EGFR signaling; breast cancer; cell cycle arrest; lipid transfer protein; metabolic reprogramming; Carrier Proteins; Humans; Female; Mitochondria/metabolism; Cell Line, Tumor; Cell Proliferation/genetics; Metabolic Reprogramming; Breast Neoplasms/metabolism; Breast Neoplasms/genetics; Breast Neoplasms/pathology; Cell Cycle Checkpoints/genetics; Carrier Proteins/genetics; Carrier Proteins/metabolism; Cellular Reprogramming/genetics; Cancer cells; Cell-cycle arrest; Cell-cycle progression; Functional links; L-methionine; Mitochondrias; Breast Neoplasms; Cell Cycle Checkpoints; Cell Proliferation; Cellular Reprogramming; Mitochondria; Medicine (miscellaneous); Biochemistry, Genetics and Molecular Biology (miscellaneous)
Abstract :
[en] Cancer cells adapt their metabolism to support aberrant cell proliferation. However, the functional link between metabolic reprogramming and cell cycle progression remains largely unexplored. Mitochondria rely on the transfer of multiple lipids from the endoplasmic reticulum (ER) to their membranes to be functional. Several mitochondrial-derived metabolites influence cancer cell proliferation by modulating the epigenome. Here, the loss of STARD7, a lipid transfer protein whose expression is enhanced in breast cancer, is shown to lead a metabolic reprogramming characterized by the accumulation of carnitine derivatives and S-Adenosyl-L-methionine (SAM). Elevated SAM levels cause the increase of H3K27 trimethylation on many gene promoters coding for candidates involved in cell cycle progression. Likewise, STARD7 deficiency triggers cell cycle arrest and impairs ERα-dependent cell proliferation. Moreover, EGFR signaling is also impaired in triple negative breast cancer cells lacking STARD7, at least due to deregulated EGFR trafficking to lysosomes. Therefore, mitochondria rely on STARD7 to support cell cycle progression in breast cancer.
Research Center/Unit :
Giga-Cancer - ULiège
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Dondajewska, Ewelina ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale ; Laboratory of Cancer Biology, Liège, Belgium ; Department of Medical Biotechnology, Poznan University of Medical Sciences (PUMS), Poznan, Poland
Allepuz-Fuster, Paula; Laboratory of Cancer Biology, Liège, Belgium ; GIGA Cancer, GIGA, University of Liege, CHU, Sart-Tilman, Liège, 4000, Belgium
Maurizy, Chloé ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale ; Laboratory of Cancer Biology, Liège, Belgium
Hego, Alexandre ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Lion, Quentin ; Université de Liège - ULiège > GIGA ; Laboratory of Cancer Biology, Liège, Belgium
Blomme, Arnaud ; Université de Liège - ULiège > Département de pharmacie ; Laboratory of Cancer Signaling, Liège, Belgium
Close, Pierre ; Université de Liège - ULiège > Département de pharmacie ; Laboratory of Cancer Signaling, Liège, Belgium ; WELBIO department, WEL Research Institute, avenue Pasteur, 6, 1300, Wavre, Belgium
Lavergne, Arnaud ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Thiry, Marc ; Université de Liège - ULiège > Département des sciences de la vie > Service collectif des enseignements de biologie en bachelier
Nemazanyy, Ivan; Platform for Metabolic Analyses, Structure Fédérative de Recherche Necker, INSERM US24/CNRS UAR 3633, Paris, 75015, France
Krishnankutty, Roopesh; Institute of Genetics and Cancer, Edinburgh Cancer Research, Scotland
Marques, Jair; Institute of Genetics and Cancer, Edinburgh Cancer Research, Scotland
von Kriegsheim, Alex; Institute of Genetics and Cancer, Edinburgh Cancer Research, Scotland
Henneman, Nathaniel F; Institut Necker-Enfants Malades (INEM), INSERM U1151/CNRS UMR 8253, 75015 Paris, France and Université de Paris Cité, Paris, 75006, France
Panasyuk, Ganna; Institut Necker-Enfants Malades (INEM), INSERM U1151/CNRS UMR 8253, 75015 Paris, France and Université de Paris Cité, Paris, 75006, France
Shostak, Kateryna ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale ; Laboratory of Cancer Biology, Liège, Belgium
Chariot, Alain ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale ; Laboratory of Cancer Biology, Liège, Belgium ; WELBIO department, WEL Research Institute, avenue Pasteur, 6, 1300, Wavre, Belgium
WELBIO - Institut wallon virtuel de recherche d'excellence dans les domaines des sciences de la vie
Funding text :
The authors are grateful to Dr. Christine Gilles (GIGA Cancer, University of Liege, Liege, Belgium) for the gift of BT549 cells. This work was supported by grants from the WELBIO (WELBIO-CR-2019C-02R), the FNRS/TELEVIE, the Belgian Foundation against Cancer (FBC/2020/1323), the University of Liege (ARC UBICOREAR) and the Leon Fredericq Foundation (Faculty of Medicine, CHU of Liege). CM, AB, PC, and AC are Senior Research Assistant, Research Associate, Senior Research Associate, and Research Director at the FNRS, respectively.The authors are grateful to Dr. Christine Gilles (GIGA Cancer, University of Liege, Liege, Belgium) for the gift of BT549 cells. This work was supported by grants from the WELBIO (WELBIO\u2010CR\u20102019C\u201002R), the FNRS/TELEVIE, the Belgian Foundation against Cancer (FBC/2020/1323), the University of Liege (ARC UBICOREAR) and the Leon Fredericq Foundation (Faculty of Medicine, CHU of Liege). CM, AB, PC, and AC are Senior Research Assistant, Research Associate, Senior Research Associate, and Research Director at the FNRS, respectively.
M. Scharwey, T. Tatsuta, T. Langer, J. Cell Sci. 2013, 126, 5317.
A. Tarasov, E. Griffiths, G. Rutter, Cell Calcium 2012, 52, 28.
P. Willems, R. Rossignol, C. Dieteren, M. Murphy, W. Koopman, Cell Metab. 2015, 22, 207.
S. Durand, S. Angeletti, S. Genti-Raimondi, Placenta 2004, 25, 37.
Y. Horibata, H. Sugimoto, J. Biol. Chem. 2010, 285, 7358.
Y. Horibata, H. Ando, P. Zhang, L. Vergnes, C. Aoyama, M. Itoh, K. Reue, H. Sugimoto, Biol. Chem. 2016, 291, 24880.
L. Yang, C. Na, S. Luo, D. Wu, S. Hogen, T. Huang, T. Weaver, Nat. Sci. Rep. 2017, 7, 46416.
S. Saita, T. Tatsuta, P. Lampe, T. König, Y. Ohba, T. Langer, EMBO J. 2018, 37, 97909.
S. Deshwal, M. Onishi, T. Tatsuta, T. Bartsch, E. Cors, K. Ried, K. Lemke, H. Nolte, P. Giavalisco, T. Langer, Nat. Cell Biol. 2023, 25, 246.
L. C. de la Rosa, C. Garcia-Ruiz, C. Vallejo, A. Baulies, S. Nunez, M. Monte, J. Marin, L. Baila-Rueda, A. Cenarro, F. Civeira, J. Fuster, J. Garcia-Valdecasas, J. Ferrer, M. Karin, V. Ribas, J. Fernandez-Checa, J. Hepatol. 2021, 74, 1429.
N. Akiyama, H. Sasaki, T. Ishizuka, T. Kishi, H. Sakamoto, M. Onda, H. Hirai, Y. Yazaki, T. Sugimura, M. Terada, Cancer Res. 1997, 57, 3548.
B. Vassilev, H. Sihto, S. Li, M. Hölttä-Vuori, J. Ilola, J. Lundin, J. Isola, P.-L. Kellokumpu-Lehtinen, H. Joensuu, E. Ikonen, Am. J. Pathol. 2015, 185, 987.
P. Li, Z. Zhang, H. Lv, P. Sun, Tissue Cell 2022, 79, 101971.
M. Zhang, Z. Xiang, F. Wang, R. Shan, L. Li, J. Chen, B.-A. Liu, J. Huang, L.-Q. Sun, W.-B. Zhou, Oncol. Rep. 2020, 44, 2487.
M. Olayioye, P. Hoffmann, T. Pomorski, J. Armes, R. Simpson, B. Kemp, G. Lindeman, J. Visvader, Cancer Res. 2004, 64, 3538.
A. Floris, J. Luo, J. Frank, J. Zhou, S. Orrù, M. Biancoletta, S. Pucci, A. Orlandi, P. Campagna, A. Balzano, K. Ramani, M. Tomasi, J. Exp. Clin. Cancer Res. 2019, 38, 4.
R. Filadi, D. Pendin, P. Pizzo, Cell Death Dis. 2018, 9, 330.
E. Smirnova, L. Griparic, D.-L. Shurland, A. van der Bliek, Mol. Biol. Cell 2001, 12, 2245.
U. Ihenacho, K. Meacham, M. Harwig, M. Widlansky, R. Hill, Front. Endocrinol. 2021, 12.
H. Yu, C. Sun, Q. Gong, D. Feng, Front. Cell Develop. Biol. 2021, 9, 629669.
M. Sassano, A. van Vliet, P. Agostinis, Front. Oncol. 2017, 7, 174.
A. Carreras-Sureda, F. Jana, H. Urra, S. Durand, D. Mortenson, A. Sagredo, G. Bustos, Y. Hazari, E. Ramos-Fernandez, M. Sassano, P. Pihan, A. van Vliet, M. Gonzales-Quiroz, A. Torres, C. Tapia-Rojas, M. Kerkhofs, R. Vicente, R. Kaufman, N. Inestrosa, C. Gonzales-Billault, R. Wiseman, P. Agostinis, G. Bultynck, F. Court, G. Kroemer, J. Cardenas, C. Hetz, Nat. Cell Biol. 2019, 21, 755.
T. Verfaillie, N. Rubio, A. Garg, G. Bultynck, R. Rizzuto, J.-P. Decuypere, J. Piette, C. Linehan, S. Gupta, A. Samali, P. Agostinis, Cell Death Differ. 2012, 19, 1880.
L. Tong, Cell. Mol. Life Sci. 2005, 62, 1784.
Q. Qu, F. Zeng, X. Liu, Q. Wang, F. Deng, Cell Death Dis. 2016, 7, 2226.
B. Jaishy, E. Abel, J. Lipid Res. 2016, 57, 1619.
A. Kuzmichev, K. Nishioka, H. Erdjument-Bromage, P. Tempst, D. Reinberg, Genes Develop. 2002, 16, 2893.
L. Boyer, K. Plath, J. Zeitlinger, T. Brambrink, L. Medeiros, T. Lee, S. Levine, M. Wernig, A. Tajonar, M. Ray, Nature 2006, 441, 349.
D. Liu, X. Ding, J. Du, X. Cai, Y. Huang, T. Ward, A. Shaw, Y. Yang, R. Hu, C. Jin, X. Yao, J. Biol. Chem. 2007, 282, 21415.
A. Nishiyama, M. Matsui, S. Iwata, K. Hirota, H. Masutani, H. Nakamura, Y. Takagi, H. Sono, Y. Gon, J. Yodoi, J. Biol. Chem. 1999, 274, 21645.
D. Mustacich, G. Powis, Biochem. J. 2000, 346, 1.
J. M. Rae, M. D. Johnson, J. O. Scheys, K. E. Cordero, J. M. Larios, M. E. Lippman, Breast Cancer Res. Treat. 2005, 92, 141.
N. Mahmood, D. Cheishvili, A. Arakelian, I. Tanvir, H. Khan, A.-S. Pépin, M. Szyf, S. Rabbani, Oncotarget 2017, 9, 5169.
K. Kasahara, M. Inagaki, Trends Cell Biol. 2021, 31, 954.
Z. Tang, L. MG, T. Stowe, S. Chen, M. Zhu, T. Stearns, B. Franco, Q. Zhong, Nature 2013, 502, 254.
J. Kim, J. Lee, S. Heynen-Genel, E. Suyama, K. Ono, T. Ideker, P. Aza-Blanc, J. Gleeson, Nature 2010, 464, 1048.
D. Foster, J. Clin. Invest. 2012, 122, 1958.
N. Ridgway, Z. Yao, D. Vance, J. Biol. Chem. 1989, 264, 1203.
J. Stefely, D. Pagliarini, Trends Biochem. Sci. 2017, 42, 824.
L. Stead, J. Brosnan, M. Brosnan, D. Vance, R. Jacobs, Am. J. Clin. Nutr. 2006, 83, 5.
M. Hamasaki, N. Furuta, A. Matsuda, A. Nezu, A. Yamamoto, N. Fujita, H. Oomori, T. Noda, T. Haraguchi, Y. Hiraoka, A. Amano, T. Yoshimori, Nature 2013, 495, 389.
P. Gomez-Suaga, S. Paillusson, R. Stoica, W. Noble, D. Hanger, C. Miller, Curr. Biol. 2017, 27, 371.
B. Floyd, E. Wilkerson, M. Veling, C. Minogue, C. Xia, E. Beebe, R. Wrobel, H. Cho, L. Kremer, C. Alston, K. Gromeek, B. Dolan, A. Ulbrich, J. Stefely, S. Bohl, K. Werner, A. Jochem, M. Wesphall, J. Rensvold, R. Taylor, H. Prokish, J.-J. Kim, J. Coon, D. Pagliarini, Mol. Cell 2016, 4, 621.
P. A. Ewels, A. Peltzer, S. Fillinger, H. Patel, J. Alneberg, A. Wilm, M. U. Garcia, P. Di Tommaso, S. Nahnsen, Nat. Biotechnol. 2020, 38, 276.
P. Bankhead, M. Loughrey, J. Fernandez, Y. Dombrowski, D. McArt, P. Dunne, S. McQuaid, R. Gray, L. Murray, H. Coleman, J. James, M. Salto-Tellez, P. Hamilton, Nat. Sci. Rep. 2017, 7, 16878.
M. Wieckowski, C. Giorgi, M. Lebiedzinska, J. Duszynski, P. Pinton, Nat. Protoc. 2009, 4, 1582.
H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin, Bioinformatics 2009, 25, 2078.
B. Langmead, S. Salzberg, Nat. Methods 2012, 9, 357.
F. Ramirez, D. Ryan, B. Grüning, V. Bhardwaj, F. Kilpert, A. Richter, S. Heyne, F. Dündar, T. Manke, Nucleic Acids Res. 2016, 44, W160.
Y. Zhang, T. Liu, C. Meyer, J. Eeckhoute, D. Johnson, B. Bernstein, C. Nusbaum, R. Myers, M. Brown, W. Li, X. Liu, Genome Biol. 2008, 9, R137.
G. Yu, L. Wang, Q. He, Bioinformatics 2015, 31, 2382.
C. Yu, L. Wang, Y. Han, Q.-Y. He, OMICS 2012, 16, 284.
S. Wu, D. Roden, G. Al-Eryani, N. Bartonicek, K. Harvey, A. Cazet, C.-L. Chan, S. Junankar, M. Hui, E. Millar, J. Beretov, L. Horvath, A. Joshua, P. Stricker, J. Wilmott, C. Quek, G. Long, R. Scolyer, B. Yeung, D. Segara, C. Mak, S. Warrier, J. Powell, S. O'Toole, E. Lim, A. Swarbrick, Genome Med. 2021, 13, 81.
C. Curtis, S. Shah, S.-F. Chin, G. Turashvili, O. Rueda, M. Dunning, D. Speed, A. Lynch, S. Samarajiwa, Y. Yuan, S. Gräf, G. Ha, G. Haffari, A. Bashashati, R. Russell, S. McKinney, METABRIC Group, A. Langerod, A. Green, E. Provenzano, G. Wishart, S. Pinder, P. Watson, F. Markowetz, L. Murphy, I. Ellis, A. Purshotham, A.-L. Borresen-Dale, J. Brenton, S. Tavaré, C. Caldas, et al., Nature 2012, 486, 346.
B. Ru, C. Wong, Y. Tong, J. Zhong, S. Zhong, W. Wu, K. Chu, C. Wong, C. Lau, I. Chen, N. Chan, J. Zhang, Bioinformatics 2019, 35, 4200.