Mechanisms Involved in the Promoting Activity of Fibroblasts in HTLV-1-Mediated Lymphomagenesis: Insights into the Plasticity of Lymphomatous Cells

Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome stu...

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Published inInternational journal of molecular sciences Vol. 22; no. 19; p. 10562
Main Authors Rigotto, Giulia, Montini, Barbara, Mattiolo, Adriana, Lazzari, Nayana, Piano, Maria Assunta, Remondini, Daniel, Marmiroli, Sandra, Bertacchini, Jessika, Chieco-Bianchi, Luigi, Calabrò, Maria Luisa
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 29.09.2021
MDPI
Subjects
Animals
Anti-Inflammatory Agents, Non-Steroidal - pharmacology
Apoptosis
Aspirin - pharmacology
Cancer
Cell Line
Cells, Cultured
Coculture Techniques
Fibroblasts
Fibroblasts - drug effects
Fibroblasts - metabolism
Fibroblasts - virology
Gene Expression Profiling - methods
Gene Expression Regulation, Neoplastic - drug effects
Gene Expression Regulation, Neoplastic - genetics
Human T-lymphotropic virus 1 - physiology
Humans
Infections
Jurkat Cells
Kinases
Leukemia
Lymphoma
Lymphoma - drug therapy
Lymphoma - genetics
Lymphoma - virology
Metabolism
Mice
Mice, Inbred NOD
Mice, Knockout
Mice, SCID
Neoplastic Stem Cells - drug effects
Neoplastic Stem Cells - metabolism
Neoplastic Stem Cells - virology
Phosphorylation
Principal components analysis
Proteins
Signal Transduction - drug effects
Signal Transduction - genetics
Xenograft Model Antitumor Assays - methods
plasticity
HTLV-1
cancer stem cells
lymphomagenesis
ATLL
stemness
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Abstract Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10+GPR77+ HFF subpopulation, but also the percentage of ALDH1bright C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1bright C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.
AbstractList Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10 GPR77 HFF subpopulation, but also the percentage of ALDH1 C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1 C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.
Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10+GPR77+ HFF subpopulation, but also the percentage of ALDH1bright C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1bright C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.
Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10+GPR77+ HFF subpopulation, but also the percentage of ALDH1bright C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1bright C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10+GPR77+ HFF subpopulation, but also the percentage of ALDH1bright C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1bright C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.
Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the contribution of stromal components remains poorly understood. To dissect the role of fibroblasts in HTLV-1-mediated lymphomagenesis, transcriptome studies, cytofluorimetric and qRT-PCR analyses of surface and intracellular markers linked to plasticity and stemness in coculture, and in vivo experiments were performed. A transcriptomic comparison between a more lymphomagenic (C91/III) and the parental (C91/PL) cell line evidenced hyperactivation of the PI3K/Akt pathway, confirmed by phospho-ELISA and 2-DE and WB analyses. C91/III cells also showed higher expression of mesenchymal and stemness genes. Short-term coculture with human foreskin fibroblasts (HFF) induced these features in C91/PL cells, and significantly increased not only the cancer stem cells (CSCs)-supporting CD10 + GPR77 + HFF subpopulation, but also the percentage of ALDH1 bright C91/PL cells. A non-cytotoxic acetylsalicylic acid treatment decreased HFF-induced ALDH1 bright C91/PL cells, downregulated mesenchymal and stemness genes in cocultured cells, and delayed lymphoma growth in immunosuppressed mice, thus hindering the supportive activity of HFF on CSCs. These data suggest that crosstalk with HFF significantly intensifies the aggressiveness and plasticity of C91/PL cells, leading to the enrichment in lymphoma-initiating cells. Additional research is needed to better characterize these preliminary findings.
Author Calabrò, Maria Luisa
Rigotto, Giulia
Bertacchini, Jessika
Mattiolo, Adriana
Marmiroli, Sandra
Chieco-Bianchi, Luigi
Remondini, Daniel
Piano, Maria Assunta
Montini, Barbara
Lazzari, Nayana
AuthorAffiliation 3 Department of Biomedical, Metabolic and Neuronal Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy; sandra.marmiroli@unimore.it (S.M.); jbertacchini@unimore.it (J.B.)
1 Immunology and Molecular Oncology, Veneto Institute of Oncology IOV—IRCCS, 35128 Padua, Italy; giulia.rigotto@iov.veneto.it (G.R.); barbara.montini1979@gmail.com (B.M.); adriana.mattiolo86@gmail.com (A.M.); nayana.lazzari@iov.veneto.it (N.L.); mariaassunta.piano@iov.veneto.it (M.A.P.)
2 Department of Physics and Astronomy, University of Bologna, and Istituto Nazionale di Fisica Nucleare, INFN, 40127 Bologna, Italy; daniel.remondini@unibo.it
4 Department of Surgery, Oncology and Gastroenterology, University of Padua, 35128 Padua, Italy; luigi.chiecobianchi@unipd.it
AuthorAffiliation_xml – name: 3 Department of Biomedical, Metabolic and Neuronal Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy; sandra.marmiroli@unimore.it (S.M.); jbertacchini@unimore.it (J.B.)
– name: 1 Immunology and Molecular Oncology, Veneto Institute of Oncology IOV—IRCCS, 35128 Padua, Italy; giulia.rigotto@iov.veneto.it (G.R.); barbara.montini1979@gmail.com (B.M.); adriana.mattiolo86@gmail.com (A.M.); nayana.lazzari@iov.veneto.it (N.L.); mariaassunta.piano@iov.veneto.it (M.A.P.)
– name: 4 Department of Surgery, Oncology and Gastroenterology, University of Padua, 35128 Padua, Italy; luigi.chiecobianchi@unipd.it
– name: 2 Department of Physics and Astronomy, University of Bologna, and Istituto Nazionale di Fisica Nucleare, INFN, 40127 Bologna, Italy; daniel.remondini@unibo.it
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Keywords plasticity
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cancer stem cells
lymphomagenesis
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Present address: Pediatric Oncohaematology, Stem Cell Transplant and Gene Therapy, Istituto di Ricerca Pediatrica Città della Speranza, 35128 Padua, Italy.
Present address: Global Site Intelligence & Activation, Site & Patient Access, PPD, 20090 Milan, Italy.
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Snippet Among the mechanisms leading to progression to Adult T-cell Leukaemia/Lymphoma in Human T-cell Leukaemia Virus type 1 (HTLV-1)-infected subjects, the...
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SubjectTerms Animals
Anti-Inflammatory Agents, Non-Steroidal - pharmacology
Apoptosis
Aspirin - pharmacology
Cancer
Cell Line
Cells, Cultured
Coculture Techniques
Fibroblasts
Fibroblasts - drug effects
Fibroblasts - metabolism
Fibroblasts - virology
Gene Expression Profiling - methods
Gene Expression Regulation, Neoplastic - drug effects
Gene Expression Regulation, Neoplastic - genetics
Human T-lymphotropic virus 1 - physiology
Humans
Infections
Jurkat Cells
Kinases
Leukemia
Lymphoma
Lymphoma - drug therapy
Lymphoma - genetics
Lymphoma - virology
Metabolism
Mice
Mice, Inbred NOD
Mice, Knockout
Mice, SCID
Neoplastic Stem Cells - drug effects
Neoplastic Stem Cells - metabolism
Neoplastic Stem Cells - virology
Phosphorylation
Principal components analysis
Proteins
Signal Transduction - drug effects
Signal Transduction - genetics
Xenograft Model Antitumor Assays - methods
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Title Mechanisms Involved in the Promoting Activity of Fibroblasts in HTLV-1-Mediated Lymphomagenesis: Insights into the Plasticity of Lymphomatous Cells
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Volume 22
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