Classification and QSAR models of leukotriene A4 hydrolase (LTA4H) inhibitors by machine learning methods

References

• V.M. Tanis, G.M. Bacani, J.M. Blevitt, C.C. Chrovian, S. Crawford, A. De Leon, A.M. Fourie, L. Gomez, C.A. Grice, K. Herman, A.M. Kearney, A.M. Landry-Bayle, A. Lee-Dutra, J. Nelson, J.P. Riley, A. Santillan Jr., J.J. Wiener, X. Xue, and A.L. Young, Azabenzthiazole inhibitors of leukotriene A(4) hydrolase, Bioorg. Med. Chem. Lett. 22 (2012), pp. 7504–7511. doi:10.1016/j.bmcl.2012.10.036.
   PubMed Web of Science ®Google Scholar
• S. Thangapandian, S. John, M. Son, V. Arulalapperumal, and K.W. Lee, Development of predictive quantitative structure-activity relationship model and its application in the discovery of human leukotriene A4 hydrolase inhibitors, Future Med. Chem. 5 (2013), pp. 27–40. doi:10.4155/fmc.12.184.
   PubMed Web of Science ®Google Scholar
• A. Stsiapanava, U. Olsson, M. Wan, T. Kleinschmidt, D. Rutishauser, R.A. Zubarev, B. Samuelsson, A. Rinaldo-Matthis, and J.Z. Haeggstrom, Binding of Pro-Gly-Pro at the active site of leukotriene A4 hydrolase/aminopeptidase and development of an epoxide hydrolase selective inhibitor, Proc. Natl. Acad. Sci. USA. 111 (2014), pp. 4227–4232. doi:10.1073/pnas.1402136111.
   PubMed Web of Science ®Google Scholar
• D. Moser, S.K. Wittmann, J. Kramer, R. Blocher, J. Achenbach, D. Pogoryelov, and E. Proschak, PENG: A neural gas-based approach for pharmacophore elucidation. method design, validation, and virtual screening for novel ligands of LTA4H, J. Chem. Inf. Model. 55 (2015), pp. 284–293. doi:10.1021/ci500618u.
   PubMed Web of Science ®Google Scholar
• L. Bhatt, K. Roinestad, T. Van, and E.B. Springman, Recent advances in clinical development of leukotriene B4 pathway drugs, Semin. Immunol. 33 (2017), pp. 65–73. doi:10.1016/j.smim.2017.08.007.
   PubMed Web of Science ®Google Scholar
• X. Jiang, L. Zhou, D. Wei, H. Meng, Y. Liu, and L. Lai, Activation and inhibition of leukotriene A4 hydrolase aminopeptidase activity by diphenyl ether and derivatives, Bioorg. Med. Chem. Lett. 18 (2008), pp. 6549–6552. doi:10.1016/j.bmcl.2008.10.044.
   PubMed Web of Science ®Google Scholar
• K. Pal, X. Feng, J.W. Steinke, M.D. Burdick, Y.M. Shim, S.S. Sung, W.G. Teague, and L. Borish, Leukotriene A4 hydrolase activation and leukotriene B4 production by eosinophils in severe asthma, Am. J. Respir. Cell. Mol. Biol. 60 (2019), pp. 413–419. doi:10.1165/rcmb.2018-0175OC.
   PubMed Web of Science ®Google Scholar
• J.M. Wells, P.J. O’Reilly, T. Szul, D.I. Sullivan, G. Handley, C. Garrett, C.M. McNicholas, M.A. Roda, B.E. Miller, R. Tal-Singer, A. Gaggar, S.I. Rennard, P.L. Jackson, and J.E. Blalock, An aberrant leukotriene A4 hydrolase-proline-glycine-proline A 4 hydrolase–proline-glycine-proline pathway in the pathogenesis of chronic obstructive pulmonary disease, Am. J. Respir. Crit. Care. Med. 190 (2014), pp. 51–61. doi:10.1164/rccm.201401-0145OC.
   PubMed Web of Science ®Google Scholar
• D.R. Crosslin, S.H. Shah, S.C. Nelson, C.S. Haynes, J.J. Connelly, S. Gadson, P.J. Goldschmidt-Clermont, J.M. Vance, J. Rose, C.B. Granger, D. Seo, S.G. Gregory, W.E. Kraus, and E.R. Hauser, Genetic effects in the leukotriene biosynthesis pathway and association with atherosclerosis, Hum. Genet. 125 (2009), pp. 217–229. doi:10.1007/s00439-008-0619-0.
   PubMed Web of Science ®Google Scholar
• S. Thangapandian, S. John, S. Sakkiah, and K.W. Lee, Pharmacophore-based virtual screening and Bayesian model for the identification of potential human leukotriene A4 hydrolase inhibitors, Eur. J. Med. Chem. 46 (2011), pp. 1593–1603. doi:10.1016/j.ejmech.2011.02.007.
   PubMed Web of Science ®Google Scholar
• S.A. Audat, N.A. Al-Shar’i, B.A. Al-Oudat, A. Bryant-Friedrich, M.F. Bedi, A.L. Zayed, and Q.A. Al-Balas, Identification of human leukotriene A4 hydrolase inhibitors using structure-based pharmacophore modeling and molecular docking, Molecules 25 (2020), pp. 2871. doi:10.3390/molecules25122871.
   Web of Science ®Google Scholar
• M.M. Thunnissen, B. Andersson, B. Samuelsson, C.H. Wong, and J. Haeggstrom, Crystal structures of leukotriene A4 A 4 hydrolase in complex with captopril and two competitive tight-binding inhibitors, Faseb J. 16 (2002), pp. 1648–1650. doi:10.1096/fj.01-1017fje.
   PubMed Web of Science ®Google Scholar
• S. Zhao, K. Yao, D. Li, K. Liu, G. Jin, M. Yan, Q. Wu, H. Chen, S.H. Shin, R. Bai, G. Wang, A.M. Bode, Z. Dong, Z. Guo, and Z. Dong, Inhibition of LTA4H by bestatin in human and mouse colorectal cancer, EBioMedicine 44 (2019), pp. 361–374. doi:10.1016/j.ebiom.2019.05.008.
   PubMed Web of Science ®Google Scholar
• A. Mira, M.A. Sabry, K. Shimizu, and F.M. Abdel Bar, A new pimarane-type diterpene obtained by biotransformation inhibits human HCT-116 colorectal carcinoma through inhibition of LTA4H activity, Med. Chem. Res. 29 (2020), pp. 759–766. doi:10.1007/s00044-020-02520-9.
   Web of Science ®Google Scholar
• L.A. Enache, I. Kennedy, D.W. Sullins, W. Chen, D. Ristic, G.L. Stahl, S. Dzekhtser, R.A. Erickson, C.R. Yan, F.W. Muellner, M.D. Krohn, J. Winger, V. Sandanayaka, J. Singh, D.E. Zembower, and A.S. Kiselyov, Development of a scalable synthetic process for DG-051B, a first-in-class inhibitior of LTA4H, Org. Process. Res. Dev. 13 (2009), pp. 1177–1184. doi:10.1021/op900231j.
   Web of Science ®Google Scholar
• V. Sandanayaka, B. Mamat, R.K. Mishra, J. Winger, M. Krohn, L.M. Zhou, M. Keyvan, L. Enache, D. Sullins, E. Onua, J. Zhang, G. Halldorsdottir, H. Sigthorsdottir, A. Thorlaksdottir, G. Sigthorsson, M. Thorsteinnsdottir, D.R. Davies, L.J. Stewart, D.E. Zembower, T. Andresson, A.S. Kiselyov, J. Singh, and M.E. Gurney, Discovery of 4-[(2S)-2-{[4-(4-chlorophenoxy)phenoxy]methyl}-1-pyrrolidinyl]butanoic 4-[(2 S)-2-{[4-(4-chlorophenoxy)phenoxy]methyl}-1-pyrrolidinyl]butanoic acid (DG-051) as a novel leukotriene A4 hydrolase inhibitor of leukotriene B4 biosynthesis, J. Med. Chem. 53 (2010), pp. 573–585. doi:10.1021/jm900838g.
   PubMed Web of Science ®Google Scholar
• T.D. Penning, N.S. Chandrakumar, B.N. Desai, S.W. Djuric, A.F. Gasiecki, C.D. Liang, J.M. Miyashiro, M.A. Russell, L.J. Askonas, J.K. Gierse, E.I. Harding, M.K. Highkin, J.F. Kachur, S.H. Kim, D. Villani-Price, E.Y. Pyla, N.S. Ghoreishi-Haack, and W.G. Smith, Pyrrolidine and piperidine analogues of SC-57461A as potent, orally active inhibitors of leukotriene A4 hydrolase, Bioorg. Med. Chem. Lett. 12 (2002), pp. 3383–3386. doi:10.1016/S0960-894X(02)00760-6.
   PubMed Web of Science ®Google Scholar
• M.H. El-Naggar, A. Mira, F.M. Abdel Bar, K. Shimizu, M.M. Amer, and F.A. Badria, Synthesis, docking, cytotoxicity, and LTA4H inhibitory activity of new gingerol derivatives as potential colorectal cancer therapy, Bioorg. Med. Chem. 25 (2017), pp. 1277–1285. doi:10.1016/j.bmc.2016.12.048.
   PubMed Web of Science ®Google Scholar
• W. Eccles, J.M. Blevitt, J.N. Booker, C.C. Chrovian, S. Crawford, A.R. De Leon, X. Deng, A.M. Fourie, C.A. Grice, K. Herman, L. Karlsson, A.M. Kearney, A. Lee-Dutra, J. Liang, R. Luna, D. Pippel, N. Rao, J.P. Riley, A. Santillan, B. Savall, V.M. Tanis, X. Xue, and A.L. Young, Identification of benzofuran central cores for the inhibition of leukotriene A(4) hydrolase, Bioorg. Med. Chem. Lett. 23 (2013), pp. 811–815. doi:10.1016/j.bmcl.2012.11.074.
   PubMed Web of Science ®Google Scholar
• A. Cherkasov, E.N. Muratov, D. Fourches, A. Varnek, I.I. Baskin, M. Cronin, J. Dearden, P. Gramatica, Y.C. Martin, R. Todeschini, V. Consonni, V.E. Kuz’min, R. Cramer, R. Benigni, C. Yang, J. Rathman, L. Terfloth, J. Gasteiger, A. Richard, and A. Tropsha, QSAR modeling: Where have you been? Where are you going to?, J. Med. Chem. 57 (2014), pp. 4977–5010. doi:10.1021/jm4004285.
   PubMed Web of Science ®Google Scholar
• P.B. Paz, E.G. Vega-Hissi, M.F. Andrada, M.R. Estrada, and J.C. Garro Martinez, Quantitative structure activity relationship and binding investigation of N-alkyl glycine amides as inhibitors of leukotriene A4 hydrolase, Med. Chem. Res. 24 (2014), pp. 496–504. doi:10.1007/s00044-014-1121-y.
   Web of Science ®Google Scholar
• Y. Xi, Z. Qin, and A. Yan, SAR and QSAR models of cyclooxygenase-1 (COX-1) inhibitors, SAR QSAR Environ. Res. 29 (2018), pp. 755–784. doi:10.1080/1062936X.2018.1513952.
   PubMed Web of Science ®Google Scholar
• Z. Qin and A. Yan, QSAR studies on hepatitis C virus NS5A protein tetracyclic inhibitors in wild type and mutants by CoMFA and CoMSIA, SAR QSAR Environ. Res. 31 (2020), pp. 281–311. doi:10.1080/1062936X.2020.1740889.
   PubMed Web of Science ®Google Scholar
• V. Sandanayaka, B. Mamat, N. Bhagat, L. Bedell, G. Halldorsdottir, H. Sigthorsdottir, T. Andresson, A. Kiselyov, M. Gurney, and J. Singh, Discovery of novel leukotriene A4 hydrolase inhibitors based on piperidine and piperazine scaffolds, Bioorg. Med. Chem. Lett. 20 (2010), pp. 2851–2854. doi:10.1016/j.bmcl.2010.03.047.
   PubMed Web of Science ®Google Scholar
• Z. Chen, Y. Wu, Y. Liu, S. Yang, Y. Chen, and L. Lai, Discovery of dual target inhibitors against cyclooxygenases and leukotriene A4 A 4 hydrolyase, J. Med. Chem. 54 (2011), pp. 3650–3660. doi:10.1021/jm200063s.
   PubMed Web of Science ®Google Scholar
• C.A. Grice, K.L. Tays, B.M. Savall, J. Wei, C.R. Butler, F.U. Axe, S.D. Bembenek, A.M. Fourie, P.J. Dunford, K. Lundeen, F. Coles, X. Xue, J.P. Riley, K.N. Williams, L. Karlsson, and J.P. Edwards, Identification of a potent, selective, and orally active leukotriene A4 A 4 hydrolase inhibitor with anti-inflammatory activity, J. Med. Chem. 51 (2008), pp. 4150–4169. doi:10.1021/jm701575k.
   PubMed Web of Science ®Google Scholar
• T.D. Penning, L.J. Askonas, S.W. Djuric, R.A. Haack, S.S. Yu, M.L. Michener, G.G. Krivi, and E.Y. Pyla, Kelatorphan and related analogs: Potent and selective inhibitors of leukotriene A4 hydrolase, Bioorg. Med. Chem. Lett. 5 (1995), pp. 2517–2522. doi:10.1016/0960-894X(95)00441-U.
   Web of Science ®Google Scholar
• H. Meng, Y. Liu, Y. Zhai, and L. Lai, Optimization of 5-hydroxytryptamines as dual function inhibitors targeting phospholipase A2 and leukotriene A4 hydrolase, Eur. J. Med. Chem. 59 (2013), pp. 160–167. doi:10.1016/j.ejmech.2012.10.057.
   PubMed Web of Science ®Google Scholar
• T.D. Penning, N.S. Chandrakumar, B.B. Chen, H.Y. Chen, B.N. Desai, S.W. Djuric, S.H. Docter, A.F. Gasiecki, R.A. Haack, J.M. Miyashiro, M.A. Russell, S.S. Yu, D.G. Corley, R.C. Durley, B.F. Kilpatrick, B.L. Parnas, L.J. Askonas, J.K. Gierse, E.I. Harding, M.K. Highkin, J.F. Kachur, S.H. Kim, G.G. Krivi, D. Villani-Price, E.Y. Pyla, W.G. Smith, and N.S. Ghoreishi-Haack, Structure−activity relationship studies on 1-[2-(4-phenylphenoxy)ethyl]pyrrolidine (SC-22716), a potent inhibitor of leukotriene A4 (LTA4) hydrolase, J. Med. Chem. 43 (2000), pp. 721–735. doi:10.1021/jm990496z.
   PubMed Web of Science ®Google Scholar
• B. Ye, J. Bauman, M. Chen, D. Davey, S.K. Khim, B. King, T. Kirkland, M. Kochanny, A. Liang, D. Lentz, K. May, L. Mendoza, G. Phillips, V. Selchau, S. Schlyer, J.L. Tseng, R.G. Wei, H. Ye, J. Parkinson, and W.J. Guilford, Synthesis of N-alkyl glycine amides as potent inhibitors of leukotriene A4 hydrolase, Bioorg. Med. Chem. Lett. 18 (2008), pp. 3891–3894. doi:10.1016/j.bmcl.2008.06.046.
   PubMed Web of Science ®Google Scholar
• T.D. Penning, M.A. Russell, B.B. Chen, H.Y. Chen, C.D. Liang, M.W. Mahoney, J.W. Malecha, J.M. Miyashiro, S.S. Yu, L.J. Askonas, J.K. Gierse, E.I. Harding, M.K. Highkin, J.F. Kachur, S.H. Kim, D. Villani-Price, E.Y. Pyla, N.S. Ghoreishi-Haack, and W.G. Smith, Synthesis of potent leukotriene A4 A 4 hydrolase inhibitors. Identification of 3-[methyl[3-[4-(phenylmethyl)phenoxy]propyl]amino]propanoic acid, J. Med. Chem. 45 (2002), pp. 3482–3490. doi:10.1021/jm0200916.
   PubMed Web of Science ®Google Scholar
• D. Penning, N.S. Chandrakumar, B.N. Desai, S.W. Djuric, A.F. Gasiecki, J.W. Malecha, J.M. Miyashiro, M.A. Russell, L.J. Askonas, J.K. Gierse, E.I. Harding, M.K. Highkin, J.F. Kachur, S.H. Kim, D. Villani-Price, E.Y. Pyla, N.S. Ghoreishi-Haack, and W.G. Smith, Synthesis of imidazopyridines and purines as potent inhibitors of leukotriene A4 hydrolase, Bioorg. Med. Chem. Lett. 13 (2003), pp. 1137–1139. doi:10.1016/s0960-894x(03)00039-8.
   PubMed Web of Science ®Google Scholar
• S.K. Khim, J. Bauman, J. Evans, B. Freeman, B. King, T. Kirkland, M. Kochanny, D. Lentz, A. Liang, L. Mendoza, G. Phillips, J.L. Tseng, R.G. Wei, H. Ye, L. Yu, J. Parkinson, and W.J. Guilford, Discovery of novel and potent aryl diamines as leukotriene A4 hydrolase inhibitors, Bioorg. Med. Chem. Lett. 18 (2008), pp. 3895–3898. doi:10.1016/j.bmcl.2008.06.041.
   PubMed Web of Science ®Google Scholar
• D. Wei, X. Jiang, L. Zhou, J. Chen, Z. Chen, C. He, K. Yang, Y. Liu, J. Pei, and L. Lai, Discovery of multitarget inhibitors by combining molecular docking with common pharmacophore matching, J. Med. Chem. 51 (2008), pp. 7882–7888. doi:10.1021/jm8010096.
   PubMed Web of Science ®Google Scholar
• E. Shang, Y. Yuan, X. Chen, Y. Liu, J. Pei, and L. Lai, De novo design of multitarget ligands with an iterative fragment-growing strategy, J. Chem. Inf. Model. 54 (2014), pp. 1235–1241. doi:10.1021/ci500021v.
   PubMed Web of Science ®Google Scholar
• W. Lu, X. Yao, P. Ouyang, N. Dong, D. Wu, X. Jiang, Z. Wu, C. Zhang, Z. Xu, Y. Tang, S. Zou, M. Liu, J. Li, M. Zeng, P. Lin, F. Cheng, and J. Huang, Drug repurposing of histone deacetylase inhibitors that alleviate neutrophilic inflammation in acute lung injury and idiopathic pulmonary fibrosis via inhibiting leukotriene A4 hydrolase and blocking LTB4 biosynthesis, J. Med. Chem. 60 (2017), pp. 1817–1828. doi:10.1021/acs.jmedchem.6b01507.
   PubMed Web of Science ®Google Scholar
• W. Yuan, B. Munoz, C.H. Wong, J.Z. Haeggstroem, A. Wetterholm, and B. Samuelsson, Development of selective tight-binding inhibitors of leukotriene A4 hydrolase, J. Med. Chem. 36 (1993), pp. 211–220. doi:10.1021/jm00054a004.
   PubMed Web of Science ®Google Scholar
• D.R. Davies, B. Mamat, O.T. Magnusson, J. Christensen, M.H. Haraldsson, R. Mishra, B. Pease, E. Hansen, J. Singh, D. Zembower, H. Kim, A.S. Kiselyov, A.B. Burgin, M.E. Gurney, and L.J. Stewart, Discovery of leukotriene A4 hydrolase inhibitors using metabolomics biased fragment crystallography, J. Med. Chem. 52 (2009), pp. 4694–4715. doi:10.1021/jm900259h.
   PubMed Web of Science ®Google Scholar
• S.K. Wittmann, L. Kalinowsky, J.S. Kramer, R. Bloecher, S. Knapp, D. Steinhilber, D. Pogoryelov, E. Proschak, and J. Heering, Thermodynamic properties of leukotriene A4 hydrolase inhibitors, Bioorg. Med. Chem. 24 (2016), pp. 5243–5248. doi:10.1016/j.bmc.2016.08.047.
   PubMed Web of Science ®Google Scholar
• M. Merkow and R.K. DeLisle, Improving the performance of self-organizing maps via growing representations, J. Chem. Inf. Model. 47 (2007), pp. 1797–1807. doi:10.1021/ci7001445.
   PubMed Web of Science ®Google Scholar
• SONNIA, available from molecular networks GmbH, Erlangen, Germany, Available at http://www.molecular-networks.com.
   Google Scholar
• J.W. Godden, L. Xue, and J. Bajorath, Combinatorial preferences affect molecular similarity/diversity calculations using binary fingerprints and tanimoto coefficients, J. Chem. Inf. Comput. Sci. 40 (2000), pp. 163–166. doi:10.1021/ci990316u.
   PubMedGoogle Scholar
• L. Hefke, K. Hiesinger, W.F. Zhu, J.S. Kramer, and E. Proschak, Computer-aided fragment growing strategies to design dual inhibitors of soluble epoxide hydrolase and LTA4 hydrolase, ACS Med. Chem. Lett. 11 (2020), pp. 1244–1249. doi:10.1021/acsmedchemlett.0c00102.
   PubMed Web of Science ®Google Scholar
• K. Hiesinger, A. Schott, J.S. Kramer, R. Blocher, F. Witt, S.K. Wittmann, D. Steinhilber, D. Pogoryelov, J. Gerstmeier, O. Werz, and E. Proschak, Design of dual inhibitors of soluble epoxide hydrolase and LTA4 LTA 4 hydrolase, ACS Med. Chem. Lett. 11 (2020), pp. 298–302. doi:10.1021/acsmedchemlett.9b00330.
   PubMed Web of Science ®Google Scholar
• C. Markert, G. Thoma, H. Srinivas, B. Bollbuck, and T.A. Rhn, Discovery of LYS006, a potent and highly selective inhibitor of leukotriene A 4 hydrolase, J. Med. Chem. 64 (2021), pp. 1889–1903. doi:10.1021/acs.jmedchem.0c01955.
   PubMed Web of Science ®Google Scholar
• B. Chen, R.P. Sheridan, V. Hornak, and J.H. Voigt, Comparison of random forest and pipeline pilot naive Bayes in prospective QSAR predictions, J. Chem. Inf. Model. 52 (2012), pp. 792–803. doi:10.1021/ci200615h.
   PubMed Web of Science ®Google Scholar
• RDKit 2019.03.4: An open-source cheminformatics software, San Francisco, CA, USA, 2019, Available at http://www.rdkit.org
   Google Scholar
• CORINA symphony, 3D structure generator CORINA, developed and distributed by molecular networks GmbH, Erlangen, Germany 2017; software available at http://www.molecular-networks.com
   Google Scholar
• E.W. Steyerberg, M.J. Eijkemans, and J.D. Habbema, Stepwise selection in small data sets: A simulation study of bias in logistic regression analysis, J. Clin. Epidemiol. 52 (1999), pp. 935–942. doi:10.1016/s0895-4356(99)00103-1.
   PubMed Web of Science ®Google Scholar
• C.Y. Liew, X.H. Ma, X. Liu, and C.W. Yap, SVM model for virtual screening of Lck inhibitors, J. Chem. Inf. Model. 49 (2009), pp. 877–885. doi:10.1021/ci800387z.
   PubMed Web of Science ®Google Scholar
• S. Palmer, N.M. O’Boyle, R.C. Glen, and J.B. Mitchell, Random forest models to predict aqueous solubility, J. Chem. Inf. Model. 47 (2007), pp. 150–158. doi:10.1021/ci060164k.
   PubMed Web of Science ®Google Scholar
• W. Zheng and A. Tropsha, Novel variable selection quantitative structure–property structure−property relationship approach based on the k-nearest-neighbor k -nearest-neighbor principle, J. Chem. Inf. Comput. Sci. 40 (2000), pp. 185–194. doi:10.1021/ci980033m.
   PubMedGoogle Scholar
• F. Pedregosa, G. Varoquaux, A. Gramfort, V. Michel, B. Thirion, O. Grisel, M. Blondel, P. Prettenhofer, R. Weiss, V. Dubourg, J. Vanderplas, A. Passos, D. Cournapeau, M. Brucher, M. Perrot, and E. Duchesnay, Scikit-learn: Machine learning in Python, J. Mach. Learn. Res. 12 (2011), pp. 2825–2830.
   Web of Science ®Google Scholar
• D.J. Livingstone and D.W. Salt, Judging the significance of multiple linear regression models, J. Med. Chem. 48 (2005), pp. 661–663. doi:10.1021/jm049111p.
   PubMed Web of Science ®Google Scholar
• N. Triballeau, F. Acher, I. Brabet, J.-P. Pin, and H.O. Bertrand, Virtual screening workflow development guided by the “receiver operating characteristic” curve approach. application to high-throughput docking on metabotropic glutamate receptor subtype 4, J. Med. Chem. 48 (2005), pp. 2534–2547. doi:10.1021/jm049092j.
   PubMed Web of Science ®Google Scholar
• X. Bo, M. Yang, T. Dacheng, and H. Kaiqi, m-SNE: Multiview stochastic neighbor embedding, IEEE Trans. Syst. Man. Cybern. B Cybern. 41 (2011), pp. 1088–1096. doi:10.1109/TSMCB.2011.2106208.
   PubMed Web of Science ®Google Scholar
• F. Camastra and A. Verri, A novel kernel method for clustering, IEEE Trans. Pattern. Anal. Mach. Intell. 27 (2005), pp. 801–805. doi:10.1109/TPAMI.2005.88.
   PubMed Web of Science ®Google Scholar
• J.D. Hunter, Matplotlib: A 2D graphics environment, Comput. Sci. Eng. 9 (2007), pp. 90–95. doi:10.1109/Mcse.2007.55.
   Web of Science ®Google Scholar