Pinning down signaling in the immune system: the role of the peptidyl-prolyl isomerase Pin1 in immune cell function.

The peptidyl prolyl isomerase (PPIase) Pin1 has been recently implicated in cell cycle control and neuropathologies. There is now growing evidence that Pin1 plays an important role in the immune system and does so differentially from the related PPIases, cyclophilinA and FKBP. This review describes how Pin1 modulates cytokine expression by activated T cells and eosinophils and participates in T-cell and eosinophil apoptotic decisions both in vitro and in vivo. We highlight several possible immunologic diseases, including asthma, as well as organ transplant rejection, where anti-Pin1 therapeutics maybe of value.

[1]  R. Sorkness,et al.  A critical role for Pin1 in allergic pulmonary eosinophilia in rats. , 2007, The Journal of allergy and clinical immunology.

[2]  R. Dalla‐Favera,et al.  Genotoxic stress regulates expression of the proto-oncogene Bcl6 in germinal center B cells , 2007, Nature Immunology.

[3]  P. Rejto,et al.  Identification and characterization of a novel and functional murine Pin1 isoform. , 2007, Biochemical and biophysical research communications.

[4]  H. Akiyama,et al.  Ablation of a peptidyl prolyl isomerase Pin1 from p53-null mice accelerated thymic hyperplasia by increasing the level of the intracellular form of Notch1 , 2007, Oncogene.

[5]  Elisabeth S Yeh,et al.  PIN1, the cell cycle and cancer , 2007, Nature Reviews Cancer.

[6]  K. Lu,et al.  Pin1 in Alzheimer's disease: multiple substrates, one regulatory mechanism? , 2007, Biochimica et biophysica acta.

[7]  R. Braun,et al.  Pin1 Modulates the Type 1 Immune Response , 2007, PloS one.

[8]  Paola Briata,et al.  The RNA-Binding Protein KSRP Promotes Decay of β-Catenin mRNA and Is Inactivated by PI3K-AKT Signaling , 2006, PLoS biology.

[9]  G. Wahl,et al.  Mouse Mutants Reveal that Putative Protein Interaction Sites in the p53 Proline-Rich Domain Are Dispensable for Tumor Suppression , 2006, Molecular and Cellular Biology.

[10]  R. Sen Control of B Lymphocyte Apoptosis by the Transcription Factor NF-κB , 2006 .

[11]  S. Esnault,et al.  The Peptidyl-Prolyl Isomerase Pin1 Regulates Granulocyte-Macrophage Colony-Stimulating Factor mRNA Stability in T Lymphocytes1 , 2006, The Journal of Immunology.

[12]  L. Hassman,et al.  A central regulatory role for eosinophils and the eotaxin/CCR3 axis in chronic experimental allergic airway inflammation , 2006, Proceedings of the National Academy of Sciences.

[13]  H. Simon,et al.  cIAP‐2 and survivin contribute to cytokine‐mediated delayed eosinophil apoptosis , 2006, European journal of immunology.

[14]  P. Krammer,et al.  How T lymphocytes switch between life and death , 2006, European journal of immunology.

[15]  J. Ashwell The many paths to p38 mitogen-activated protein kinase activation in the immune system , 2006, Nature Reviews Immunology.

[16]  K. Lu,et al.  Regulation of Bruton Tyrosine Kinase by the Peptidylprolyl Isomerase Pin1* , 2006, Journal of Biological Chemistry.

[17]  Xiao Zhen Zhou,et al.  Targeting carcinogenesis: A role for the prolyl isomerase Pin1? , 2006, Molecular carcinogenesis.

[18]  H. Akiyama,et al.  Comparative analysis of enzyme activities and mRNA levels of peptidyl prolyl cis/trans isomerases in various organs of wild type and Pin1 −/− mice , 2006, FEBS letters.

[19]  Shizuo Akira,et al.  Negative regulation of interferon-regulatory factor 3–dependent innate antiviral response by the prolyl isomerase Pin1 , 2006, Nature Immunology.

[20]  V. Lang,et al.  PI3-kinase and the control of T cell growth and proliferation by FoxOs. , 2006, Bulletin du cancer.

[21]  L. Nicholson,et al.  The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production , 2006, Nature.

[22]  Esther B. E. Becker,et al.  Pin1 Mediates Neural-Specific Activation of the Mitochondrial Apoptotic Machinery , 2006, Neuron.

[23]  A. Wells,et al.  The role of cyclin-dependent kinases in T-cell development, proliferation, and function. , 2006, Critical reviews in immunology.

[24]  S. Esnault,et al.  The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils , 2005, Nature Immunology.

[25]  J. Gutkind,et al.  Regulation of the Transcriptional Activity of c-Fos by ERK , 2005, Journal of Biological Chemistry.

[26]  J. Harty,et al.  Dynamic Regulation of IFN-γ Signaling in Antigen-Specific CD8+ T Cells Responding to Infection1 , 2005, The Journal of Immunology.

[27]  Helmut Geiger,et al.  Prediction of Acute Renal Allograft Rejection by Urinary Monokine Induced by IFN-γ (MIG) , 2005 .

[28]  T. Grodzki,et al.  Synergistic effect of low dose cyclosporine A and human interleukin 10 overexpression on acute rejection in rat lung allotransplantation. , 2005, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[29]  S. Bhorade,et al.  Successful use in lung transplantation of an immunosuppressive regimen aimed at reducing target blood levels of sirolimus and tacrolimus. , 2005, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[30]  D. Wilkes,et al.  Transplant-related immunosuppression: a review of immunosuppression and pulmonary infections. , 2005, Proceedings of the American Thoracic Society.

[31]  Ryan T. Phan,et al.  The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells , 2004, Nature.

[32]  R. Sorkness,et al.  Systemic and pulmonary effects of fluticasone administered through a metered-dose inhaler in rats. , 2004, The Journal of allergy and clinical immunology.

[33]  A. Strasser,et al.  T-lymphocyte death during shutdown of an immune response. , 2004, Trends in immunology.

[34]  S. Phipps,et al.  A role for eosinophils in airway remodelling in asthma. , 2004, Trends in immunology.

[35]  Priti Garg,et al.  Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis , 2004, The EMBO journal.

[36]  Bruce Stillman,et al.  Deregulation of cyclin E in human cells interferes with prereplication complex assembly , 2004, The Journal of cell biology.

[37]  R. Mantovani,et al.  Pin1 links the activities of c-Abl and p300 in regulating p73 function. , 2004, Molecular cell.

[38]  G. Kroemer,et al.  Fatal liaisons of p53 with Bax and Bak , 2004, Nature Cell Biology.

[39]  Joseph R. Nevins,et al.  A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells , 2004, Nature Cell Biology.

[40]  S. Cook,et al.  Extracellular Signal-regulated Kinases 1/2 Are Serum-stimulated “BimEL Kinases” That Bind to the BH3-only Protein BimEL Causing Its Phosphorylation and Turnover* , 2004, Journal of Biological Chemistry.

[41]  U. Certa,et al.  Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. , 2004, Nucleic acids research.

[42]  J. Diehl The Cyclin D3 Knockout: A Pound of Redundancy with a Dash of Tissue Specificity , 2004, Cancer biology & therapy.

[43]  A. Haverich,et al.  Contributions from the European Respiratory Monograph Series "lung Transplantation" Edited Immunosuppressive Therapy after Human Lung Transplantation , 2003 .

[44]  S. Esnault,et al.  Hyaluronic Acid or TNF-α Plus Fibronectin Triggers Granulocyte Macrophage-Colony-Stimulating Factor mRNA Stabilization in Eosinophils Yet Engages Differential Intracellular Pathways and mRNA Binding Proteins1 , 2003, The Journal of Immunology.

[45]  A. Ryo,et al.  Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. , 2003, Molecular cell.

[46]  A. Wells Cell‐cycle regulation of T‐cell responses – novel approaches to the control of alloimmunity , 2003, Immunological reviews.

[47]  O. Cummings,et al.  Differential Expression of Smad7 Transcripts Identifies the CD4+CD45RChigh Regulatory T Cells That Mediate Type V Collagen-Induced Tolerance to Lung Allografts 1 , 2003, The Journal of Immunology.

[48]  A. Means,et al.  Pin1 regulates the timing of mammalian primordial germ cell proliferation , 2003, Development.

[49]  D. Postma,et al.  Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. , 2003, American journal of respiratory and critical care medicine.

[50]  Y. Wan,et al.  The survival of antigen-stimulated T cells requires NFkappaB-mediated inhibition of p73 expression. , 2003, Immunity.

[51]  P. Paré,et al.  Polymorphisms of the GM-CSF genes and the development of atopic diseases in at-risk children. , 2003, Chest.

[52]  Makio Iwashima,et al.  Kinetic perspectives of T cell antigen receptor signaling , 2003, Immunological reviews.

[53]  Sam W. Lee,et al.  Role of Pin1 in the Regulation of p53 Stability and p21 Transactivation, and Cell Cycle Checkpoints in Response to DNA Damage* , 2002, The Journal of Biological Chemistry.

[54]  Kenneth M. Murphy,et al.  Decision making in the immune system: The lineage decisions of helper T cells , 2002, Nature Reviews Immunology.

[55]  S. Murray,et al.  The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response , 2002, Nature.

[56]  P. Libby,et al.  Differential Expression of the IFN-γ-Inducible CXCR3-Binding Chemokines, IFN-Inducible Protein 10, Monokine Induced by IFN, and IFN-Inducible T Cell α Chemoattractant in Human Cardiac Allografts: Association with Cardiac Allograft Vasculopathy and Acute Rejection1 , 2002, The Journal of Immunology.

[57]  A. Strasser,et al.  Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. , 2002, Immunity.

[58]  G. Koretzky,et al.  Control of T Cell Function by Positive and Negative Regulators , 2002, Science.

[59]  S. Romagnani Cytokines and chemoattractants in allergic inflammation. , 2002, Molecular immunology.

[60]  Marius Sudol,et al.  WW and SH3 domains, two different scaffolds to recognize proline‐rich ligands , 2002, FEBS letters.

[61]  T. Taniguchi,et al.  The interferon-α/β system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors , 2002 .

[62]  T. Hunter,et al.  Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  S. Haldar,et al.  Proteasomal degradation of human peptidyl prolyl isomerase pin1-pointing phospho Bcl2 toward dephosphorylation. , 2002, Neoplasia.

[64]  M. Mann,et al.  AU Binding Proteins Recruit the Exosome to Degrade ARE-Containing mRNAs , 2001, Cell.

[65]  S. Esnault,et al.  Y Box-Binding Factor Promotes Eosinophil Survival by Stabilizing Granulocyte-Macrophage Colony-Stimulating Factor mRNA1 , 2001, The Journal of Immunology.

[66]  A. Shyu,et al.  Versatile Role for hnRNP D Isoforms in the Differential Regulation of Cytoplasmic mRNA Turnover , 2001, Molecular and Cellular Biology.

[67]  P. Maasilta,et al.  Immune cells and immunosuppression in a porcine bronchial model of obliterative bronchiolitis. , 2001, Transplantation.

[68]  Tianhua Niu,et al.  Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c‐Jun towards cyclin D1 , 2001, The EMBO journal.

[69]  T. Hsu,et al.  Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis , 2001, Nature Cell Biology.

[70]  Xiao Zhen Zhou,et al.  Binding and regulation of the transcription factor NFAT by the peptidyl prolyl cis–trans isomerase Pin1 , 2001, FEBS letters.

[71]  G. M. Wilson,et al.  Folding of A+U-rich RNA Elements Modulates AUF1 Binding , 2001, The Journal of Biological Chemistry.

[72]  Paige Lacy,et al.  Immune effector functions of eosinophils in allergic airway inflammation , 2001, Current opinion in allergy and clinical immunology.

[73]  F. Alderuccio,et al.  Local Transgenic Expression of Granulocyte Macrophage-Colony Stimulating Factor Initiates Autoimmunity1 , 2001, Journal of Immunology.

[74]  John C. Reed,et al.  Erratum: Microtubule-targeting drugs induce Bcl-2 phosphorylation and association with Pin1 (Neoplasia (2001) 3 (550-559) , 2001 .

[75]  J C Reed,et al.  Microtubule-targeting drugs induce bcl-2 phosphorylation and association with Pin1. , 2001, Neoplasia.

[76]  K. Chung,et al.  Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsìveness, and the late asthmatic response , 2000, The Lancet.

[77]  A. Kay,et al.  Attenuation of the allergen-induced late asthmatic reaction by cyclosporin A is associated with inhibition of bronchial eosinophils, interleukin-5, granulocyte macrophage colony-stimulating factor, and eotaxin. , 2000, American journal of respiratory and critical care medicine.

[78]  S. Peters,et al.  Effect of IL‐5, glucocorticoid, and Fas ligation on Bcl‐2 homologue expression and caspase activation in circulating human eosinophils , 2000, Clinical and experimental immunology.

[79]  P. Blackshear,et al.  Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. , 2000, Blood.

[80]  A. Means,et al.  Requirement of the prolyl isomerase Pin1 for the replication checkpoint. , 2000, Science.

[81]  S. Esnault,et al.  Primary peripheral blood eosinophils rapidly degrade transfected granulocyte-macrophage colony-stimulating factor mRNA. , 1999, Journal of immunology.

[82]  A. Capron,et al.  Expression of Cd28 and Cd86 by Human Eosinophils and Role in the Secretion of Type 1 Cytokines (Interleukin 2 and Interferon γ) , 1999, The Journal of experimental medicine.

[83]  C. Y. Chen,et al.  Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. , 1999, Genes & development.

[84]  P. Davies,et al.  The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein , 1999, Nature.

[85]  R. Ross,et al.  HuD, a neuronal-specific RNA-binding protein, is a putative regulator of N-myc pre-mRNA processing/stability in malignant human neuroblasts , 1999, Oncogene.

[86]  W. Busse,et al.  Segmental antigen challenge increases fibronectin in bronchoalveolar lavage fluid. , 1999, American journal of respiratory and critical care medicine.

[87]  S. Esnault,et al.  Stabilization of granulocyte-macrophage colony-stimulating factor RNA in a human eosinophil-like cell line requires the AUUUA motifs. , 1998, Proceedings of the Association of American Physicians.

[88]  S. Uh,et al.  Granulocyte macrophage colony-stimulating factor is the main cytokine enhancing survival of eosinophils in asthmatic airways. , 1998, The European respiratory journal.

[89]  W. May,et al.  A Functional Role for Mitochondrial Protein Kinase Cα in Bcl2 Phosphorylation and Suppression of Apoptosis* , 1998, The Journal of Biological Chemistry.

[90]  S. Cory,et al.  The Bcl-2 protein family: arbiters of cell survival. , 1998, Science.

[91]  H. Simon,et al.  Role for Bcl-xL in Delayed Eosinophil Apoptosis Mediated by Granulocyte-Macrophage Colony-Stimulating Factor and Interleukin-5 , 1998 .

[92]  T. Ruzicka,et al.  Human eosinophils produce biologically active IL-12: implications for control of T cell responses. , 1998, Journal of immunology.

[93]  J. Steitz,et al.  Overexpression of HuR, a nuclear–cytoplasmic shuttling protein, increases the in vivo stability of ARE‐containing mRNAs , 1998, The EMBO journal.

[94]  A. Means,et al.  The mitotic peptidyl‐prolyl isomerase, Pin1, interacts with Cdc25 and Plx1 , 1998, The EMBO journal.

[95]  C. Martínez-A,et al.  IL-2-induced cellular events. , 1998, Critical reviews in immunology.

[96]  G. L. Miklos,et al.  The dodo gene family encodes a novel protein involved in signal transduction and protein folding. , 1997, Gene.

[97]  K. Mikoshiba,et al.  Characterization of the pleckstrin homology domain of Btk as an inositol polyphosphate and phosphoinositide binding domain. , 1997, Biochemical and biophysical research communications.

[98]  L. Staudt,et al.  Control of inflammation, cytokine expression, and germinal center formation by BCL-6. , 1997, Science.

[99]  E. Querfurth,et al.  Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. , 1996, The EMBO journal.

[100]  J. Malter,et al.  Turnover and Translation of in Vitro Synthesized Messenger RNAs in Transfected, Normal Cells* , 1996, The Journal of Biological Chemistry.

[101]  T. Hunter,et al.  A human peptidyl–prolyl isomerase essential for regulation of mitosis , 1996, Nature.

[102]  M. Jordana,et al.  Transfer of granulocyte-macrophage colony-stimulating factor gene to rat lung induces eosinophilia, monocytosis, and fibrotic reactions. , 1996, The Journal of clinical investigation.

[103]  G. L. Miklos,et al.  The Drosophila melanogaster dodo (dod) gene, conserved in humans, is functionally interchangeable with the ESS1 cell division gene of Saccharomyces cerevisiae. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[104]  J. Virchow,et al.  T cells and cytokines in bronchoalveolar lavage fluid after segmental allergen provocation in atopic asthma. , 1995, American journal of respiratory and critical care medicine.

[105]  K. Resch,et al.  T-cell antigen receptor-induced signal-transduction pathways Activation and function of protein kinases C in T lymphocytes , 1995 .

[106]  R. Coffman,et al.  IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. , 1995, Journal of immunology.

[107]  J. Hacker,et al.  Confirmation of the existence of a third family among peptidyl‐prolyl cis/trans isomerases Amino acid sequence and recombinant production of parvulin , 1994, FEBS letters.

[108]  G. Fischer,et al.  A novel peptidyl‐prolyl cisltrans isomerase from Escherichia coli , 1994, FEBS letters.

[109]  W Zhang,et al.  Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1 , 1993, Molecular and cellular biology.

[110]  D J Rawlings,et al.  Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. , 1993, Science.

[111]  B. Kahan Cyclosporin A, FK506, rapamycin: the use of a quantitative analytic tool to discriminate immunosuppressive drug interactions. , 1992, Journal of the American Society of Nephrology : JASN.

[112]  G. Baldwin The biology of granulocyte-macrophage colony-stimulating factor: effects on hematopoietic and nonhematopoietic cells. , 1992, Developmental biology.

[113]  S. Schreiber,et al.  The mechanism of action of cyclosporin A and FK506. , 1992, Immunology today.

[114]  J. Arm,et al.  The pathobiology of bronchial asthma. , 1992, Advances in immunology.

[115]  H. Kita,et al.  Materials and Methods Brief Definitive Report Granulocyte/macrophage Colony-stimulating Factor and Interleukin 3 Release from Human Peripheral Blood Eosinophils and Neutrophils , 2022 .

[116]  Stuart L. Schreiber,et al.  Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes , 1991, Cell.

[117]  G. Brewer,et al.  An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro , 1991, Molecular and cellular biology.

[118]  E. Vellenga,et al.  A double-blind placebo-controlled study with granulocyte-macrophage colony-stimulating factor during chemotherapy for ovarian carcinoma. , 1991, Cancer research.

[119]  P. Tai,et al.  The effects of recombinant granulocyte‐macrophage colony‐stimulating factor (GM‐CSF) and interleukin‐3 on the secretory capacity of human blood eosinophils , 1990, Clinical and experimental immunology.

[120]  C. Sanderson,et al.  Human interleukin-5 (IL-5) regulates the production of eosinophils in human bone marrow cultures: comparison and interaction with IL-1, IL-3, IL-6, and GMCSF. , 1989, Blood.

[121]  C. Thompson,et al.  Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. , 1989, Science.

[122]  I. Hariharan,et al.  A lethal myeloproliferative syndrome in mice transplanted with bone marrow cells infected with a retrovirus expressing granulocyte‐macrophage colony stimulating factor. , 1989, The EMBO journal.

[123]  K. Bostian,et al.  Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae , 1989, Yeast.

[124]  Richard Treisman,et al.  Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3′ AU-rich sequences , 1988, Nature.

[125]  R. Cuthbertson,et al.  Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage , 1987, Cell.

[126]  G. Shaw,et al.  A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation , 1986, Cell.

[127]  S. Sahu,et al.  Hyaluronic acid in the pulmonary secretions of patients with asthma. , 1978, The Biochemical journal.