Lentiviral vectors escape innate sensing but trigger p53 in human hematopoietic stem and progenitor cells

Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited...

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Published inEMBO molecular medicine Vol. 9; no. 9; pp. 1198 - 1211
Main Authors Piras, Francesco, Riba, Michela, Petrillo, Carolina, Lazarevic, Dejan, Cuccovillo, Ivan, Bartolaccini, Sara, Stupka, Elia, Gentner, Bernhard, Cittaro, Davide, Naldini, Luigi, Kajaste‐Rudnitski, Anna
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.09.2017
John Wiley & Sons, Inc
EMBO Press
John Wiley and Sons Inc
Springer Nature
Subjects
Animals
Apoptosis
Cell cycle
Deoxyribonucleic acid
DNA
EMBO16
EMBO18
Engraftment
Expression vectors
Gene therapy
Genes
Genetic Therapy
Genetic Vectors - genetics
Genetic Vectors - immunology
Genomes
hematopoietic stem and progenitor cells
Hematopoietic Stem Cell Transplantation
Hematopoietic stem cells
Hematopoietic Stem Cells - immunology
Humans
Immune response
Immunity, Innate
innate sensing
Integration
Interferon
lentiviral vectors
Lentivirus - genetics
Lentivirus - immunology
Mice
p53 Protein
p53 signaling
Raltegravir
Research Article
Short term
Signal transduction
Stem cells
Transcription
Transplantation
Tumor proteins
Tumor Suppressor Protein p53 - genetics
Tumor Suppressor Protein p53 - immunology
hematopoietic stem and progenitor cells
gene therapy
p53 signaling
innate sensing
lentiviral vectors
Online AccessGet full text
ISSN1757-4676
1757-4684
1757-4684
DOI10.15252/emmm.201707922

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Abstract Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo . These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies. Synopsis Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells. LV transduction remains remarkably stealth in human HSPC, avoiding innate immune activation but triggering p53 signaling in human HSPC. p53 signaling occurs upon ATM‐dependent nuclear sensing of vector DNA (LV, IDLV, AAV) independently of integration into the host genome. Vector‐mediated activation of p53 leads to cell cycle arrest and apoptosis ex vivo ultimately leading to lower engraftment of short‐term HSPC in vivo . Inhibition of LV‐signaling rescues ex vivo apoptosis and early engraftment of human HSPC. Graphical Abstract Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells.
AbstractList Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo . These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies. Synopsis Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells. LV transduction remains remarkably stealth in human HSPC, avoiding innate immune activation but triggering p53 signaling in human HSPC. p53 signaling occurs upon ATM‐dependent nuclear sensing of vector DNA (LV, IDLV, AAV) independently of integration into the host genome. Vector‐mediated activation of p53 leads to cell cycle arrest and apoptosis ex vivo ultimately leading to lower engraftment of short‐term HSPC in vivo . Inhibition of LV‐signaling rescues ex vivo apoptosis and early engraftment of human HSPC. Graphical Abstract Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells.
Abstract Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo. These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.
Clinical application of lentiviral vector (LV)-based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV-mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma-retroviral vector. However, reverse-transcribed LV DNA did trigger p53 signaling, activated also by non-integrating Adeno-associated vector, ultimately leading to lower cell recovery and engraftment These effects were more pronounced in the short-term repopulating cells while long-term HSC frequencies remained unaffected. Blocking LV-induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.
Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo . These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.
Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo. These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies. Synopsis Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells. LV transduction remains remarkably stealth in human HSPC, avoiding innate immune activation but triggering p53 signaling in human HSPC. p53 signaling occurs upon ATM‐dependent nuclear sensing of vector DNA (LV, IDLV, AAV) independently of integration into the host genome. Vector‐mediated activation of p53 leads to cell cycle arrest and apoptosis ex vivo ultimately leading to lower engraftment of short‐term HSPC in vivo. Inhibition of LV‐signaling rescues ex vivo apoptosis and early engraftment of human HSPC. Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells.
Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo . These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies. image Lentiviral (LV) gene therapy vectors escape innate sensing but trigger p53 signaling in human hematopoietic stem and progenitor cells (HSPC), ultimately leading to lower engraftment of short‐term repopulating cells. LV transduction remains remarkably stealth in human HSPC, avoiding innate immune activation but triggering p53 signaling in human HSPC. p53 signaling occurs upon ATM‐dependent nuclear sensing of vector DNA (LV, IDLV, AAV) independently of integration into the host genome. Vector‐mediated activation of p53 leads to cell cycle arrest and apoptosis ex vivo ultimately leading to lower engraftment of short‐term HSPC in vivo . Inhibition of LV‐signaling rescues ex vivo apoptosis and early engraftment of human HSPC.
Clinical application of lentiviral vector (LV)-based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV-mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma-retroviral vector. However, reverse-transcribed LV DNA did trigger p53 signaling, activated also by non-integrating Adeno-associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo These effects were more pronounced in the short-term repopulating cells while long-term HSC frequencies remained unaffected. Blocking LV-induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.Clinical application of lentiviral vector (LV)-based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV-mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma-retroviral vector. However, reverse-transcribed LV DNA did trigger p53 signaling, activated also by non-integrating Adeno-associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo These effects were more pronounced in the short-term repopulating cells while long-term HSC frequencies remained unaffected. Blocking LV-induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.
Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless, LV‐mediated signaling and its potential functional consequences on HSPC biology remain poorly understood. We unravel here a remarkably limited impact of LV on the HSPC transcriptional landscape. LV escaped innate immune sensing that instead led to robust IFN responses upon transduction with a gamma‐retroviral vector. However, reverse‐transcribed LV DNA did trigger p53 signaling, activated also by non‐integrating Adeno‐associated vector, ultimately leading to lower cell recovery ex vivo and engraftment in vivo. These effects were more pronounced in the short‐term repopulating cells while long‐term HSC frequencies remained unaffected. Blocking LV‐induced signaling partially rescued both apoptosis and engraftment, highlighting a novel strategy to further dampen the impact of ex vivo gene transfer on HSPC. Overall, our results shed light on viral vector sensing in HSPC and provide critical insight for the development of more stealth gene therapy strategies.
Audience Academic
Author Cittaro, Davide
Riba, Michela
Bartolaccini, Sara
Piras, Francesco
Naldini, Luigi
Gentner, Bernhard
Lazarevic, Dejan
Kajaste‐Rudnitski, Anna
Petrillo, Carolina
Stupka, Elia
Cuccovillo, Ivan
AuthorAffiliation 1 San Raffaele Telethon Institute for Gene Therapy IRCCS San Raffaele Scientific Institute Milan Italy
2 Vita‐Salute San Raffaele University Milan Italy
3 Center for Translational Genomics and Bioinformatics IRCCS San Raffaele Scientific Institute Milan Italy
4 Present address: Boehringer Ingelheim Biberach an der Riß Germany
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– name: 3 Center for Translational Genomics and Bioinformatics IRCCS San Raffaele Scientific Institute Milan Italy
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– name: 4 Present address: Boehringer Ingelheim Biberach an der Riß Germany
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  surname: Petrillo
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  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute, Vita‐Salute San Raffaele University
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  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute
– sequence: 6
  givenname: Sara
  surname: Bartolaccini
  fullname: Bartolaccini, Sara
  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute
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  givenname: Elia
  surname: Stupka
  fullname: Stupka, Elia
  organization: Center for Translational Genomics and Bioinformatics, IRCCS San Raffaele Scientific Institute, Boehringer Ingelheim
– sequence: 8
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  surname: Gentner
  fullname: Gentner, Bernhard
  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute
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  givenname: Davide
  surname: Cittaro
  fullname: Cittaro, Davide
  organization: Center for Translational Genomics and Bioinformatics, IRCCS San Raffaele Scientific Institute
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  givenname: Luigi
  surname: Naldini
  fullname: Naldini, Luigi
  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute, Vita‐Salute San Raffaele University
– sequence: 11
  givenname: Anna
  orcidid: 0000-0003-1549-2426
  surname: Kajaste‐Rudnitski
  fullname: Kajaste‐Rudnitski, Anna
  email: kajaste.anna@hsr.it
  organization: San Raffaele Telethon Institute for Gene Therapy, IRCCS San Raffaele Scientific Institute
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28667090$$D View this record in MEDLINE/PubMed
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Issue 9
Keywords hematopoietic stem and progenitor cells
gene therapy
p53 signaling
innate sensing
lentiviral vectors
Language English
License Attribution
2017 The Authors. Published under the terms of the CC BY 4.0 license.
This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless,...
Clinical application of lentiviral vector (LV)-based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality. Nevertheless,...
Abstract Clinical application of lentiviral vector (LV)‐based hematopoietic stem and progenitor cells (HSPC) gene therapy is rapidly becoming a reality....
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StartPage 1198
SubjectTerms Animals
Apoptosis
Cell cycle
Deoxyribonucleic acid
DNA
EMBO16
EMBO18
Engraftment
Expression vectors
Gene therapy
Genes
Genetic Therapy
Genetic Vectors - genetics
Genetic Vectors - immunology
Genomes
hematopoietic stem and progenitor cells
Hematopoietic Stem Cell Transplantation
Hematopoietic stem cells
Hematopoietic Stem Cells - immunology
Humans
Immune response
Immunity, Innate
innate sensing
Integration
Interferon
lentiviral vectors
Lentivirus - genetics
Lentivirus - immunology
Mice
p53 Protein
p53 signaling
Raltegravir
Research Article
Short term
Signal transduction
Stem cells
Transcription
Transplantation
Tumor proteins
Tumor Suppressor Protein p53 - genetics
Tumor Suppressor Protein p53 - immunology
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Title Lentiviral vectors escape innate sensing but trigger p53 in human hematopoietic stem and progenitor cells
URI https://link.springer.com/article/10.15252/emmm.201707922
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Femmm.201707922
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Volume 9
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