SUMOylation modulates eIF5A activities in both yeast and pancreatic ductal adenocarcinoma cells

doi:10.1186/s11658-024-00533-5

. 2024 Jan 16;29(1):15.

doi: 10.1186/s11658-024-00533-5.

SUMOylation modulates eIF5A activities in both yeast and pancreatic ductal adenocarcinoma cells

Rocío Seoane^{1

2}, Tomás Lama-Díaz^{1

3}, Antonia María Romero^{4

5}, Ahmed El Motiam^{1

6}, Arantxa Martínez-Férriz⁷, Santiago Vidal^{1

2}, Yanis H Bouzaher¹, María Blanquer¹, Rocío M Tolosa¹, Juan Castillo Mewa⁸, Manuel S Rodríguez⁹, Adolfo García-Sastre^{2

10

11

12}, Dimitris Xirodimas¹³, James D Sutherland¹⁴, Rosa Barrio¹⁴, Paula Alepuz^{4

15}, Miguel G Blanco^{1

3}, Rosa Farràs⁷, Carmen Rivas^{16

17}

Affiliations

¹ Centro de Investigación en Medicina Molecular (CIMUS), IDIS, Universidade de Santiago de Compostela, Avda Barcelona, 15706, Santiago de Compostela, Spain.
² Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
³ Departamento de Bioquímica e Bioloxía Molecular, Universidade de Santiago de Compostela, 15706, Santiago de Compostela, Spain.
⁴ Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Biológicas, Universitat de València, Burjassot, 46100, Valencia, Spain.
⁵ Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER), C/ Américo Vespucio 24, Edificio Cabimer, 41092, Seville, Spain.
⁶ Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, M5G 1X5, Canada.
⁷ Centro de Investigación Príncipe Felipe, 46012, Valencia, Spain.
⁸ Research Department in Genomics and Proteomics, Instituto Conmemorativo Gorgas de Estudios de la Salud, 0816-02593, Panamá, Republic of Panama.
⁹ Laboratoire de Chimie de Coordination LCC-UPR 8241-CNRS, 31400, Toulouse, France.
¹⁰ Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.
¹¹ Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹² The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹³ Montpellier Cell Biology Research Center (CRBM), CNRS-UMR 5237 Université de Montpellier, Montpellier, France.
¹⁴ Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, Building 801A, 48160, Derio, Spain.
¹⁵ Instituto Bio TecMed, Universitat de València, Burjassot, 46100, Valencia, Spain.
¹⁶ Centro de Investigación en Medicina Molecular (CIMUS), IDIS, Universidade de Santiago de Compostela, Avda Barcelona, 15706, Santiago de Compostela, Spain. mcarmen.rivas@usc.es.
¹⁷ Departamento de Biología Molecular y Celular, Centro Nacional de Biotecnología (CNB), CSIC, Darwin 3, 28049, Madrid, Spain. mcarmen.rivas@usc.es.

PMID: 38229033
PMCID: PMC10790418
DOI: 10.1186/s11658-024-00533-5

SUMOylation modulates eIF5A activities in both yeast and pancreatic ductal adenocarcinoma cells

Rocío Seoane et al. Cell Mol Biol Lett. 2024.

. 2024 Jan 16;29(1):15.

doi: 10.1186/s11658-024-00533-5.

Authors

Affiliations

¹ Centro de Investigación en Medicina Molecular (CIMUS), IDIS, Universidade de Santiago de Compostela, Avda Barcelona, 15706, Santiago de Compostela, Spain.
² Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
³ Departamento de Bioquímica e Bioloxía Molecular, Universidade de Santiago de Compostela, 15706, Santiago de Compostela, Spain.
⁴ Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Biológicas, Universitat de València, Burjassot, 46100, Valencia, Spain.
⁵ Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER), C/ Américo Vespucio 24, Edificio Cabimer, 41092, Seville, Spain.
⁶ Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, M5G 1X5, Canada.
⁷ Centro de Investigación Príncipe Felipe, 46012, Valencia, Spain.
⁸ Research Department in Genomics and Proteomics, Instituto Conmemorativo Gorgas de Estudios de la Salud, 0816-02593, Panamá, Republic of Panama.
⁹ Laboratoire de Chimie de Coordination LCC-UPR 8241-CNRS, 31400, Toulouse, France.
¹⁰ Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.
¹¹ Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹² The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹³ Montpellier Cell Biology Research Center (CRBM), CNRS-UMR 5237 Université de Montpellier, Montpellier, France.
¹⁴ Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, Building 801A, 48160, Derio, Spain.
¹⁵ Instituto Bio TecMed, Universitat de València, Burjassot, 46100, Valencia, Spain.
¹⁶ Centro de Investigación en Medicina Molecular (CIMUS), IDIS, Universidade de Santiago de Compostela, Avda Barcelona, 15706, Santiago de Compostela, Spain. mcarmen.rivas@usc.es.
¹⁷ Departamento de Biología Molecular y Celular, Centro Nacional de Biotecnología (CNB), CSIC, Darwin 3, 28049, Madrid, Spain. mcarmen.rivas@usc.es.

PMID: 38229033
PMCID: PMC10790418
DOI: 10.1186/s11658-024-00533-5

Abstract

Background: The eukaryotic translation initiation protein eIF5A is a highly conserved and essential factor that plays a critical role in different physiological and pathological processes including stress response and cancer. Different proteomic studies suggest that eIF5A may be a small ubiquitin-like modifier (SUMO) substrate, but whether eIF5A is indeed SUMOylated and how relevant is this modification for eIF5A activities are still unknown.

Methods: SUMOylation was evaluated using in vitro SUMOylation assays, Histidine-tagged proteins purification from His6-SUMO2 transfected cells, and isolation of endogenously SUMOylated proteins using SUMO-binding entities (SUBES). Mutants were engineered by site-directed mutagenesis. Protein stability was measured by a cycloheximide chase assay. Protein localization was determined using immunofluorescence and cellular fractionation assays. The ability of eIF5A1 constructs to complement the growth of Saccharomyces cerevisiae strains harboring thermosensitive mutants of a yeast EIF5A homolog gene (HYP2) was analyzed. The polysome profile and the formation of stress granules in cells expressing Pab1-GFP (a stress granule marker) by immunofluorescence were determined in yeast cells subjected to heat shock. Cell growth and migration of pancreatic ductal adenocarcinoma PANC-1 cells overexpressing different eIF5A1 constructs were evaluated using crystal violet staining and transwell inserts, respectively. Statistical analysis was performed with GraphPad Software, using unpaired Student's t-test, or one-way or two-way analysis of variance (ANOVA).

Results: We found that eIF5A is modified by SUMO2 in vitro, in transfected cells and under endogenous conditions, revealing its physiological relevance. We identified several SUMO sites in eIF5A and found that SUMOylation modulates both the stability and the localization of eIF5A in mammalian cells. Interestingly, the SUMOylation of eIF5A responds to specific stresses, indicating that it is a regulated process. SUMOylation of eIF5A is conserved in yeast, the eIF5A SUMOylation mutants are unable to completely suppress the defects of HYP2 mutants, and SUMOylation of eIF5A is important for both stress granules formation and disassembly of polysomes induced by heat-shock. Moreover, mutation of the SUMOylation sites in eIF5A abolishes its promigratory and proproliferative activities in PANC-1 cells.

Conclusions: SUMO2 conjugation to eIF5A is a stress-induced response implicated in the adaptation of yeast cells to heat-shock stress and required to promote the growth and migration of pancreatic ductal adenocarcinoma cells.

Keywords: Pancreatic ductal adenocarcinoma; SUMO2; Stress granules; Stress response; eIF5A.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

**Fig. 1**
eIF5A1 protein is modified by SUMO2 in vitro and in vivo in an hypusine-independent manner. A In vitro SUMOylation assay with SUMO2 using ³⁵S-methionine labeled in vitro translated HA–eIF5A1 protein. B HEK-293 cells were cotransfected with a plasmid encoding Flag–eIF5A1 and pcDNA or Flag–eIF5A1, Ubc9, and His6–SUMO2. Thirty-six hours after transfection, total protein extracts (WCE) and proteins fused to Histidine (His) tag were analyzed by western blot with the indicated antibodies. C SUMOylation of endogenous eIF5A1. SUMOylated proteins purified from HEK-293 cells using SUBES were analyzed by western blot with anti-eIF5A1 or anti-SUMO2 antibody. D Amino acid sequence homology between human eIF5A1 and eIF5A2. E In vitro SUMOylation assay using ³⁵S-methionine labeled in vitro translated eIF5A2 protein and SUMO2. F HEK-293 cells were co-transfected with Flag–eIF5A2 and pcDNA or Flag–eIF5A2, UBC9, and His6–SUMO2. Thirty-six hours after transfection, total protein extracts and proteins fused to Histidine tag were analyzed by western blot with the indicated antibodies. G In vitro SUMOylation assay in the presence of SUMO2 and using ³⁵S-methionine labeled in vitro translated eIF5A1–WT or the eIF5A1–K50R hypusination mutant as a substrate. H HEK-293 cells were transfected with HA–eIF5A1–WT or HA–eIF5A1–K50R together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies (left panel). The ratio of SUMOylated eIF5A to unmodified eIF5A is shown (right panel). Data represent the mean and error bars of three biological replicates. I In vitro translated Flag–eIF5A1–WT protein was subjected to an in vitro SUMOylation assay in the presence of SUMO2 and the SUMOylation products were analyzed by western blot with anti-hypusine or anti-Flag antibodies. Arrowheads in all panels indicate unconjugated eIF5A protein. Arrows indicate the SUMO2-conjugated eIF5A protein

**Fig. 2**
Identification of the SUMO conjugation sites on eIF5A1. A, B In vitro SUMOylation assay with SUMO2 and the indicated ³⁵S-methionine-labeled in vitro translated eIF5A1 proteins. C HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT, eIF5A1–3KA, or eIF5A1–5KA. Thirty-six hours after transfection, cells were treated with MG132 for 16 h and protein extracts were analyzed by western blot with anti-HA and anti-GAPDH antibodies. D HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT, eIF5A1–3KA, or eIF5A1–5KA together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were treated with MG132 for 16 h and whole-protein extracts (WCE) and Histidine (His)-tagged purified proteins were analyzed by western blot with the indicated antibodies. E HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT, eIF5A1–3KR, or eIF5A1–5KR together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were treated with MG132 for 16 h and whole-protein extracts (WCE) and Histidine (His)-tagged purified proteins were analyzed by western blot with the indicated antibodies. Arrowheads in all panels indicate unconjugated eIF5A1 protein. Arrows indicate the SUMO2-conjugated eIF5A1 protein

**Fig. 3**
Mutation of the SUMOylation sites in eIF5A1 modulates its stability. A HEK-293 cells were transfected with HA–eIF5A1–WT, HA–eIF5A1–3KR, or HA–eIF5A1–5KR, and treated with cycloheximide (CHX) 24 h after transfection. Samples were collected at the indicated hours post treatment (hpt) and protein extracts were analyzed by western blot with the indicated antibodies (left panel). The intensity of the bands was quantified using ImageJ software. eIF5A band intensities were normalized to GAPDH bands from each respective time and plotted (right panel). Data represent the mean and error bars of three biological replicates. Statistical analysis was assessed by a Student’s t-test. *P < 0.05, **P < 0.01, compared with WT. B HEK-293 cells were transfected and treated as indicated in A but in presence or absence of MG132 treatment. At the indicated times after CHX treatment, protein extracts were analyzed by western blot with the indicated antibodies (upper panels). The intensity of the bands was quantified using ImageJ software. eIF5A band intensities were normalized to actin bands from each respective time and plotted (lower panels). Data represent the mean and error bars of three biological replicates. Statistical analysis was assessed by a Student’s t-test. *P < 0.05, **P < 0.01. C HEK-293 cells were transfected with HA–eIF5A1–WT, HA–eIF5A1–5KR, or HA–eIF5A–3KR, and 24 h after transfection cells were treated with DMSO or ML-792 (500 nM) for 16 h. Then, the cells were treated with cycloheximide (CHX) for the indicated times and protein extracts were analyzed by western blot with anti-HA antibody (upper panels). The intensity of the bands was quantified using ImageJ software. eIF5A band intensities were normalized to GAPDH bands from each respective time and plotted (lower panels). Data represent the mean and error bars of three biological replicates. Statistical analysis was assessed by a Student’s t-test. *P < 0.05

**Fig. 4**
Mutation of the SUMOylation sites in eIF5A1 modulates its subcellular localization. A U2Os cells were transfected with HA–eIF5A1–WT, HA–eIF5A1–3KR, or HA–eIF5A1–5KR and 36 h after transfection localization of eIF5A was evaluated using immunofluorescence assay with anti-HA antibody. The nuclear to cytoplasmic ratio was analyzed from images using ImageJ analysis software. Data represent the mean and error bars of 50 cells. Statistical analysis was assessed by a Student’s t-test.***P < 0.001. B HEK-293 cells were transfected with HA–eIF5A1–WT, HA–eIF5A1–3KR, or HA–eIF5A–5KR, as indicated. Thirty-six hours after transfection, cells were subjected to subcellular fractionation and the levels of eIF5A1 protein in the nucleus and cytoplasm were evaluated using western blot analysis with anti-HA antibody. C HEK-293 cells treated with DMSO or the SUMOylation inhibitor ML-792 were subjected to subcellular fractionation and then the levels of the eIF5A1 protein in the nucleus and cytoplasm were evaluated using western blot analysis with anti-eIF5A1 antibody

**Fig. 5**
Modulation of eIF5A1 SUMO2 modification upon stress. A HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were treated with DMSO or MG132 for 16 h and whole-protein extracts (WCE) and Histidine (His)-tagged purified proteins were analyzed by western blot with the indicated antibodies. B HEK-293 cells were transfected with HA–eIF5A1–WT together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were subjected to UV irradiation (20 J/m²) followed by 2 h or 6 h rest, and then whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. Arrow indicates eIF5A–SUMO2 protein. C HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were incubated in hypoxic conditions (1% O₂) for 8 h or treated with adriamycin 1 μM for 4 h and then whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. Arrow indicates eIF5A1–SUMO2 protein. D HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were incubated at 43 °C for 2 h and then whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. E HEK-293 cells were transfected with a plasmid encoding HA-tagged eIF5A1–WT together with pcDNA or Ubc9 and His6–SUMO2. Thirty-six hours after transfection, cells were first incubated at 43 °C for 2 h (HS) and then incubated at 37 °C for 0.5 or 2 h (hpt HS), as indicated. Then, whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. Arrowheads in all panels indicate unconjugated eIF5A1 protein

**Fig. 6**
Upregulation of eIF5A1 SUMO2 modification upon stress. A HEK-293 cells were cotransfected with HA–eIF5A1–WT, Ubc9, and His6–SUMO2–K11RK48R or His6–SUMO2–K0. 36 h after transfection cells were treated with DMSO or MG132 for 16 h and whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. B HEK-293 cells were cotransfected with HA–eIF5A1–WT, pcDNA, Ubc9, and His6–SUMO2 or Ubc9 and His6–SUMO2–K0. Thirty-six hours after transfection, cells were incubated at 43 °C for 2 h, as indicated, and whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies. C HEK-293 cells were cotransfected with HA–eIF5A1–WT and pcDNA or Ubc9 and His6–SUMO2–K0. Twenty-four hours after transfection, cells were treated with DMSO or TAK-243, as indicated, and at 12 h after treatment, cells were incubated at 43 °C for 2 h. Whole-protein extracts and Histidine-tagged purified proteins were analyzed by western blot with the indicated antibodies

**Fig. 7**
An eIF5A1 SUMOylation-deficient mutant cannot completely substitute for yeast *HYP2*. A Histidine-tagged proteins were purified from yeast cells transformed with an empty vector or with Histidine- and Flag-tagged human eIF5A1–WT under denaturing conditions. Then, purified proteins were analyzed by western blot using anti-Smt3 antibody. Arrow indicates Smt3-conjugated eIF5A1 protein. B Histidine-tagged proteins were purified from yeast cells transformed with an empty vector, Histidine- and Flag-tagged human eIF5A1–WT or Histidine- and Flag-tagged human eIF5A1–5KR under denaturing conditions. Purified proteins were then analyzed by western blot using anti-Smt3 antibody. C WT and *hyp2-1* (upper row) or *hyp2-3* (lower row) yeast strains were transformed with different alleles of Histidine- and Flag-tagged human eIF5A1 in a pAG425GPD vector or with the empty vector. The resulting strains were streaked on SC–Leu plates, incubated at 25 °C or 37 °C for 3 days and imaged in a GelDoc documentation system. D Expression levels of the different versions of eIF5A in the indicated strains, growing at 25 °C or after 4 h at 37 °C, were analyzed by western blot. Ponceau staining of the membrane is shown as a loading control

**Fig. 8**
SUMOylation of eIF5A1 is important for polysome disassembly and SG formation upon heat-shock stress. A Yeast cells with temperature-sensitive eIF5A mutant *hyp2-1* were transformed with different alleles of Histidine- and Flag-tagged human eIF5A1 in a pAG425GPD vector or with the empty vector. Cells were grown in SC–Leu medium until early exponential phase, incubated at 37 °C for 4 h to deplete endogenous eIF5A and then subjected to severe heat shock stress (46 °C, 30 min). Representative polysome profiles after gradient fractionation of yeast extracts are shown and the ribosomal subunits (40S and 60S), monosomes (80S), and polysomes are indicated (upper panel). When translation is arrested during stress, a reduction in the intensity of polysome peaks is seen because fewer ribosomes initiate translation. At the same time, the 60S and 80S peaks increase. The percentage of polysomes from three (eIF5A WT, vector, eIF5A–K50R, eIF5A–3KA) or two (eIF5A–3KR) independent experiments is shown as the median and standard deviation (lower panel). Statistical analysis was assessed by a Student’s t-test. *P < 0.05. B *hyp2-1* yeast strains were cotransformed with the SG marker Pab1–GFP together with the Histidine- and Flag-tagged human eIF5A1 WT or 5KR or an empty vector. WT yeast transformed with Pab1–GFP was included as a positive control. The resulting strains were incubated at 25 °C or heat shocked at 46 °C for 10 min and the formation of SG was then evaluated using a fluorescence microscope

**Fig. 9**
SUMOylation sites in eIF5A are essential to drive proliferation of PANC-1 cells and to promote PANC-1 cells migration in vitro. A Western blot analysis of RhoA and Ras in PANC-1 cells transiently transfected with HA–eIF5A1–WT, HA–eIF5A1–3KR, HA–eIF5A1–5KR, or the empty vector pcDNA. B PANC-1 cells stably transfected with pcDNA, HA–eIF5A1–WT, HA–eIF5A1–3KR, or HA–eIF5A1–5KR were evaluated for cell growth. Graphs show the proliferation of PANC-1 cells after the indicated times of growth. Data represent the mean and error bars of three biological replicates. ANOVA **P < 0.01, ****P < 0.0001 compared with the cells overexpressing eIF5A–WT; ###P < 0.001, ####P < 0.0001 compared with the pcDNA transfected cells. C, Migration of PANC1 cells stably transfected with pcDNA, HA–eIF5A1–WT, HA–eIF5A1–3KR, or HA–eIF5A1–5KR was determined by transwell migration assay (left panel). Data represent the mean and error bars of three biological replicates. ANOVA *P < 0.05, **P < 0.01, ***P < 0.001 compared with the cells overexpressing eIF5A–WT; ##P < 0.01 compared with the pcDNA transfected cells. Right panel shows western blot analysis of the expression of HA–eIF5A–WT or the mutant proteins in the PANC-1 cells analyzed in B and C

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References

1. Mathews MB, Hershey JW. The translation factor eIF5A and human cancer. Biochim Biophys Acta. 2015;1849(7):836–844. doi: 10.1016/j.bbagrm.2015.05.002. - DOI - PMC - PubMed
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[1] Mathews MB, Hershey JW. The translation factor eIF5A and human cancer. Biochim Biophys Acta. 2015;1849(7):836–844. doi: 10.1016/j.bbagrm.2015.05.002. - DOI - PMC - PubMed

[2] Mathews MB, Hershey JW. The translation factor eIF5A and human cancer. Biochim Biophys Acta. 2015;1849(7):836–844. doi: 10.1016/j.bbagrm.2015.05.002. - DOI - PMC - PubMed

[3] Li CH, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE. 2010;5(4):e9942. doi: 10.1371/journal.pone.0009942. - DOI - PMC - PubMed

[4] Li CH, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE. 2010;5(4):e9942. doi: 10.1371/journal.pone.0009942. - DOI - PMC - PubMed

[5] Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol. 2008;10(10):1224–1231. doi: 10.1038/ncb1783. - DOI - PMC - PubMed

[6] Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol. 2008;10(10):1224–1231. doi: 10.1038/ncb1783. - DOI - PMC - PubMed

[7] Schuller AP, Wu CC, Dever TE, Buskirk AR, Green R. eIF5A functions globally in translation elongation and termination. Mol Cell. 2017;66(2):194–205.e5. doi: 10.1016/j.molcel.2017.03.003. - DOI - PMC - PubMed

[8] Schuller AP, Wu CC, Dever TE, Buskirk AR, Green R. eIF5A functions globally in translation elongation and termination. Mol Cell. 2017;66(2):194–205.e5. doi: 10.1016/j.molcel.2017.03.003. - DOI - PMC - PubMed

[9] Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459(7243):118–121. doi: 10.1038/nature08034. - DOI - PMC - PubMed

[10] Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459(7243):118–121. doi: 10.1038/nature08034. - DOI - PMC - PubMed

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SUMOylation modulates eIF5A activities in both yeast and pancreatic ductal adenocarcinoma cells

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SUMOylation modulates eIF5A activities in both yeast and pancreatic ductal adenocarcinoma cells

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