{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T08:39:49Z","timestamp":1790671189229,"version":"4.1.0"},"reference-count":112,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T00:00:00Z","timestamp":1661817600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell Dev. Biol."],"abstract":"<jats:p>More than 20\u00a0years since its discovery, our understanding of Pin1 function in various diseases continues to improve. Pin1 plays a crucial role in pathogenesis and has been implicated in metabolic disorders, cardiovascular diseases, inflammatory diseases, viral infection, cancer and neurodegenerative diseases such as Alzheimer\u2019s, Parkinson\u2019s and Huntington\u2019s disease. In particular, the role of Pin1 in neurodegenerative diseases and cancer has been extensively studied. Our understanding of Pin1 in cancer also led to the development of cancer therapeutic drugs targeting Pin1, with some currently in clinical trial phases. However, identifying a Pin1-specific drug with good cancer therapeutic effect remains elusive, thus leading to the continued efforts in Pin1 research. The importance of Pin1 is highlighted by the presence of Pin1 orthologs across various species: from vertebrates to invertebrates and Kingdom Animalia to Plantae. Among these Pin1 orthologs, their sequence and structural similarity demonstrate the presence of conservation. Moreover, their similar functionality between species further highlights the conservancy of Pin1. As researchers continue to unlock the mysteries of Pin1 in various diseases, using different Pin1 models might shed light on how to better target Pin1 for disease therapeutics. This review aims to highlight the various Pin1 orthologs in numerous species and their divergent functional roles. We will examine their sequence and structural similarities and discuss their functional similarities and uniqueness to demonstrate the interconnectivity of Pin1 orthologs in multiple diseases.<\/jats:p>","DOI":"10.3389\/fcell.2022.956071","type":"journal-article","created":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T08:26:27Z","timestamp":1661847987000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["The kingdom of the prolyl-isomerase Pin1: The structural and functional convergence and divergence of Pin1"],"prefix":"10.3389","volume":"10","author":[{"given":"Yew Mun","family":"Lee","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Deryn En-Jie","family":"Teoh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kay","family":"Yeung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yih-Cherng","family":"Liou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,8,30]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"110","DOI":"10.3389\/fncel.2016.00110","article-title":"Effects of Pin1 loss in hdh(q111) knock-in mice","volume":"10","author":"Agostoni","year":"2016","journal-title":"Front. Cell. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"e14656","DOI":"10.1371\/journal.pone.0014656","article-title":"Prolyl isomerase pin1 protects mice from endotoxin shock","volume":"6","author":"Akiyama","year":"2011","journal-title":"PLoS ONE"},{"key":"B3","doi-asserted-by":"publisher","first-page":"9340","DOI":"10.1523\/jneurosci.22-21-09340.2002","article-title":"Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein","volume":"22","author":"Allen","year":"2002","journal-title":"J. Neurosci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"3579","DOI":"10.1242\/dev.00584","article-title":"Pin1 regulates the timing of mammalian primordial germ cell proliferation","volume":"130","author":"Atchison","year":"2003","journal-title":"Development"},{"key":"B5","doi-asserted-by":"publisher","first-page":"E4203","DOI":"10.1073\/pnas.1310001110","article-title":"Autophosphorylation and Pin1 binding coordinate DNA damage-induced HIPK2 activation and cell death","volume":"110","author":"Bitomsky","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B6","doi-asserted-by":"publisher","first-page":"812","DOI":"10.1016\/j.celrep.2015.09.026","article-title":"Prolyl isomerase Pin1 regulates axon guidance by stabilizing CRMP2A selectively in distal axons","volume":"13","author":"Balastik","year":"2015","journal-title":"Cell Rep."},{"key":"B7","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1002\/ame2.12209","article-title":"Animal models in the study of alzheimer's disease and Parkinson's disease: A historical perspective","volume":"5","author":"Banerjee","year":"2022","journal-title":"Anim. Model. Exp. Med."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1016\/j.jmb.2006.10.078","article-title":"Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution","volume":"365","author":"Behrsin","year":"2007","journal-title":"J. Mol. Biol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"15772","DOI":"10.1038\/ncomms15772","article-title":"A covalent PIN1 inhibitor selectively targets cancer cells by a dual mechanism of action","volume":"8","author":"Campaner","year":"2017","journal-title":"Nat. Commun."},{"key":"B10","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1093\/nar\/29.3.767","article-title":"Juglone, an inhibitor of the peptidyl-prolyl isomerase Pin1, also directly blocks transcription","volume":"29","author":"Chao","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"698","DOI":"10.1242\/dev.146001","article-title":"Tissue-specific regulation of alternative polyadenylation represses expression of a neuronal ankyrin isoform in C. elegans epidermal development","volume":"144","author":"Chen","year":"2017","journal-title":"Development"},{"key":"B12","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1038\/s41419-018-0844-y","article-title":"Prolyl isomerase Pin1: A promoter of cancer and a target for therapy","volume":"9","author":"Chen","year":"2018","journal-title":"Cell Death Dis."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1367","DOI":"10.3389\/fphar.2018.01367","article-title":"PIN1 in cell cycle control and cancer","volume":"9","author":"Cheng","year":"2018","journal-title":"Front. Pharmacol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"369","DOI":"10.3389\/fcell.2019.00369","article-title":"Targeting PIN1 as a therapeutic approach for hepatocellular carcinoma","volume":"7","author":"Cheng","year":"2019","journal-title":"Front. Cell Dev. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"359","DOI":"10.3390\/biomedicines9040359","article-title":"Targeting Pin1 for modulation of cell motility and cancer therapy","volume":"9","author":"Chuang","year":"2021","journal-title":"Biomedicines"},{"key":"B16","doi-asserted-by":"publisher","first-page":"D480","DOI":"10.1093\/nar\/gkaa1100","article-title":"UniProt: The universal protein knowledgebase in 2021","volume":"49","author":"Consortium","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"B17","doi-asserted-by":"publisher","first-page":"e304","DOI":"10.1038\/bcj.2015.25","article-title":"Acute promyelocytic leukemia: Where did we start, where are we now, and the future","volume":"5","author":"Coombs","year":"2015","journal-title":"Blood Cancer J."},{"key":"B18","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1186\/s12868-015-0158-2","article-title":"Death Associated Protein Kinase (DAPK) -mediated neurodegenerative mechanisms in nematode excitotoxicity","volume":"16","author":"Del Rosario","year":"2015","journal-title":"BMC Neurosci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"9622","DOI":"10.1021\/acs.jmedchem.6b00411","article-title":"Peptidyl-proline isomerases (PPIases): Targets for natural products and natural product-inspired compounds","volume":"59","author":"Dunyak","year":"2016","journal-title":"J. Med. Chem."},{"key":"B20","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1016\/j.molbiopara.2007.03.004","article-title":"The Trypanosoma cruzi PIN1 gene encodes a parvulin peptidyl-prolyl cis\/trans isomerase able to replace the essential ESS1 in Saccharomyces cerevisiae","volume":"153","author":"Erben","year":"2007","journal-title":"Mol. Biochem. Parasitol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1016\/j.bbrc.2012.05.157","article-title":"The Caenorhabditis elegans parvulin gene subfamily and their expression under cold or heat stress along with the fkb subfamily","volume":"423","author":"Fasseas","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B22","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1006\/bbrc.1999.1736","article-title":"Mice lacking Pin1 develop normally but are defective in entering cell cycle from G0 arrest","volume":"265","author":"Fujimori","year":"1999","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B23","doi-asserted-by":"publisher","first-page":"2226","DOI":"10.1126\/science.282.5397.2226","article-title":"Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue","volume":"282","author":"G\u00e4lweiler","year":"1998","journal-title":"Science"},{"key":"B24","doi-asserted-by":"publisher","first-page":"21955","DOI":"10.1074\/jbc.m112.444224","article-title":"The peptidyl-prolyl isomerase Pin1 up-regulation and proapoptotic function in dopaminergic neurons","volume":"288","author":"Ghosh","year":"2013","journal-title":"J. Biol. Chem."},{"key":"B25","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1016\/j.ccr.2011.06.004","article-title":"A Pin1\/mutant p53 axis promotes aggressiveness in breast cancer","volume":"20","author":"Girardini","year":"2011","journal-title":"Cancer Cell"},{"key":"B26","doi-asserted-by":"publisher","first-page":"2901","DOI":"10.1016\/j.febslet.2010.04.077","article-title":"Functional characterization of two novel parvulins in Trypanosoma brucei","volume":"584","author":"Goh","year":"2010","journal-title":"FEBS Lett."},{"key":"B27","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1111\/j.1750-3639.2007.00051.x","article-title":"A decade of tau transgenic animal models and beyond","volume":"17","author":"G\u00f6tz","year":"2007","journal-title":"Brain Pathol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"17979","DOI":"10.1073\/pnas.1106198108","article-title":"Ser46 phosphorylation and prolyl-isomerase Pin1-mediated isomerization of p53 are key events in p53-dependent apoptosis induced by mutant huntingtin","volume":"108","author":"Grison","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B29","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1002\/yea.320050108","article-title":"Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae","volume":"5","author":"Hanes","year":"1989","journal-title":"Yeast"},{"key":"B30","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1074\/jbc.274.1.108","article-title":"Mutations in a peptidylprolyl-cis\/trans-isomerase gene lead to a defect in 3'-end formation of a pre-mRNA in Saccharomyces cerevisiae","volume":"274","author":"Hani","year":"1999","journal-title":"J. Biol. Chem."},{"key":"B31","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/0014-5793(95)00471-k","article-title":"PTF1 encodes an essential protein in Saccharomyces cerevisiae, which shows strong homology with a new putative family of PPIases.","volume":"365","author":"Hani","year":"1995","journal-title":"FEBS Lett."},{"key":"B32","doi-asserted-by":"publisher","first-page":"538","DOI":"10.1038\/35078508","article-title":"Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis","volume":"3","author":"Hsu","year":"2001","journal-title":"Nat. Cell Biol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"3779","DOI":"10.1242\/jcs.114.20.3779","article-title":"Isolation and characterization of the Pin1\/Ess1p homologue in Schizosaccharomyces pombe","volume":"114","author":"Huang","year":"2001","journal-title":"J. Cell Sci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1016\/s0197-4580(00)00221-9","article-title":"Mitotic activation: A convergent mechanism for a cohort of neurodegenerative diseases","volume":"21","author":"Husseman","year":"2000","journal-title":"Neurobiol. Aging"},{"key":"B35","doi-asserted-by":"publisher","first-page":"e0175939","DOI":"10.1371\/journal.pone.0175939","article-title":"Dynamic regulation of Pin1 expression and function during zebrafish development","volume":"12","author":"Ibarra","year":"2017","journal-title":"PLoS One"},{"key":"B36","doi-asserted-by":"publisher","first-page":"7092","DOI":"10.1128\/MCB.25.16.7092-7106.2005","article-title":"WW domains provide a platform for the assembly of multiprotein networks","volume":"25","author":"Ingham","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"104501","DOI":"10.1016\/j.jprot.2022.104501","article-title":"Phosphopeptide enrichment using Phos-tag technology reveals functional phosphorylation of the nucleocapsid protein of SARS-CoV-2","volume":"255","author":"Ino","year":"2022","journal-title":"J. Proteomics"},{"key":"B38","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1038\/nrneurol.2015.225","article-title":"Tau and neurodegenerative disease: The story so far","volume":"12","author":"Iqbal","year":"2016","journal-title":"Nat. Rev. Neurol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"9390","DOI":"10.1002\/jcp.26774","article-title":"Peptidyl-prolyl cis-trans isomerase NIMA interacting 1 regulates skeletal muscle fusion through structural modification of Smad3 in the linker region","volume":"233","author":"Islam","year":"2018","journal-title":"J. Cell. Physiol."},{"key":"B112","first-page":"583","article-title":"Highly accurate protein structure prediction with AlphaFold","volume-title":"Nature","author":"Jumper","year":"2021"},{"key":"B40","doi-asserted-by":"publisher","first-page":"3069","DOI":"10.1038\/s41467-018-05402-2","article-title":"Arsenic targets Pin1 and cooperates with retinoic acid to inhibit cancer-driving pathways and tumor-initiating cells","volume":"9","author":"Kozono","year":"2018","journal-title":"Nat. Commun."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.cell.2021.07.020","article-title":"Targeting Pin1 renders pancreatic cancer","volume":"184","author":"Koikawa","year":"2021","journal-title":"Cell"},{"key":"B42","first-page":"415","volume-title":"Methods in molecular biology","author":"Kondo","year":"2017"},{"key":"B43","doi-asserted-by":"publisher","first-page":"31971","DOI":"10.1074\/jbc.273.48.31971","article-title":"Ssp1, a site-specific parvulin homolog from Neurospora crassa active in protein folding","volume":"273","author":"Kops","year":"1998","journal-title":"J. Biol. Chem."},{"key":"B44","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1104\/pp.108.132415","article-title":"Molecular and biochemical characterization of the parvulin-type PPIases in Lotus japonicus","volume":"150","author":"Kouri","year":"2009","journal-title":"Plant Physiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"10577","DOI":"10.1074\/jbc.275.14.10577","article-title":"The Arabidopsis thaliana PIN1At gene encodes a single-domain phosphorylation-dependent peptidyl prolylcis\/trans isomerase","volume":"275","author":"Landrieu","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B46","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1093\/carcin\/bgp027","article-title":"The prolyl isomerase Pin1 interacts with a ribosomal protein S6 kinase to enhance insulin-induced AP-1 activity and cellular transformation","volume":"30","author":"Lee","year":"2009","journal-title":"Carcinogenesis"},{"key":"B47","doi-asserted-by":"publisher","first-page":"e21","DOI":"10.1017\/S1462399411001906","article-title":"Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease","volume":"13","author":"Lee","year":"2011","journal-title":"Expert Rev. Mol. Med."},{"key":"B48","doi-asserted-by":"publisher","first-page":"469","DOI":"10.3389\/fonc.2018.00469","article-title":"Gears-In-Motion: The interplay of WW and PPIase domains in Pin1","volume":"8","author":"Lee","year":"2018","journal-title":"Front. Oncol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/78078","article-title":"Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein","volume":"25","author":"Lewis","year":"2000","journal-title":"Nat. Genet."},{"key":"B50","doi-asserted-by":"publisher","first-page":"3348","DOI":"10.7150\/thno.45889","article-title":"Roles of peptidyl-prolyl isomerase Pin1 in disease pathogenesis","volume":"11","author":"Li","year":"2021","journal-title":"Theranostics"},{"key":"B51","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1172\/JCI34308","article-title":"Pin1 has opposite effects on wild-type and P301L tau stability and tauopathy","volume":"118","author":"Lim","year":"2008","journal-title":"J. Clin. Invest."},{"key":"B52","doi-asserted-by":"publisher","first-page":"8777","DOI":"10.1128\/JVI.02533-10","article-title":"Peptidyl-prolyl isomerase Pin1 is a cellular factor required for hepatitis C virus propagation","volume":"85","author":"Lim","year":"2011","journal-title":"J. Virol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1177\/1535370215570829","article-title":"Landscape of Pin1 in the cell cycle","volume":"240","author":"Lin","year":"2015","journal-title":"Exp. Biol. Med."},{"key":"B54","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1073\/pnas.032404099","article-title":"Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes","volume":"99","author":"Liou","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B55","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1038\/nature01832","article-title":"Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration","volume":"424","author":"Liou","year":"2003","journal-title":"Nature"},{"key":"B56","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/j.tibs.2011.07.001","article-title":"Prolyl isomerase Pin1 as a molecular switch to determine the fate of phosphoproteins","volume":"36","author":"Liou","year":"2012","journal-title":"Trends biochem. Sci."},{"key":"B57","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1038\/nchembio.2007.35","article-title":"Prolyl cis-trans isomerization as a molecular timer","volume":"3","author":"Lu","year":"2007","journal-title":"Nat. Chem. Biol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"544","DOI":"10.1038\/380544a0","article-title":"A human peptidyl\u2013prolyl isomerase essential for regulation of mitosis","volume":"380","author":"Lu","year":"1996","journal-title":"Nature"},{"key":"B59","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1002\/bies.10223","article-title":"Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer's Disease","volume":"25","author":"Lu","year":"2003","journal-title":"Bioessays"},{"key":"B60","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/s0962-8924(02)02253-5","article-title":"Pinning down proline-directed phosphorylation signaling","volume":"12","author":"Lu","year":"2002","journal-title":"Trends Cell Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1016\/j.tibs.2004.02.002","article-title":"Pinning down cell signaling, cancer and Alzheimer's disease","volume":"29","author":"Lu","year":"2004","journal-title":"Trends biochem. Sci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"904","DOI":"10.1038\/nrm2261","article-title":"The prolyl isomerase PIN1: A pivotal new twist in phosphorylation signalling and disease","volume":"8","author":"Lu","year":"2007","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1038\/21650","article-title":"The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein","volume":"399","author":"Lu","year":"1999","journal-title":"Nature"},{"key":"B64","doi-asserted-by":"publisher","first-page":"1325","DOI":"10.1126\/science.283.5406.1325","article-title":"Function of WW domains as phosphoserine- or phosphothreonine-binding modules","volume":"283","author":"Lu","year":"1999","journal-title":"Science"},{"key":"B65","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.febslet.2008.12.011","article-title":"Nuclear import of Pin1 is mediated by a novel sequence in the PPIase domain","volume":"583","author":"Lufei","year":"2009","journal-title":"FEBS Lett."},{"key":"B66","doi-asserted-by":"publisher","first-page":"34518","DOI":"10.1074\/jbc.M110.104133","article-title":"Proline isomerase Pin1 represses terminal differentiation and myocyte enhancer factor 2C function in skeletal muscle cells","volume":"285","author":"Magli","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B67","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1073\/pnas.93.1.447","article-title":"The Drosophila melanogaster dodo (dod) gene, conserved in humans, is functionally interchangeable with the ESS1 cell division gene of Saccharomyces cerevisiae","volume":"93","author":"Maleszka","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B68","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1038\/nm.2102","article-title":"Concerted action of cellular JNK and Pin1 restricts HIV-1 genome integration to activated CD4+ T lymphocytes","volume":"16","author":"Manganaro","year":"2010","journal-title":"Nat. Med."},{"key":"B69","doi-asserted-by":"publisher","first-page":"7707","DOI":"10.1021\/bi400700b","article-title":"Kinetic isotope effects support the twisted amide mechanism of Pin1 peptidyl-prolyl isomerase","volume":"52","author":"Mercedes-Camacho","year":"2013","journal-title":"Biochemistry"},{"key":"B70","doi-asserted-by":"publisher","first-page":"13524","DOI":"10.1074\/jbc.M007005200","article-title":"Functional replacement of the essential ESS1 in yeast by the plant parvulin DlPar13","volume":"276","author":"Metzner","year":"2001","journal-title":"J. Biol. Chem."},{"key":"B71","doi-asserted-by":"publisher","first-page":"31583","DOI":"10.1074\/jbc.274.44.31583","article-title":"Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3'-end formation","volume":"274","author":"Morris","year":"1999","journal-title":"J. Biol. Chem."},{"key":"B72","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1016\/j.cell.2012.02.016","article-title":"Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer's disease","volume":"149","author":"Nakamura","year":"2012","journal-title":"Cell"},{"key":"B73","doi-asserted-by":"publisher","first-page":"24255","DOI":"10.1074\/jbc.M115.658559","article-title":"Prolyl isomerase Pin1 negatively regulates AMP-activated protein kinase (AMPK) by associating with the CBS domain in the \u03b3 subunit","volume":"290","author":"Nakatsu","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B74","doi-asserted-by":"publisher","first-page":"11886","DOI":"10.1074\/jbc.M117.780726","article-title":"The prolyl isomerase Pin1 increases \u03b2-cell proliferation and enhances insulin secretion","volume":"292","author":"Nakatsu","year":"2017","journal-title":"J. Biol. Chem."},{"key":"B75","doi-asserted-by":"publisher","first-page":"20812","DOI":"10.1074\/jbc.M110.206904","article-title":"Peptidyl-prolyl cis\/trans isomerase NIMA-interacting 1 associates with insulin receptor substrate-1 and enhances insulin actions and adipogenesis","volume":"286","author":"Nakatsu","year":"2011","journal-title":"J. Biol. Chem."},{"key":"B76","doi-asserted-by":"publisher","first-page":"109694","DOI":"10.1016\/j.celrep.2021.109694","article-title":"The prolyl-isomerase PIN1 is essential for nuclear Lamin-B structure and function and protects heterochromatin under mechanical stress","volume":"36","author":"Napoletano","year":"2021","journal-title":"Cell Rep."},{"key":"B77","doi-asserted-by":"publisher","first-page":"2120","DOI":"10.1128\/JVI.02634-12","article-title":"Pin1 interacts with the epstein-barr virus DNA polymerase catalytic subunit and regulates viral DNA replication","volume":"87","author":"Narita","year":"2013","journal-title":"J. Virol."},{"key":"B78","year":"2004"},{"key":"B79","doi-asserted-by":"publisher","first-page":"26","DOI":"10.3389\/fcell.2020.00026","article-title":"Prolyl isomerase Pin1 regulates the stability of hepatitis B virus core protein","volume":"8","author":"Nishi","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"B80","doi-asserted-by":"publisher","first-page":"817","DOI":"10.1093\/eurheartj\/ehu179","article-title":"Targeting prolyl-isomerase Pin1 prevents mitochondrial oxidative stress and vascular dysfunction: Insights in patients with diabetes","volume":"36","author":"Paneni","year":"2015","journal-title":"Eur. Heart J."},{"key":"B81","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1038\/nature04543","article-title":"The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production","volume":"440","author":"Pastorino","year":"2006","journal-title":"Nature"},{"key":"B82","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1038\/s41589-020-0550-9","article-title":"Identification of a potent and selective covalent Pin1 inhibitor","volume":"16","author":"Pinch","year":"2020","journal-title":"Nat. Chem. Biol."},{"key":"B83","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/S0171-9335(98)80032-0","article-title":"Mitotic phosphorylation of tau protein in neuronal cell lines resembles phosphorylation in Alzheimer's disease","volume":"76","author":"Preuss","year":"1998","journal-title":"Eur. J. Cell Biol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1016\/0014-5793(94)00932-5","article-title":"Confirmation of the existence of a third family among peptidyl-prolyl cis\/trans isomerases Amino acid sequence and recombinant production of parvulin","volume":"352","author":"Rahfeld","year":"1994","journal-title":"FEBS Lett."},{"key":"B85","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1016\/s0092-8674(00)80273-1","article-title":"Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent","volume":"89","author":"Ranganathan","year":"1997","journal-title":"Cell"},{"key":"B86","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1515\/BC.1999.057","article-title":"The WW domain of dystrophin requires EF-hands region to interact with beta-dystroglycan","volume":"380","author":"Rentschler","year":"1999","journal-title":"Biol. Chem."},{"key":"B87","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1007\/978-3-642-80481-6_5","article-title":"WW (WWP) domains: From structure to function","volume":"228","author":"Rotin","year":"1998","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"B88","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1002\/emmm.201302909","article-title":"Prolyl-isomerase Pin1 controls normal and cancer stem cells of the breast","volume":"6","author":"Rustighi","year":"2014","journal-title":"EMBO Mol. Med."},{"key":"B89","doi-asserted-by":"publisher","first-page":"5281","DOI":"10.1128\/mcb.22.15.5281-5295.2002","article-title":"PIN1 is an E2F target gene essential for neu\/ras-induced transformation of mammary epithelial cells","volume":"22","author":"Ryo","year":"2002","journal-title":"Mol. Cell. Biol."},{"key":"B90","doi-asserted-by":"publisher","first-page":"4117","DOI":"10.1074\/jbc.M507026200","article-title":"Prolyl-isomerase Pin1 accumulates in Lewy bodies of Parkinson disease and facilitates formation of \u03b1-synuclein inclusions","volume":"281","author":"Ryo","year":"2006","journal-title":"J. Biol. Chem."},{"key":"B91","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1038\/cdd.2012.112","article-title":"The prolyl-isomerase Pin1 activates the mitochondrial death program of p53","volume":"20","author":"Sorrentino","year":"2003","journal-title":"Cell Death Differ."},{"key":"B92","doi-asserted-by":"publisher","first-page":"4128e4125","DOI":"10.1016\/j.cub.2020.08.002","article-title":"Synaptic protein degradation controls sexually dimorphic circuits through regulation of DCC\/UNC-40","volume":"30","author":"Salzberg","year":"2020","journal-title":"Curr. Biol."},{"key":"B93","doi-asserted-by":"publisher","first-page":"2371","DOI":"10.1002\/j.1460-2075.1996.tb00593.x","article-title":"WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome","volume":"15","author":"Staub","year":"1996","journal-title":"EMBO J."},{"key":"B94","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/0014-5793(95)00550-s","article-title":"Characterization of a novel protein-binding module--the WW domain.","volume":"369","author":"Sudol","year":"1995","journal-title":"FEBS Lett."},{"key":"B95","doi-asserted-by":"publisher","first-page":"1260419","DOI":"10.1126\/science.1260419","article-title":"Proteomics. Tissue-based map of the human proteome","volume":"347","author":"Uhl\u00e9n","year":"2015","journal-title":"Science"},{"key":"B96","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1038\/77929","article-title":"Structural basis for phosphoserine-proline recognition by group IV WW domains","volume":"7","author":"Verdecia","year":"2000","journal-title":"Nat. Struct. Biol."},{"key":"B97","doi-asserted-by":"publisher","first-page":"355","DOI":"10.3389\/fcell.2020.00355","article-title":"Peptidyl-prolyl cis\/trans isomerase Pin1 and alzheimer's disease","volume":"8","author":"Wang","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"B98","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.molcel.2009.12.020","article-title":"Pin1At encoding a peptidyl-prolyl cis\/trans isomerase regulates flowering time in Arabidopsis","volume":"37","author":"Wang","year":"2010","journal-title":"Mol. Cell"},{"key":"B99","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1038\/nm.3839","article-title":"Active Pin1 is a key target of all-trans retinoic acid in acute promyelocytic leukemia and breast cancer","volume":"21","author":"Wei","year":"2015","journal-title":"Nat. Med."},{"key":"B100","doi-asserted-by":"publisher","first-page":"47976","DOI":"10.1074\/jbc.C200538200","article-title":"Role of Pin1 in the regulation of p53 stability and p21 transactivation, and cell cycle checkpoints in response to DNA damage","volume":"277","author":"Wulf","year":"2002","journal-title":"J. Biol. Chem."},{"key":"B101","doi-asserted-by":"publisher","first-page":"10430","DOI":"10.1038\/ncomms10430","article-title":"Pin1At regulates PIN1 polar localization and root gravitropism","volume":"7","author":"Xi","year":"2016","journal-title":"Nat. Commun."},{"key":"B102","doi-asserted-by":"publisher","first-page":"2765","DOI":"10.1101\/gad.1135503","article-title":"Pin1 modulates the structure and function of human RNA polymerase II","volume":"17","author":"Xu","year":"2003","journal-title":"Genes Dev."},{"key":"B103","doi-asserted-by":"publisher","first-page":"18581","DOI":"10.1038\/s41598-021-97972-3","article-title":"Prolyl isomerase Pin1 plays an essential role in SARS-CoV-2 proliferation, indicating its possibility as a novel therapeutic target","volume":"11","author":"Yamamotoya","year":"2021","journal-title":"Sci. Rep."},{"key":"B104","doi-asserted-by":"publisher","first-page":"13517","DOI":"10.1074\/jbc.M007006200","article-title":"Functional conservation of phosphorylation-specific prolyl isomerases in plants","volume":"276","author":"Yao","year":"2001","journal-title":"J. Biol. Chem."},{"key":"B105","doi-asserted-by":"publisher","first-page":"120","DOI":"10.3389\/fcell.2020.00120","article-title":"Function of PIN1 in cancer development and its inhibitors as cancer therapeutics","volume":"8","author":"Yu","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"B106","doi-asserted-by":"publisher","first-page":"853","DOI":"10.1038\/nature01120","article-title":"The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults","volume":"419","author":"Zacchi","year":"2002","journal-title":"Nature"},{"key":"B107","doi-asserted-by":"publisher","first-page":"94","DOI":"10.3389\/fonc.2019.00094","article-title":"Oncogenic hijacking of the PIN1 signaling network","volume":"9","author":"Zannini","year":"2019","journal-title":"Front. Oncol."},{"key":"B108","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1158\/1535-7163.MCT-19-0656","article-title":"Pin1 inhibition sensitizes chemotherapy in gastric cancer cells by targeting stem cell-like traits and multiple biomarkers","volume":"19","author":"Zhang","year":"2020","journal-title":"Mol. Cancer Ther."},{"key":"B109","doi-asserted-by":"publisher","first-page":"29771","DOI":"10.18632\/oncotarget.15967","article-title":"Inhibition of the prolyl isomerase Pin1 enhances the ability of sorafenib to induce cell death and inhibit tumor growth in hepatocellular carcinoma","volume":"8","author":"Zheng","year":"2017","journal-title":"Oncotarget"},{"key":"B110","doi-asserted-by":"publisher","first-page":"1526","DOI":"10.3389\/fpls.2017.01526","article-title":"Overexpression of PvPin1, a bamboo homolog of PIN1-type parvulin 1, delays flowering time in transgenic Arabidopsis and rice","volume":"8","author":"Zheng","year":"2017","journal-title":"Front. Plant Sci."},{"key":"B111","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1016\/s1097-2765(05)00083-3","article-title":"Pin1-Dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins","volume":"6","author":"Zhou","year":"2000","journal-title":"Mol. Cell"}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2022.956071\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T08:26:34Z","timestamp":1661847994000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2022.956071\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,30]]},"references-count":112,"alternative-id":["10.3389\/fcell.2022.956071"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2022.956071","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,30]]},"article-number":"956071"}}