Molecular activities and ligand-binding specificities of StAR-related lipid transfer domains: exploring integrated in silico methods and ensemble-docking approaches

References

• W.L. Miller and H.S. Bose, Early steps in steroidogenesis: Intracellular cholesterol trafficking, J. Lipid. Res. 52 (2011), pp. 2111–2135.
   PubMed Web of Science ®Google Scholar
• P.R. Manna, M.T. Dyson, and D.M. Stocco, Regulation of the steroidogenic acute regulatory protein gene expression: Present and future perspectives, Mol. Hum. Reprod. 15 (2009), pp. 321–333.
   PubMed Web of Science ®Google Scholar
• C.B. Kallen, J.T. Billheimer, S.A. Summers, S.E. Stayrook, M. Lewis, and J.F. Strauss III, Steroidogenic acute regulatory protein (StAR) is a sterol transfer protein, J. Biol. Chem. 273 (1998), pp. 26285–26288.
   PubMed Web of Science ®Google Scholar
• H.S. Bose, R.M. Whittal, M.A. Baldwin, and W.L. Miller, The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule, Proc. Natl. Acad. Sci. U.S.A. 96 (1999), pp. 7250–7255.
   PubMed Web of Science ®Google Scholar
• F. Alpy, Give lipids a START: The StAR-related lipid transfer (START) domain in mammals, J. Cell. Sci. 118 (2005), pp. 2791–2801.
   PubMed Web of Science ®Google Scholar
• J. Reitz, K. Gehrig-Burger, J.F. Strauss, and G. Gimpl, Cholesterol interaction with the related steroidogenic acute regulatory lipid-transfer (START) domains of StAR (STARD1) and MLN64 (STARD3), FEBS J. 275 (2008), pp. 1790–1802.
   PubMed Web of Science ®Google Scholar
• J.B. Pinto and A. Graham, The role of endosomal cholesterol trafficking protein, StAR-related lipid transfer domain 3 (StarD3/MLN64), in BRIN-BD11 insulinoma cells, Clin. Sci. (Lond) 7 (2016), pp. 833–838.
   Google Scholar
• M. Calderon-Dominguez, G. Gil, M.A. Medina, W.M. Pandak, and D. Rodríguez-Agudo, The StarD4 subfamily of steroidogenic acute regulatory-related lipid transfer (START) domain proteins: New players in cholesterol metabolism, Int. J. Biochem. Cell. Biol. 49 (2014), pp. 64–68.
   PubMed Web of Science ®Google Scholar
• D. Rodriguez-Agudo, S. Ren, E. Wong, D. Marques, K. Redford, G. Gil, P. Hylemon, and W.M. Pandak, Intracellular cholesterol transporter StarD4 binds free cholesterol and increases cholesteryl ester formation, J. Lipid. Res. 49 (2008), pp. 1409–1419.
   PubMed Web of Science ®Google Scholar
• R.E. Soccio, R.M. Adams, M.J. Romanowski, E. Sehayek, S.K. Burley, and J.L. Breslow, The cholesterol-regulated StarD4 gene encodes a StAR-related lipid transfer protein with two closely related homologues, StarD5 and StarD6, Proc. Natl. Acad. Sci. U S A. 99 (2002), pp. 6943–6948.
   PubMed Web of Science ®Google Scholar
• A.G. Thorsell, W.H. Lee, C. Persson, M.I. Siponen, M. Nilsson, R.D. Busam, T. Kotenyova, H. Schüler, and L. Lehtiö, Comparative structural analysis of lipid binding START domains, PLoS ONE. 6 (2011), pp. 1–11. 10.1371/journal.pone.0019521.
   Web of Science ®Google Scholar
• Y. Tsujishita and J.H. Hurley, Structure and lipid transport mechanism of a StAR-related domain, Nat Struct Biol. 7 (2000), pp. 408–14.
   PubMedGoogle Scholar
• D. Letourneau, M. Bedard, A. Lefebvre, J. Lehoux, and P. Lavigne, Solution structure of StAR-related lipid transfer domain protein 6 (STARD6), (2014). 10.2210/pdb2mou/pdb. (https://www.rcsb.org/structure/2MOU)
   Google Scholar
• R.M. Sharpe, Environmental/lifestyle effects on spermatogenesis, Philos. Trans. R Soc. Lond. B Biol. Sci. 365 (2010), pp. 1697–1712.
   PubMed Web of Science ®Google Scholar
• C. Supriya, B.P. Girish, and P.S. Reddy, Aflatoxin B1-induced reproductive toxicity in male rats, Int. J. Toxicol. 33 (2014), pp. 155–161.
   PubMed Web of Science ®Google Scholar
• F. Acconcia, V. Pallottini, and M. Marino, Molecular mechanisms of action of BPA, Dose-Resp. 13 (2015), p. 155932581561058.
   Web of Science ®Google Scholar
• K.P. Reddy and P.S. Reddy, Testicular and epididymal toxicity induced by benzo(a)pyrene, alcohol, and their combination in Wistar rats, Toxicol. Res. 5 (2016), pp. 420–433.
   Web of Science ®Google Scholar
• H. Zhang, Y. Lu, B. Luo, S. Yan, X. Guo, and J. Dai, Proteomic analysis of mouse testis reveals perfluorooctanoic acid-induced reproductive dysfunction via direct disturbance of testicular steroidogenic machinery, J. Proteome Res. 13 (2014), pp. 3370–3385.
   PubMed Web of Science ®Google Scholar
• K. Glass and M. Girvan, Annotation enrichment analysis: An alternative method for evaluating the functional properties of gene sets, Sci. Rep. 4 (2014), pp. 1–9. 10.1038/srep04191.
   Web of Science ®Google Scholar
• B.S. Chen and C.C. Wu, Systems biology as an integrated platform for bioinformatics, systems synthetic biology, and systems metabolic engineering, Cells. 2 (2013), pp. 635–688.
   PubMedGoogle Scholar
• D. Szklarczyk, J.H. Morris, H. Cook, M. Kuhn, S. Wyder, M. Simonovic, A. Santos, N.T. Doncheva, A. Roth, P. Bork, L.J. Jensen, and C. von Mering, The STRING database in 2017: Quality-controlled protein–protein association networks, made broadly accessible, Nucleic Acids Res. 45 (2016). pp. D362–D368.
   PubMed Web of Science ®Google Scholar
• J. Cao and S. Zhang, A Bayesian extension of the hypergeometric test for functional enrichment analysis, Biometrics 70 (2013), pp. 84–94.
   PubMed Web of Science ®Google Scholar
• M. Topf and A. Sali, Combining electron microscopy and comparative protein structure modeling, Curr. Opin. Struct. Biol. 15 (2005), pp. 578–585.
   PubMed Web of Science ®Google Scholar
• M. Topf, M.L. Baker, B. John, W. Chiu, and A. Sali, Structural characterization of components of protein assemblies by comparative modeling and electron cryo-microscopy, J. Struct. Biol. 149 (2005), pp. 191–203.
   PubMed Web of Science ®Google Scholar
• M. Topf, M.L. Baker, M.A. Marti-Renom, W. Chiu, and A. Sali, Refinement of protein structures by iterative comparative modeling and CryoEM density fitting, J. Mol. Biol. 357 (2006), pp. 1655–1668.
   PubMed Web of Science ®Google Scholar
• R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton, AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR. 8 (1996), pp. 477–486.
   PubMed Web of Science ®Google Scholar
• R. Lüthy, J.U. Bowie, and D. Eisenberg, Assessment of protein models with three-dimensional profiles, Nature. 356 (1992), pp. 83–85.
   PubMed Web of Science ®Google Scholar
• M. Wiederstein and M.J. Sippl, ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins, Nucleic Acids Res. 35 (2007), pp. 407–410.
   PubMed Web of Science ®Google Scholar
• D. Szklarczyk, A. Santos, C. Von Mering, L.J. Jensen, P. Bork, and M. Kuhn, STITCH 5: Augmenting protein–chemical interaction networks with tissue and affinity data, Nucleic Acids Res. 44 (2015), pp. D380–D384.
   PubMed Web of Science ®Google Scholar
• J. Xia, M.J. Benner, and R.E.W. Hancock, NetworkAnalyst - integrative approaches for protein–protein interaction network analysis and visual exploration, Nucleic Acids Res. 42 (2014), pp. W167–W174.
   PubMed Web of Science ®Google Scholar
• P. Shannon, Cytoscape: A software environment for integrated models of biomolecular interaction networks, Genome Res. 13 (2003), pp. 2498–2504.
   PubMed Web of Science ®Google Scholar
• K.K. Kumar, B.U. Devi, and P. Neeraja, Integration of in silico approaches to determination of endocrine-disrupting perfluorinated chemicals binding potency with steroidogenic acute regulatory protein, Biochem. Biophys. Res. Commun. 491 (2017), pp. 1007–1014.
   PubMed Web of Science ®Google Scholar
• S. Dallakyan and A.J. Olson, Small-molecule library screening by docking with PyRx, Meth. Molec. Biol. Chem. Biol. 1263 (2014), pp. 243–250.
   Google Scholar
• M. Pathan, S. Keerthikumar, C.S. Ang, L. Gangoda, C.Y. Quek, N.A. Williamson, D. Mouradov, O.M. Sieber, R.J. Simpson, A. Salim, A. Bacic, A.F. Hill, D.A. Stroud, M.T. Ryan, J.I. Agbinya, J.M. Mariadason, A.W. Burgess, and S. Mathivanan, FunRich: An open access standalone functional enrichment and interaction network analysis tool, Proteomics. 15 (2015), pp. 2597–2601.
   PubMed Web of Science ®Google Scholar
• H. Chen, Y. Fang, H. Zhu, S. Li, T. Wang, P. Gu, X. Fang, Y. Wu, J. Liang, Y. Zeng, L. Zhang, W. Qiu, L. Zhang, and X. Yi, Protein–protein interaction analysis of distinct molecular pathways in two subtypes of colorectal carcinoma, Mol. Med. Rep. 10 (2014), pp. 2868–2674.
   PubMed Web of Science ®Google Scholar
• M. Murcia, J. Faraldo-Gomez, F. Maxfield, and B. Roux, Model of the structure of the StART domains of human MLN64 in complex with cholesterol, 47, J. Lipid Res. (2006), pp. 2614–2630.
   PubMed Web of Science ®Google Scholar
• T.J. Huang and P.S. Li, Dexamethasone inhibits luteinizing hormone-induced synthesis of steroidogenic acute regulatory protein in cultured rat preovulatory follicles1, Biol. Reprod. 64 (2001), pp. 163–170.
   PubMed Web of Science ®Google Scholar