SLFN5 Regulates LAT1-Mediated mTOR Activation in Castration-Resistant Prostate Cancer.

Activating Transcription Factor 4 / genetics Animals Apoptosis Biomarkers, Tumor / genetics Cell Cycle Proteins / genetics Cell Proliferation Gene Expression Regulation, Neoplastic Humans Large Neutral Amino Acid-Transporter 1 / genetics Male Mechanistic Target of Rapamycin Complex 1 / genetics Metabolome Mice Mice, Nude Prognosis Prostatic Neoplasms, Castration-Resistant / genetics Proteome Survival Rate TOR Serine-Threonine Kinases / genetics Transcriptome Tumor Cells, Cultured Xenograft Model Antitumor Assays

Journal

Cancer research

ISSN: 1538-7445

Titre abrégé: Cancer Res

Pays: United States

ID NLM: 2984705R

Informations de publication

Date de publication:
01 07 2021

Historique:

received: 03 11 2020

revised: 15 03 2021

accepted: 11 05 2021

pubmed: 15 5 2021

medline: 15 12 2021

entrez: 14 5 2021

Statut: ppublish

Résumé

Androgen deprivation therapy (ADT) is the standard of care for treatment of nonresectable prostate cancer. Despite high treatment efficiency, most patients ultimately develop lethal castration-resistant prostate cancer (CRPC). In this study, we performed a comparative proteomic analysis of three

Identifiants

DOI: 10.1158/0008-5472.CAN-20-3694 PMID: 33985973

pubmed: 33985973

pii: 0008-5472.CAN-20-3694

doi: 10.1158/0008-5472.CAN-20-3694

doi:

Substances chimiques

ATF4 protein, human 0

Biomarkers, Tumor 0

Cell Cycle Proteins 0

Large Neutral Amino Acid-Transporter 1 0

Proteome 0

SLC7A5 protein, human 0

SLFN5 protein, human 0

Activating Transcription Factor 4 145891-90-3

MTOR protein, human EC 2.7.1.1

Mechanistic Target of Rapamycin Complex 1 EC 2.7.11.1

TOR Serine-Threonine Kinases EC 2.7.11.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

Pagination

3664-3678

Subventions

Organisme : Cancer Research UK

ID : C596/A17196

Pays : United Kingdom

Organisme : Medical Research Council

ID : MR/L017997/1

Pays : United Kingdom

Informations de copyright

Références

Sanderson SM, Gao X, Dai Z, Locasale JW. Methionine metabolism in health and cancer: a nexus of diet and precision medicine. Nat Rev Cancer. 2019;19:625–37.

Eidelman E, Twum-Ampofo J, Ansari J, Siddiqui MM. The metabolic phenotype of prostate cancer. Front Oncol. 2017;7:131.

Zadra G, Loda M. Metabolic vulnerabilities of prostate cancer: diagnostic and therapeutic opportunities. Cold Spring Harb Perspect Med. 2018;8:a030569.

Wu X, Daniels G, Lee P, Monaco ME. Lipid metabolism in prostate cancer. Am J Clin Exp Urol. 2014;2:111–20.

Massie CE, Lynch A, Ramos-Montoya A, Boren J, Stark R, Fazli L, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011;30:2719–33.

Blomme A, Ford CA, Mui E, Patel R, Ntala C, Jamieson LE, et al. 2,4-dienoyl-CoA reductase regulates lipid homeostasis in treatment-resistant prostate cancer. Nat Commun. 2020;11:2508.

Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell. 2010;18:11–22.

Statz CM, Patterson SE, Mockus SM. mTOR inhibitors in castration-resistant prostate cancer: a systematic review. Target Oncol. 2017;12:47–59.

Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell. 2010;141:290–303.

Prasad PD, Wang H, Huang W, Kekuda R, Rajan DP, Leibach FH, et al. Human LAT1, a subunit of system L amino acid transporter: molecular cloning and transport function. Biochem Biophys Res Commun. 1999;255:283–8.

Salisbury TB, Arthur S. The regulation and function of the L-type amino acid transporter 1 (LAT1) in cancer. Int J Mol Sci. 2018;19:2373.

Xu M, Sakamoto S, Matsushima J, Kimura T, Ueda T, Mizokami A, et al. Up-regulation of LAT1 during antiandrogen therapy contributes to progression in prostate cancer cells. J Urol. 2016;195:1588–97.

Wang Q, Bailey CG, Ng C, Tiffen J, Thoeng A, Minhas V, et al. Androgen receptor and nutrient signaling pathways coordinate the demand for increased amino acid transport during prostate cancer progression. Cancer Res. 2011;71:7525–36.

Mavrommatis E, Fish EN, Platanias LC. The schlafen family of proteins and their regulation by interferons. J Interferon Cytokine Res. 2013;33:206–10.

Katsoulidis E, Mavrommatis E, Woodard J, Shields MA, Sassano A, Carayol N, et al. Role of interferon {alpha} (IFN{alpha})-inducible schlafen-5 in regulation of anchorage-independent growth and invasion of malignant melanoma cells. J Biol Chem. 2010;285:40333–41.

Wan G, Liu Y, Zhu J, Guo L, Li C, Yang Y, et al. SLFN5 suppresses cancer cell migration and invasion by inhibiting MT1-MMP expression via AKT/GSK-3beta/beta-catenin pathway. Cell Signal. 2019;59:1–12.

Sassano A, Mavrommatis E, Arslan AD, Kroczynska B, Beauchamp EM, Khuon S, et al. Human schlafen 5 (SLFN5) is a regulator of motility and invasiveness of renal cell carcinoma cells. Mol Cell Biol. 2015;35:2684–98.

Wan G, Zhu J, Gu X, Yang Y, Liu Y, Wang Z, et al. Human schlafen 5 regulates reversible epithelial and mesenchymal transitions in breast cancer by suppression of ZEB1 transcription. Br J Cancer. 2020;123:633–43.

Arslan AD, Sassano A, Saleiro D, Lisowski P, Kosciuczuk EM, Fischietti M, et al. Human SLFN5 is a transcriptional co-repressor of STAT1-mediated interferon responses and promotes the malignant phenotype in glioblastoma. Oncogene. 2017;36:6006–19.

Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DGNational Centre for the Replacement, Refinement, and Reduction of Animals in Research. Animal research: reporting in vivo experiments–the ARRIVE guidelines. J Cereb Blood Flow Metab. 2011;31:991–3.

Mackay GM, Zheng L, van den Broek NJ, Gottlieb E. Analysis of cell metabolism using LC-MS and isotope tracers. Methods Enzymol. 2015;561:171–96.

Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27:1017–8.

Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47:D442–D50.

Cunningham D, You Z. In vitro and in vivo model systems used in prostate cancer research. J Biol Methods. 2015;2:e17.

Mills IG. Maintaining and reprogramming genomic androgen receptor activity in prostate cancer. Nat Rev Cancer. 2014;14:187–98.

Kounatidou E, Nakjang S, McCracken SRC, Dehm SM, Robson CN, Jones D, et al. A novel CRISPR-engineered prostate cancer cell line defines the AR-V transcriptome and identifies PARP inhibitor sensitivities. Nucleic Acids Res. 2019;47:5634–47.

Abida W, Cyrta J, Heller G, Prandi D, Armenia J, Coleman I, et al. Genomic correlates of clinical outcome in advanced prostate cancer. Proc Natl Acad Sci U S A. 2019;116:11428–36.

Wang Q, Tiffen J, Bailey CG, Lehman ML, Ritchie W, Fazli L, et al. Targeting amino acid transport in metastatic castration-resistant prostate cancer: effects on cell cycle, cell growth, and tumor development. J Natl Cancer Inst. 2013;105:1463–73.

Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang H, Nyfeler B, et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell. 2009;136:521–34.

Joseph JD, Lu N, Qian J, Sensintaffar J, Shao G, Brigham D, et al. A clinically relevant androgen receptor mutation confers resistance to second-generation antiandrogens enzalutamide and ARN-509. Cancer Discov. 2013;3:1020–9.

Korpal M, Korn JM, Gao X, Rakiec DP, Ruddy DA, Doshi S, et al. An F876L mutation in androgen receptor confers genetic and phenotypic resistance to MDV3100 (enzalutamide). Cancer Discov. 2013;3:1030–43.

Bluemn EG, Coleman IM, Lucas JM, Coleman RT, Hernandez-Lopez S, Tharakan R, et al. Androgen receptor pathway-independent prostate cancer is sustained through FGF signaling. Cancer Cell. 2017;32:474–89.

Visakorpi T, Hyytinen E, Koivisto P, Tanner M, Keinanen R, Palmberg C, et al. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet. 1995;9:401–6.

Sharma NL, Massie CE, Ramos-Montoya A, Zecchini V, Scott HE, Lamb AD, et al. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell. 2013;23:35–47.

Arora VK, Schenkein E, Murali R, Subudhi SK, Wongvipat J, Balbas MD, et al. Glucocorticoid receptor confers resistance to antiandrogens by bypassing androgen receptor blockade. Cell. 2013;155:1309–22.

Watson PA, Arora VK, Sawyers CL. Emerging mechanisms of resistance to androgen receptor inhibitors in prostate cancer. Nat Rev Cancer. 2015;15:701–11.

Chang KH, Li R, Kuri B, Lotan Y, Roehrborn CG, Liu J, et al. A gain-of-function mutation in DHT synthesis in castration-resistant prostate cancer. Cell. 2013;154:1074–84.

Shao Y, Ye G, Ren S, Piao HL, Zhao X, Lu X, et al. Metabolomics and transcriptomics profiles reveal the dysregulation of the tricarboxylic acid cycle and related mechanisms in prostate cancer. Int J Cancer. 2018;143:396–407.

Schlaepfer IR, Rider L, Rodrigues LU, Gijon MA, Pac CT, Romero L, et al. Lipid catabolism via CPT1 as a therapeutic target for prostate cancer. Mol Cancer Ther. 2014;13:2361–71.

Flaig TW, Salzmann-Sullivan M, Su LJ, Zhang Z, Joshi M, Gijon MA, et al. Lipid catabolism inhibition sensitizes prostate cancer cells to antiandrogen blockade. Oncotarget. 2017;8:56051–65.

Ahmad I, Mui E, Galbraith L, Patel R, Tan EH, Salji M, et al. Sleeping beauty screen reveals Pparg activation in metastatic prostate cancer. Proc Natl Acad Sci U S A. 2016;113:8290–5.

Collett GP, Betts AM, Johnson MI, Pulimood AB, Cook S, Neal DE, et al. Peroxisome proliferator-activated receptor alpha is an androgen-responsive gene in human prostate and is highly expressed in prostatic adenocarcinoma. Clin Cancer Res. 2000;6:3241–8.

Barfeld SJ, Urbanucci A, Itkonen HM, Fazli L, Hicks JL, Thiede B, et al. c-Myc antagonises the transcriptional activity of the androgen receptor in prostate cancer affecting key gene networks. EBioMedicine. 2017;18:83–93.

Pomerantz MM, Li F, Takeda DY, Lenci R, Chonkar A, Chabot M, et al. The androgen receptor cistrome is extensively reprogrammed in human prostate tumorigenesis. Nat Genet. 2015;47:1346–51.

Pallmann N, Livgard M, Tesikova M, Nenseth HZ, Akkus E, Sikkeland J, et al. Regulation of the unfolded protein response through ATF4 and FAM129A in prostate cancer. Oncogene. 2019;38:6301–18.

Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, et al. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature. 2012;485:55–61.

Han J, Back SH, Hur J, Lin YH, Gildersleeve R, Shan J, et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol. 2013;15:481–90.