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Title: A Versatile Viral System for Expression and Depletion of Proteins in Mammalian Cells

Journal Article · · PLoS ONE
 [1];  [2];  [3];  [2];  [2];  [4];  [3];  [4];  [4];  [2]
  1. University of Massachusetts, Worcester, MA (United States); DOE/OSTI
  2. University of Massachusetts, Worcester, MA (United States)
  3. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Buck Institute for Age Research, Novato, CA (United States)
  4. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
+ Show Author Affiliations

The ability to express or deplete proteins in living cells is crucial for the study of biological processes. Viral vectors are often useful to deliver DNA constructs to cells that are difficult to transfect by other methods. Lentiviruses have the additional advantage of being able to integrate into the genomes of non-dividing mammalian cells. However, existing viral expression systems generally require different vector backbones for expression of cDNA, small hairpin RNA (shRNA) or microRNA (miRNA) and provide limited drug selection markers. Furthermore, viral backbones are often recombinogenic in bacteria, complicating the generation and maintenance of desired clones. Here, we describe a collection of 59 vectors that comprise an integrated system for constitutive or inducible expression of cDNAs, shRNAs or miRNAs, and use a wide variety of drug selection markers. These vectors are based on the Gateway technology (Invitrogen) whereby the cDNA, shRNA or miRNA of interest is cloned into an Entry vector and then recombined into a Destination vector that carries the chosen viral backbone and drug selection marker. This recombination reaction generates the desired product with >95% efficiency and greatly reduces the frequency of unwanted recombination in bacteria. We generated Destination vectors for the production of both retroviruses and lentiviruses. Further, we characterized each vector for its viral titer production as well as its efficiency in expressing or depleting proteins of interest. We also generated multiple types of vectors for the production of fusion proteins and confirmed expression of each. We demonstrated the utility of these vectors in a variety of functional studies. First, we show that the FKBP12 Destabilization Domain system can be used to either express or deplete the protein of interest in mitotically-arrested cells. Also, we generate primary fibroblasts that can be induced to senesce in the presence or absence of DNA damage. Finally, we determined that both isoforms of the AT-Rich Interacting Domain 4B (ARID4B) protein could induce G1 arrest when overexpressed. As new technologies emerge, the vectors in this collection can be easily modified and adapted without the need for extensive recloning.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627380
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 8 Vol. 4; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Efficient lentiviral transduction of different human and mouse cells posted_content January 2018
ESCRT-mediated lysosome repair precedes lysophagy and promotes cell survival posted_content May 2018
HOPS-dependent endosomal fusion required for efficient cytosolic delivery of therapeutic peptides and small proteins posted_content July 2018
Modeling the MYC-driven normal-to-tumour switch in breast cancer posted_content August 2018
Sae2/CtIP prevents R-loop accumulation in eukaryotic cells posted_content August 2018
Role of PML-Nuclear Bodies in Human Herpesvirus 6A and 6B Genome Integration posted_content September 2018
Telomeric dysfunction triggers an unstable growth arrest leading to irreparable genomic lesions and entry into cellular senescence posted_content October 2018
Direct genome editing of patient-derived xenografts using CRISPR-Cas9 enables rapid in vivo functional genomics posted_content March 2019
Promotion of adipogenesis by JMJD6 requires the AT hook-like domain and is independent of its catalytic function posted_content April 2019
HOTAIR promotes an epithelial-to-mesenchymal transition through relocation of the histone demethylase Lsd1 posted_content August 2019
Establishing RPTE-derived cell lines expressing hTERT for studying BK polyomavirus posted_content September 2019
“A memory of RPS25 loss drives resistance phenotypes” posted_content March 2020
Collective MAPK Signaling Dynamics Coordinates Epithelial Homeostasis posted_content October 2019
Mechanism of Activation of Protein Kinase JAK2 by the Growth Hormone Receptor journal May 2014
Use of human embryonic stem cells to model pediatric gliomas with H3.3K27M histone mutation journal November 2014
Gene essentiality and synthetic lethality in haploid human cells journal October 2015
Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps journal October 2016
Transformation by Polyomavirus Middle T Antigen Involves a Unique Bimodal Interaction with the Hippo Effector YAP journal August 2016
Inherited Chromosomally Integrated Human Herpesvirus 6 Demonstrates Tissue-Specific RNA Expression In Vivo That Correlates with an Increased Antibody Immune Response journal December 2019
Key Role of the Scavenger Receptor MARCO in Mediating Adenovirus Infection and Subsequent Innate Responses of Macrophages journal September 2017
Dengue Virus NS Proteins Inhibit RIG-I/MAVS Signaling by Blocking TBK1/IRF3 Phosphorylation: Dengue Virus Serotype 1 NS4A Is a Unique Interferon-Regulating Virulence Determinant journal July 2015
Establishing Renal Proximal Tubule Epithelial-Derived Cell Lines Expressing Human Telomerase Reverse Transcriptase for Studying BK Polyomavirus journal October 2019
STF-62247 accumulates in lysosomes and blocks late stages of autophagy to selectively target von Hippel-Lindau-inactivated cells journal May 2019
Hedgehog and retinoid signaling alters multiple myeloma microenvironment and generates bortezomib resistance journal October 2016
TFEB-driven lysosomal biogenesis is pivotal for PGC1α-dependent renal stress resistance journal August 2020
Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells journal March 2010
EBNA3B-deficient EBV promotes B cell lymphomagenesis in humanized mice and is found in human tumors journal April 2012
A versatile modular vector system for rapid combinatorial mammalian genetics journal March 2015
Dynamin impacts homology-directed repair and breast cancer response to chemotherapy journal October 2018
Necdin modulates proliferative cell survival of human cells in response to radiation-induced genotoxic stress journal June 2012
p16INK4a and its regulator miR-24 link senescence and chondrocyte terminal differentiation-associated matrix remodeling in osteoarthritis journal January 2014
SIRT1 ameliorates oxidative stress induced neural cell death and is down-regulated in Parkinson’s disease journal June 2017
A novel somatic mutation in ACD induces telomere lengthening and apoptosis resistance in leukemia cells journal September 2015
TrkA is amplified in malignant melanoma patients and induces an anti-proliferative response in cell lines journal October 2015
Role of peptidylarginine deiminase 2 (PAD2) in mammary carcinoma cell migration journal May 2017
Establishment of an erythroid progenitor cell line capable of enucleation achieved with an inducible c-Myc vector journal April 2019
Efficient CRISPR/Cas9 genome editing in a salmonid fish cell line using a lentivirus delivery system journal June 2020
SOX5 is involved in balanced MITF regulation in human melanoma cells journal February 2016
Expression levels of Fv1: effects on retroviral restriction specificities journal June 2016
Optimization of proximity ligation assay (PLA) for detection of protein interactions and fusion proteins in non-adherent cells: application to pre-B lymphocytes journal July 2017
Functional and mechanistic studies reveal MAGEA3 as a pro-survival factor in pancreatic cancer cells journal July 2019
Identification of SMCHD1 domains for nuclear localization, homo-dimerization, and protein cleavage journal August 2018
EF-hand domain containing 2 (Efhc2) is crucial for distal segmentation of pronephros in zebrafish journal October 2018
DGAT2 partially compensates for lipid-induced ER stress in human DGAT1-deficient intestinal stem cells journal October 2019
Human prostate luminal cell differentiation requires NOTCH3 induction by p38-MAPK and MYC journal June 2017
Modelling the MYC-driven normal-to-tumour switch in breast cancer journal July 2019
Human prostate luminal cell differentiation requires NOTCH3 induction by p38-MAPK and MYC journal January 2017
plexin-A4/plexin-D1 complexes convey semaphorin-3C signals to induce cytoskeletal collapse in the absence of neuropilins journal January 2018
FGFR2b activating mutations disrupt cell polarity to potentiate migration and invasion in endometrial cancer journal January 2018
Rab34 small GTPase is required for Hedgehog signaling and an early step of ciliary vesicle formation in the mouse journal January 2018
RACK1 on and off the ribosome journal April 2019
Prmt7 is dispensable in tissue culture models for adipogenic differentiation journal January 2013
A mechanistic pan-cancer pathway model informed by multi-omics data interprets stochastic cell fate responses to drugs and mitogens journal March 2018
BTN3A2 Expression in Epithelial Ovarian Cancer Is Associated with Higher Tumor Infiltrating T Cells and a Better Prognosis journal June 2012
Impairment of Endothelial-Myocardial Interaction Increases the Susceptibility of Cardiomyocytes to Ischemia/Reperfusion Injury journal July 2013
Multi-color fluorescent reporter dengue viruses with improved stability for analysis of a multi-virus infection journal March 2018
CLCA2 is a positive regulator of store-operated calcium entry and TMEM16A journal May 2018
PIK3CA missense mutations promote glioblastoma pathogenesis, but do not enhance targeted PI3K inhibition journal July 2018
Crystal structures of human procathepsin H journal July 2018
Promotion of adipogenesis by JMJD6 requires the AT hook-like domain and is independent of its catalytic function journal August 2019
Kaposi's Sarcoma Herpesvirus MicroRNAs Induce Metabolic Transformation of Infected Cells journal September 2014
E3 Ubiquitin Ligase NEDD4 Promotes Influenza Virus Infection by Decreasing Levels of the Antiviral Protein IFITM3 journal August 2015
Merkel Cell Polyomavirus Small T Antigen Promotes Pro-Glycolytic Metabolic Perturbations Required for Transformation journal November 2016
Cell-Based Screen Identifies Human Interferon-Stimulated Regulators of Listeria monocytogenes Infection journal December 2016
Herpesviruses shape tumour microenvironment through exosomal transfer of viral microRNAs journal August 2017
Merkel cell polyomavirus recruits MYCL to the EP400 complex to promote oncogenesis journal October 2017
The TLR4 adaptor TRAM controls the phagocytosis of Gram-negative bacteria by interacting with the Rab11-family interacting protein 2 journal March 2019
ERAD‐dependent control of the Wnt secretory factor Evi journal January 2018
ESCRT ‐mediated lysosome repair precedes lysophagy and promotes cell survival journal October 2018
AGO 2 promotes telomerase activity and interaction between the telomerase components TERT and TERC journal December 2018
Toward an integrated map of genetic interactions in cancer cells journal February 2018
Genetic and pharmacological inhibition of TTK impairs pancreatic cancer cell line growth by inducing lethal chromosomal instability text January 2017
Interplay between transcription regulators RUNX1 and FUBP1 activates an enhancer of the oncogene c-KIT and amplifies cell proliferation. text January 2018
CLIC4 and CLIC1 bridge plasma membrane and cortical actin network for a successful cytokinesis journal December 2019
ASCs-Exosomes Recover Coupling Efficiency and Mitochondrial Membrane Potential in an in vitro Model of ALS journal October 2019
DUSP10 Is a Regulator of YAP1 Activity Promoting Cell Proliferation and Colorectal Cancer Progression journal November 2019
Polymeric Nanoparticles Based on Tyrosine-Modified, Low Molecular Weight Polyethylenimines for siRNA Delivery journal November 2019
Lung macrophage scavenger receptor SR-A6 (MARCO) is an adenovirus type-specific virus entry receptor text January 2018
A versatile modular vector system for rapid combinatorial mammalian genetics text January 2015
The serine protease hepsin mediates urinary secretion and polymerisation of Zona Pellucida domain protein uromodulin text January 2015
FAT1 mutations cause a glomerulotubular nephropathy text January 2016
Opposing effects of Nrf2 and Nrf2-activating compounds on the NLRP3 inflammasome independent of Nrf2-mediated gene expression text January 2017
Key role of the scavenger receptor MARCO in mediating adenovirus infection and subsequent innate responses of macrophages text January 2017
Lung macrophage scavenger receptor SR-A6 (MARCO) is an adenovirus type-specific virus entry receptor text January 2018
Redundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells text January 2019
The serine protease hepsin mediates urinary secretion and polymerisation of Zona Pellucida domain protein uromodulin journal December 2015
KChIP2 is a core transcriptional regulator of cardiac excitability journal March 2017
Environmental cystine drives glutamine anaplerosis and sensitizes cancer cells to glutaminase inhibition journal August 2017
A map of human PRDM9 binding provides evidence for novel behaviors of PRDM9 and other zinc-finger proteins in meiosis journal October 2017
Sae2/CtIP prevents R-loop accumulation in eukaryotic cells journal December 2018
CCL5 promotes breast cancer recurrence through macrophage recruitment in residual tumors journal April 2019
Dynamic change of electrostatic field in TMEM16F permeation pathway shifts its ion selectivity journal July 2019
Structural and functional insights into the bona fide catalytic state of Streptococcus pyogenes Cas9 HNH nuclease domain journal July 2019
Critical role for Piccolo in synaptic vesicle retrieval journal May 2019
Selective clearance of the inner nuclear membrane protein emerin by vesicular transport during ER stress journal October 2019
Stem cell transplantation rescued a primary open-angle glaucoma mouse model journal January 2021

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59 BASIC BIOLOGICAL SCIENCES
RNA interference
cloning
immunofluorescence
microRNAs
plasmid construction
transfection
vector cloning
viral vectors