Lactate regulates cell cycle by remodelling the anaphase promoting complex
Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation 1 – 6 . However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of...
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| Published in | Nature (London) Vol. 616; no. 7958; pp. 790 - 797 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
27.04.2023
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/s41586-023-05939-3 |
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| Abstract | Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation
1
–
6
. However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation.
Discovery of a biochemical mechanism through which lactate binds and inhibits the SUMO protease SENP1, stimulating timed degradation of cell cycle proteins, and resulting in mitotic exit. |
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| AbstractList | Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation
. However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation. Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation1-6. However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation.Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation1-6. However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation. Lactate is abundant in rapidly dividing cells due to the requirement for elevated glucose catabolism to support proliferation 1 – 6 . However, it is not known whether accumulated lactate affects the proliferative state. Here, we deploy a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we elucidate a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodeling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We discover that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. The above mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient replete growth phase to stimulate timed opening of APC/C, cell division, and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodeling and can overcome anti-mitotic pharmacology via mitotic slippage. Taken together, we define a biochemical mechanism through which lactate directly regulates protein function to control cell cycle and proliferation. Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation1-6. However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling ofAPC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation oftwo residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation. Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation 1 – 6 . However, it is not known whether accumulated lactate affects the proliferative state. Here we use a systematic approach to determine lactate-dependent regulation of proteins across the human proteome. From these data, we identify a mechanism of cell cycle regulation whereby accumulated lactate remodels the anaphase promoting complex (APC/C). Remodelling of APC/C in this way is caused by direct inhibition of the SUMO protease SENP1 by lactate. We find that accumulated lactate binds and inhibits SENP1 by forming a complex with zinc in the SENP1 active site. SENP1 inhibition by lactate stabilizes SUMOylation of two residues on APC4, which drives UBE2C binding to APC/C. This direct regulation of APC/C by lactate stimulates timed degradation of cell cycle proteins, and efficient mitotic exit in proliferative human cells. This mechanism is initiated upon mitotic entry when lactate abundance reaches its apex. In this way, accumulation of lactate communicates the consequences of a nutrient-replete growth phase to stimulate timed opening of APC/C, cell division and proliferation. Conversely, persistent accumulation of lactate drives aberrant APC/C remodelling and can overcome anti-mitotic pharmacology via mitotic slippage. In sum, we define a biochemical mechanism through which lactate directly regulates protein function to control the cell cycle and proliferation. Discovery of a biochemical mechanism through which lactate binds and inhibits the SUMO protease SENP1, stimulating timed degradation of cell cycle proteins, and resulting in mitotic exit. |
| Author | Xu, Andrew Z. Winther, Sally Burger, Nils Song, Kijun Chouchani, Edward T. He, Xiadi Tran, Nhien Mills, Evanna L. Sprenger, Hans-Georg Arthanari, Haribabu Sebastian, Luke Che, Jianwei Liu, Weihai Hinshaw, Stephen M. Bozi, Luiz H. M. Fischer, Patrick D. Reddy, Anita Zhao, Jean J. Shen, Jingnan Shin, Sanghee Jedrychowski, Mark P. Gygi, Steven P. Wu, Tao Seo, Hyuk-Soo Xiao, Haopeng Wang, Yun Darabedian, Narek Dhe-Paganon, Sirano |
| AuthorAffiliation | 1 Department of Cancer Biology, Dana–Farber Cancer Institute, Boston, MA, USA 5 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA 9 Broad Institute of Harvard and MIT, Cambridge, MA, USA 4 Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, Guangdong 510000, China 7 Department of Systems Biology, Harvard Medical School, Boston, MA, USA 8 Stanford Cancer Institute, School of Medicine, Stanford University, Stanford, California 94305, United States 3 Department of Musculoskeletal Oncology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong 510080, China 2 Department of Cell Biology, Harvard Medical School, Boston, MA, USA 6 Department of Pharmacy, Pharmaceutical and Medicinal Chemistry, Saarland University, Saarbrücken, Germany |
| AuthorAffiliation_xml | – name: 8 Stanford Cancer Institute, School of Medicine, Stanford University, Stanford, California 94305, United States – name: 6 Department of Pharmacy, Pharmaceutical and Medicinal Chemistry, Saarland University, Saarbrücken, Germany – name: 7 Department of Systems Biology, Harvard Medical School, Boston, MA, USA – name: 9 Broad Institute of Harvard and MIT, Cambridge, MA, USA – name: 1 Department of Cancer Biology, Dana–Farber Cancer Institute, Boston, MA, USA – name: 3 Department of Musculoskeletal Oncology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong 510080, China – name: 4 Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, Guangdong 510000, China – name: 2 Department of Cell Biology, Harvard Medical School, Boston, MA, USA – name: 5 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA |
| Author_xml | – sequence: 1 givenname: Weihai surname: Liu fullname: Liu, Weihai organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School, Department of Musculoskeletal Oncology, The First Affiliated Hospital, Sun Yat-sen University – sequence: 2 givenname: Yun surname: Wang fullname: Wang, Yun organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School, Hospital of Stomatology, Guanghua School of Stomatology, Sun Yat-sen University – sequence: 3 givenname: Luiz H. M. surname: Bozi fullname: Bozi, Luiz H. M. organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 4 givenname: Patrick D. orcidid: 0000-0003-4160-5295 surname: Fischer fullname: Fischer, Patrick D. organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Department of Pharmacy, Pharmaceutical and Medicinal Chemistry, Saarland University – sequence: 5 givenname: Mark P. surname: Jedrychowski fullname: Jedrychowski, Mark P. organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 6 givenname: Haopeng orcidid: 0000-0002-4166-647X surname: Xiao fullname: Xiao, Haopeng organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 7 givenname: Tao surname: Wu fullname: Wu, Tao organization: Department of Systems Biology, Harvard Medical School – sequence: 8 givenname: Narek surname: Darabedian fullname: Darabedian, Narek organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 9 givenname: Xiadi surname: He fullname: He, Xiadi organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 10 givenname: Evanna L. orcidid: 0000-0003-0447-8995 surname: Mills fullname: Mills, Evanna L. organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 11 givenname: Nils orcidid: 0000-0003-3227-8894 surname: Burger fullname: Burger, Nils organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 12 givenname: Sanghee surname: Shin fullname: Shin, Sanghee organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 13 givenname: Anita surname: Reddy fullname: Reddy, Anita organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 14 givenname: Hans-Georg surname: Sprenger fullname: Sprenger, Hans-Georg organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 15 givenname: Nhien surname: Tran fullname: Tran, Nhien organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 16 givenname: Sally surname: Winther fullname: Winther, Sally organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 17 givenname: Stephen M. surname: Hinshaw fullname: Hinshaw, Stephen M. organization: Stanford Cancer Institute, School of Medicine, Stanford University – sequence: 18 givenname: Jingnan surname: Shen fullname: Shen, Jingnan organization: Department of Musculoskeletal Oncology, The First Affiliated Hospital, Sun Yat-sen University – sequence: 19 givenname: Hyuk-Soo orcidid: 0000-0003-0646-2102 surname: Seo fullname: Seo, Hyuk-Soo organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 20 givenname: Kijun orcidid: 0000-0002-6037-9345 surname: Song fullname: Song, Kijun organization: Department of Cancer Biology, Dana–Farber Cancer Institute – sequence: 21 givenname: Andrew Z. surname: Xu fullname: Xu, Andrew Z. organization: Department of Cancer Biology, Dana–Farber Cancer Institute – sequence: 22 givenname: Luke orcidid: 0000-0002-6863-9420 surname: Sebastian fullname: Sebastian, Luke organization: Department of Cancer Biology, Dana–Farber Cancer Institute – sequence: 23 givenname: Jean J. orcidid: 0000-0002-4561-5688 surname: Zhao fullname: Zhao, Jean J. organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Broad Institute of Harvard and MIT – sequence: 24 givenname: Sirano orcidid: 0000-0003-0824-5929 surname: Dhe-Paganon fullname: Dhe-Paganon, Sirano organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 25 givenname: Jianwei surname: Che fullname: Che, Jianwei organization: Department of Cancer Biology, Dana–Farber Cancer Institute – sequence: 26 givenname: Steven P. orcidid: 0000-0001-7626-0034 surname: Gygi fullname: Gygi, Steven P. organization: Department of Cell Biology, Harvard Medical School – sequence: 27 givenname: Haribabu surname: Arthanari fullname: Arthanari, Haribabu organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 28 givenname: Edward T. orcidid: 0000-0002-9776-8790 surname: Chouchani fullname: Chouchani, Edward T. email: edwardt_chouchani@dfci.harvard.edu organization: Department of Cancer Biology, Dana–Farber Cancer Institute, Department of Cell Biology, Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36921622$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. 2023. The Author(s), under exclusive licence to Springer Nature Limited. Copyright Nature Publishing Group Apr 27, 2023 |
| Copyright_xml | – notice: The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. – notice: 2023. The Author(s), under exclusive licence to Springer Nature Limited. – notice: Copyright Nature Publishing Group Apr 27, 2023 |
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| DOI | 10.1038/s41586-023-05939-3 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author Contributions: W.L. and E.T.C. conceived of and designed the study. W.L., Y.W. and L.H.M.B performed cellular experiments and analyzed data. M.P.J., H.X., and N.D. carried out and analyzed data from mass spectrometry experiments. P.F. performed and analyzed data from NMR experiments. S.W. and E.L.M. carried out thermal proteome profiling experiments. T.W. assisted with design of APC/C experiments. N.D. assisted with protein expression and purification. X.H. assisted with timelapse microscopy. E.L.M. performed T cells experiments and metabolomics experiments. N.B. assisted with LMO overexpression and metabolomics experiments. S.S. performed SUMO proteomics experiments. A.R. carried out and analyzed data from metabolomics experiments and assisted with experiments under hypoxia. H.G.S performed cellular volume experiments. S.M.H assisted with the expression and purification of SENPs. N.T. assisted with the construction of plasmids. J.S. assisted with design of mitosis and proliferation experiments. H.S. carried out SENP1 expression and purification. K.S., A.Z.X. and L.S. assisted with SENP1 expression and purification. J.Z. oversaw timelapse microscopy. S.D.P. oversaw SENP1 expression and purification. J.C. performed molecular modeling. H.A. oversaw NMR experiments. S.P.G. oversaw mass spectrometry experiments. E.T.C. directed research, oversaw the experiments, and wrote the manuscript with assistance from the other authors. These authors contributed equally |
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| Snippet | Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation
1
–
6
. However, it is not... Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation . However, it is not known... Lactate is abundant in rapidly dividing cells owing to the requirement for elevated glucose catabolism to support proliferation1-6. However, it is not known... Lactate is abundant in rapidly dividing cells due to the requirement for elevated glucose catabolism to support proliferation 1 – 6 . However, it is not known... |
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| SubjectTerms | 631/80/304 631/80/86 82 82/58 Accumulation Anaphase Anaphase-promoting complex Anaphase-Promoting Complex-Cyclosome - metabolism Catabolism Cell Cycle Cell Cycle Proteins - metabolism Cell division Humanities and Social Sciences Humans Lactic acid Lactic Acid - metabolism Mass spectrometry Metabolism Mitosis multidisciplinary Pharmacology Proteins Proteomes Science Science (multidisciplinary) Scientific imaging SUMO protein |
| Title | Lactate regulates cell cycle by remodelling the anaphase promoting complex |
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