Canine parvovirus induces G1/S cell cycle arrest that involves EGFR Tyr1086 phosphorylation

ABSTRACT Canine parvovirus (CPV) has been used in cancer control as a drug delivery vehicle or anti-tumor reagent due to its multiple natural advantages. However, potential host cell cycle arrest induced by virus infection may impose a big challenge to CPV associated cancer control as it could prevent host cancer cells from undergoing cell lysis and foster them regain viability once the virotherapy was ceased. To explore CPV-induced cell cycle arrest and the underlying mechanism toward improved virotherapeutic design, we focus on epidermal growth factor receptor (EGFR), a cellular receptor interacting with TfR that mediates CPV-host interactions, and alterations on its tyrosine phosphorylation sites in response to CPV infection. We found that CPV could trigger host G1/S cell cycle arrest via the EGFR (Y1086)/p27 and EGFR (Y1068)/STAT3/cyclin D1 axes, and EGFR inhibitor could not reverse this process. Our results contribute to our understandings on the mechanism of CPV-induced host cellular response and can be used in the onco-therapeutic design utilizing CPV by preventing host cancer cells from entering cell cycle arrest.

[1]  S. Favaro,et al.  Quantitative , 2020, Psychology through Critical Auto-Ethnography.

[2]  M. Kucherlapati.  Modulation of proliferation factors in lung adenocarcinoma with an analysis of the transcriptional consequences of genomic EGFR activation , 2019, Oncotarget.

[3]  Dong-Hyun Kim,et al.  Peroxiredoxin V (PrdxV) negatively regulates EGFR/Stat3-mediated fibrogenesis via a Cys48-dependent interaction between PrdxV and Stat3 , 2019, Scientific Reports.

[4]  N. Yamashita,et al.  Accumulation of quaternary ammonium compounds as emerging contaminants in sediments collected from the Pearl River Estuary, China and Tokyo Bay, Japan. , 2018, Marine Pollution Bulletin.

[5]  M. Chien,et al.  The interplay of reactive oxygen species and the epidermal growth factor receptor in tumor progression and drug resistance , 2018, Journal of experimental & clinical cancer research : CR.

[6]  J. Rommelaere,et al.  The Oncolytic Virotherapy Era in Cancer Management: Prospects of Applying H-1 Parvovirus to Treat Blood and Solid Cancers , 2017, Front. Oncol..

[7]  B. Shi,et al.  EGFR regulates iron homeostasis to promote cancer growth through redistribution of transferrin receptor 1. , 2016, Cancer letters.

[8]  M. Hottiger,et al.  ARTD1 regulates cyclin E expression and consequently cell-cycle re-entry and G1/S progression in T24 bladder carcinoma cells , 2016, Cell cycle.

[9]  S. V. Van Gool,et al.  Immune Suppression during Oncolytic Virotherapy for High-Grade Glioma; Yes or No? , 2015, Journal of Cancer.

[10]  J. Settleman,et al.  Differential Effects of Tyrosine Kinase Inhibitors on Normal and Oncogenic EGFR Signaling and Downstream Effectors , 2015, Molecular Cancer Research.

[11]  D. Pintel,et al.  Replication of Minute Virus of Mice in Murine Cells Is Facilitated by Virally Induced Depletion of p21 , 2012, Journal of Virology.

[12]  B. Leuchs,et al.  Regression of Glioma in Rat Models by Intranasal Application of Parvovirus H-1 , 2011, Clinical Cancer Research.

[13]  J. Qiu,et al.  Parvovirus infection-induced cell death and cell cycle arrest. , 2010, Future virology.

[14]  H. Zentgraf,et al.  Through Its Nonstructural Protein NS1, Parvovirus H-1 Induces Apoptosis via Accumulation of Reactive Oxygen Species , 2010, Journal of Virology.

[15]  S. Skvortsov,et al.  Quantitative proteomics and phosphoproteomics reveal novel insights into complexity and dynamics of the EGFR signaling network , 2008, Proteomics.

[16]  Marco Foiani,et al.  Regulation of DNA repair throughout the cell cycle , 2008, Nature Reviews Molecular Cell Biology.

[17]  J. Verweij,et al.  A phase I dose escalation study of BIBW 2992, an irreversible dual inhibitor of epidermal growth factor receptor 1 (EGFR) and 2 (HER2) tyrosine kinase in a 2-week on, 2-week off schedule in patients with advanced solid tumours , 2007, British Journal of Cancer.

[18]  Wen-Hwa Lee,et al.  CtIP Activates Its Own and Cyclin D1 Promoters via the E2F/RB Pathway during G1/S Progression , 2006, Molecular and Cellular Biology.

[19]  P. Singh,et al.  Canine parvovirus-like particles, a novel nanomaterial for tumor targeting , 2006, Journal of Nanobiotechnology.

[20]  R. Mikkelsen,et al.  Requirement of Tyr-992 and Tyr-1173 in Phosphorylation of the Epidermal Growth Factor Receptor by Ionizing Radiation and Modulation by SHP2* , 2005, Journal of Biological Chemistry.

[21]  Joseph Bertolini,et al.  Transferrin: structure, function and potential therapeutic actions. , 2005, Drug discovery today.

[22]  M. Büchler,et al.  Transferrin receptor is a marker of malignant phenotype in human pancreatic cancer and in neuroendocrine carcinoma of the pancreas. , 2004, European journal of cancer.

[23]  L. Munaron,et al.  Intracellular calcium signals and control of cell proliferation: how many mechanisms? , 2004, Journal of cellular and molecular medicine.

[24]  A. Lompré,et al.  Alteration in temporal kinetics of Ca2+ signaling and control of growth and proliferation , 2004, Biology of the cell.

[25]  J. Sobczak-Thépot,et al.  NS1- and Minute Virus of Mice-Induced Cell Cycle Arrest: Involvement of p53 and p21cip1 , 2001, Journal of Virology.

[26]  Deqi Huang,et al.  E2F mediates induction of the Sp1-controlled promoter of the human DNA polymerase B-subunit gene POLE2 , 2001, Nucleic Acids Res..

[27]  Y. Niitsu,et al.  In vivo gene delivery to tumor cells by transferrin‐streptavidin‐DNA conjugate , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[28]  Wolfhard Semmler,et al.  Macromolecular Contrast Agents for Optical Imaging of Tumors: Comparison of Indotricarbocyanine-labeled Human Serum Albumin and Transferrin¶ , 2000, Photochemistry and photobiology.

[29]  D. Johnson,et al.  Cyclins and cell cycle checkpoints. , 1999, Annual review of pharmacology and toxicology.

[30]  J. Rommelaere,et al.  The nonstructural proteins of the autonomous parvovirus minute virus of mice interfere with the cell cycle, inducing accumulation in G2. , 1995, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[31]  S. Gamou,et al.  Hydrogen peroxide preferentially enhances the tyrosine phosphorylation of epidermal growth factor receptor , 1995, FEBS letters.

[32]  N. Brünner,et al.  Differences in transferrin response and numbers of transferrin receptors in rat and human mammary carcinoma lines of different metastatic potentials , 1993, Journal of cellular physiology.

[33]  A. Iwamoto,et al.  Role of Ca2+ influx in bombesin-induced mitogenesis in Swiss 3T3 fibroblasts. , 1991, The Journal of biological chemistry.

[34]  M. Jokela,et al.  E2F mediates induction of the Sp1-controlled promoter of the human DNA polymerase epsilon B-subunit gene POLE2. , 2001, Nucleic acids research.