Cyclophilin A supports translation of intrinsically disordered proteins and affects haematopoietic stem cell ageing.

Intrinsically Disordered Proteins / chemistry Cyclophilin A / genetics RNA-Binding Proteins Hematopoietic Stem Cells / metabolism

Journal

Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575

Informations de publication

Date de publication:
Apr 2024
Historique:
received: 25 04 2022
accepted: 23 02 2024
medline: 18 4 2024
pubmed: 30 3 2024
entrez: 30 3 2024
Statut: ppublish

Résumé

Loss of protein function is a driving force of ageing. We have identified peptidyl-prolyl isomerase A (PPIA or cyclophilin A) as a dominant chaperone in haematopoietic stem and progenitor cells. Depletion of PPIA accelerates stem cell ageing. We found that proteins with intrinsically disordered regions (IDRs) are frequent PPIA substrates. IDRs facilitate interactions with other proteins or nucleic acids and can trigger liquid-liquid phase separation. Over 20% of PPIA substrates are involved in the formation of supramolecular membrane-less organelles. PPIA affects regulators of stress granules (PABPC1), P-bodies (DDX6) and nucleoli (NPM1) to promote phase separation and increase cellular stress resistance. Haematopoietic stem cell ageing is associated with a post-transcriptional decrease in PPIA expression and reduced translation of IDR-rich proteins. Here we link the chaperone PPIA to the synthesis of intrinsically disordered proteins, which indicates that impaired protein interaction networks and macromolecular condensation may be potential determinants of haematopoietic stem cell ageing.

Identifiants

DOI: 10.1038/s41556-024-01387-x PMID: 38553595 PMC: PMC11021199
pubmed: 38553595
doi: 10.1038/s41556-024-01387-x
pii: 10.1038/s41556-024-01387-x
pmc: PMC11021199
doi:

Substances chimiques

Intrinsically Disordered Proteins 0
Cyclophilin A EC 5.2.1.-
RNA-Binding Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

593-603

Subventions

Organisme : NCI NIH HHS
ID : P30 CA125123
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK056338
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK115454
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR024574
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK060445
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM142143
Pays : United States

Informations de copyright

© 2024. The Author(s).

Références

Sun, J. et al. Clonal dynamics of native haematopoiesis. Nature 514, 322–327 (2014).
pubmed: 25296256 pmcid: 4408613 doi: 10.1038/nature13824
Lopez-Otin, C., Blasco, M. A., Partridge, L., Serrano, M. & Kroemer, G. The hallmarks of aging. Cell 153, 1194–1217 (2013).
pubmed: 23746838 pmcid: 3836174 doi: 10.1016/j.cell.2013.05.039
Signer, R. A., Magee, J. A., Salic, A. & Morrison, S. J. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509, 49–54 (2014).
pubmed: 24670665 pmcid: 4015626 doi: 10.1038/nature13035
Hidalgo San Jose, L. et al. Modest declines in proteome quality impair hematopoietic stem cell self-renewal. Cell Rep. 30, 69–80 (2020).
pubmed: 31914399 doi: 10.1016/j.celrep.2019.12.003
Mohrin, M. et al. Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 347, 1374–1377 (2015).
pubmed: 25792330 pmcid: 4447312 doi: 10.1126/science.aaa2361
Kruta, M. et al. Hsf1 promotes hematopoietic stem cell fitness and proteostasis in response to ex vivo culture stress and aging. Cell Stem Cell 28, 1950–1965 (2021).
pubmed: 34388375 pmcid: 8571035 doi: 10.1016/j.stem.2021.07.009
Hipp, M. S., Kasturi, P. & Hartl, F. U. The proteostasis network and its decline in ageing. Nat. Rev. Mol. Cell Biol. 20, 421–435 (2019).
pubmed: 30733602 doi: 10.1038/s41580-019-0101-y
Brehme, M. et al. A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep. 9, 1135–1150 (2014).
pubmed: 25437566 pmcid: 4255334 doi: 10.1016/j.celrep.2014.09.042
Pálovics, R. et al. Molecular hallmarks of heterochronic parabiosis at single-cell resolution. Nature 603, 309–314 (2022).
pubmed: 35236985 pmcid: 9387403 doi: 10.1038/s41586-022-04461-2
Boraldi, F. et al. Proteome analysis of dermal fibroblasts cultured in vitro from human healthy subjects of different ages. Proteomics 3, 917–929 (2003).
pubmed: 12833515 doi: 10.1002/pmic.200300386
Babu, M. et al. Proline/arginine dipeptide repeat polymers derail protein folding in amyotrophic lateral sclerosis. Nat. Commun. 12, 3396 (2021).
pubmed: 34099711 pmcid: 8184751 doi: 10.1038/s41467-021-23691-y
Wright, P. E. & Dyson, H. J. Intrinsically disordered proteins in cellular signalling and regulation. Nat. Rev. Mol. Cell Biol. 16, 18–29 (2015).
pubmed: 25531225 pmcid: 4405151 doi: 10.1038/nrm3920
Mollica, L. et al. Binding mechanisms of intrinsically disordered proteins: theory, simulation and experiment. Front. Mol. Biosci. 3, 52 (2016).
pubmed: 27668217 pmcid: 5016563 doi: 10.3389/fmolb.2016.00052
Nilsson, J., Grahn, M. & Wright, A. P. Proteome-wide evidence for enhanced positive Darwinian selection within intrinsically disordered regions in proteins. Genome Biol. 12, R65 (2011).
pubmed: 21771306 pmcid: 3218827 doi: 10.1186/gb-2011-12-7-r65
Afanasyeva, A., Bockwoldt, M., Cooney, C. R., Heiland, I. & Gossmann, T. I. Human long intrinsically disordered protein regions are frequent targets of positive selection. Genome Res. 28, 975–982 (2018).
pubmed: 29858274 pmcid: 6028134 doi: 10.1101/gr.232645.117
Zaro, B. W. et al. Proteomic analysis of young and old mouse hematopoietic stem cells and their progenitors reveals post-transcriptional regulation in stem cells. eLife 9, e62210 (2020).
pubmed: 33236985 pmcid: 7688314 doi: 10.7554/eLife.62210
Davis, T. L. et al. Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases. PLoS Biol. 8, e1000439 (2010).
pubmed: 20676357 pmcid: 2911226 doi: 10.1371/journal.pbio.1000439
Schmidpeter, P. A., Koch, J. R. & Schmid, F. X. Control of protein function by prolyl isomerization. Biochim. Biophys. Acta 1850, 1973–1982 (2015).
pubmed: 25542300 doi: 10.1016/j.bbagen.2014.12.019
Colgan, J. et al. Cyclophilin A regulates TCR signal strength in CD4
pubmed: 15308100 doi: 10.1016/j.immuni.2004.07.005
Satoh, K. et al. Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation 117, 3088–3098 (2008).
pubmed: 18541741 pmcid: 2775430 doi: 10.1161/CIRCULATIONAHA.107.756106
Beerman, I. et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc. Natl Acad. Sci. USA 107, 5465–5470 (2010).
pubmed: 20304793 pmcid: 2851806 doi: 10.1073/pnas.1000834107
Rossi, D. J., Jamieson, C. H. & Weissman, I. L. Stems cells and the pathways to aging and cancer. Cell 132, 681–696 (2008).
pubmed: 18295583 doi: 10.1016/j.cell.2008.01.036
Oh, J., Lee, Y. D. & Wagers, A. J. Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat. Med. 20, 870–880 (2014).
pubmed: 25100532 pmcid: 4160113 doi: 10.1038/nm.3651
Goodell, M. A. & Rando, T. A. Stem cells and healthy aging. Science 350, 1199–1204 (2015).
pubmed: 26785478 doi: 10.1126/science.aab3388
Geiger, H., de Haan, G. & Florian, M. C. The ageing haematopoietic stem cell compartment. Nat. Rev. Immunol. 13, 376–389 (2013).
pubmed: 23584423 doi: 10.1038/nri3433
Wang, P. & Heitman, J. The cyclophilins. Genome Biol. 6, 226 (2005).
pubmed: 15998457 pmcid: 1175980 doi: 10.1186/gb-2005-6-7-226
Nigro, P., Pompilio, G. & Capogrossi, M. C. Cyclophilin A: a key player for human disease. Cell Death Dis. 4, e888 (2013).
pubmed: 24176846 pmcid: 3920964 doi: 10.1038/cddis.2013.410
Lang, K., Schmid, F. X. & Fischer, G. Catalysis of protein folding by prolyl isomerase. Nature 329, 268–270 (1987).
pubmed: 3306408 doi: 10.1038/329268a0
Kiefhaber, T., Quaas, R., Hahn, U. & Schmid, F. X. Folding of ribonuclease T1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29, 3061–3070 (1990).
pubmed: 2110824 doi: 10.1021/bi00464a024
Wedemeyer, W. J., Welker, E. & Scheraga, H. A. Proline cis–trans isomerization and protein folding. Biochemistry 41, 14637–14644 (2002).
pubmed: 12475212 doi: 10.1021/bi020574b
Jakob, R. P., Zoldák, G., Aumüller, T. & Schmid, F. X. Chaperone domains convert prolyl isomerases into generic catalysts of protein folding. Proc. Natl Acad. Sci. USA 106, 20282–20287 (2009).
pubmed: 19920179 pmcid: 2787138 doi: 10.1073/pnas.0909544106
Cardenas, M. E., Lim, E. & Heitman, J. Mutations that perturb cyclophilin A ligand binding pocket confer cyclosporin A resistance in Saccharomyces cerevisiae. J. Biol. Chem. 270, 20997–21002 (1995).
pubmed: 7673124 doi: 10.1074/jbc.270.36.20997
Boeynaems, S. et al. Protein phase separation: a new phase in cell biology. Trends Cell Biol. 28, 420–435 (2018).
pubmed: 29602697 pmcid: 6034118 doi: 10.1016/j.tcb.2018.02.004
Gomes, E. & Shorter, J. The molecular language of membraneless organelles. J. Biol. Chem. 294, 7115–7127 (2019).
pubmed: 30045872 doi: 10.1074/jbc.TM118.001192
Schwanhausser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337–342 (2011).
pubmed: 21593866 doi: 10.1038/nature10098
Pentony, M. M. & Jones, D. T. Modularity of intrinsic disorder in the human proteome. Proteins 78, 212–221 (2010).
pubmed: 19626706 doi: 10.1002/prot.22504
Ni, S. et al. Discovering potent small molecule inhibitors of cyclophilin A using de novo drug design approach. J. Med. Chem. 52, 5295–5298 (2009).
pubmed: 19691347 doi: 10.1021/jm9008295
Jain, S. & Parker, R. The discovery and analysis of P Bodies. Adv. Exp. Med. Biol. 768, 23–43 (2013).
pubmed: 23224963 doi: 10.1007/978-1-4614-5107-5_3
Anderson, P., Kedersha, N. & Ivanov, P. Stress granules, P-bodies and cancer. Biochim. Biophys. Acta 1849, 861–870 (2015).
pubmed: 25482014 doi: 10.1016/j.bbagrm.2014.11.009
Hondele, M. et al. DEAD-box ATPases are global regulators of phase-separated organelles. Nature 573, 144–148 (2019).
pubmed: 31435012 doi: 10.1038/s41586-019-1502-y
Markmiller, S. et al. Context-dependent and disease-specific diversity in protein interactions within stress granules. Cell 172, 590–604 (2018).
pubmed: 29373831 pmcid: 5969999 doi: 10.1016/j.cell.2017.12.032
Lallemand-Breitenbach, V. & de Thé, H. PML nuclear bodies: from architecture to function. Curr. Opin. Cell Biol. 52, 154–161 (2018).
pubmed: 29723661 doi: 10.1016/j.ceb.2018.03.011
Kato, M. et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753–767 (2012).
pubmed: 22579281 pmcid: 6347373 doi: 10.1016/j.cell.2012.04.017
Tabula Muris Consortium. A single-cell transcriptomic atlas characterizes ageing tissues in the mouse. Nature 583, 590–595 (2020).
doi: 10.1038/s41586-020-2496-1
Flohr Svendsen, A. et al. A comprehensive transcriptome signature of murine hematopoietic stem cell aging. Blood 138, 439–451 (2021).
pubmed: 33876187 doi: 10.1182/blood.2020009729
Nott, T. J. et al. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 57, 936–947 (2015).
pubmed: 25747659 pmcid: 4352761 doi: 10.1016/j.molcel.2015.01.013
Sanders, D. W. et al. Competing protein–RNA interaction networks control multiphase intracellular organization. Cell 181, 306–324 (2020).
pubmed: 32302570 pmcid: 7816278 doi: 10.1016/j.cell.2020.03.050
Alberti, S., Gladfelter, A. & Mittag, T. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176, 419–434 (2019).
pubmed: 30682370 pmcid: 6445271 doi: 10.1016/j.cell.2018.12.035
Riback, J. A. et al. Stress-triggered phase separation is an adaptive, evolutionarily tuned response. Cell 168, 1028–1040 (2017).
pubmed: 28283059 pmcid: 5401687 doi: 10.1016/j.cell.2017.02.027
Vanderweyde, T., Youmans, K., Liu-Yesucevitz, L. & Wolozin, B. Role of stress granules and RNA-binding proteins in neurodegeneration: a mini-review. Gerontology 59, 524–533 (2013).
pubmed: 24008580 doi: 10.1159/000354170
Kornmann, B. & Weis, K. Liquid but not contactless. Science 367, 507–508 (2020).
pubmed: 32001641 doi: 10.1126/science.aba3771
Chua, B. A. et al. Hematopoietic stem cells preferentially traffic misfolded proteins to aggresomes and depend on aggrephagy to maintain protein homeostasis. Cell Stem Cell 30, 460–472 (2023).
pubmed: 36948186 pmcid: 10164413 doi: 10.1016/j.stem.2023.02.010
Hartl, F. U. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858 (2002).
pubmed: 11884745 doi: 10.1126/science.1068408
Kandala, D. T., Del Piano, A., Minati, L. & Clamer, M. Targeting translation activity at the ribosome interface with UV-active small molecules. ACS Omega 4, 10336–10345 (2019).
pubmed: 31460127 pmcid: 6648492 doi: 10.1021/acsomega.9b00366
Favretto, F. et al. Catalysis of proline isomerization and molecular chaperone activity in a tug-of-war. Nat. Commun. 11, 6046 (2020).
pubmed: 33247146 pmcid: 7695863 doi: 10.1038/s41467-020-19844-0
Xiang, S. et al. The LC domain of hnRNPA2 adopts similar conformations in hydrogel polymers, liquid-like droplets and nuclei. Cell 163, 829–839 (2015).
pubmed: 26544936 pmcid: 4879888 doi: 10.1016/j.cell.2015.10.040
Ciferri, A. & Orofino, T. A. Phase separation of poly-L-proline in salt solutions. J. Phys. Chem. 70, 3277–3285 (1966).
doi: 10.1021/j100882a042
Jahn, T. R., Parker, M. J., Homans, S. W. & Radford, S. E. Amyloid formation under physiological conditions proceeds via a native-like folding intermediate. Nat. Struct. Mol. Biol. 13, 195–201 (2006).
pubmed: 16491092 doi: 10.1038/nsmb1058
Wolozin, B. & Ivanov, P. Stress granules and neurodegeneration. Nat. Rev. Neurosci. 20, 649–666 (2019).
pubmed: 31582840 pmcid: 6986315 doi: 10.1038/s41583-019-0222-5
Nakamura, K. et al. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer’s disease. Cell 149, 232–244 (2012).
pubmed: 22464332 pmcid: 3601591 doi: 10.1016/j.cell.2012.02.016
Riback, J. A. et al. Composition-dependent thermodynamics of intracellular phase separation. Nature 581, 209–214 (2020).
pubmed: 32405004 pmcid: 7733533 doi: 10.1038/s41586-020-2256-2
Babu, M., Favretto, F., Rankovic, M. & Zweckstetter, M. Peptidyl prolyl isomerase a modulates the liquid-liquid phase separation of proline-rich IDPs. J. Am. Chem. Sci. 144, 16157–16163 (2022).
doi: 10.1021/jacs.2c07149
Daito, T. et al. Cyclophilin inhibitors reduce phosphorylation of RNA-dependent protein kinase to restore expression of IFN-stimulated genes in HCV-infected cells. Gastroenterology 147, 463–472 (2014).
pubmed: 24786893 doi: 10.1053/j.gastro.2014.04.035
Selbach, M. et al. Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63 (2008).
pubmed: 18668040 doi: 10.1038/nature07228
De Maio, A. et al. RBM17 Interacts with U2SURP and CHERP to regulate expression and splicing of RNA-processing proteins. Cell Rep. 25, 726–736 (2018).
pubmed: 30332651 pmcid: 6292215 doi: 10.1016/j.celrep.2018.09.041
Jung, S. Y. et al. An anatomically resolved mouse brain proteome reveals Parkinson disease-relevant pathways. Mol. Cell. Proteomics 16, 581–593 (2017).
pubmed: 28153913 pmcid: 5383780 doi: 10.1074/mcp.M116.061440
Ferreon, J. C. et al. Acetylation disfavors tau phase separation. Int. J. Mol. Sci. 19, 1360 (2018).
pubmed: 29734651 pmcid: 5983838 doi: 10.3390/ijms19051360
Mészáros, B., Erdős, G. & Dosztányi, Z. IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res. 46, W329–W337 (2018).
pubmed: 29860432 pmcid: 6030935 doi: 10.1093/nar/gky384
Erdős, G. & Dosztányi, Z. Analyzing protein disorder with IUPred2A. Curr. Protoc. Bioinformatics 70, e99 (2020).
pubmed: 32237272 doi: 10.1002/cpbi.99
Lo Celso, C., Lin, C. P. & Scadden, D. T. In vivo imaging of transplanted hematopoietic stem and progenitor cells in mouse calvarium bone marrow. Nat. Protoc. 6, 1–14 (2011).
pubmed: 21212779 doi: 10.1038/nprot.2010.168
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772 doi: 10.1038/nmeth.2019
Brunetti, L., Gundry, M.C., Kitano, A., Nakada, D. & Goodell, M. A. Highly efficient gene disruption of murine and human hematopoietic progenitor cells by CRISPR/Cas9. J. Vis. Exp. 2018, 57278 (2018).
Moreno-Mateos, M. A. et al. CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat. Methods 12, 982–988 (2015).
pubmed: 26322839 pmcid: 4589495 doi: 10.1038/nmeth.3543
Mai, T. T., Tran, D. Q., Roos, S., Rhoads, J. M. & Liu, Y. Human breast milk promotes the secretion of potentially beneficial metabolites by probiotic Lactobacillus reuteri DSM 17938. Nutrients 11, 1548 (2019).
pubmed: 31323989 pmcid: 6683045 doi: 10.3390/nu11071548
Wilkinson, A. C., Ishida, R., Nakauchi, H. & Yamazaki, S. Long-term ex vivo expansion of mouse hematopoietic stem cells. Nat. Protoc. 15, 628–648 (2020).
pubmed: 31915389 pmcid: 7206416 doi: 10.1038/s41596-019-0263-2
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
pubmed: 23618408 pmcid: 4053844 doi: 10.1186/gb-2013-14-4-r36
Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46–53 (2013).
pubmed: 23222703 doi: 10.1038/nbt.2450
Garcia-Fossa, F. et al. Interpreting image-based profiles using similarity clustering and single-cell visualization. Curr. Protoc. 3, e713 (2023).
pubmed: 36921124 pmcid: 10027367 doi: 10.1002/cpz1.713
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Hou, C. et al. PhaSepDB in 2022: annotating phase separation-related proteins with droplet states, co-phase separation partners and other experimental information. Nucleic Acids Res. 51, D460–D465 (2023).
pubmed: 36124686 doi: 10.1093/nar/gkac783

Auteurs

Laure Maneix (L)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA.
Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.
ORCID: 0000-0003-0044-5395

Polina Iakova (P)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA.
Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.

Charles G Lee (CG)

Department of BioSciences, Rice University, Houston, TX, USA.

Shannon E Moree (SE)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA.
Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.
ORCID: 0000-0001-9479-6385

Xuan Lu (X)

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.

Gandhar K Datar (GK)

Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.

Cedric T Hill (CT)

Center for Regenerative Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Eric Spooner (E)

Whitehead Institute for Biomedical Research, Cambridge, MA, USA.

Jordon C K King (JCK)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA.
Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.

David B Sykes (DB)

Center for Regenerative Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Borja Saez (B)

Center for Applied Medical Research, Hematology-Oncology Unit, Pamplona, Navarra, Spain.
ORCID: 0000-0001-7908-7089

Bruno Di Stefano (B)

Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.
ORCID: 0000-0003-2532-3087

Xi Chen (X)

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
ORCID: 0000-0002-7995-6202

Daniela S Krause (DS)

Georg-Speyer-Haus, Institute for Tumor Biology and Experimental Therapy, Frankfurt am Main, Germany.
ORCID: 0000-0003-3603-1119

Ergun Sahin (E)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, TX, USA.

Francis T F Tsai (FTF)

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Department of Biochemistry and Molecular Pharmacology, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA.

Margaret A Goodell (MA)

Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA.
ORCID: 0000-0003-1111-2932

Bradford C Berk (BC)

Department of Medicine, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA.

David T Scadden (DT)

Center for Regenerative Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

André Catic (A)

Huffington Center on Aging, Baylor College of Medicine, Houston, TX, USA. catic@bcm.edu.
Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX, USA. catic@bcm.edu.
Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX, USA. catic@bcm.edu.
Cell and Gene Therapy Program at the Dan L. Duncan Comprehensive Cancer Center, Houston, TX, USA. catic@bcm.edu.
Michael E. DeBakey Veterans Affairs Medical Center, Houston, TX, USA. catic@bcm.edu.
ORCID: 0000-0002-3572-7598

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Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines intrinsèquement désordonnées › Cyclophilin A supports translation of...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Isomerases › Cis-trans-isomerases › Peptidylpropyl isomerase › Cyclophiline A › Cyclophilin A supports translation of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Cyclophilin A supports translation of...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système hématopoïétique › Cellules de la moelle osseuse › Cellules souches hématopoïétiques › Cyclophilin A supports translation of...