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Potent antiproliferative cembrenoids accumulate in tobacco upon infection with Rhodococcus fascians and trigger unusual microtubule dynamics in human glioblastoma cells

Aminata P Nacoulma, Veronique Megalizzi, Laurent R Pottier, Manuela De Lorenzi, Sylviane Thoret, Joëlle Dubois, Olivier M Vandeputte, Pierre Duez, Danny Vereecke UGent and Mondher El Jaziri (2013) PLOS ONE. 8(10).
abstract
Aims: Though plant metabolic changes are known to occur during interactions with bacteria, these were rarely challenged for pharmacologically active compounds suitable for further drug development. Here, the occurrence of specific chemicals with antiproliferative activity against human cancer cell lines was evidenced in hyperplasia (leafy galls) induced when plants interact with particular phytopathogens, such as the Actinomycete Rhodococcus fascians. Methods: We examined leafy galls fraction F3.1.1 on cell proliferation, cell division and cytoskeletal disorganization of human cancer cell lines using time-lapse videomicroscopy imaging, combined with flow cytometry and immunofluorescence analysis. We determined the F3.1.1-fraction composition by gas chromatography coupled to mass spectrometry. Results: The leafy galls induced on tobacco by R. fascians yielded fraction F3.1.1 which inhibited proliferation of glioblastoma U373 cells with an IC50 of 4.5 mu g/mL, F.3.1.1 was shown to increase cell division duration, cause nuclear morphological deformations and cell enlargement, and, at higher concentrations, karyokinesis defects leading to polyploidization and apoptosis. F3.1.1 consisted of a mixture of isomers belonging to the cembrenoids. The cellular defects induced by F3.1.1 were caused by a peculiar cytoskeletal disorganization, with the occurrence of fragmented tubulin and strongly organized microtubule aggregates within the same cell. Colchicine, paclitaxel, and cembrene also affected U373 cell proliferation and karyokinesis, but the induced microtubule rearrangement was very different from that provoked by F3.1.1. Altogether our data indicate that the cembrenoid isomers in F3.1.1 have a unique mode of action and are able to simultaneously modulate microtubule polymerization and stability.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
IN-VITRO, NICOTIANA-TABACUM, TUBULIN, COLCHICINE, TRICHOMES, EXTRACTS, CANCER, DEATH, cancer, death, trichomes, colchicine, tubulin, Nicotiana tabacum
journal title
PLOS ONE
PLoS One
volume
8
issue
10
article number
e77529
pages
12 pages
Web of Science type
Article
Web of Science id
000326034500035
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.534 (2013)
JCR rank
8/55 (2013)
JCR quartile
1 (2013)
ISSN
1932-6203
DOI
10.1371/journal.pone.0077529
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
4210357
handle
http://hdl.handle.net/1854/LU-4210357
date created
2013-12-16 16:01:01
date last changed
2017-04-03 09:26:05
@article{4210357,
  abstract     = {Aims: Though plant metabolic changes are known to occur during interactions with bacteria, these were rarely challenged for pharmacologically active compounds suitable for further drug development. Here, the occurrence of specific chemicals with antiproliferative activity against human cancer cell lines was evidenced in hyperplasia (leafy galls) induced when plants interact with particular phytopathogens, such as the Actinomycete Rhodococcus fascians.
Methods: We examined leafy galls fraction F3.1.1 on cell proliferation, cell division and cytoskeletal disorganization of human cancer cell lines using time-lapse videomicroscopy imaging, combined with flow cytometry and immunofluorescence analysis. We determined the F3.1.1-fraction composition by gas chromatography coupled to mass spectrometry.
Results: The leafy galls induced on tobacco by R. fascians yielded fraction F3.1.1 which inhibited proliferation of glioblastoma U373 cells with an IC50 of 4.5 mu g/mL, F.3.1.1 was shown to increase cell division duration, cause nuclear morphological deformations and cell enlargement, and, at higher concentrations, karyokinesis defects leading to polyploidization and apoptosis. F3.1.1 consisted of a mixture of isomers belonging to the cembrenoids. The cellular defects induced by F3.1.1 were caused by a peculiar cytoskeletal disorganization, with the occurrence of fragmented tubulin and strongly organized microtubule aggregates within the same cell. Colchicine, paclitaxel, and cembrene also affected U373 cell proliferation and karyokinesis, but the induced microtubule rearrangement was very different from that provoked by F3.1.1. Altogether our data indicate that the cembrenoid isomers in F3.1.1 have a unique mode of action and are able to simultaneously modulate microtubule polymerization and stability.},
  articleno    = {e77529},
  author       = {Nacoulma, Aminata P and Megalizzi, Veronique and Pottier, Laurent R and De Lorenzi, Manuela and Thoret, Sylviane and Dubois, Jo{\"e}lle and Vandeputte, Olivier M and Duez, Pierre and Vereecke, Danny and El Jaziri, Mondher},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {IN-VITRO,NICOTIANA-TABACUM,TUBULIN,COLCHICINE,TRICHOMES,EXTRACTS,CANCER,DEATH,cancer,death,trichomes,colchicine,tubulin,Nicotiana tabacum},
  language     = {eng},
  number       = {10},
  pages        = {12},
  title        = {Potent antiproliferative cembrenoids accumulate in tobacco upon infection with Rhodococcus fascians and trigger unusual microtubule dynamics in human glioblastoma cells},
  url          = {http://dx.doi.org/10.1371/journal.pone.0077529},
  volume       = {8},
  year         = {2013},
}

Chicago
Nacoulma, Aminata P, Veronique Megalizzi, Laurent R Pottier, Manuela De Lorenzi, Sylviane Thoret, Joëlle Dubois, Olivier M Vandeputte, Pierre Duez, Danny Vereecke, and Mondher El Jaziri. 2013. “Potent Antiproliferative Cembrenoids Accumulate in Tobacco Upon Infection with Rhodococcus Fascians and Trigger Unusual Microtubule Dynamics in Human Glioblastoma Cells.” Plos One 8 (10).
APA
Nacoulma, A. P., Megalizzi, V., Pottier, L. R., De Lorenzi, M., Thoret, S., Dubois, J., Vandeputte, O. M., et al. (2013). Potent antiproliferative cembrenoids accumulate in tobacco upon infection with Rhodococcus fascians and trigger unusual microtubule dynamics in human glioblastoma cells. PLOS ONE, 8(10).
Vancouver
1.
Nacoulma AP, Megalizzi V, Pottier LR, De Lorenzi M, Thoret S, Dubois J, et al. Potent antiproliferative cembrenoids accumulate in tobacco upon infection with Rhodococcus fascians and trigger unusual microtubule dynamics in human glioblastoma cells. PLOS ONE. 2013;8(10).
MLA
Nacoulma, Aminata P, Veronique Megalizzi, Laurent R Pottier, et al. “Potent Antiproliferative Cembrenoids Accumulate in Tobacco Upon Infection with Rhodococcus Fascians and Trigger Unusual Microtubule Dynamics in Human Glioblastoma Cells.” PLOS ONE 8.10 (2013): n. pag. Print.