TMEM127 suppresses tumor development by promoting RET ubiquitination, positioning, and degradation
The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements...
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| Published in | Cell reports (Cambridge) Vol. 42; no. 9; p. 113070 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
26.09.2023
Elsevier |
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| Online Access | Get full text |
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| Abstract | The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET. Additionally, TMEM127-mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo. Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma.
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•TMEM127 loss of function leads to increased RET surface expression and activation•TMEM127 recruits the NEDD4 E3 ligase to RET and promotes its ubiquitination•NEDD4-mediated RET ubiquitination involves the TMEM127 C terminus•Oncogenesis due to TMEM127 deficiency is responsive to RET inhibition
Guo et al. report that TMEM127 deficiency leads to pheochromocytoma by reducing NEDD4-mediated RET ubiquitination, positioning, and degradation and that the resulting cell proliferation is responsive to RET selective inhibition. |
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| AbstractList | The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET. Additionally, TMEM127-mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo. Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma. The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127 -mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET . Additionally, TMEM127 -mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo . Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma. Guo et al. report that TMEM127 deficiency leads to pheochromocytoma by reducing NEDD4-mediated RET ubiquitination, positioning, and degradation and that the resulting cell proliferation is responsive to RET selective inhibition. The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET. Additionally, TMEM127-mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo. Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma. [Display omitted] •TMEM127 loss of function leads to increased RET surface expression and activation•TMEM127 recruits the NEDD4 E3 ligase to RET and promotes its ubiquitination•NEDD4-mediated RET ubiquitination involves the TMEM127 C terminus•Oncogenesis due to TMEM127 deficiency is responsive to RET inhibition Guo et al. report that TMEM127 deficiency leads to pheochromocytoma by reducing NEDD4-mediated RET ubiquitination, positioning, and degradation and that the resulting cell proliferation is responsive to RET selective inhibition. The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET. Additionally, TMEM127-mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo. Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma.The TMEM127 gene encodes a transmembrane protein of poorly known function that is mutated in pheochromocytomas, neural crest-derived tumors of adrenomedullary cells. Here, we report that, at single-nucleus resolution, TMEM127-mutant tumors share precursor cells and transcription regulatory elements with pheochromocytomas carrying mutations of the tyrosine kinase receptor RET. Additionally, TMEM127-mutant pheochromocytomas, human cells, and mouse knockout models of TMEM127 accumulate RET and increase its signaling. TMEM127 contributes to RET cellular positioning, trafficking, and lysosome-mediated degradation. Mechanistically, TMEM127 binds to RET and recruits the NEDD4 E3 ubiquitin ligase for RET ubiquitination and degradation via TMEM127 C-terminal PxxY motifs. Lastly, increased cell proliferation and tumor burden after TMEM127 loss can be reversed by selective RET inhibitors in vitro and in vivo. Our results define TMEM127 as a component of the ubiquitin system and identify aberrant RET stabilization as a likely mechanism through which TMEM127 loss-of-function mutations cause pheochromocytoma. |
| ArticleNumber | 113070 |
| Author | Lopez, Hector Gonzalez-Cantú, Hector Huelgas-Morales, Gabriela Qiu, Zhijun Song, Wan Wang, Exing Li, Faqian Walker, Timothy J. Rotondi, Matthew Dahia, Patricia L.M. Guo, Qianjin Lefkowitz, Jonathan Khan, Mohammad Aasif Ding, Yanli Cheng, Zi-Ming Goyal, Shivi Estrada-Zuniga, Cynthia M. Mulligan, Lois M. Ethiraj, Purushoth Landry, Bethany N. Aguiar, Ricardo C.T. |
| AuthorAffiliation | 5 Mays Cancer Center, UTHSCSA, San Antonio, TX, USA 2 Division of Cancer Biology and Genetics, Cancer Research Institute, Queen’s University, Kingston, ON, Canada 6 South Texas Veterans Health Care System, Audie Murphy VA Hospital, San Antonio, TX 78229, USA 1 Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA 3 Department Cell Structure and Anatomy, UTHSCSA, San Antonio, TX, USA 4 Department of Pathology, UTHSCSA, San Antonio, TX, USA 7 Lead contact |
| AuthorAffiliation_xml | – name: 7 Lead contact – name: 5 Mays Cancer Center, UTHSCSA, San Antonio, TX, USA – name: 3 Department Cell Structure and Anatomy, UTHSCSA, San Antonio, TX, USA – name: 2 Division of Cancer Biology and Genetics, Cancer Research Institute, Queen’s University, Kingston, ON, Canada – name: 4 Department of Pathology, UTHSCSA, San Antonio, TX, USA – name: 1 Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – name: 6 South Texas Veterans Health Care System, Audie Murphy VA Hospital, San Antonio, TX 78229, USA |
| Author_xml | – sequence: 1 givenname: Qianjin surname: Guo fullname: Guo, Qianjin organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 2 givenname: Zi-Ming surname: Cheng fullname: Cheng, Zi-Ming organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 3 givenname: Hector surname: Gonzalez-Cantú fullname: Gonzalez-Cantú, Hector organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 4 givenname: Matthew surname: Rotondi fullname: Rotondi, Matthew organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 5 givenname: Gabriela surname: Huelgas-Morales fullname: Huelgas-Morales, Gabriela organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 6 givenname: Purushoth surname: Ethiraj fullname: Ethiraj, Purushoth organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 7 givenname: Zhijun surname: Qiu fullname: Qiu, Zhijun organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 8 givenname: Jonathan surname: Lefkowitz fullname: Lefkowitz, Jonathan organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 9 givenname: Wan surname: Song fullname: Song, Wan organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 10 givenname: Bethany N. surname: Landry fullname: Landry, Bethany N. organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 11 givenname: Hector surname: Lopez fullname: Lopez, Hector organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 12 givenname: Cynthia M. surname: Estrada-Zuniga fullname: Estrada-Zuniga, Cynthia M. organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 13 givenname: Shivi surname: Goyal fullname: Goyal, Shivi organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 14 givenname: Mohammad Aasif surname: Khan fullname: Khan, Mohammad Aasif organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 15 givenname: Timothy J. surname: Walker fullname: Walker, Timothy J. organization: Division of Cancer Biology and Genetics, Cancer Research Institute, Queen’s University, Kingston, ON, Canada – sequence: 16 givenname: Exing surname: Wang fullname: Wang, Exing organization: Department Cell Structure and Anatomy, UTHSCSA, San Antonio, TX, USA – sequence: 17 givenname: Faqian surname: Li fullname: Li, Faqian organization: Department of Pathology, UTHSCSA, San Antonio, TX, USA – sequence: 18 givenname: Yanli surname: Ding fullname: Ding, Yanli organization: Department of Pathology, UTHSCSA, San Antonio, TX, USA – sequence: 19 givenname: Lois M. surname: Mulligan fullname: Mulligan, Lois M. organization: Division of Cancer Biology and Genetics, Cancer Research Institute, Queen’s University, Kingston, ON, Canada – sequence: 20 givenname: Ricardo C.T. surname: Aguiar fullname: Aguiar, Ricardo C.T. organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA – sequence: 21 givenname: Patricia L.M. orcidid: 0000-0002-7757-370X surname: Dahia fullname: Dahia, Patricia L.M. email: dahia@uthscsa.edu organization: Division of Hematology/Medical Oncology, Department of Medicine, University of Texas Health San Science Center at Antonio (UTHSCSA), San Antonio, TX, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37659079$$D View this record in MEDLINE/PubMed |
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| Keywords | RET TMEM127 NEDD4 positioning CP: Cancer pheochromocytoma degradation single-nucleus sequencing oncogene tumor suppressor gene ubiquitin paraganglioma |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, Q.G., P.L.M.D., and R.C.T.A.; snRNA-seq and bioinformatics, Q.G.; molecular studies, Q.G., Z.-M.C., M.R., H.G.C, M.A.K., W.S., B.N.L., C.E.Z., H.K., M.A.K., S.G., P.E., and Z.Q.; mouse models, Q.G., P.E., and Z.Q.; confocal microscopy, Q.G., G.H.-M., W.S., and E.W.; pathology, Y.D. and F.L.; resources, Q.G., H.C.G., H.L., S.G., R.C.T.A., T.J.W., L.M.M., and P.L.M.D.; writing, Q.G., R.C.T.A., and P.L.M.; supervision, P.L.M.D.; funding acquisition, R.C.T.A. and P.L.M.D. |
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| SubjectTerms | Adrenal Gland Neoplasms - genetics Adrenal Gland Neoplasms - metabolism Adrenal Gland Neoplasms - pathology Animals CP: Cancer degradation Germ-Line Mutation Humans Membrane Proteins - genetics Membrane Proteins - metabolism Mice Mutation - genetics NEDD4 oncogene paraganglioma pheochromocytoma Pheochromocytoma - genetics Pheochromocytoma - metabolism Pheochromocytoma - pathology positioning Proto-Oncogene Proteins c-ret - genetics Proto-Oncogene Proteins c-ret - metabolism RET single-nucleus sequencing TMEM127 tumor suppressor gene ubiquitin Ubiquitination |
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| Title | TMEM127 suppresses tumor development by promoting RET ubiquitination, positioning, and degradation |
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