181
Views
11
CrossRef citations to date
0
Altmetric
Research Article

Estimation of pH effect on the structure and stability of kinase domain of human integrin-linked kinase

, , , , , & ORCID Icon show all
Pages 156-165 | Received 28 Nov 2017, Accepted 13 Dec 2017, Published online: 07 Jan 2018

References

  • Ahmed, A. U., Yim, H. C., Alorro, M., Ernst, M., & Williams, B. R. (2017). Integrin-linked kinase expression in myeloid cells promotes inflammatory signaling during experimental colitis. The Journal of Immunology, 199, 2128–2139.10.4049/jimmunol.1700125
  • Amith, S. R., Wilkinson, J. M., & Fliegel, L. (2016). Na+/H+ exchanger NHE1 regulation modulates metastatic potential and epithelial-mesenchymal transition of triple-negative breast cancer cells. Oncotarget, 7, 21091–21113.10.18632/oncotarget.v7i16
  • Biovia, D. S. (2013). Discovery Studio Modeling Environment. San Diego, CA: Dassault Systèmes.
  • Chang, L.-H., Pan, S.-L., Lai, C.-Y., Tsai, A.-C., & Teng, C.-M. (2013). Activated PAR-2 regulates pancreatic cancer progression through ILK/HIF-α–induced TGF-α expression and MEK/VEGF-A–mediated angiogenesis. The American Journal of Pathology, 183, 566–575.10.1016/j.ajpath.2013.04.022
  • Chiswell, B. P., Zhang, R., Murphy, J. W., Boggon, T. J., & Calderwood, D. A. (2008). The structural basis of integrin-linked kinase–PINCH interactions. Proceedings of the National Academy of Sciences, 105, 20677–20682.10.1073/pnas.0811415106
  • Edelhoch, H. (1967). Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry, 6, 1948–1954.10.1021/bi00859a010
  • Fuchs, B. C., Fujii, T., Dorfman, J. D., Goodwin, J. M., Zhu, A. X., Lanuti, M., & Tanabe, K. K. (2008). Epithelial-to-mesenchymal transition and integrin-linked kinase mediate sensitivity to epidermal growth factor receptor inhibition in human hepatoma cells. Cancer Research, 68, 2391–2399.10.1158/0008-5472.CAN-07-2460
  • Fukuda, K., Gupta, S., Chen, K., Wu, C., & Qin, J. (2009). The pseudoactive site of ILK is essential for its binding to α-parvin and localization to focal adhesions. Molecular Cell, 36, 819–830.10.1016/j.molcel.2009.11.028
  • Fukuda, K., Knight, J. D., Piszczek, G., Kothary, R., & Qin, J. (2011). Biochemical, proteomic, structural, and thermodynamic characterizations of integrin-linked kinase (ILK) cross-validation of the pseudokinase. Journal of Biological Chemistry, 286, 21886–21895.10.1074/jbc.M111.240093
  • Ghisaidoobe, A. B., & Chung, S. J. (2014). Intrinsic tryptophan fluorescence in the detection and analysis of proteins: A focus on förster resonance energy transfer techniques. International Journal of Molecular Sciences, 15, 22518–22538.10.3390/ijms151222518
  • Greenfield, N. J. (2006). Using circular dichroism spectra to estimate protein secondary structure. Nature protocols, 1, 2876–2890.
  • Greenfield, N. J. (2015). Circular dichroism (CD) analyses of protein–protein interactions. Protein–Protein Interactions: Methods and Applications, 239–265.
  • Gross, S., Rahal, R., Stransky, N., Lengauer, C., & Hoeflich, K. P. (2015). Targeting cancer with kinase inhibitors. The Journal of clinical investigation, 125, 1780–1789.10.1172/JCI76094
  • Hannigan, G. E., Coles, J. G., & Dedhar, S. (2007). Integrin-linked kinase at the heart of cardiac contractility, repair, and disease. Circulation Research, 100, 1408–1414.10.1161/01.RES.0000265233.40455.62
  • Hannigan, G., McDonald, P., Walsh, M., & Dedhar, S. (2011). Integrin-linked kinase: Not so ‘pseudo’ after all. Oncogene, 30, 4375–4385.10.1038/onc.2011.177
  • Hannigan, G., Troussard, A. A., & Dedhar, S. (2005). Integrin-linked kinase: A cancer therapeutic target unique among its ILK. Nature Reviews Cancer, 5, 51–63.10.1038/nrc1524
  • Hassan, M. I., Naeem, A., Khan, K. A., Khan, R. H., Singh, S., Singh, T. P., & Yadav, S. (2012). Protective effect of prolactin induced protein on zinc? 2-glycoprotein against various denaturants. Journal of Proteins & Proteomics, 3, 105–111.
  • Hoda, N., Naz, H., Jameel, E., Shandilya, A., Dey, S., Hassan, M. I., … Jayaram, B. (2016). Curcumin specifically binds to the human calcium-calmodulin-dependent protein kinase IV: Fluorescence and molecular dynamics simulation studies. Journal of Biomolecular Structure and Dynamics, 34, 572–584. doi:10.1080/07391102.2015.1046934
  • Hospes, M., Hendriks, J., & Hellingwerf, K. J. (2013). Tryptophan fluorescence as a reporter for structural changes in photoactive yellow protein elicited by photo-activation. Photochemical & Photobiological Sciences, 12, 479–488.10.1039/C2PP25222H
  • Huang, J., & MacKerell, A. D., Jr (2013). CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34, 2135–2145. doi:10.1002/jcc.23354
  • Idrees, D., Prakash, A., Haque, M. A., Islam, A., Ahmad, F., & Hassan, M. I. (2016a). Spectroscopic and MD simulation studies on unfolding processes of mitochondrial carbonic anhydrase VA induced by urea. Journal of Biomolecular Structure and Dynamics, 34, 1987–1997. doi:10.1080/07391102.2015.1100552
  • Idrees, D., Prakash, A., Haque, M. A., Islam, A., Hassan, M. I., & Ahmad, F. (2016b). GdnHCl-induced unfolding intermediate in the mitochondrial carbonic anhydrase VA. International Journal of Biological Macromolecules, 91, 1151–1160. doi:10.1016/j.ijbiomac.2016.06.080 S0141-8130(16)30631-6 [pii]
  • Idrees, D., Rahman, S., Shahbaaz, M., Haque, M. A., Islam, A., Ahmad, F., & Hassan, M. I. (2017). Estimation of thermodynamic stability of human carbonic anhydrase IX from urea-induced denaturation and MD simulation studies. International Journal of Biological Macromolecules, 105, 183–189. doi:10.1016/j.ijbiomac.2017.07.010 S0141-8130(17)31526-X [pii].
  • Idrees, D., Shahbaaz, M., Bisetty, K., Islam, A., Ahmad, F., & Hassan, M. I. (2017). Effect of pH on structure, function, and stability of mitochondrial carbonic anhydrase VA. Journal of Biomolecular Structure and Dynamics, 35, 449–461. doi:10.1080/07391102.2016.1149097
  • Juszczak, L. J., & Eisenberg, A. S. (2017). The color of cation–π interactions: Subtleties of amine-tryptophan interaction energetics allow for radical-like visible absorbance and fluorescence. Journal of the American Chemical Society, 139, 8302–8311.
  • Khajah, M. A., Mathew, P. M., Alam-Eldin, N. S., & Luqmani, Y. A. (2015). Bleb formation is induced by alkaline but not acidic pH in estrogen receptor silenced breast cancer cells. International Journal of Oncology, 46, 1685–1698.10.3892/ijo.2015.2884
  • Khan, F. I., Aamir, M., Wei, D. Q., Ahmad, F., & Hassan, M. I. (2017). Molecular mechanism of Ras-related protein Rab-5A and effect of mutations in the catalytically active phosphate-binding loop. Journal of Biomolecular Structure and Dynamics, 35, 105–118. doi:10.1080/07391102.2015.1134346
  • Khan, P., Parkash, A., Islam, A., Ahmad, F., & Hassan, M. I. (2016). Molecular basis of the structural stability of hemochromatosis factor E: A combined molecular dynamic simulation and GdmCl-induced denaturation study. Biopolymers, 105, 133–142. doi:10.1002/bip.22760
  • Khan, P., Prakash, A., Haque, M. A., Islam, A., Hassan, M. I., & Ahmad, F. (2016). Structural basis of urea-induced unfolding: Unraveling the folding pathway of hemochromatosis factor E. International Journal of Biological Macromolecules, 91, 1051–1061. doi:10.1016/j.ijbiomac.2016.06.055 S0141-8130(16)30593-1 [pii].
  • Khan, F. I., Shahbaaz, M., Bisetty, K., Waheed, A., Sly, W. S., Ahmad, F., & Hassan, M. I. (2016). Large scale analysis of the mutational landscape in beta-glucuronidase: A major player of mucopolysaccharidosis type VII. Gene, 576, 36–44. doi:10.1016/j.gene.2015.09.062 S0378-1119(15)01171-3 [pii].
  • Khan, P., Shandilya, A., Jayaram, B., Islam, A., Ahmad, F., & Hassan, M. I. (2017). Effect of pH on the stability of hemochromatosis factor E: A combined spectroscopic and molecular dynamics simulation-based study. Journal of Biomolecular Structure and Dynamics, 35, 1582–1598. doi:10.1080/07391102.2016.1189359
  • Khan, F. I., Wei, D. Q., Gu, K. R., Hassan, M. I., & Tabrez, S. (2016). Current updates on computer aided protein modeling and designing. International Journal of Biological Macromolecules, 85, 48–62. doi:10.1016/j.ijbiomac.2015.12.072 S0141-8130(15)30260-9 [pii].
  • Legate, K. R., Montañez, E., Kudlacek, O., & Füssler, R. (2005). ILK, PINCH and parvin: The tIPP of integrin signalling. Nature Reviews Molecular Cell Biology, 7, nrm1789.
  • Legate, K. R., Montañez, E., Kudlacek, O., & Füssler, R. (2006). ILK, PINCH and parvin: The tIPP of integrin signalling. Nature Reviews Molecular Cell Biology, 7, 20–31.10.1038/nrm1789
  • Naiyer, A., Hassan, M. I., Islam, A., Sundd, M., & Ahmad, F. (2015). Structural characterization of MG and pre-MG states of proteins by MD simulations, NMR, and other techniques. Journal of Biomolecular Structure and Dynamics, 33, 2267–2284. doi:10.1080/07391102.2014.999354
  • Naz, F., Anjum, F., Islam, A., Ahmad, F., & Hassan, M. I. (2013). Microtubule affinity-regulating kinase 4: Structure, function, and regulation. Cell Biochemistry and Biophysics, 67, 485–499. doi:10.1007/s12013-013-9550-7
  • Naz, H., Islam, A., Ahmad, F., & Hassan, M. I. (2016). Calcium/calmodulin-dependent protein kinase IV: A multifunctional enzyme and potential therapeutic target. Progress in Biophysics and Molecular Biology, 121, 54–65. doi:10.1016/j.pbiomolbio.2015.12.016 S0079-6107(15)30001-8 [pii].
  • Naz, H., Jameel, E., Hoda, N., Shandilya, A., Khan, P., Islam, A., … Hassan, M. I. (2016). Structure guided design of potential inhibitors of human calcium-calmodulin dependent protein kinase IV containing pyrimidine scaffold. Bioorganic & Medicinal Chemistry Letters, 26, 782–788. doi:10.1016/j.bmcl.2015.12.098 S0960-894X(15)30411-X [pii].
  • Naz, F., Khan, F. I., Mohammad, T., Khan, P., Manzoor, S., Hasan, G. M., … Hassan, M. I. (2017). Investigation of molecular mechanism of recognition between citral and MARK4: A newer therapeutic approach to attenuate cancer cell progression. International Journal of Biological Macromolecules, 107, 2580–2589. doi:10.1016/j.ijbiomac.2017.10.143 S0141-8130(17)33729-7 [pii].
  • Naz, F., Shahbaaz, M., Bisetty, K., Islam, A., Ahmad, F., & Hassan, M. I. (2015). designing new kinase inhibitor derivatives as therapeutics against common complex diseases: Structural basis of microtubule affinity-regulating kinase 4 (MARK4) inhibition. OMICS: A Journal of Integrative Biology, 19, 700–711. doi:10.1089/omi.2015.0111
  • Naz, H., Shahbaaz, M., Bisetty, K., Islam, A., Ahmad, F., & Hassan, M. I. (2016). Effect of pH on the structure, function, and stability of human calcium/calmodulin-dependent protein kinase IV: Combined spectroscopic and MD simulation studies. Biochemistry and Cell Biology, 94, 221–228. doi:10.1139/bcb-2015-0132
  • Naz, H., Shahbaaz, M., Haque, M. A., Bisetty, K., Islam, A., Ahmad, F., & Hassan, M. I. (2017). Urea-induced denaturation of human calcium/calmodulin-dependent protein kinase IV: A combined spectroscopic and MD simulation studies. Journal of Biomolecular Structure and Dynamics, 35, 463–475. doi:10.1080/07391102.2016.1150203
  • Nikolopoulos, S. N., & Turner, C. E. (2001). Integrin-linked Kinase (ILK) binding to paxillin LD1 Motif regulates ILK localization to focal adhesions. Journal of Biological Chemistry, 276, 23499–23505.10.1074/jbc.M102163200
  • Nikolopoulos, S. N., & Turner, C. E. (2002). Molecular dissection of actopaxin-integrin-linked kinase–paxillin interactions and their role in subcellular localization. Journal of Biological Chemistry, 277, 1568–1575.10.1074/jbc.M108612200
  • Onufriev, A. V., & Alexov, E. (2013). Protonation and pK changes in protein–ligand binding. Quarterly Reviews of Biophysics, 46, 181–209.10.1017/S0033583513000024
  • Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., & Gray, T. (1995). How to measure and predict the molar absorption coefficient of a protein. Protein Science, 4, 2411–2423.10.1002/pro.v4:11
  • Park, K., Perczel, A., & Fasman, G. D. (1992). Differentiation between transmembrane helices and peripheral helices by the deconvolution of circular dichroism spectra of membrane proteins. Protein Science, 1, 1032–1049.10.1002/pro.v1:8
  • Perez-Iratxeta, C., & Andrade-Navarro, M. A. (2008). K2D2: Estimation of protein secondary structure from circular dichroism spectra. BMC Structural Biology, 8, 25.10.1186/1472-6807-8-25
  • Persad, S., & Dedhar, S. (2003). The role of integrin-linked kinase (ILK) in cancer progression. Cancer and Metastasis Reviews, 22, 375–384.10.1023/A:1023777013659
  • Prakash, A., Idrees, D., Haque, M. A., Islam, A., Ahmad, F., & Hassan, M. I. (2017). GdmCl-induced unfolding studies of human carbonic anhydrase IX: A combined spectroscopic and MD simulation approach. Journal of Biomolecular Structure and Dynamics, 35, 1295–1306. doi:10.1080/07391102.2016.1179596
  • Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854. doi:10.1093/bioinformatics/btt055 btt055 [pii].
  • Reshkin, S. J., Bellizzi, A., Caldeira, S., Albarani, V., Malanchi, I., Poignee, M., … Tommasino, M. (2000). Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. The FASEB Journal, 14, 2185–2197.10.1096/fj.00-0029com
  • Shahbaaz, M., Bisetty, K., Ahmad, F., & Hassan, M. I. (2015). Towards new drug targets? Function prediction of putative proteins of neisseria meningitidis MC58 and their virulence characterization. OMICS: A Journal of Integrative Biology, 19, 416–434. doi:10.1089/omi.2015.0032
  • Sharma, A., & Schulman, S. G. (1999). Introduction to fluorescence spectroscopy. Hoboken, NJ: Wiley-interscience.
  • Shirmanova, M. V., Druzhkova, I. N., Lukina, M. M., Dudenkova, V. V., Ignatova, N. I., Snopova, L. B., … Zagaynova, E. V. (2017). Chemotherapy with cisplatin: Insights into intracellular pH and metabolic landscape of cancer cells in vitro and in vivo. Scientific Reports, 7, 8911.10.1038/s41598-017-09426-4
  • Stiegler, A. L., Draheim, K. M., Li, X., Chayen, N. E., Calderwood, D. A., & Boggon, T. J. (2012). Structural basis for paxillin binding and focal adhesion targeting of β-parvin. Journal of Biological Chemistry, 287, 32566–32577.10.1074/jbc.M112.367342
  • Talley, K., & Alexov, E. (2010). On the pH-optimum of activity and stability of proteins. Proteins, 78, 2699–2706. doi:10.1002/prot.22786
  • Ulmschneider, B., Grillo-Hill, B. K., Benitez, M., Azimova, D. R., Barber, D. L., & Nystul, T. G. (2016). Increased intracellular pH is necessary for adult epithelial and embryonic stem cell differentiation. The Journal of Cell Biology, 215, 345–355.10.1083/jcb.201606042
  • Vivian, J. T., & Callis, P. R. (2001). Mechanisms of tryptophan fluorescence shifts in proteins. Biophysical Journal, 80, 2093–2109.10.1016/S0006-3495(01)76183-8
  • Wang, S.-C., Makino, K., Xia, W., Kim, J. S., Im, S.-A., Peng, H., … Hung, M.-C. (2001). DOC-2/hDab-2 inhibits ILK activity and induces anoikis in breast cancer cells through an Akt-independent pathway. Oncogene, 20, 6960–6964.10.1038/sj.onc.1204873
  • White, K. A., Grillo-Hill, B. K., & Barber, D. L. (2017). Cancer cell behaviors mediated by dysregulated pH dynamics at a glance. Journal of Cell Science, 130, 663–669.10.1242/jcs.195297
  • Wickström, S. A., Lange, A., Montanez, E., & Fässler, R. (2010). The ILK/PINCH/parvin complex: The kinase is dead, long live the pseudokinase! The EMBO Journal, 29, 281–291.10.1038/emboj.2009.376
  • Wu, C., & Dedhar, S. (2001). Integrin-linked kinase (ILK) and its interactors. The Journal of Cell Biology, 155, 505–510.10.1083/jcb.200108077
  • Wu, P.-A., Li, S.-S., Tang, Q.-L., Liu, B.-B., & Yang, X.-M. (2017). Clinical significance of integrin-linked kinase in laryngeal squamous cell carcinoma. Auris Nasus Larynx, 44, 458–463.10.1016/j.anl.2016.09.002
  • Yang, Y., Wang, X., Hawkins, C. A., Chen, K., Vaynberg, J., Mao, X., … Wang, Y.-X. (2009). Structural basis of focal adhesion localization of LIM-only adaptor PINCH by integrin-linked kinase. Journal of Biological Chemistry, 284, 5836–5844.10.1074/jbc.M805319200
  • Zhang, Y., Guo, L., Chen, K., & Wu, C. (2002). A critical role of the PINCH-integrin-linked kinase interaction in the regulation of cell shape change and migration. Journal of Biological Chemistry, 277, 318–326.10.1074/jbc.M108257200
  • Zhou, W., & Li, Y. (2017). Advances in the research of role of integrin-linked kinase in angiogenesis. Zhonghua shao shang za zhi=Zhonghua shaoshang zazhi=Chinese journal of burns, 33, 317.
  • Zielkiewicz, J. (2005). Structural properties of water: Comparison of the SPC, SPCE, TIP4P, and TIP5P models of water. The Journal of Chemical Physics, 123, 104501. doi:10.1063/1.2018637

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.