All-trans retinoic acid (ATRA)-induced TFEB expression is required for myeloid differentiation in acute promyelocytic leukemia (APL).
Antineoplastic Agents
/ pharmacology
Autophagy
/ genetics
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
/ genetics
Biopsy
Bone Marrow
/ pathology
Cell Differentiation
/ drug effects
Cell Line, Tumor
Gene Expression Regulation, Leukemic
/ drug effects
Gene Knockdown Techniques
Humans
Leukemia, Promyelocytic, Acute
/ drug therapy
Oncogene Proteins, Fusion
/ genetics
RNA Interference
RNA, Small Interfering
/ genetics
Signal Transduction
/ drug effects
Tretinoin
/ pharmacology
acute myeloid leukemia
autophagy
differentiation
hematopoiesis
retinoid
transcription factor EB
Journal
European journal of haematology
ISSN: 1600-0609
Titre abrégé: Eur J Haematol
Pays: England
ID NLM: 8703985
Informations de publication
Date de publication:
Mar 2020
Mar 2020
Historique:
received:
28
08
2017
revised:
14
02
2019
accepted:
18
02
2019
pubmed:
8
12
2019
medline:
8
10
2020
entrez:
8
12
2019
Statut:
ppublish
Résumé
In acute promyelocytic leukemia (APL), normal retinoid signaling is disrupted by an abnormal PML-RARα fusion oncoprotein, leading to a block in cell differentiation. Therapeutic concentrations of all-trans-retinoic acid (ATRA) can restore retinoid-induced transcription and promote degradation of the PML-RARα protein. Autophagy is a catabolic pathway that utilizes lysosomal machinery to degrade intracellular material and facilitate cellular re-modeling. Recent studies have identified autophagy as an integral component of ATRA-induced myeloid differentiation. As the molecular communication between retinoid signaling and the autophagy pathway is not defined, we performed RNA sequencing of NB4 APL cells treated with ATRA and examined autophagy-related transcripts. ATRA altered the expression of >80 known autophagy-related transcripts, including the key transcriptional regulator of autophagy and lysosomal biogenesis, TFEB (11.5-fold increase). Induction of TFEB and its transcriptional target, sequestosome 1 (SQSTM1, p62), is reduced in ATRA-resistant NB4R cells compared to NB4 cells. TFEB knockdown in NB4 cells alters the expression of transcriptional targets of TFEB and reduces CD11b transcript levels in response to ATRA. We show for the first time that TFEB plays an important role in ATRA-induced autophagy during myeloid differentiation and that autophagy induction potentiates leukemic cell differentiation (Note: this study includes data obtained from NCT00195156, https://clinicaltrials.gov/show/NCT00195156).
Substances chimiques
Antineoplastic Agents
0
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
0
Oncogene Proteins, Fusion
0
RNA, Small Interfering
0
TFEB protein, human
0
promyelocytic leukemia-retinoic acid receptor alpha fusion oncoprotein
0
Tretinoin
5688UTC01R
Banques de données
ClinicalTrials.gov
['NCT00195156']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
236-250Subventions
Organisme : Breakthrough Cancer Research (BCR)
Organisme : Haematology Education and Research Trust (H.E.R.O)
Organisme : NCI NIH HHS
ID : R01CA043796
Pays : United States
Organisme : NCI NIH HHS
ID : R01CA043796
Pays : United States
Informations de copyright
© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Tang XH, Gudas LJ. Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol. 2011;6:345-364.
Urvalek A, Laursen KB, Gudas LJ. The roles of retinoic acid and retinoic acid receptors in inducing epigenetic changes. Subcell Biochem. 2014;70:129-149.
Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood. 2008;111(5):2505-2515.
Orfali N, McKenna SL, Cahill MR, Gudas LJ, Mongan NP. Retinoid receptor signaling and autophagy in acute promyelocytic leukemia. Exp Cell Res. 2014;324(1):1-12.
Grignani F, De Matteis S, Nervi C, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature. 1998;391(6669):815-818.
Collins SJ. Retinoic acid receptors, hematopoiesis and leukemogenesis. Curr Opin Hematol. 2008;15(4):346-351.
Martens JH, Brinkman AB, Simmer F, et al. PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell. 2010;17(2):173-185.
Coombs CC, Tavakkoli M, Tallman MS. Acute promyelocytic leukemia: where did we start, where are we now, and the future. Blood Cancer J. 2015;5:e304.
Ablain J, Leiva M, Peres L, Fonsart J, Anthony E, de The H. Uncoupling RARA transcriptional activation and degradation clarifies the bases for APL response to therapies. J Exp Med. 2013;210(4):647-653.
Trocoli A, Mathieu J, Priault M, et al. ATRA-induced upregulation of Beclin 1 prolongs the life span of differentiated acute promyelocytic leukemia cells. Autophagy. 2011;7(10):1108-1114.
Orfali N, O'Donovan TR, Nyhan MJ, et al. Induction of autophagy is a key component of all-trans-retinoic acid-induced differentiation in leukemia cells and a potential target for pharmacologic modulation. Exp Hematol. 2015;43(9):781-793.e2.
Wang Z, Cao L, Kang R, et al. Autophagy regulates myeloid cell differentiation by p62/SQSTM1-mediated degradation of PML-RARalpha oncoprotein. Autophagy. 2011;7(4):401-411.
Isakson P, Bjoras M, Boe SO, Simonsen A. Autophagy contributes to therapy-induced degradation of the PML/RARA oncoprotein. Blood. 2010;116(13):2324-2331.
Fullgrabe J, Klionsky DJ, Joseph B. The return of the nucleus: transcriptional and epigenetic control of autophagy. Nat Rev Mol Cell Biol. 2014;15(1):65-74.
Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med. 2013;368(19):1845-1846.
Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10(7):458-467.
Birgisdottir AB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci. 2013;126(Pt 15):3237-3247.
Feng Y, He D, Yao Z, Klionsky DJ. The machinery of macroautophagy. Cell Res. 2014;24(1):24-41.
Rubinsztein DC, Marino G, Kroemer G. Autophagy and aging. Cell. 2011;146(5):682-695.
Cuervo AM. Cell biology. Autophagy's top chef. Science. 2011;332(6036):1392-1393.
Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429-1433.
Roczniak-Ferguson A, Petit CS, Froehlich F, et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal. 2012;5(228):ra42.
Humbert M, Mueller C, Fey MF, Tschan MP. Inhibition of damage-regulated autophagy modulator-1 (DRAM-1) impairs neutrophil differentiation of NB4 APL cells. Leuk Res. 2012;36(12):1552-1556.
Faria TN, Rivi R, Derguini F, Pandolfi PP, Gudas LJ. 4-Oxoretinol, a metabolite of retinol in the human promyelocytic leukemia cell line NB4, induces cell growth arrest and granulocytic differentiation. Cancer Res. 1998;58(9):2007-2013.
Nason-Burchenal K, Gandini D, Botto M, et al. Interferon augments PML and PML/RAR alpha expression in normal myeloid and acute promyelocytic cells and cooperates with all-trans retinoic acid to induce maturation of a retinoid-resistant promyelocytic cell line. Blood. 1996;88(10):3926-3936.
David KA, Mongan NP, Smith C, Gudas LJ, Nanus DM. Phase I trial of ATRA-IV and Depakote in patients with advanced solid tumor malignancies. Cancer Biol Ther. 2010;9(9):678-684.
Kashyap V, Ahmad S, Nilsson EM, et al. The lysine specific demethylase-1 (LSD1/KDM1A) regulates VEGF-A expression in prostate cancer. Mol Oncol. 2013;7(3):555-566
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562-578.
Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis toolkit (webgestalt): update 2013. Nucleic Acids Res. 2013;41(Web Server issue):W77-W83.
Sotoca AM, Prange KH, Reijnders B, et al. The oncofusion protein FUS-ERG targets key hematopoietic regulators and modulates the all-trans retinoic acid signaling pathway in t(16;21) acute myeloid leukemia. Oncogene. 2016;35(15):1965-1976.
Rosenbauer F, Tenen DG. Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol. 2007;7(2):105-117.
Collin M, Dickinson R, Bigley V. Haematopoietic and immune defects associated with GATA2 mutation. Br J Haematol. 2015;169(2):173-187.
Hoffman B, Amanullah A, Shafarenko M, Liebermann DA. The proto-oncogene c-myc in hematopoietic development and leukemogenesis. Oncogene. 2002;21(21):3414-3421.
Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer. 2003;3(2):89-101.
Settembre C, Ballabio A. TFEB regulates autophagy: an integrated coordination of cellular degradation and recycling processes. Autophagy. 2011;7(11):1379-1381.
Lippai M, Low P. The role of the selective adaptor p62 and ubiquitin-like proteins in autophagy. Biomed Res Int. 2014;2014: 1-11.
Boorjian SA, Milowsky MI, Kaplan J, et al. Phase 1/2 clinical trial of interferon alpha2b and weekly liposome-encapsulated all-trans retinoic acid in patients with advanced renal cell carcinoma. J Immunother. 2007;30(6):655-662.
Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473-477.
Ong CH, He Z, Kriazhev L, Shan X, Palfree RG, Bateman A. Regulation of progranulin expression in myeloid cells. Am J Physiol Regul Integr Comp Physiol. 2006;291(6):R1602-R1612.
Zanocco-Marani T, Vignudelli T, Gemelli C, et al. Tfe3 expression is closely associated to macrophage terminal differentiation of human hematopoietic myeloid precursors. Exp Cell Res. 2006;312(20):4079-4089.
Cao Y, Zhang S, Yuan N, et al. Hierarchal autophagic divergence of hematopoietic system. The Journal of biological chemistry. 2015;290(38):23050-23063.
Haimovici A, Brigger D, Torbett BE, Fey MF, Tschan MP. Induction of the autophagy-associated gene MAP1S via PU.1 supports APL differentiation. Leuk Res. 2014;38(9):1041-1047.
Mueller BU, Pabst T, Fos J, et al. ATRA resolves the differentiation block in t(15;17) acute myeloid leukemia by restoring PU.1 expression. Blood. 2006;107(8):3330-3338.
Rajawat Y, Hilioti Z, Bossis I. Retinoic acid induces autophagosome maturation through redistribution of the cation-independent mannose-6-phosphate receptor. Antioxid Redox Signal. 2011;14(11):2165-2177.
Seok S, Fu T, Choi SE, et al. Transcriptional regulation of autophagy by an FXR-CREB axis. Nature. 2014;516(7529):108-111.
Zhang X, Odom DT, Koo SH, et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA. 2005;102(12):4459-4464.
Saeki K, Saeki K, Yuo A. Distinct involvement of cAMP-response element-dependent transcriptions in functional and morphological maturation during retinoid-mediated human myeloid differentiation. J Leukoc Biol. 2003;73(5):673-681.
Martina JA, Chen Y, Gucek M, Puertollano R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 2012;8(6):903-914.
Wang J, Fang Y, Yan L, et al. Erythroleukemia cells acquire an alternative mitophagy capability. Sci Rep. 2016;6:24641.