An integrative proteomics method identifies a regulator of translation during stem cell maintenance and differentiation.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 11 2021
Historique:
received: 25 11 2020
accepted: 25 10 2021
entrez: 13 11 2021
pubmed: 14 11 2021
medline: 28 12 2021
Statut: epublish

Résumé

Detailed characterization of cell type transitions is essential for cell biology in general and particularly for the development of stem cell-based therapies in regenerative medicine. To systematically study such transitions, we introduce a method that simultaneously measures protein expression and thermal stability changes in cells and provide the web-based visualization tool ProteoTracker. We apply our method to study differences between human pluripotent stem cells and several cell types including their parental cell line and differentiated progeny. We detect alterations of protein properties in numerous cellular pathways and components including ribosome biogenesis and demonstrate that modulation of ribosome maturation through SBDS protein can be helpful for manipulating cell stemness in vitro. Using our integrative proteomics approach and the web-based tool, we uncover a molecular basis for the uncoupling of robust transcription from parsimonious translation in stem cells and propose a method for maintaining pluripotency in vitro.

Identifiants

pubmed: 34772928
doi: 10.1038/s41467-021-26879-4
pii: 10.1038/s41467-021-26879-4
pmc: PMC8590018
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6558

Informations de copyright

© 2021. The Author(s).

Références

Am J Hum Genet. 2006 Jun;78(6):936-46
pubmed: 16685645
Am J Hum Genet. 2007 Oct;81(4):756-67
pubmed: 17847000
Hematol Oncol Clin North Am. 2009 Apr;23(2):233-48
pubmed: 19327581
J Proteome Res. 2019 Nov 1;18(11):4027-4037
pubmed: 31545609
Cell Stem Cell. 2013 Jun 6;12(6):727-36
pubmed: 23602541
Sci Rep. 2015 Jan 28;5:8081
pubmed: 25628230
Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):E1848-57
pubmed: 22645348
Nat Protoc. 2015 Oct;10(10):1567-93
pubmed: 26379230
Cell Stem Cell. 2021 Nov 4;28(11):1950-1965.e6
pubmed: 34388375
Elife. 2015 Jul 21;4:
pubmed: 26194807
Nature. 2019 Oct;574(7778):418-422
pubmed: 31619793
Science. 2018 Mar 9;359(6380):1170-1177
pubmed: 29439025
Cell Rep. 2020 Oct 6;33(1):108222
pubmed: 33027665
Cell Stem Cell. 2013 Jan 3;12(1):127-37
pubmed: 23168164
PLoS One. 2013 Aug 12;8(8):e71098
pubmed: 23951090
Wiley Interdiscip Rev Dev Biol. 2017 Mar;6(2):
pubmed: 27911036
Nat Commun. 2019 Dec 16;10(1):5715
pubmed: 31844049
Stem Cell Reports. 2017 Dec 12;9(6):1754-1764
pubmed: 29173898
Nat Cell Biol. 2017 Nov;19(11):1298-1306
pubmed: 29058720
BMC Bioinformatics. 2009 Feb 03;10:48
pubmed: 19192299
Science. 1998 Nov 6;282(5391):1145-7
pubmed: 9804556
Cell Stem Cell. 2018 Mar 1;22(3):369-383.e8
pubmed: 29499153
Nat Methods. 2020 May;17(5):495-503
pubmed: 32284610
Nature. 2019 Feb;566(7742):100-104
pubmed: 30700908
Reprod Fertil Dev. 2014 Dec;27(1):82-8
pubmed: 25472047
Nat Commun. 2021 Feb 26;12(1):1296
pubmed: 33637753
Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):452-6
pubmed: 7831309
Nat Commun. 2016 Apr 07;7:11208
pubmed: 27052461
Physiol Rev. 2019 Jan 1;99(1):79-114
pubmed: 30328784
PLoS Comput Biol. 2007 Mar 23;3(3):e39
pubmed: 17381235
Cell. 2018 May 31;173(6):1495-1507.e18
pubmed: 29706546
Nat Cell Biol. 2020 Sep;22(9):1033-1041
pubmed: 32884148
Cell. 2016 Feb 11;164(4):757-69
pubmed: 26871635
Haematologica. 2015 Oct;100(10):1285-93
pubmed: 26185170
Cell Stem Cell. 2010 Aug 6;7(2):249-57
pubmed: 20682450
EMBO J. 2015 Jan 13;34(2):138-53
pubmed: 25476451
Cell Stem Cell. 2016 Feb 4;18(2):276-90
pubmed: 26669894
Cell Stem Cell. 2016 Jan 7;18(1):79-90
pubmed: 26549106
Science. 2013 Jul 5;341(6141):84-7
pubmed: 23828940
Exp Mol Med. 2020 Sep;52(9):1443-1451
pubmed: 32929224
Nature. 2016 Jun 15;534(7607):335-40
pubmed: 27306184
Proc Natl Acad Sci U S A. 2017 Jul 25;114(30):E6072-E6078
pubmed: 28696312
Gastroenterol Res Pract. 2016;2016:6089658
pubmed: 27047543
Nat Genet. 2003 Jan;33(1):97-101
pubmed: 12496757
Proteomics. 2018 Dec;18(24):e1800118
pubmed: 30382632
Genes Dev. 2011 May 1;25(9):917-29
pubmed: 21536732
Proc Natl Acad Sci U S A. 2020 Jan 14;117(2):1015-1020
pubmed: 31892536
Cell Stem Cell. 2008 May 8;2(5):448-60
pubmed: 18462695
Science. 2014 Oct 3;346(6205):1255784
pubmed: 25278616
Biophys J. 2012 Apr 18;102(8):1907-15
pubmed: 22768947
Nat Methods. 2015 Dec;12(12):1129-31
pubmed: 26524241
Cell Stem Cell. 2008 May 8;2(5):437-47
pubmed: 18462694
Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3225-30
pubmed: 19218428
Nat Rev Mol Cell Biol. 2011 Jan;12(1):36-47
pubmed: 21179060
Hum Mutat. 2015 May;36(5):524-534
pubmed: 25689729
Nat Protoc. 2014 Oct;9(10):2354-68
pubmed: 25211513
Cell. 2018 May 31;173(6):1481-1494.e13
pubmed: 29706543
Stem Cells Transl Med. 2017 Dec;6(12):2173-2185
pubmed: 29076267
Stem Cell Reports. 2015 Feb 10;4(2):282-96
pubmed: 25680479
Curr Opin Struct Biol. 2015 Jun;32:18-24
pubmed: 25658850
Nature. 2017 May 25;545(7655):432-438
pubmed: 28514439
Sci Data. 2014 Sep 30;1:140035
pubmed: 25984343
Nat Struct Mol Biol. 2015 Nov;22(11):914-9
pubmed: 26479198
Nat Biotechnol. 2014 Oct;32(10):1036-44
pubmed: 25218519
Biomed Microdevices. 2014 Feb;16(1):79-90
pubmed: 24085533

Auteurs

Pierre Sabatier (P)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.

Christian M Beusch (CM)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.

Amir A Saei (AA)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.
Department of Cell Biology, Harvard Medical School, Boston, MA, USA.

Mike Aoun (M)

Division of Medical Inflammation Research, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.

Noah Moruzzi (N)

The Rolf Luft Research Center for Diabetes and Endocrinology, Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, 17176, Sweden.

Ana Coelho (A)

Division of Medical Inflammation Research, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.

Niels Leijten (N)

Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Padualaan 8, Utrecht, 3584 CH, The Netherlands.

Magnus Nordenskjöld (M)

Center for Molecular Medicine, Karolinska University Hospital, Stockholm, 171 76, Sweden.
Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, 17177, Sweden.
Department of Clinical Genetics, Karolinska University Hospital, Stockholm, 171 76, Sweden.

Patrick Micke (P)

Immunology, Genetics and Pathology, Rudbecklaboratoriet, Uppsala University, Uppsala, 751 85, Sweden.

Diana Maltseva (D)

Faculty of biology and biotechnology, National Research University Higher School of Economics, Myasnitskaya Street, 13/4, Moscow, 117997, Russia.

Alexander G Tonevitsky (AG)

Faculty of biology and biotechnology, National Research University Higher School of Economics, Myasnitskaya Street, 13/4, Moscow, 117997, Russia.
Scientific Research Center Bioclinicum, Ugreshskaya str. 2/85, Moscow, 115088, Russia.

Vincent Millischer (V)

Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, 17177, Sweden.
Translational Psychiatry, Center for Molecular Medicine, Karolinska University Hospital, Stockholm, 171 76, Sweden.
Department of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, 1090, Austria.

J Carlos Villaescusa (J)

Neurogenetic Unit, Department of Molecular Medicine and Surgery, Karolinska University Hospital, Stockholm, 171 76, Sweden.
Stem Cell R&D-TRU, Novo Nordisk A/S, Måløv, Denmark.

Sandeep Kadekar (S)

Department of Surgical Sciences, Uppsala University, Uppsala, 752 37, Sweden.

Massimiliano Gaetani (M)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.
Chemical Proteomics Core Facility, Division of Physiological Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, 171 77, Sweden.
Chemical Proteomics, Science for Life Laboratory (SciLifeLab), Stockholm, 17 177, Sweden.

Kamilya Altynbekova (K)

geneXplain GmbH, Am Exer 19B, 38302, Wolfenbuettel, Germany.

Alexander Kel (A)

geneXplain GmbH, Am Exer 19B, 38302, Wolfenbuettel, Germany.

Per-Olof Berggren (PO)

The Rolf Luft Research Center for Diabetes and Endocrinology, Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, 17176, Sweden.

Oscar Simonson (O)

Department of Surgical Sciences, Uppsala University, Uppsala, 752 37, Sweden.
Department of Cardio-thoracic Surgery and Anesthesiology, Uppsala University Hospital, Uppsala, 751 85, Sweden.

Karl-Henrik Grinnemo (KH)

Department of Surgical Sciences, Uppsala University, Uppsala, 752 37, Sweden.
Department of Cardio-thoracic Surgery and Anesthesiology, Uppsala University Hospital, Uppsala, 751 85, Sweden.

Rikard Holmdahl (R)

Division of Medical Inflammation Research, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden.

Sergey Rodin (S)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden. sergey.rodin@surgsci.uu.se.
Department of Surgical Sciences, Uppsala University, Uppsala, 752 37, Sweden. sergey.rodin@surgsci.uu.se.
Department of Cardio-thoracic Surgery and Anesthesiology, Uppsala University Hospital, Uppsala, 751 85, Sweden. sergey.rodin@surgsci.uu.se.

Roman A Zubarev (RA)

Chemistry I, Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, 17177, Sweden. roman.zubarev@ki.se.
Department of Pharmacological & Technological Chemistry, I.M. Sechenov First Moscow State Medical University, Moscow, 119146, Russia. roman.zubarev@ki.se.
The National Medical Research Center for Endocrinology, Moscow, 115478, Russia. roman.zubarev@ki.se.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH