Germinal epimutation of Fragile Histidine Triad (FHIT) gene is associated with progression to acute and chronic adult T-cell leukemia diseases.


Journal

Molecular cancer
ISSN: 1476-4598
Titre abrégé: Mol Cancer
Pays: England
ID NLM: 101147698

Informations de publication

Date de publication:
06 06 2021
Historique:
received: 16 03 2021
accepted: 12 05 2021
entrez: 7 6 2021
pubmed: 8 6 2021
medline: 12 1 2022
Statut: epublish

Résumé

Human T cell Leukemia virus type 1 (HTLV-I) is etiologically linked to adult T cell leukemia/lymphoma (ATL) and an inflammatory neurodegenerative disease called HTLV-I-associated myelopathy or tropical spastic paraparesis (HAM/TSP). The exact genetic or epigenetic events and/or environmental factors that influence the development of ATL, or HAM/TSP diseases are largely unknown. The tumor suppressor gene, Fragile Histidine Triad Diadenosine Triphosphatase (FHIT), is frequently lost in cancer through epigenetic modifications and/or deletion. FHIT is a tumor suppressor acting as genome caretaker by regulating cellular DNA repair. Indeed, FHIT loss leads to replicative stress and accumulation of double DNA strand breaks. Therefore, loss of FHIT expression plays a key role in cellular transformation. Here, we studied over 400 samples from HTLV-I-infected individuals with ATL, TSP/HAM, or asymptomatic carriers (AC) for FHIT loss and expression. We examined the epigenetic status of FHIT through methylation specific PCR and bisulfite sequencing; and correlated these results to FHIT expression in patient samples. We found that epigenetic alteration of FHIT is specifically found in chronic and acute ATL but is absent in asymptomatic HTLV-I carriers and TSP/HAM patients' samples. Furthermore, the extent of FHIT methylation in ATL patients was quantitatively comparable in virus-infected and virus non-infected cells. We also found that longitudinal HTLV-I carriers that progressed to smoldering ATL and descendants of ATL patients harbor FHIT methylation. These results suggest that germinal epigenetic mutation of FHIT represents a preexisting mark predisposing to the development of ATL diseases. These findings have important clinical implications as patients with acute ATL are rarely cured. Our study suggests an alternative strategy to the current "wait and see approach" in that early screening of HTLV-I-infected individuals for germinal epimutation of FHIT and early treatment may offer significant clinical benefits.

Sections du résumé

BACKGROUND
Human T cell Leukemia virus type 1 (HTLV-I) is etiologically linked to adult T cell leukemia/lymphoma (ATL) and an inflammatory neurodegenerative disease called HTLV-I-associated myelopathy or tropical spastic paraparesis (HAM/TSP). The exact genetic or epigenetic events and/or environmental factors that influence the development of ATL, or HAM/TSP diseases are largely unknown. The tumor suppressor gene, Fragile Histidine Triad Diadenosine Triphosphatase (FHIT), is frequently lost in cancer through epigenetic modifications and/or deletion. FHIT is a tumor suppressor acting as genome caretaker by regulating cellular DNA repair. Indeed, FHIT loss leads to replicative stress and accumulation of double DNA strand breaks. Therefore, loss of FHIT expression plays a key role in cellular transformation.
METHODS
Here, we studied over 400 samples from HTLV-I-infected individuals with ATL, TSP/HAM, or asymptomatic carriers (AC) for FHIT loss and expression. We examined the epigenetic status of FHIT through methylation specific PCR and bisulfite sequencing; and correlated these results to FHIT expression in patient samples.
RESULTS
We found that epigenetic alteration of FHIT is specifically found in chronic and acute ATL but is absent in asymptomatic HTLV-I carriers and TSP/HAM patients' samples. Furthermore, the extent of FHIT methylation in ATL patients was quantitatively comparable in virus-infected and virus non-infected cells. We also found that longitudinal HTLV-I carriers that progressed to smoldering ATL and descendants of ATL patients harbor FHIT methylation.
CONCLUSIONS
These results suggest that germinal epigenetic mutation of FHIT represents a preexisting mark predisposing to the development of ATL diseases. These findings have important clinical implications as patients with acute ATL are rarely cured. Our study suggests an alternative strategy to the current "wait and see approach" in that early screening of HTLV-I-infected individuals for germinal epimutation of FHIT and early treatment may offer significant clinical benefits.

Identifiants

pubmed: 34092254
doi: 10.1186/s12943-021-01370-2
pii: 10.1186/s12943-021-01370-2
pmc: PMC8183032
doi:

Substances chimiques

Neoplasm Proteins 0
fragile histidine triad protein 0
Acid Anhydride Hydrolases EC 3.6.-

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

86

Subventions

Organisme : NCI NIH HHS
ID : P01 CA100730
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA201309
Pays : United States

Références

J Virol. 2010 Jul;84(14):6966-77
pubmed: 20444901
Lancet Oncol. 2014 Oct;15(11):e517-26
pubmed: 25281470
Ann Clin Lab Sci. 2010 Summer;40(3):267-72
pubmed: 20689140
Genome Biol. 2017 Mar 10;18(1):50
pubmed: 28283040
PLoS Genet. 2012;8(11):e1003077
pubmed: 23209436
Blood. 2006 Aug 1;108(3):1021-9
pubmed: 16569765
Proc Natl Acad Sci U S A. 2018 Feb 6;115(6):E1269-E1278
pubmed: 29358408
Am J Pathol. 2010 Jan;176(1):402-15
pubmed: 20019193
Blood. 2017 Mar 2;129(9):1071-1081
pubmed: 28115366
Blood. 2016 May 19;127(20):2439-50
pubmed: 26813676
Blood. 2010 Aug 26;116(8):1211-9
pubmed: 20448111
Proc Natl Acad Sci U S A. 2020 May 26;117(21):11685-11691
pubmed: 32393644
Oncotarget. 2017 Nov 6;8(60):102199-102211
pubmed: 29254236
Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20344-9
pubmed: 18077326
Nat Commun. 2019 Mar 27;10(1):1383
pubmed: 30918249
Blood Adv. 2017 Jun 27;1(15):1195-1205
pubmed: 29296760
J Clin Oncol. 2010 Sep 20;28(27):4177-83
pubmed: 20585095
Leukemia. 2006 Feb;20(2):264-71
pubmed: 16357833
Blood. 2018 Oct 4;132(14):1507-1518
pubmed: 30104217
Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3615-20
pubmed: 11891319
Blood. 2015 Jun 4;125(23):3527-35
pubmed: 25847015
Oncol Lett. 2012 Jan;3(1):190-192
pubmed: 22740879
Exp Cell Res. 2006 Aug 1;312(13):2433-42
pubmed: 16733051
Leukemia. 2005 Aug;19(8):1367-75
pubmed: 15902282
Blood. 2010 Jun 3;115(22):4337-43
pubmed: 20348391
PLoS One. 2012;7(8):e42226
pubmed: 22916124
Eur J Cancer. 2002 Mar;38(5):728-35
pubmed: 11916557
Nat Genet. 2017 Jan;49(1):131-138
pubmed: 27918535
Nat Rev Cancer. 2001 Dec;1(3):214-21
pubmed: 11902576
Cytogenet Genome Res. 2016;150(3-4):208-216
pubmed: 28199992
Oncogene. 2015 Apr 16;34(16):2072-82
pubmed: 24909176
Leukemia. 2021 Mar;35(3):764-776
pubmed: 32555298
Lancet. 1985 Aug 24;2(8452):407-10
pubmed: 2863442
Cancer Sci. 2008 Jan;99(1):98-106
pubmed: 17970785
Blood. 2020 Jun 4;135(23):2023-2032
pubmed: 32160278
Annu Rev Genet. 1998;32:7-31
pubmed: 9928473
Blood. 2020 Aug 13;136(7):871-884
pubmed: 32391874
Genes Chromosomes Cancer. 2019 May;58(5):317-323
pubmed: 30242938
Oncogene. 2004 Dec 2;23(56):9102-10
pubmed: 15489891
Mol Cancer. 2014 Sep 04;13:205
pubmed: 25185513
J Clin Oncol. 2019 Mar 10;37(8):677-687
pubmed: 30657736
Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415-9
pubmed: 6261256
Front Microbiol. 2016 Oct 28;7:1674
pubmed: 27840624
Carcinogenesis. 2004 Nov;25(11):2165-71
pubmed: 15231689
Blood. 2006 Mar 15;107(6):2493-500
pubmed: 16304050
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3845-50
pubmed: 9520455
Blood. 2015 Dec 10;126(24):2570-7
pubmed: 26361794
Genome Biol. 2014 May 29;15(5):R73
pubmed: 24887635
Virology. 1985 Oct 30;146(2):272-81
pubmed: 2413616
Cancer Biother Radiopharm. 2011 Jun;26(3):365-72
pubmed: 21711110
J Clin Oncol. 2009 Jan 20;27(3):453-9
pubmed: 19064971
Front Microbiol. 2019 May 08;10:999
pubmed: 31134031
J Oncol. 2015;2015:183590
pubmed: 26170835
Blood Adv. 2020 Mar 24;4(6):1062-1071
pubmed: 32196559
Nat Genet. 2015 Nov;47(11):1304-15
pubmed: 26437031
Eur J Haematol. 2005 Dec;75(6):505-10
pubmed: 16313263
Cancer Res. 2004 Mar 15;64(6):2000-6
pubmed: 15026336
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10250-5
pubmed: 11517343
ScientificWorldJournal. 2010 Jun 16;10:1142-51
pubmed: 20563537
Oncogene. 2006 May 11;25(20):2860-72
pubmed: 16407838
Future Oncol. 2008 Dec;4(6):815-24
pubmed: 19086848
Mol Ther. 2020 Apr 8;28(4):1105-1118
pubmed: 32059763

Auteurs

Marcia Bellon (M)

Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, KS, 66160, USA.

Izabela Bialuk (I)

Animal Models and Retroviral Vaccines Section, Vaccine Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Veronica Galli (V)

Animal Models and Retroviral Vaccines Section, Vaccine Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Xue-Tao Bai (XT)

Comprehensive Cancer Center, Department of Health Sciences, Ohio State University, Columbus, OH, USA.

Lourdes Farre (L)

Program in Molecular Mechanisms and Experimental Therapy in Oncology, IDIBELL, Hospitalet de Llobregat, Barcelona, Spain.

Achilea Bittencourt (A)

Department of Pathology, Prof. Edgard Santos Teaching Hospital, Federal University of Bahia, Salvador, Bahia, Brazil.

Ambroise Marçais (A)

Institut Necker-Enfants Malades, Institut National de la Santé et de la Recherche Médicale U1151, Laboratoire Onco-Hématologie, Paris, France.

Michael N Petrus (MN)

Lymphoid Malignancies Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Lee Ratner (L)

Division of Oncology, Department of Medicine, Washington University, St Louis, MO, USA.

Thomas A Waldmann (TA)

Lymphoid Malignancies Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Vahid Asnafi (V)

Université de Paris (Descartes), Institut Necker-Enfants Malades, Institut National de la Santé et de la Recherche Médicale (INSERM) U1151 Laboratoire Onco-Hematology, Paris, France.

Antoine Gessain (A)

Unité d'épidémiologie et de Physiopathologie des virus Oncogene, Institut Pasteur, 75015, Paris, France.
Centre National de la Recherche Scientifique (CNRS) UMR 3569, 75015, Paris, France.

Masao Matsuoka (M)

Laboratory of Virus Control, Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan.
Department of Hematology, Rheumatology, and Infectious Disease, Graduate School of Medical Sciences, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan.

Genoveffa Franchini (G)

Animal Models and Retroviral Vaccines Section, Vaccine Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Olivier Hermine (O)

Institut Necker-Enfants Malades, Institut National de la Santé et de la Recherche Médicale U1151, Laboratoire Onco-Hématologie, Paris, France.

Toshiki Watanabe (T)

Department of Hematology/Oncology, IMSUT Hospital, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Christophe Nicot (C)

Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, KS, 66160, USA. cnicot@kumc.edu.

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