.
36. Jackson, M., & Mantsch, H. H. (1991). Beware of Proteins in Dmso. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1078(2), 231-235.
37. Zhang, G., Babenko, V., Dzwolak, W., & Keiderling, T. A. (2015). Dimethyl Sulfoxide Induced Destabilization and Disassembly of Various Structural Variants of Insulin Fibrils Monitored by Vibrational Circular Dichroism. Biochemistry, 54(49), 7193-7202.
38. Arnau, J., Lauritzen, C., Petersen, G. E., & Pedersen, J. (2006). Current Strategies for the Use of Affinity Tags and Tag Removal for the Purification of Recombinant Proteins. Protein Expression and Purification, 48(1), 1-13.
39. Terpe, K. (2003). Overview of Tag Protein Fusions: From Molecular and Biochemical Fundamentals to Commercial Systems. Applied Microbiology and Biotechnology, 60(5), 523-533.
40. Niesen, F. H., Berglund, H., & Vedadi, M. (2007). The Use of Differential Scanning Fluorimetry to Detect Ligand Interactions That Promote Protein Stability. [10.1038/nprot.2007.321]. Nat. Protocols, 2(9), 2212-2221.
41. Steinberg, T. H., Lauber, W. M., Berggren, K., Kemper, C., Yue, S., & Patton, W. F. (2000). Fluorescence Detection of Proteins in Sodium Dodecyl Sulfate-Polyacrylamide Gels Using Environmentally Benign, Nonfixative, Saline Solution. ELECTROPHORESIS, 21(3), 497-508.
42. Maheshwari, A. S., & Archunan, G. (2013). Mutational Effect of Structural Parameters on Coiled-Coil Stability of Proteins. Proteomics Insights, 6, PRI.S10988.
43. Alexandrov, A. I., Mileni, M., Chien, E. Y. T., Hanson, M. A., & Stevens, R. C. (2008). Microscale Fluorescent Thermal Stability Assay for Membrane Proteins. Structure, 16(3), 351-359.
44. Yip, K. S., Stillman, T. J., Britton, K. L., Artymiuk, P. J., Baker, P. J., Sedelnikova, S. E., et al. (1995). The Structure of Pyrococcus Furiosus Glutamate Dehydrogenase Reveals a Key Role for Ion-Pair Networks in Maintaining Enzyme Stability at Extreme Temperatures. Structure, 3(11), 1147-1158.
45. Yip, K. S., Britton, K. L., Stillman, T. J., Lebbink, J., De Vos, W. M., Robb, F. T., et al. (1998). Insights into the Molecular Basis of Thermal Stability from the Analysis of Ion-Pair Networks in the Glutamate Dehydrogenase Family. Eur J Biochem, 255(2), 336-346.
46. Yu, Y., Monera, O. D., Hodges, R. S., & Privalov, P. L. (1996). Ion Pairs Significantly Stabilize Coiled-Coils in the Absence of Electrolyte. J Mol Biol, 255(3), 367-372.
47. Xu, C., Joss, L., Wang, C., Pechar, M., & Kopeček, J. (2002). The Influence of Fusion Sequences on the Thermal Stabilities of Coiled-Coil Proteins. Macromolecular Bioscience, 2(8), 395-401.
48. Vogt, G., & Argos, P. (1997). Protein Thermal Stability: Hydrogen Bonds or Internal Packing? Fold Des, 2(4), S40-46.
49. Arakawa, T., Kita, Y., & Timasheff, S. N. (2007). Protein Precipitation and Denaturation by Dimethyl Sulfoxide. Biophys Chem, 131(1-3), 62-70.
50. Voets, I. K., Cruz, W. A., Moitzi, C., Lindner, P., Arêas, E. P. G., & Schurtenberger, P. (2010). Dmso-Induced Denaturation of Hen Egg White Lysozyme. The Journal of Physical Chemistry B, 114(36), 11875-11883.