Pancreatic cancer-initiating cell exosome message transfer into noncancer-initiating cells: the importance of CD44v6 in reprogramming.


Journal

Journal of experimental & clinical cancer research : CR
ISSN: 1756-9966
Titre abrégé: J Exp Clin Cancer Res
Pays: England
ID NLM: 8308647

Informations de publication

Date de publication:
19 Mar 2019
Historique:
received: 04 01 2019
accepted: 06 03 2019
entrez: 21 3 2019
pubmed: 21 3 2019
medline: 25 7 2019
Statut: epublish

Résumé

Cancer-initiating cell (CIC) exosomes (CIC-TEX) are suggested reprogramming Non-CIC. Mode of message transfer and engagement of CIC-markers being disputed, we elaborated the impact of CD44v6 and Tspan8 on the response of Non-CIC. Non-metastasizing CD44v6- and Tspan8-knockdown (kd) pancreatic cancer cells served as Non-CIC. CIC-TEX coculture-induced changes were evaluated by deep-sequencing and functional assays. Tumor progression was surveyed during in vivo CIC-TEX treatment. Deep-sequencing of CIC-TEX-cocultured CD44v6kd-Non-CIC revealed pronounced mRNA changes in signaling, transport, transcription and translation; altered miRNA affected metabolism, signaling and transcription. CIC-TEX coculture-induced changes in Tspan8kd-Non-CIC mostly relied on CIC-TEX-Tspan8 being required for targeting. CIC-TEX transfer supported apoptosis resistance and significantly promoted epithelial mesenchymal transition, migration, invasion and (lymph)angiogenesis of the kd Non-CIC in vitro and in vivo, deep-sequencing allowing individual mRNA and miRNA assignment to altered functions. Importantly, CIC-TEX act as a hub, initiated by CD44v6-dependent RTK, GPCR and integrin activation and involving CD44v6-assisted transcription and RNA processing. Accordingly, a kinase inhibitor hampered CIC-TEX-fostered tumor progression, which was backed by an anti-Tspan8 blockade of CIC-TEX binding. This in depth report on the in vitro and in vivo impact of CIC-TEX on CD44v6kd and Tspan8kd Non-CIC unravels hub CIC-TEX activity, highlighting a prominent contribution of the CIC-markers CD44v6 to signaling cascade activation, transcription, translation and miRNA processing in Non-CIC and of Tspan8 to CIC-TEX targeting. Blocking CIC-TEX binding/uptake and uptake-initiated target cell activation significantly mitigated the deleterious CIC-TEX impact on CD44v6kd and Tspan8kd Non-CIC.

Sections du résumé

BACKGROUND BACKGROUND
Cancer-initiating cell (CIC) exosomes (CIC-TEX) are suggested reprogramming Non-CIC. Mode of message transfer and engagement of CIC-markers being disputed, we elaborated the impact of CD44v6 and Tspan8 on the response of Non-CIC.
METHODS METHODS
Non-metastasizing CD44v6- and Tspan8-knockdown (kd) pancreatic cancer cells served as Non-CIC. CIC-TEX coculture-induced changes were evaluated by deep-sequencing and functional assays. Tumor progression was surveyed during in vivo CIC-TEX treatment.
RESULTS RESULTS
Deep-sequencing of CIC-TEX-cocultured CD44v6kd-Non-CIC revealed pronounced mRNA changes in signaling, transport, transcription and translation; altered miRNA affected metabolism, signaling and transcription. CIC-TEX coculture-induced changes in Tspan8kd-Non-CIC mostly relied on CIC-TEX-Tspan8 being required for targeting. CIC-TEX transfer supported apoptosis resistance and significantly promoted epithelial mesenchymal transition, migration, invasion and (lymph)angiogenesis of the kd Non-CIC in vitro and in vivo, deep-sequencing allowing individual mRNA and miRNA assignment to altered functions. Importantly, CIC-TEX act as a hub, initiated by CD44v6-dependent RTK, GPCR and integrin activation and involving CD44v6-assisted transcription and RNA processing. Accordingly, a kinase inhibitor hampered CIC-TEX-fostered tumor progression, which was backed by an anti-Tspan8 blockade of CIC-TEX binding.
CONCLUSIONS CONCLUSIONS
This in depth report on the in vitro and in vivo impact of CIC-TEX on CD44v6kd and Tspan8kd Non-CIC unravels hub CIC-TEX activity, highlighting a prominent contribution of the CIC-markers CD44v6 to signaling cascade activation, transcription, translation and miRNA processing in Non-CIC and of Tspan8 to CIC-TEX targeting. Blocking CIC-TEX binding/uptake and uptake-initiated target cell activation significantly mitigated the deleterious CIC-TEX impact on CD44v6kd and Tspan8kd Non-CIC.

Identifiants

pubmed: 30890157
doi: 10.1186/s13046-019-1129-8
pii: 10.1186/s13046-019-1129-8
pmc: PMC6425561
doi:

Substances chimiques

CD44v6 antigen 0
Hyaluronan Receptors 0
MicroRNAs 0
RNA, Messenger 0

Types de publication

Journal Article

Langues

eng

Pagination

132

Subventions

Organisme : Deutsche Krebshilfe
ID : 110836
Organisme : National Natural Science Foundation of China (CN)
ID : NSFC 81702877

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Auteurs

Zhe Wang (Z)

Department of Oncology, The First Affiliated Hospital of Guangdong Pharmaceutical University, Guangzhou, China.
Pancreas Section, University Hospital of Surgery, Im Neuenheimer Feld 110, D69120, Heidelberg, Germany.

Hanxue Sun (H)

Pancreas Section, University Hospital of Surgery, Im Neuenheimer Feld 110, D69120, Heidelberg, Germany.

Jan Provaznik (J)

Gene Core Unit, EMBL, Heidelberg, Germany.

Thilo Hackert (T)

Pancreas Section, University Hospital of Surgery, Im Neuenheimer Feld 110, D69120, Heidelberg, Germany.

Margot Zöller (M)

Department of Oncology, The First Affiliated Hospital of Guangdong Pharmaceutical University, Guangzhou, China. margot.zoeller@gmx.net.
Pancreas Section, University Hospital of Surgery, Im Neuenheimer Feld 110, D69120, Heidelberg, Germany. margot.zoeller@gmx.net.

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Classifications MeSH