Development of Pin1 Inhibitors and their Potential as Therapeutic Agents

Author(s): Yusuke Nakatsu, Yasuka Matsunaga, Koji Ueda, Takeshi Yamamotoya, Yuki Inoue, Masa-ki Inoue, Yu Mizuno, Akifumi Kushiyama, Hiraku Ono, Midori Fujishiro, Hisanaka Ito, Takayoshi Okabe, Tomoichiro Asano*

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 20 , 2020

DOI : 10.2174/0929867325666181105120911

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

The prolyl isomerase Pin1 is a unique enzyme, which isomerizes the cis-trans conformation between pSer/pThr and proline and thereby regulates the function, stability and/or subcellular distribution of its target proteins. Such regulations by Pin1 are involved in numerous physiological functions as well as the pathogenic mechanisms underlying various diseases. Notably, Pin1 deficiency or inactivation is a potential cause of Alzheimer’s disease, since Pin1 induces the degradation of Tau. In contrast, Pin1 overexpression is highly correlated with the degree of malignancy of cancers, as Pin1 controls a number of oncogenes and tumor suppressors. Accordingly, Pin1 inhibitors as anti-cancer drugs have been developed. Interestingly, recent intensive studies have demonstrated Pin1 to be responsible for the onset or development of nonalcoholic steatosis, obesity, atherosclerosis, lung fibrosis, heart failure and so on, all of which have been experimentally induced in Pin1 deficient mice.

In this review, we discuss the possible applications of Pin1 inhibitors to a variety of diseases including malignant tumors and also introduce the recent advances in Pin1 inhibitor research, which have been reported.

Keywords: Prolyl isomerase Pin1, Pin1 inhibitors, juglone, ATRA, cancer, metabolic syndromes, fibrosis

[1]
Lu, K.P.; Hanes, S.D.; Hunter, T. A Human Peptidyl-Prolyl Isomerase Essential for Regulation of Mi-tosis Nature 1996, 380(6574), 544-547.,
[http://dx.doi.org/10.1038/380544a0] [PMID: 8606777]
[2]
Chen, Y.; Wu, Y.R.; Yang, H.Y.; Li, X.Z.; Jie, M.M.; Hu, C.J.; Wu, Y.Y.; Yang, S.M.; Yang, Y.B. Prolyl isomerase Pin1: a promoter of cancer and a target for therapy. Cell Death Dis., 2018, 9(9), 883.
[http://dx.doi.org/10.1038/s41419-018-0844-y] [PMID: 30158600]
[3]
Fanghänel, J.; Fischer, G. Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front. Biosci., 2004, 9, 3453-3478.
[http://dx.doi.org/10.2741/1494] [PMID: 15353370]
[4]
Liu, J.; Farmer, J.D., Jr; Lane, W.S.; Friedman, J.; Weissman, I.; Schreiber, S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell, 1991, 66(4), 807-815.
[http://dx.doi.org/10.1016/0092-8674(91)90124-H] [PMID: 1715244]
[5]
Harding, M.W.; Galat, A.; Uehling, D.E.; Schreiber, S.L. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature, 1989, 341(6244), 758-760.
[http://dx.doi.org/10.1038/341758a0] [PMID: 2477715]
[6]
Fischer, G.; Wittmann-Liebold, B.; Lang, K.; Kiefhaber, T.; Schmid, F.X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature, 1989, 337(6206), 476-478.
[http://dx.doi.org/10.1038/337476a0] [PMID: 2492638]
[7]
Flanagan, W.M.; Corthésy, B.; Bram, R.J.; Crabtree, G.R. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature, 1991, 352(6338), 803-807.
[http://dx.doi.org/10.1038/352803a0] [PMID: 1715516]
[8]
Fujiyama, S.; Yanagida, M.; Hayano, T.; Miura, Y.; Isobe, T.; Fujimori, F.; Uchida, T.; Takahashi, N. Isolation and proteomic characterization of human Parvulin-associating preribosomal ribonucleoprotein complexes. J. Biol. Chem., 2002, 277(26), 23773-23780.
[http://dx.doi.org/10.1074/jbc.M201181200] [PMID: 11960984]
[9]
Nakatsu, Y.; Matsunaga, Y.; Yamamotoya, T.; Ueda, K.; Inoue, Y.; Mori, K.; Sakoda, H.; Fujishiro, M.; Ono, H.; Kushiyama, A.; Asano, T. Physiological and pathogenic roles of prolyl isomerase pin1 in metabolic regulations via multiple signal transduction pathway modulations. Int. J. Mol. Sci., 2016, 17(9), 1495.
[http://dx.doi.org/10.3390/ijms17091495] [PMID: 27618008]
[10]
Uchida, T.; Fujimori, F.; Tradler, T.; Fischer, G.; Rahfeld, J.U. Identification and characterization of a 14 kDa human protein as a novel parvulin-like peptidyl prolyl cis/trans isomerase. FEBS Lett., 1999, 446(2-3), 278-282.
[http://dx.doi.org/10.1016/S0014-5793(99)00239-2] [PMID: 10100858]
[11]
Uchida, T.; Takamiya, M.; Takahashi, M.; Miyashita, H.; Ikeda, H.; Terada, T.; Matsuo, Y.; Shirouzu, M.; Yokoyama, S.; Fujimori, F.; Hunter, T. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol., 2003, 10(1), 15-24.
[http://dx.doi.org/10.1016/S1074-5521(02)00310-1] [PMID: 12573694]
[12]
Zhang, J.; Nakatsu, Y.; Shinjo, T.; Guo, Y.; Sakoda, H.; Yamamotoya, T.; Otani, Y.; Okubo, H.; Kushiyama, A.; Fujishiro, M.; Fukushima, T.; Tsuchiya, Y.; Kamata, H.; Iwashita, M.; Nishimura, F.; Katagiri, H.; Takahashi, S.; Kurihara, H.; Uchida, T.; Asano, T. Par14 protein associates with insulin receptor substrate 1 (IRS-1), thereby enhancing insulin-induced IRS-1 phosphorylation and metabolic actions. J. Biol. Chem., 2013, 288(28), 20692-20701.
[http://dx.doi.org/10.1074/jbc.M113.485730] [PMID: 23720771]
[13]
Lu, K.P.; Zhou, X.Z. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat. Rev. Mol. Cell Biol., 2007, 8(11), 904-916.
[http://dx.doi.org/10.1038/nrm2261] [PMID: 17878917]
[14]
Lu, K.P.; Finn, G.; Lee, T.H.; Nicholson, L.K. Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol., 2007, 3(10), 619-629.
[http://dx.doi.org/10.1038/nchembio.2007.35] [PMID: 17876319]
[15]
Lu, P.J.; Zhou, X.Z.; Shen, M.; Lu, K.P. Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science, 1999, 283(5406), 1325-1328.
[http://dx.doi.org/10.1126/science.283.5406.1325] [PMID: 10037602]
[16]
Lu, P.J.; Zhou, X.Z.; Liou, Y.C.; Noel, J.P.; Lu, K.P. Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J. Biol. Chem., 2002, 277(4), 2381-2384.
[http://dx.doi.org/10.1074/jbc.C100228200] [PMID: 11723108]
[17]
Kim, G.; Khanal, P.; Kim, J.Y.; Yun, H.J.; Lim, S.C.; Shim, J.H.; Choi, H.S. COT phosphorylates prolyl-isomerase Pin1 to promote tumorigenesis in breast cancer. Mol. Carcinog., 2015, 54(6), 440-448.
[http://dx.doi.org/10.1002/mc.22112] [PMID: 24265246]
[18]
Cho, Y.S.; Park, S.Y.; Kim, D.J.; Lee, S.H.; Woo, K.M.; Lee, K.A.; Lee, Y.J.; Cho, Y.Y.; Shim, J.H. TPA-induced cell transformation provokes a complex formation between Pin1 and 90 kDa ribosomal protein S6 kinase 2. Mol. Cell. Biochem., 2012, 367(1-2), 85-92.
[http://dx.doi.org/10.1007/s11010-012-1322-y] [PMID: 22562304]
[19]
Lee, Y.C.; Que, J.; Chen, Y.C.; Lin, J.T.; Liou, Y.C.; Liao, P.C.; Liu, Y.P.; Lee, K.H.; Lin, L.C.; Hsiao, M.; Hung, L.Y.; Huang, C.Y.; Lu, P.J. Pin1 acts as a negative regulator of the G2/M transition by interacting with the Aurora-A-Bora complex. J. Cell Sci., 2013, 126(Pt 21), 4862-4872.
[http://dx.doi.org/10.1242/jcs.121368] [PMID: 23970419]
[20]
Lee, T.H.; Chen, C.H.; Suizu, F.; Huang, P.; Schiene-Fischer, C.; Daum, S.; Zhang, Y.J.; Goate, A.; Chen, R.H.; Zhou, X.Z.; Lu, K.P. Death-associated protein kinase 1 phosphorylates Pin1 and inhibits its prolyl isomerase activity and cellular function. Mol. Cell, 2011, 42(2), 147-159.
[http://dx.doi.org/10.1016/j.molcel.2011.03.005] [PMID: 21497122]
[21]
Rangasamy, V.; Mishra, R.; Sondarva, G.; Das, S.; Lee, T.H.; Bakowska, J.C.; Tzivion, G.; Malter, J.S.; Rana, B.; Lu, K.P.; Kanthasamy, A.; Rana, A. Mixed-lineage kinase 3 phosphorylates prolyl-isomerase Pin1 to regulate its nuclear translocation and cellular function. Proc. Natl. Acad. Sci. USA, 2012, 109(21), 8149-8154.
[http://dx.doi.org/10.1073/pnas.1200804109] [PMID: 22566623]
[22]
Eckerdt, F.; Yuan, J.; Saxena, K.; Martin, B.; Kappel, S.; Lindenau, C.; Kramer, A.; Naumann, S.; Daum, S.; Fischer, G.; Dikic, I.; Kaufmann, M.; Strebhardt, K. Polo-like kinase 1-mediated phosphorylation stabilizes Pin1 by inhibiting its ubiquitination in human cells. J. Biol. Chem., 2005, 280(44), 36575-36583.
[http://dx.doi.org/10.1074/jbc.M504548200] [PMID: 16118204]
[23]
Chen, C.H.; Chang, C.C.; Lee, T.H.; Luo, M.; Huang, P.; Liao, P.H.; Wei, S.; Li, F.A.; Chen, R.H.; Zhou, X.Z.; Shih, H.M.; Lu, K.P. SENP1 deSUMOylates and regulates Pin1 protein activity and cellular function. Cancer Res., 2013, 73(13), 3951-3962.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-4360] [PMID: 23633483]
[24]
Yeh, E.S.; Means, A.R. PIN1, the cell cycle and cancer. Nat. Rev. Cancer, 2007, 7(5), 381-388.
[http://dx.doi.org/10.1038/nrc2107] [PMID: 17410202]
[25]
Ryo, A.; Liou, Y.C.; Lu, K.P.; Wulf, G. Prolyl isomerase Pin1: a catalyst for oncogenesis and a potential therapeutic target in cancer. J. Cell Sci., 2003, 116(Pt 5), 773-783.
[http://dx.doi.org/10.1242/jcs.00276] [PMID: 12571275]
[26]
Lu, P.J.; Wulf, G.; Zhou, X.Z.; Davies, P.; Lu, K.P. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature, 1999, 399(6738), 784-788.
[http://dx.doi.org/10.1038/21650] [PMID: 10391244]
[27]
Pastorino, L.; Sun, A.; Lu, P.J.; Zhou, X.Z.; Balastik, M.; Finn, G.; Wulf, G.; Lim, J.; Li, S.H.; Li, X.; Xia, W.; Nicholson, L.K.; Lu, K.P. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature, 2006, 440(7083), 528-534.
[http://dx.doi.org/10.1038/nature04543] [PMID: 16554819]
[28]
Liou, Y.C.; Sun, A.; Ryo, A.; Zhou, X.Z.; Yu, Z.X.; Huang, H.K.; Uchida, T.; Bronson, R.; Bing, G.; Li, X.; Hunter, T.; Lu, K.P. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature, 2003, 424(6948), 556-561.
[http://dx.doi.org/10.1038/nature01832] [PMID: 12891359]
[29]
Shen, Z.J.; Hu, J.; Shiizaki, K.; Kuro-o, M.; Malter, J.S. Phosphate-induced renal fibrosis requires the prolyl isomerase Pin1. PLoS One, 2016, 11(2)e0150093
[http://dx.doi.org/10.1371/journal.pone.0150093] [PMID: 26914452]
[30]
Shen, Z.J.; Esnault, S.; Rosenthal, L.A.; Szakaly, R.J.; Sorkness, R.L.; Westmark, P.R.; Sandor, M.; Malter, J.S. Pin1 regulates TGF-beta1 production by activated human and murine eosinophils and contributes to allergic lung fibrosis. J. Clin. Invest., 2008, 118(2), 479-490.
[PMID: 18188456]
[31]
Fujimori, F.; Takahashi, K.; Uchida, C.; Uchida, T. Mice lacking Pin1 develop normally, but are defective in entering cell cycle from G(0) arrest. Biochem. Biophys. Res. Commun., 1999, 265(3), 658-663.
[http://dx.doi.org/10.1006/bbrc.1999.1736] [PMID: 10600477]
[32]
Wang, Z.Y.; Chen, Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood, 2008, 111(5), 2505-2515.
[http://dx.doi.org/10.1182/blood-2007-07-102798] [PMID: 18299451]
[33]
de Thé, H.; Chen, Z. Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat. Rev. Cancer, 2010, 10(11), 775-783.
[http://dx.doi.org/10.1038/nrc2943] [PMID: 20966922]
[34]
Wei, S.; Kozono, S.; Kats, L.; Nechama, M.; Li, W.; Guarnerio, J.; Luo, M.; You, M.H.; Yao, Y.; Kondo, A.; Hu, H.; Bozkurt, G.; Moerke, N.J.; Cao, S.; Reschke, M.; Chen, C.H.; Rego, E.M.; Lo-Coco, F.; Cantley, L.C.; Lee, T.H.; Wu, H.; Zhang, Y.; Pandolfi, P.P.; Zhou, X.Z.; Lu, K.P. Active Pin1 is a key target of all-trans retinoic acid in acute promyelocytic leukemia and breast cancer. Nat. Med., 2015, 21(5), 457-466.
[http://dx.doi.org/10.1038/nm.3839] [PMID: 25849135]
[35]
Kozono, S.; Lin, Y.M.; Seo, H.S.; Pinch, B.; Lian, X.; Qiu, C.; Herbert, M.K.; Chen, C.H.; Tan, L.; Gao, Z.J.; Massefski, W.; Doctor, Z.M.; Jackson, B.P.; Chen, Y.; Dhe-Paganon, S.; Lu, K.P.; Zhou, X.Z. Arsenic targets Pin1 and cooperates with retinoic acid to inhibit cancer-driving pathways and tumor-initiating cells. Nat. Commun., 2018, 9(1), 3069.
[http://dx.doi.org/10.1038/s41467-018-05402-2] [PMID: 30093655]
[36]
Ryo, A.; Liou, Y.C.; Wulf, G.; Nakamura, M.; Lee, S.W.; Lu, K.P. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol., 2002, 22(15), 5281-5295.
[http://dx.doi.org/10.1128/MCB.22.15.5281-5295.2002] [PMID: 12101225]
[37]
Nakatsu, Y.; Otani, Y.; Sakoda, H.; Zhang, J.; Guo, Y.; Okubo, H.; Kushiyama, A.; Fujishiro, M.; Kikuch, T.; Fukushima, T.; Ohno, H.; Tsuchiya, Y.; Kamata, H.; Nagamachi, A.; Inaba, T.; Nishimura, F.; Katagiri, H.; Takahashi, S.; Kurihara, H.; Uchida, T.; Asano, T. Role of Pin1 protein in the pathogenesis of nonalcoholic steatohepatitis in a rodent model. J. Biol. Chem., 2012, 287(53), 44526-44535.
[http://dx.doi.org/10.1074/jbc.M112.397133] [PMID: 23112047]
[38]
Ryo, A.; Suizu, F.; Yoshida, Y.; Perrem, K.; Liou, Y.C.; Wulf, G.; Rottapel, R.; Yamaoka, S.; Lu, K.P. Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell, 2003, 12(6), 1413-1426.
[http://dx.doi.org/10.1016/S1097-2765(03)00490-8] [PMID: 14690596]
[39]
Wulf, G.M.; Ryo, A.; Wulf, G.G.; Lee, S.W.; Niu, T.; Petkova, V.; Lu, K.P. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J., 2001, 20(13), 3459-3472.
[http://dx.doi.org/10.1093/emboj/20.13.3459] [PMID: 11432833]
[40]
Ryo, A.; Nakamura, M.; Wulf, G.; Liou, Y.C.; Lu, K.P. Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nat. Cell Biol., 2001, 3(9), 793-801.
[http://dx.doi.org/10.1038/ncb0901-793] [PMID: 11533658]
[41]
Yang, W.; Zheng, Y.; Xia, Y.; Ji, H.; Chen, X.; Guo, F.; Lyssiotis, C.A.; Aldape, K.; Cantley, L.C.; Lu, Z. ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat. Cell Biol., 2012, 14(12), 1295-1304.
[http://dx.doi.org/10.1038/ncb2629] [PMID: 23178880]
[42]
Bao, L.; Kimzey, A.; Sauter, G.; Sowadski, J.M.; Lu, K.P.; Wang, D.G. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am. J. Pathol., 2004, 164(5), 1727-1737.
[http://dx.doi.org/10.1016/S0002-9440(10)63731-5] [PMID: 15111319]
[43]
Girardini, J.E.; Napoli, M.; Piazza, S.; Rustighi, A.; Marotta, C.; Radaelli, E.; Capaci, V.; Jordan, L.; Quinlan, P.; Thompson, A.; Mano, M.; Rosato, A.; Crook, T.; Scanziani, E.; Means, A.R.; Lozano, G.; Schneider, C.; Del Sal, G. A Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell, 2011, 20(1), 79-91.
[http://dx.doi.org/10.1016/j.ccr.2011.06.004] [PMID: 21741598]
[44]
Rustighi, A.; Zannini, A.; Tiberi, L.; Sommaggio, R.; Piazza, S.; Sorrentino, G.; Nuzzo, S.; Tuscano, A.; Eterno, V.; Benvenuti, F.; Santarpia, L.; Aifantis, I.; Rosato, A.; Bicciato, S.; Zambelli, A.; Del Sal, G. Prolyl-isomerase Pin1 controls normal and cancer stem cells of the breast. EMBO Mol. Med., 2014, 6(1), 99-119.
[http://dx.doi.org/10.1002/emmm.201302909] [PMID: 24357640]
[45]
Lu, J.; Yang, L.; Zhao, H.; Liu, B.; Li, Y.; Wu, H.; Li, Q.; Zeng, B.; Wang, Y.; Ji, W.; Zhou, Y. The polymorphism and haplotypes of PIN1 gene are associated with the risk of lung cancer in Southern and Eastern Chinese populations. Hum. Mutat., 2011, 32(11), 1299-1308.
[http://dx.doi.org/10.1002/humu.21574] [PMID: 21850685]
[46]
Lu, J.; Hu, Z.; Wei, S.; Wang, L.E.; Liu, Z.; El-Naggar, A.K.; Sturgis, E.M.; Wei, Q. A novel functional variant (-842G>C) in the PIN1 promoter contributes to decreased risk of squamous cell carcinoma of the head and neck by diminishing the promoter activity. Carcinogenesis, 2009, 30(10), 1717-1721.
[http://dx.doi.org/10.1093/carcin/bgp171] [PMID: 19625347]
[47]
Liou, Y.C.; Ryo, A.; Huang, H.K.; Lu, P.J.; Bronson, R.; Fujimori, F.; Uchida, T.; Hunter, T.; Lu, K.P. Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes. Proc. Natl. Acad. Sci. USA, 2002, 99(3), 1335-1340.
[http://dx.doi.org/10.1073/pnas.032404099] [PMID: 11805292]
[48]
Peloponese, J.M., Jr; Yasunaga, J.; Kinjo, T.; Watashi, K.; Jeang, K.T. Peptidylproline cis-trans-isomerase Pin1 interacts with human T-cell leukemia virus type 1 tax and modulates its activation of NF-kappaB. J. Virol., 2009, 83(7), 3238-3248.
[http://dx.doi.org/10.1128/JVI.01824-08] [PMID: 19158244]
[49]
Nicole Tsang, Y.H.; Wu, X.W.; Lim, J.S.; Wee Ong, C.; Salto-Tellez, M.; Ito, K.; Ito, Y.; Chen, L.F. Prolyl isomerase Pin1 downregulates tumor suppressor RUNX3 in breast cancer. Oncogene, 2013, 32(12), 1488-1496.
[http://dx.doi.org/10.1038/onc.2012.178] [PMID: 22580604]
[50]
Shen, Z.J.; Esnault, S.; Schinzel, A.; Borner, C.; Malter, J.S. The peptidyl-prolyl isomerase Pin1 facilitates cytokine-induced survival of eosinophils by suppressing Bax activation. Nat. Immunol., 2009, 10(3), 257-265.
[http://dx.doi.org/10.1038/ni.1697] [PMID: 19182807]
[51]
Nakatsu, Y.; Iwashita, M.; Sakoda, H.; Ono, H.; Nagata, K.; Matsunaga, Y.; Fukushima, T.; Fujishiro, M.; Kushiyama, A.; Kamata, H.; Takahashi, S.; Katagiri, H.; Honda, H.; Kiyonari, H.; Uchida, T.; Asano, T. Prolyl isomerase Pin1 negatively regulates AMP-activated protein kinase (AMPK) by associating with the CBS domain in the γ subunit. J. Biol. Chem., 2015, 290(40), 24255-24266.
[http://dx.doi.org/10.1074/jbc.M115.658559] [PMID: 26276391]
[52]
Yeh, E.; Cunningham, M.; Arnold, H.; Chasse, D.; Monteith, T.; Ivaldi, G.; Hahn, W.C.; Stukenberg, P.T.; Shenolikar, S.; Uchida, T.; Counter, C.M.; Nevins, J.R.; Means, A.R.; Sears, R. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat. Cell Biol., 2004, 6(4), 308-318.
[http://dx.doi.org/10.1038/ncb1110] [PMID: 15048125]
[53]
Rizzolio, F.; Lucchetti, C.; Caligiuri, I.; Marchesi, I.; Caputo, M.; Klein-Szanto, A.J.; Bagella, L.; Castronovo, M.; Giordano, A. Retinoblastoma tumor-suppressor protein phosphorylation and inactivation depend on direct interaction with Pin1. Cell Death Differ., 2012, 19(7), 1152-1161.
[http://dx.doi.org/10.1038/cdd.2011.202] [PMID: 22322860]
[54]
Min, S.H.; Zhou, X.Z.; Lu, K.P. The role of Pin1 in the development and treatment of cancer. Arch. Pharm. Res., 2016, 39(12), 1609-1620.
[http://dx.doi.org/10.1007/s12272-016-0821-x] [PMID: 27572155]
[55]
Zhou, X.Z.; Lu, K.P. The isomerase PIN1 controls numerous cancer-driving pathways and is a unique drug target. Nat. Rev. Cancer, 2016, 16(7), 463-478.
[http://dx.doi.org/10.1038/nrc.2016.49] [PMID: 27256007]
[56]
Kim, M.R.; Choi, H.K.; Cho, K.B.; Kim, H.S.; Kang, K.W. Involvement of Pin1 induction in epithelial-mesenchymal transition of tamoxifen-resistant breast cancer cells. Cancer Sci., 2009, 100(10), 1834-1841.
[http://dx.doi.org/10.1111/j.1349-7006.2009.01260.x] [PMID: 19681904]
[57]
Kanaoka, R.; Kushiyama, A.; Seno, Y.; Nakatsu, Y.; Matsunaga, Y.; Fukushima, T.; Tsuchiya, Y.; Sakoda, H.; Fujishiro, M.; Yamamotoya, T.; Kamata, H.; Matsubara, A.; Asano, T. Pin1 inhibitor juglone exerts anti-oncogenic effects on LNCaP and DU145 cells despite the patterns of gene regulation by Pin1 differing between these cell lines. PLoS One, 2015, 10(6)e0127467
[http://dx.doi.org/10.1371/journal.pone.0127467] [PMID: 26039047]
[58]
Wulf, G.; Garg, P.; Liou, Y.C.; Iglehart, D.; Lu, K.P. Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J., 2004, 23(16), 3397-3407.
[http://dx.doi.org/10.1038/sj.emboj.7600323] [PMID: 15257284]
[59]
Nakatsu, Y.; Sakoda, H.; Kushiyama, A.; Zhang, J.; Ono, H.; Fujishiro, M.; Kikuchi, T.; Fukushima, T.; Yoneda, M.; Ohno, H.; Horike, N.; Kanna, M.; Tsuchiya, Y.; Kamata, H.; Nishimura, F.; Isobe, T.; Ogihara, T.; Katagiri, H.; Oka, Y.; Takahashi, S.; Kurihara, H.; Uchida, T.; Asano, T. Peptidyl-prolyl cis/trans isomerase NIMA-interacting 1 associates with insulin receptor substrate-1 and enhances insulin actions and adipogenesis. J. Biol. Chem., 2011, 286(23), 20812-20822.
[http://dx.doi.org/10.1074/jbc.M110.206904] [PMID: 21454638]
[60]
Uchida, T.; Furumai, K.; Fukuda, T.; Akiyama, H.; Takezawa, M.; Asano, T.; Fujimori, F.; Uchida, C. Prolyl isomerase Pin1 regulates mouse embryonic fibroblast differentiation into adipose cells. PLoS One, 2012, 7(3)e31823
[http://dx.doi.org/10.1371/journal.pone.0031823] [PMID: 22412843]
[61]
Nakatsu, Y.; Sakoda, H.; Kushiyama, A.; Ono, H.; Fujishiro, M.; Horike, N.; Yoneda, M.; Ohno, H.; Tsuchiya, Y.; Kamata, H.; Tahara, H.; Isobe, T.; Nishimura, F.; Katagiri, H.; Oka, Y.; Fukushima, T.; Takahashi, S.; Kurihara, H.; Uchida, T.; Asano, T. Pin1 associates with and induces translocation of CRTC2 to the cytosol, thereby suppressing cAMP-responsive element transcriptional activity. J. Biol. Chem., 2010, 285(43), 33018-33027.
[http://dx.doi.org/10.1074/jbc.M110.137836] [PMID: 20675384]
[62]
Han, Y.; Lee, S.H.; Bahn, M.; Yeo, C.Y.; Lee, K.Y. Pin1 enhances adipocyte differentiation by positively regulating the transcriptional activity of PPARγ. Mol. Cell. Endocrinol., 2016, 436(C), 150-158.
[http://dx.doi.org/10.1016/j.mce.2016.07.030] [PMID: 27475846]
[63]
Lee, Y.M.; Shin, S.Y.; Jue, S.S.; Kwon, I.K.; Cho, E.H.; Cho, E.S.; Park, S.H.; Kim, E.C. The role of PIN1 on odontogenic and adipogenic differentiation in human dental pulp stem cells. Stem Cells Dev., 2014, 23(6), 618-630.
[http://dx.doi.org/10.1089/scd.2013.0339] [PMID: 24219242]
[64]
Toko, H.; Konstandin, M.H.; Doroudgar, S.; Ormachea, L.; Joyo, E.; Joyo, A.Y.; Din, S.; Gude, N.A.; Collins, B.; Völkers, M.; Thuerauf, D.J.; Glembotski, C.C.; Chen, C.H.; Lu, K.P.; Müller, O.J.; Uchida, T.; Sussman, M.A. Regulation of cardiac hypertrophic signaling by prolyl isomerase Pin1. Circ. Res., 2013, 112(9), 1244-1252.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301084] [PMID: 23487407]
[65]
Liu, X.; Liang, E.; Song, X.; Du, Z.; Zhang, Y.; Zhao, Y. Inhibition of Pin1 alleviates myocardial fibrosis and dysfunction in STZ-induced diabetic mice. Biochem. Biophys. Res. Commun., 2016, 479(1), 109-115.
[http://dx.doi.org/10.1016/j.bbrc.2016.09.050] [PMID: 27634219]
[66]
Wu, X.; Li, M.; Chen, S.Q.; Li, S.; Guo, F. Pin1 facilitates isoproterenol‑induced cardiac fibrosis and collagen deposition by promoting oxidative stress and activating the MEK1/2‑ERK1/2 signal transduction pathway in rats. Int. J. Mol. Med., 2018, 41(3), 1573-1583.
[PMID: 29286102]
[67]
Chiasson, V.L.; Munshi, N.; Chatterjee, P.; Young, K.J.; Mitchell, B.M. Pin1 deficiency causes endothelial dysfunction and hypertension. Hypertension, 2011, 58(3), 431-438.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.172338] [PMID: 21810655]
[68]
Wang, Y.; Li, Z.; Zhang, Y.; Yang, W.; Sun, J.; Shan, L.; Li, W. Targeting Pin1 Protects Mouse Cardiomyocytes from High-Dose Alcohol-Induced Apoptosis. Oxid. Med. Cell. Longev., 2016, 20164528906
[http://dx.doi.org/10.1155/2016/4528906] [PMID: 26697133]
[69]
Kennard, S.; Ruan, L.; Buffett, R.J.; Fulton, D.; Venema, R.C. TNFα reduces eNOS activity in endothelial cells through serine 116 phosphorylation and Pin1 binding: Confirmation of a direct, inhibitory interaction of Pin1 with eNOS. Vascul. Pharmacol., 2016, 81, 61-68.
[http://dx.doi.org/10.1016/j.vph.2016.04.003] [PMID: 27073025]
[70]
Wang, J.Z.; Li, S.R.; Li, Y.L.; Zhang, Y.Z.; Zhang, T.; Zhao, C.X.; Yao, C.X.; Du, L.F. Could Pin1 help us conquer essential hypertension at an earlier stage? A promising early-diagnostic biomarker and its therapeutic implications for the disease. Med. Hypotheses, 2013, 81(5), 931-935.
[http://dx.doi.org/10.1016/j.mehy.2013.08.020] [PMID: 24021617]
[71]
Chiasson, V.L.; Munshi, N.; Young, K.J.; Tinsley, J.H.; Mitchell, B.M. Inhibition of the prolyl isomerase pin1 increases eNOS Ser116 phosphorylation, endothelial dysfunction, and blood pressure. Hypertension, 2009, 54(4), E95-E95.
[72]
Hennig, L.; Christner, C.; Kipping, M.; Schelbert, B.; Rücknagel, K.P.; Grabley, S.; Küllertz, G.; Fischer, G. Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry, 1998, 37(17), 5953-5960.
[http://dx.doi.org/10.1021/bi973162p] [PMID: 9558330]
[73]
Urusova, D.V.; Shim, J.H.; Kim, D.J.; Jung, S.K.; Zykova, T.A.; Carper, A.; Bode, A.M.; Dong, Z. Epigallocatechin-gallate suppresses tumorigenesis by directly targeting Pin1. Cancer Prev. Res. (Phila.), 2011, 4(9), 1366-1377.
[http://dx.doi.org/10.1158/1940-6207.CAPR-11-0301] [PMID: 21750208]
[74]
Zhang, Y.X. Inhibitors targeting the enzymatic activity and biological function of Pin1. Mini Rev. Org. Chem., 2004, 1(4), 359-366.
[http://dx.doi.org/10.2174/1570193043403055]
[75]
Zheng, Y.; Pu, W.; Li, J.; Shen, X.; Zhou, Q.; Fan, X.; Yang, S.Y.; Yu, Y.; Chen, Q.; Wang, C.; Wu, X.; Peng, Y. Discovery of a Prenylated Flavonol Derivative as a Pin1 Inhibitor to Suppress Hepatocellular Carcinoma by Modulating MicroRNA Biogenesis. Chem. Asian J., 2019, 14(1), 130-134.
[http://dx.doi.org/10.1002/asia.201801461] [PMID: 30474357]
[76]
Wu, D.; Huang, D.; Li, L.L.; Ni, P.; Li, X.X.; Wang, B.; Han, Y.N.; Shao, X.Q.; Zhao, D.; Chu, W.F.; Li, B.Y. TGF-β1-PML SUMOylation-peptidyl-prolyl cis-trans isomerase NIMA-interacting 1 (Pin1) form a positive feedback loop to regulate cardiac fibrosis. J. Cell. Physiol., 2019, 234(5), 6263-6273.
[http://dx.doi.org/10.1002/jcp.27357] [PMID: 30246389]
[77]
Wang, J.; Liu, K.; Wang, X.F.; Sun, D.J. Juglone reduces growth and migration of U251 glioblastoma cells and disrupts angiogenesis. Oncol. Rep., 2017, 38(4), 1959-1966.
[http://dx.doi.org/10.3892/or.2017.5878] [PMID: 28791366]
[78]
Kim, M.R.; Choi, H.S.; Yang, J.W.; Park, B.C.; Kim, J.A.; Kang, K.W. Enhancement of vascular endothelial growth factor-mediated angiogenesis in tamoxifen-resistant breast cancer cells: role of Pin1 overexpression. Mol. Cancer Ther., 2009, 8(8), 2163-2171.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-1061] [PMID: 19671742]
[79]
Lee, N.Y.; Choi, H.K.; Shim, J.H.; Kang, K.W.; Dong, Z.; Choi, H.S. The prolyl isomerase Pin1 interacts with a ribosomal protein S6 kinase to enhance insulin-induced AP-1 activity and cellular transformation. Carcinogenesis, 2009, 30(4), 671-681.
[http://dx.doi.org/10.1093/carcin/bgp027] [PMID: 19168580]
[80]
Fan, G.; Fan, Y.; Gupta, N.; Matsuura, I.; Liu, F.; Zhou, X.Z.; Lu, K.P.; Gélinas, C. Peptidyl-prolyl isomerase Pin1 markedly enhances the oncogenic activity of the rel proteins in the nuclear factor-kappaB family. Cancer Res., 2009, 69(11), 4589-4597.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-4117] [PMID: 19458071]
[81]
Khanal, P.; Namgoong, G.M.; Kang, B.S.; Woo, E.R.; Choi, H.S. The prolyl isomerase Pin1 enhances HER-2 expression and cellular transformation via its interaction with mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1. Mol. Cancer Ther., 2010, 9(3), 606-616.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0560] [PMID: 20179161]
[82]
Zhou, L.; Park, B.H.; Park, J.H.; Jang, K.Y.; Park, H.S.; Wagle, S.; Lee, K.B.; Kim, J.R. Overexpression of the prolyl isomerase PIN1 promotes cell growth in osteosarcoma cells. Oncol. Rep., 2013, 29(1), 193-198.
[http://dx.doi.org/10.3892/or.2012.2112] [PMID: 23129219]
[83]
Klotz, L.O.; Hou, X.; Jacob, C. 1,4-naphthoquinones: from oxidative damage to cellular and inter-cellular signaling. Molecules, 2014, 19(9), 14902-14918.
[http://dx.doi.org/10.3390/molecules190914902] [PMID: 25232709]
[84]
Klaus, V.; Hartmann, T.; Gambini, J.; Graf, P.; Stahl, W.; Hartwig, A.; Klotz, L.O. 1,4-Naphthoquinones as inducers of oxidative damage and stress signaling in HaCaT human keratinocytes. Arch. Biochem. Biophys., 2010, 496(2), 93-100.
[http://dx.doi.org/10.1016/j.abb.2010.02.002] [PMID: 20153715]
[85]
Fila, C.; Metz, C.; van der Sluijs, P. Juglone inactivates cysteine-rich proteins required for progression through mitosis. J. Biol. Chem., 2008, 283(31), 21714-21724.
[http://dx.doi.org/10.1074/jbc.M710264200] [PMID: 18539601]
[86]
Xi, L.; Wang, Y.; He, Q.; Zhang, Q.; Du, L. Interaction between Pin1 and its natural product inhibitor epigallocatechin-3-gallate by spectroscopy and molecular dynamics simulations. Spectrochim. Acta A Mol. Biomol. Spectrosc., 2016, 169, 134-143.
[http://dx.doi.org/10.1016/j.saa.2016.06.036] [PMID: 27372509]
[87]
Kumazoe, M.; Sugihara, K.; Tsukamoto, S.; Huang, Y.; Tsurudome, Y.; Suzuki, T.; Suemasu, Y.; Ueda, N.; Yamashita, S.; Kim, Y.; Yamada, K.; Tachibana, H. 67-kDa laminin receptor increases cGMP to induce cancer-selective apoptosis. J. Clin. Invest., 2013, 123(2), 787-799.
[http://dx.doi.org/10.1172/JCI64768] [PMID: 23348740]
[88]
Martinotti, S.; Ranzato, E.; Burlando, B. (-)- Epigallocatechin-3-gallate induces GRP78 accumulation in the ER and shifts mesothelioma constitutive UPR into proapoptotic ER stress. J. Cell. Physiol., 2018, 233(10), 7082-7090.
[http://dx.doi.org/10.1002/jcp.26631] [PMID: 29744892]
[89]
Liu, T.; Liu, Y.; Kao, H.Y.; Pei, D. Membrane permeable cyclic peptidyl inhibitors against human Peptidylprolyl Isomerase Pin1. J. Med. Chem., 2010, 53(6), 2494-2501.
[http://dx.doi.org/10.1021/jm901778v] [PMID: 20180533]
[90]
Wildemann, D.; Erdmann, F.; Alvarez, B.H.; Stoller, G.; Zhou, X.Z.; Fanghänel, J.; Schutkowski, M.; Lu, K.P.; Fischer, G. Nanomolar inhibitors of the peptidyl prolyl cis/trans isomerase Pin1 from combinatorial peptide libraries. J. Med. Chem., 2006, 49(7), 2147-2150.
[http://dx.doi.org/10.1021/jm060036n] [PMID: 16570909]
[91]
Zhang, Y.; Daum, S.; Wildemann, D.; Zhou, X.Z.; Verdecia, M.A.; Bowman, M.E.; Lücke, C.; Hunter, T.; Lu, K.P.; Fischer, G.; Noel, J.P. Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem. Biol., 2007, 2(5), 320-328.
[http://dx.doi.org/10.1021/cb7000044] [PMID: 17518432]
[92]
Bedewy, W.; Liao, H.; Abou-Taleb, N.A.; Hammad, S.F.; Nasr, T.; Pei, D. Generation of a cell-permeable cycloheptapeptidyl inhibitor against the peptidyl-prolyl isomerase Pin1. Org. Biomol. Chem., 2017, 15(21), 4540-4543.
[http://dx.doi.org/10.1039/C7OB00430C] [PMID: 28517007]
[93]
Lian, X.; Lin, Y.M.; Kozono, S.; Herbert, M.K.; Li, X.; Yuan, X.; Guo, J.; Guo, Y.; Tang, M.; Lin, J.; Huang, Y.; Wang, B.; Qiu, C.; Tsai, C.Y.; Xie, J.; Gao, Z.J.; Wu, Y.; Liu, H.; Zhou, X.Z.; Lu, K.P.; Chen, Y. Pin1 inhibition exerts potent activity against acute myeloid leukemia through blocking multiple cancer-driving pathways. J. Hematol. Oncol., 2018, 11(1), 73.
[http://dx.doi.org/10.1186/s13045-018-0611-7] [PMID: 29848341]
[94]
Liao, X.H.; Zhang, A.L.; Zheng, M.; Li, M.Q.; Chen, C.P.; Xu, H.; Chu, Q.S.; Yang, D.; Lu, W.; Tsai, T.F.; Liu, H.; Zhou, X.Z.; Lu, K.P. Chemical or genetic Pin1 inhibition exerts potent anticancer activity against hepatocellular carcinoma by blocking multiple cancer-driving pathways. Sci. Rep., 2017, 7, 43639.
[http://dx.doi.org/10.1038/srep43639] [PMID: 28262728]
[95]
Zheng, M.; Xu, H.; Liao, X.H.; Chen, C.P.; Zhang, A.L.; Lu, W.; Wang, L.; Yang, D.; Wang, J.; Liu, H.; Zhou, X.Z.; Lu, K.P. Inhibition of the prolyl isomerase Pin1 enhances the ability of sorafenib to induce cell death and inhibit tumor growth in hepatocellular carcinoma. Oncotarget, 2017, 8(18), 29771-29784.
[http://dx.doi.org/10.18632/oncotarget.15967] [PMID: 28404959]
[96]
Wei, S.; Yoshida, N.; Finn, G.; Kozono, S.; Nechama, M.; Kyttaris, V.C.; Zhen Zhou, X.; Tsokos, G.C.; Ping Lu, K. Pin1-Targeted Therapy for Systemic Lupus Erythematosus. Arthritis Rheumatol., 2016, 68(10), 2503-2513.
[http://dx.doi.org/10.1002/art.39741] [PMID: 27159270]
[97]
Nechama, M.; Kwon, J.; Wei, S.; Kyi, A.T.; Welner, R.S.; Ben-Dov, I.Z.; Arredouani, M.S.; Asara, J.M.; Chen, C.H.; Tsai, C.Y.; Nelson, K.F.; Kobayashi, K.S.; Israel, E.; Zhou, X.Z.; Nicholson, L.K.; Lu, K.P. The IL-33-PIN1-IRAK-M axis is critical for type 2 immunity in IL-33-induced allergic airway inflammation. Nat. Commun., 2018, 9(1), 1603.
[http://dx.doi.org/10.1038/s41467-018-03886-6] [PMID: 29686383]
[98]
Campaner, E.; Rustighi, A.; Zannini, A.; Cristiani, A.; Piazza, S.; Ciani, Y.; Kalid, O.; Golan, G.; Baloglu, E.; Shacham, S.; Valsasina, B.; Cucchi, U.; Pippione, A.C.; Lolli, M.L.; Giabbai, B.; Storici, P.; Carloni, P.; Rossetti, G.; Benvenuti, F.; Bello, E.; D’Incalci, M.; Cappuzzello, E.; Rosato, A.; Del Sal, G. A covalent PIN1 inhibitor selectively targets cancer cells by a dual mechanism of action. Nat. Commun., 2017, 8, 15772.
[http://dx.doi.org/10.1038/ncomms15772] [PMID: 28598431]
[99]
Pu, W.; Li, J.; Zheng, Y.; Shen, X.; Fan, X.; Zhou, J.K.; He, J.; Deng, Y.; Liu, X.; Wang, C.; Yang, S.; Chen, Q.; Liu, L.; Zhang, G.; Wei, Y.Q.; Peng, Y. Targeting Pin1 by inhibitor API-1 regulates microRNA biogenesis and suppresses hepatocellular carcinoma development. Hepatology, 2018, 68(2), 547-560.
[http://dx.doi.org/10.1002/hep.29819] [PMID: 29381806]
[100]
Dong, L.; Marakovits, J.; Hou, X.; Guo, C.; Greasley, S.; Dagostino, E.; Ferre, R.; Johnson, M.C.; Kraynov, E.; Thomson, J.; Pathak, V.; Murray, B.W. Structure-based design of novel human Pin1 inhibitors (II). Bioorg. Med. Chem. Lett., 2010, 20(7), 2210-2214.
[http://dx.doi.org/10.1016/j.bmcl.2010.02.033] [PMID: 20207139]
[101]
Russo Spena, C.; De Stefano, L.; Palazzolo, S.; Salis, B.; Granchi, C.; Minutolo, F.; Tuccinardi, T.; Fratamico, R.; Crotti, S.; D’Aronco, S.; Agostini, M.; Corona, G.; Caligiuri, I.; Canzonieri, V.; Rizzolio, F. Liposomal delivery of a Pin1 inhibitor complexed with cyclodextrins as new therapy for high-grade serous ovarian cancer. J. Control. Release, 2018, 281, 1-10.
[http://dx.doi.org/10.1016/j.jconrel.2018.04.055] [PMID: 29746956]
[102]
Potter, A.; Oldfield, V.; Nunns, C.; Fromont, C.; Ray, S.; Northfield, C.J.; Bryant, C.J.; Scrace, S.F.; Robinson, D.; Matossova, N.; Baker, L.; Dokurno, P.; Surgenor, A.E.; Davis, B.; Richardson, C.M.; Murray, J.B.; Moore, J.D. Discovery of cell-active phenyl-imidazole Pin1 inhibitors by structure-guided fragment evolution. Bioorg. Med. Chem. Lett., 2010, 20(22), 6483-6488.
[http://dx.doi.org/10.1016/j.bmcl.2010.09.063] [PMID: 20932746]
[103]
Potter, A.J.; Ray, S.; Gueritz, L.; Nunns, C.L.; Bryant, C.J.; Scrace, S.F.; Matassova, N.; Baker, L.; Dokurno, P.; Robinson, D.A.; Surgenor, A.E.; Davis, B.; Murray, J.B.; Richardson, C.M.; Moore, J.D. Structure-guided design of alpha-amino acid-derived Pin1 inhibitors. Bioorg. Med. Chem. Lett., 2010, 20(2), 586-590.
[http://dx.doi.org/10.1016/j.bmcl.2009.11.090] [PMID: 19969456]
[104]
Guo, C.; Hou, X.; Dong, L.; Marakovits, J.; Greasley, S.; Dagostino, E.; Ferre, R.; Johnson, M.C.; Humphries, P.S.; Li, H.; Paderes, G.D.; Piraino, J.; Kraynov, E.; Murray, B.W. Structure-based design of novel human Pin1 inhibitors (III): optimizing affinity beyond the phosphate recognition pocket. Bioorg. Med. Chem. Lett., 2014, 24(17), 4187-4191.
[http://dx.doi.org/10.1016/j.bmcl.2014.07.044] [PMID: 25091930]
[105]
Liu, X.; Chen, Y.; Zhang, Y.; Du, J.; Lv, Y.; Mo, S.; Liu, Y.; Ding, F.; Wu, J.; Li, J. Juglone potentiates TRAIL‑induced apoptosis in human melanoma cells via activating the ROS‑p38‑p53 pathway. Mol. Med. Rep., 2017, 16(6), 9645-9651.
[http://dx.doi.org/10.3892/mmr.2017.7806] [PMID: 29039537]
[106]
Yang, D.; Luo, W.; Wang, J.; Zheng, M.; Liao, X.H.; Zhang, N.; Lu, W.; Wang, L.; Chen, A.Z.; Wu, W.G.; Liu, H.; Wang, S.B.; Zhou, X.Z.; Lu, K.P. A novel controlled release formulation of the Pin1 inhibitor ATRA to improve liver cancer therapy by simultaneously blocking multiple cancer pathways. J. Control. Release, 2018, 269, 405-422.
[http://dx.doi.org/10.1016/j.jconrel.2017.11.031] [PMID: 29170140]
[107]
Wang, J.Z.; Liu, G.J.; Li, Z.Y.; Wang, X.H. Pin1 in cardiovascular dysfunction: A potential double-edge role. Int. J. Cardiol., 2016, 212, 280-283.
[http://dx.doi.org/10.1016/j.ijcard.2016.03.181] [PMID: 27057935]
[108]
Costantino, S.; Paneni, F.; Lüscher, T.F.; Cosentino, F. Pin1 inhibitor Juglone prevents diabetic vascular dysfunction. Int. J. Cardiol., 2016, 203, 702-707.
[http://dx.doi.org/10.1016/j.ijcard.2015.10.221] [PMID: 26583846]
[109]
Ruan, L.; Torres, C.M.; Qian, J.; Chen, F.; Mintz, J.D.; Stepp, D.W.; Fulton, D.; Venema, R.C. Pin1 prolyl isomerase regulates endothelial nitric oxide synthase. Arterioscler. Thromb. Vasc. Biol., 2011, 31(2), 392-398.
[http://dx.doi.org/10.1161/ATVBAHA.110.213181] [PMID: 21051667]
[110]
Liu, M.; Yu, P.; Jiang, H.; Yang, X.; Zhao, J.; Zou, Y.; Ge, J. The essential role of pin1 via NF-κB Signaling in vascular inflammation and atherosclerosis in ApoE-/- mice. Int. J. Mol. Sci., 2017, 18(3)pii: E644
[http://dx.doi.org/10.3390/ijms18030644] [PMID: 28300760]
[111]
Lv, L.; Ye, M.; Duan, R.; Yuan, K.; Chen, J.; Liang, W.; Zhou, Z.; Zhang, L. Downregulation of pin1 in human atherosclerosis and its association with vascular smooth muscle cell senescence. J. Vasc. Surg., 2017, S0741-5214(17), 32213-32219,
[112]
Shen, Z.J.; Braun, R.K.; Hu, J.; Xie, Q.; Chu, H.; Love, R.B.; Stodola, L.A.; Rosenthal, L.A.; Szakaly, R.J.; Sorkness, R.L.; Malter, J.S. Pin1 protein regulates Smad protein signaling and pulmonary fibrosis. J. Biol. Chem., 2012, 287(28), 23294-23305.
[http://dx.doi.org/10.1074/jbc.M111.313684] [PMID: 22613712]
[113]
Yang, J.W.; Hien, T.T.; Lim, S.C.; Jun, D.W.; Choi, H.S.; Yoon, J.H.; Cho, I.J.; Kang, K.W. Pin1 induction in the fibrotic liver and its roles in TGF-β1 expression and Smad2/3 phosphorylation. J. Hepatol., 2014, 60(6), 1235-1241.
[http://dx.doi.org/10.1016/j.jhep.2014.02.004] [PMID: 24530597]
[114]
Mori, T.; Hidaka, M.; Ikuji, H.; Yoshizawa, I.; Toyohara, H.; Okuda, T.; Uchida, C.; Asano, T.; Yotsu-Yamashita, M.; Uchida, T. A high-throughput screen for inhibitors of the prolyl isomerase, Pin1, identifies a seaweed polyphenol that reduces adipose cell differentiation. Biosci. Biotechnol. Biochem., 2014, 78(5), 832-838.
[http://dx.doi.org/10.1080/09168451.2014.905189] [PMID: 25035986]
[115]
Marsolier, J.; Perichon, M.; DeBarry, J.D.; Villoutreix, B.O.; Chluba, J.; Lopez, T.; Garrido, C.; Zhou, X.Z.; Lu, K.P.; Fritsch, L.; Ait-Si-Ali, S.; Mhadhbi, M.; Medjkane, S.; Weitzman, J.B. Theileria parasites secrete a prolyl isomerase to maintain host leukocyte transformation. Nature, 2015, 520(7547), 378-382.
[http://dx.doi.org/10.1038/nature14044] [PMID: 25624101]
[116]
Shen, Z.J.; Hu, J.; Ali, A.; Pastor, J.; Shiizaki, K.; Blank, R.D.; Kuro-o, M.; Malter, J.S. Pin1 null mice exhibit low bone mass and attenuation of BMP signaling. PLoS One, 2013, 8(5)e63565
[http://dx.doi.org/10.1371/journal.pone.0063565] [PMID: 23675491]
[117]
Atchison, F.W.; Means, A.R. Spermatogonial depletion in adult Pin1-deficient mice. Biol. Reprod., 2003, 69(6), 1989-1997.
[http://dx.doi.org/10.1095/biolreprod.103.020859] [PMID: 12930711]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 27
ISSUE: 20
Year: 2020
Published on: 08 June, 2020
Page: [3314 - 3329]
Pages: 16
DOI: 10.2174/0929867325666181105120911
Price: $65

Article Metrics

PDF: 71
HTML: 3



Related Article(s)

Most Downloaded Article(s)