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Published in: Tumor Biology 5/2016

01-05-2016 | Original Article

PGC-1β regulates HER2-overexpressing breast cancer cells proliferation by metabolic and redox pathways

Authors: Vanessa Jacob Victorino, W. A. Barroso, A. K. M. Assunção, V. Cury, I. C. Jeremias, R. Petroni, B. Chausse, S. K. Ariga, A. C. S. A. Herrera, C. Panis, T. M. Lima, H. P. Souza

Published in: Tumor Biology | Issue 5/2016

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Abstract

Breast cancer is a prevalent neoplastic disease among women worldwide which treatments still present several side effects and resistance. Considering that cancer cells present derangements in their energetic homeostasis, and that peroxisome proliferator-activated receptor- gamma coactivator 1 (PGC-1) is crucial for cellular metabolism and redox signaling, the main objective of this study was to investigate whether there is a relationship between PGC-1 expression, the proliferation of breast cancer cells and the mechanisms involved. We initially assessed PGC-1β expression in complementary DNA (cDNA) from breast tumor of patients bearing luminal A, luminal B, and HER2-overexpressed and triple negative tumors. Our data showed that PGC-1β expression is increased in patients bearing HER2-overexpressing tumors as compared to others subtypes. Using quantitative PCR and immunoblotting, we showed that breast cancer cells with HER2-amplification (SKBR-3) have greater expression of PGC-1β as compared to a non-tumorous breast cell (MCF-10A) and higher proliferation rate. PGC-1β expression was knocked down with short interfering RNA in HER2-overexpressing cells, and cells decreased proliferation. In these PGC-1β-inhibited cells, we found increased citrate synthase activity and no marked changes in mitochondrial respiration. Glycolytic pathway was decreased, characterized by lower intracellular lactate levels. In addition, after PGC-1β knockdown, SKBR-3 cells showed increased reactive oxygen species production, no changes in antioxidant activity, and decreased expression of ERRα, a modulator of metabolism. In conclusion, we show an association of HER2-overexpression and PGC-1β. PGC-1β knockdown impairs HER2-overexpressing cells proliferation acting on ERRα signaling, metabolism, and redox balance.
Literature
2.
go back to reference Untch M, Gerber B, Harbeck N, Jackisch C, Marschner N, Möbus V, et al. 13th st. Gallen International Breast Cancer Conference 2013: primary therapy of early breast cancer evidence, controversies, consensus—opinion of a German team of experts (Zurich 2013). Breast Care (Basel). 2013;8(3):221–9. doi:10.1159/000351692. Untch M, Gerber B, Harbeck N, Jackisch C, Marschner N, Möbus V, et al. 13th st. Gallen International Breast Cancer Conference 2013: primary therapy of early breast cancer evidence, controversies, consensus—opinion of a German team of experts (Zurich 2013). Breast Care (Basel). 2013;8(3):221–9. doi:10.​1159/​000351692.
3.
4.
go back to reference Victorino VJ, Pizzatti L, Michelletti P, Panis C. Oxidative stress, redox signaling and cancer chemoresistance: putting together the pieces of the puzzle. Curr Med Chem. 2014;21(28):3211–26. Victorino VJ, Pizzatti L, Michelletti P, Panis C. Oxidative stress, redox signaling and cancer chemoresistance: putting together the pieces of the puzzle. Curr Med Chem. 2014;21(28):3211–26.
6.
go back to reference Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spielgman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92:829–39.CrossRefPubMed Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spielgman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92:829–39.CrossRefPubMed
7.
go back to reference Lin J, Handschin C, Spielgman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1(6):361–70.CrossRefPubMed Lin J, Handschin C, Spielgman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1(6):361–70.CrossRefPubMed
8.
9.
go back to reference Jones AWE, Yao Z, Vicencio JM, Wieckowska AK, Szabadkai G. PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria–nucleus signalling. Mitochondrion. 2012;12:86–99. doi:10.1016/j.mito.2011.09.009.CrossRefPubMed Jones AWE, Yao Z, Vicencio JM, Wieckowska AK, Szabadkai G. PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria–nucleus signalling. Mitochondrion. 2012;12:86–99. doi:10.​1016/​j.​mito.​2011.​09.​009.CrossRefPubMed
10.
go back to reference Vazquez F, Lim JH, Chim H, Bhalla K, Girnun G, Pierce K, et al. PGC1α expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell. 2013;23:287–301.CrossRefPubMedPubMedCentral Vazquez F, Lim JH, Chim H, Bhalla K, Girnun G, Pierce K, et al. PGC1α expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell. 2013;23:287–301.CrossRefPubMedPubMedCentral
11.
go back to reference Victorino VJ, Campos FC, Herrera AC, Colado Simão AN, Cecchini AL, Panis C, et al. Overexpression of HER-2/neu protein attenuates the oxidative systemic profile in women diagnosed with breast cancer. Tumour Biol. 2014;35(4):3025–34. doi:10.1007/s13277-013-1391-x.CrossRefPubMed Victorino VJ, Campos FC, Herrera AC, Colado Simão AN, Cecchini AL, Panis C, et al. Overexpression of HER-2/neu protein attenuates the oxidative systemic profile in women diagnosed with breast cancer. Tumour Biol. 2014;35(4):3025–34. doi:10.​1007/​s13277-013-1391-x.CrossRefPubMed
12.
go back to reference Bradford MM. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54.CrossRefPubMed Bradford MM. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54.CrossRefPubMed
13.
go back to reference Panis C, Pizzatti L, Herrera ACSA, Cecchini R, Abdelhay E. Putative circulating markers of the early and advanced stages of breast cancer identified by high-resolution label-free proteomics. Cancer Letters. 2013;330:57–66.CrossRefPubMed Panis C, Pizzatti L, Herrera ACSA, Cecchini R, Abdelhay E. Putative circulating markers of the early and advanced stages of breast cancer identified by high-resolution label-free proteomics. Cancer Letters. 2013;330:57–66.CrossRefPubMed
14.
15.
go back to reference Chausse B, Solon C, da Silva CC C, Masselli Dos Reis IG, Manchado-Gobatto FB, Gobatto CA, et al. Intermittent fasting induces hypothalamic modifications resulting in low feeding efficiency, low body mass and overeating. Endocrinology. 2014;155(7):2456–66. doi:10.1210/en.2013-2057.CrossRefPubMed Chausse B, Solon C, da Silva CC C, Masselli Dos Reis IG, Manchado-Gobatto FB, Gobatto CA, et al. Intermittent fasting induces hypothalamic modifications resulting in low feeding efficiency, low body mass and overeating. Endocrinology. 2014;155(7):2456–66. doi:10.​1210/​en.​2013-2057.CrossRefPubMed
16.
go back to reference Panis C, Victorino VJ, Herrera AC, Freitas LF, De Rossi T, Campos FC, et al. Differential oxidative status and immune characterization of the early and advanced stages of human breast cancer. Breast Cancer Res Treat. 2012;133(3):881–8. doi:10.1007/s10549-011-1851-1.CrossRefPubMed Panis C, Victorino VJ, Herrera AC, Freitas LF, De Rossi T, Campos FC, et al. Differential oxidative status and immune characterization of the early and advanced stages of human breast cancer. Breast Cancer Res Treat. 2012;133(3):881–8. doi:10.​1007/​s10549-011-1851-1.CrossRefPubMed
22.
go back to reference St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006;127:397–408.CrossRefPubMed St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006;127:397–408.CrossRefPubMed
24.
go back to reference Deblois G, Hall JA, Perry MC, Laganière J, Ghahremani M, Park M, et al. Genome-wide identification of direct target genes implicates estrogen-related receptor alpha as a determinant of breast cancer heterogeneity. Cancer Res. 2009;69(15):6149–57. doi:10.1158/0008-5472.CAN-09-1251.CrossRefPubMed Deblois G, Hall JA, Perry MC, Laganière J, Ghahremani M, Park M, et al. Genome-wide identification of direct target genes implicates estrogen-related receptor alpha as a determinant of breast cancer heterogeneity. Cancer Res. 2009;69(15):6149–57. doi:10.​1158/​0008-5472.​CAN-09-1251.CrossRefPubMed
25.
go back to reference Schreiber SN, Knutti D, Brogli K, Uhlmann T, Kralli A. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptorestrogen-related receptor alpha (ERRalpha). J Biol Chem. 2003;278(11):9013–8.CrossRefPubMed Schreiber SN, Knutti D, Brogli K, Uhlmann T, Kralli A. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptorestrogen-related receptor alpha (ERRalpha). J Biol Chem. 2003;278(11):9013–8.CrossRefPubMed
Metadata
Title
PGC-1β regulates HER2-overexpressing breast cancer cells proliferation by metabolic and redox pathways
Authors
Vanessa Jacob Victorino
W. A. Barroso
A. K. M. Assunção
V. Cury
I. C. Jeremias
R. Petroni
B. Chausse
S. K. Ariga
A. C. S. A. Herrera
C. Panis
T. M. Lima
H. P. Souza
Publication date
01-05-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 5/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-4449-0

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