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Research Paper - Basic Science

Improved efficacy of mitochondrial disrupting agents upon inhibition of autophagy in a mouse model of BRCA1-deficient breast cancer

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Pages 1214-1225 | Received 12 Jun 2017, Accepted 26 Mar 2018, Published online: 20 Jul 2018

References

  • Birgisdottir V, Stefansson OA, Bodvarsdottir SK, et al. Epigenetic silencing and deletion of the BRCA1 gene in sporadic breast cancer. Breast Cancer Res. 2006;8(4):R38. PubMed PMID: 16846527; PubMed Central PMCID: PMC1779478. eng.
  • Lord CJ, Ashworth A. BRCAness revisited. Nat Rev Cancer. 2016 Feb;16(2):110–120. PubMed PMID: 26775620; eng.
  • Venkitaraman AR. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell. 2002 Jan;108(2):171–182. PubMed PMID: 11832208; eng.
  • Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003 Jul;100(14):8418–8423. PubMed PMID: 12829800; PubMed Central PMCID: PMCPMC166244. eng.
  • Lim E, Vaillant F, Wu D, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med. 2009 Aug;15(8):907–913. PubMed PMID: 19648928; eng.
  • Nolan E, Vaillant F, Branstetter D, et al. RANK ligand as a potential target for breast cancer prevention in BRCA1-mutation carriers. Nat Med. 2016 Aug;22(8):933–939. PubMed PMID: 27322743; eng.
  • Proia TA, Keller PJ, Gupta PB, et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell. 2011 Feb;8(2):149–163. PubMed PMID: 21295272; PubMed Central PMCID: PMCPMC3050563. eng.
  • Sau A, Lau R, Cabrita MA, et al. Persistent Activation of NF-κB in BRCA1-Deficient Mammary Progenitors Drives Aberrant Proliferation and Accumulation of DNA Damage. Cell Stem Cell. 2016 Jul;19(1):52–65. PubMed PMID: 27292187; eng.
  • Sawyer SL, Tian L, Kähkönen M, et al. Biallelic mutations in BRCA1 cause a new Fanconi anemia subtype. Cancer Discov. 2015 Feb;5(2):135–142. PubMed PMID: 25472942; PubMed Central PMCID: PMCPMC4320660. eng.
  • Sedic M, Skibinski A, Brown N, et al. Haploinsufficiency for BRCA1 leads to cell-type-specific genomic instability and premature senescence. Nat Commun. 2015 Jun;6:7505. PubMed PMID: 26106036; PubMed Central PMCID: PMCPMC4491827. eng.
  • Gorrini C, Baniasadi PS, Harris IS, et al. BRCA1 interacts with Nrf2 to regulate antioxidant signaling and cell survival. J Exp Med. 2013 Jul;210(8):1529–1544. PubMed PMID: 23857982; PubMed Central PMCID: PMCPMC3727320. eng.
  • Gorrini C, Gang BP, Bassi C, et al. Estrogen controls the survival of BRCA1-deficient cells via a PI3K-NRF2-regulated pathway. Proc Natl Acad Sci U S A. 2014 Mar;111(12):4472–4477. PubMed PMID: 24567396; PubMed Central PMCID: PMCPMC3970526. eng.
  • Martinez-Outschoorn UE, Balliet R, Lin Z, et al. BRCA1 mutations drive oxidative stress and glycolysis in the tumor microenvironment: implications for breast cancer prevention with antioxidant therapies. Cell Cycle. 2012 Dec;11(23):4402–4413. PubMed PMID: 23172369; PubMed Central PMCID: PMCPMC3552923. eng.
  • Cuyàs E, Fernández-Arroyo S, Alarcón T, et al. Germline BRCA1 mutation reprograms breast epithelial cell metabolism towards mitochondrial-dependent biosynthesis: evidence for metformin-based “starvation” strategies in BRCA1 carriers. Oncotarget. 2016 May. PubMed PMID: 27259235; ENG. DOI:10.18632/oncotarget.9732
  • Sumpter R, Sirasanagandla S, Fernández Á, et al. Fanconi Anemia Proteins Function in Mitophagy and Immunity. Cell. 2016 May;165(4):867–881. PubMed PMID: 27133164; PubMed Central PMCID: PMCPMC4881391. eng.
  • Brunet J, Vazquez-Martin A, Colomer R, et al. BRCA1 and acetyl-CoA carboxylase: the metabolic syndrome of breast cancer. Mol Carcinog. 2008 Feb;47(2):157–163. PubMed PMID: 17620310; eng.
  • Moreau K, Dizin E, Ray H, et al. BRCA1 affects lipid synthesis through its interaction with acetyl-CoA carboxylase. J Biol Chem. 2006 Feb;281(6):3172–3181. PubMed PMID: 16326698; eng.
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728–741.
  • Lock R, Roy S, Kenific CM, et al. Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol Biol Cell. 2011 Jan;22(2):165–178. PubMed PMID: 21119005; PubMed Central PMCID: PMCPMC3020913. eng.
  • Guo JY, Teng X, Laddha SV, et al. Autophagy provides metabolic substrates to maintain energy charge and nucleotide pools in Ras-driven lung cancer cells. Genes Dev. 2016 Aug;30(15):1704–1717. PubMed PMID: 27516533; PubMed Central PMCID: PMCPMC5002976. eng.
  • Karantza-Wadsworth V, Patel S, Kravchuk O, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 2007 Jul;21(13):1621–1635. PubMed PMID: 17606641; PubMed Central PMCID: PMCPMC1899472. eng.
  • Strohecker AM, White E. Autophagy promotes BrafV600E-driven lung tumorigenesis by preserving mitochondrial metabolism. Autophagy. 2014 Feb;10(2):384–385. PubMed PMID: 24362353; eng.
  • Wei H, Wei S, Gan B, et al. Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev. 2011;25:1510–1527.
  • White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer. 2012 Jun;12(6):401–410. PubMed PMID: 22534666; PubMed Central PMCID: PMCPMC3664381. eng.
  • Cicchini M, Chakrabarti R, Kongara S, et al. Autophagy regulator BECN1 suppresses mammary tumorigenesis driven by WNT1 activation and following parity. Autophagy. 2014;10(11):2036–2052. PubMed PMID: 25483966; PubMed Central PMCID: PMCPMC4502817. eng.
  • Huo Y, Cai H, Teplova I, et al. Autophagy opposes p53-mediated tumor barrier to facilitate tumorigenesis in a model of PALB2-associated hereditary breast cancer. Cancer Discov. 2013 Aug;3(8):894–907. PubMed PMID: 23650262; PubMed Central PMCID: PMCPMC3740014. eng.
  • Lozy F, Cai-McRae X, Teplova I, et al. ERBB2 overexpression suppresses stress-induced autophagy and renders ERBB2-induced mammary tumorigenesis independent of monoallelic Becn1 loss. Autophagy. 2014 Apr;10(4):662–676. PubMed PMID: 24492513; PubMed Central PMCID: PMCPMC4091153. eng.
  • Liu X, Holstege H, Van Der Gulden H, et al. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc Natl Acad Sci U S A. 2007 Jul;104(29):12111–12116. PubMed PMID: 17626182; PubMed Central PMCID: PMCPMC1924557. ENG.
  • Cunningham JT, Rodgers JT, Arlow DH, et al. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature. 2007 Nov;450(7170):736–740. PubMed PMID: 18046414; eng.
  • Morita M, Gravel SP, Chénard V, et al. mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation. Cell Metab. 2013 Nov;18(5):698–711. PubMed PMID: 24206664; eng.
  • Sulkowski PL, Corso CD, Robinson ND, et al. 2-Hydroxyglutarate produced by neomorphic IDH mutations suppresses homologous recombination and induces PARP inhibitor sensitivity. Sci Transl Med. 2017 Feb;9(375). PubMed PMID: 28148839; eng. DOI:10.1126/scitranslmed.aal2463
  • Lu Y, Kwintkiewicz J, Liu Y, et al. Chemosensitivity of IDH1-Mutated Gliomas Due to an Impairment in PARP1-Mediated DNA Repair. Cancer Res. 2017 Apr;77(7):1709–1718. PubMed PMID: 28202508; PubMed Central PMCID: PMCPMC5380481. eng.
  • Chourasia AH, Tracy K, Frankenberger C, et al. Mitophagy defects arising from BNip3 loss promote mammary tumor progression to metastasis. EMBO Rep. 2015 Sep;16(9):1145–1163. PubMed PMID: 26232272; PubMed Central PMCID: PMCPMC4576983. eng.
  • Oliveras-Ferraros C, Vazquez-Martin A, Cuyàs E, et al. Acquired resistance to metformin in breast cancer cells triggers transcriptome reprogramming toward a degradome-related metastatic stem-like profile. Cell Cycle. 2014;13(7):1132–1144. PubMed PMID: 24553122; PubMed Central PMCID: PMCPMC4013163. eng.
  • Janzer A, German NJ, Gonzalez-Herrera KN, et al. Metformin and phenformin deplete tricarboxylic acid cycle and glycolytic intermediates during cell transformation and NTPs in cancer stem cells. Proc Natl Acad Sci U S A. 2014 Jul;111(29):10574–10579. PubMed PMID: 25002509; PubMed Central PMCID: PMCPMC4115496. eng.
  • Wu L, Zhou B, Oshiro-Rapley N, et al. An ancient, unified mechanism for metformin growth inhibition in C. elegans and cancer. Cell. 2016 Dec;167(7):1705–1718.e13. PubMed PMID: 27984722; eng.
  • Goodwin PJ, Parulekar WR, Gelmon KA, et al. Effect of metformin vs placebo on and metabolic factors in NCIC CTG MA.32. J Natl Cancer Inst. 2015 Mar;107(3). PubMed PMID: 25740979; PubMed Central PMCID: PMCPMC4565534. eng. DOI:10.1093/jnci/djv006
  • Lalau JD, Lemaire-Hurtel AS, Lacroix C. Establishment of a database of metformin plasma concentrations and erythrocyte levels in normal and emergency situations. Clin Drug Investig. 2011;31(6):435–438. PubMed PMID: 21401215; eng.
  • Hirsch HA, Iliopoulos D, Tsichlis PN, et al. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res. 2009 Oct;69(19):7507–7511. PubMed PMID: 19752085; PubMed Central PMCID: PMCPMC2756324. eng.
  • Brooks MD, Burness ML, Wicha MS. Therapeutic implications of cellular heterogeneity and plasticity in breast cancer. Cell Stem Cell. 2015 Sep;17(3):260–271. PubMed PMID: 26340526; PubMed Central PMCID: PMCPMC4560840. eng.
  • Yeo SK, Wen J, Chen S, et al. Autophagy differentially regulates distinct breast cancer stem-like cells in murine models via EGFR/Stat3 and Tgfβ/Smad Signaling. Cancer Res. 2016 Jun;76(11):3397–3410. PubMed PMID: 27197172; PubMed Central PMCID: PMCPMC4990205. eng.
  • Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, et al. Autophagy positively regulates the CD44(+) CD24(-/low) breast cancer stem-like phenotype. Cell Cycle. 2011;10(22):3871–3885.
  • Gong C, Bauvy C, Tonelli G, et al. Beclin1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene. 2013;32(18):2261–2272.
  • Maycotte P, Jones KL, Goodall ML, et al. Autophagy supports breast cancer stem cell maintenance by regulating IL6 secretion. Mol Cancer Res. 2015 Apr;13(4):651–658. 10.1158/1541-7786.MCR-14-0487. PubMed PMID: 25573951; eng.
  • Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999 Dec;402(6762):672–676. PubMed PMID: 10604474; eng.
  • Qu X, Yu J, Bhagat G, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003 Dec;112(12):1809–1820. PubMed PMID: 14638851; PubMed Central PMCID: PMCPMC297002. eng.
  • Laddha SV, Ganesan S, Chan CS, et al. Mutational landscape of the essential autophagy gene BECN1 in human cancers. Mol Cancer Res. 2014 Apr;12(4):485–490. 10.1158/1541-7786.MCR-13-0614. PubMed PMID: 24478461; PubMed Central PMCID: PMCPMC3989371. eng.
  • Chen S, Wang C, Yeo S, et al. Distinct roles of autophagy-dependent and -independent functions of FIP200 revealed by generation and analysis of a mutant knock-in mouse model. Genes Dev. 2016 Apr;30(7):856–869. PubMed PMID: 27013233; PubMed Central PMCID: PMCPMC4826400. eng.
  • Wei H, Gan B, Wu X, et al. Inactivation of FIP200 leads to inflammatory skin disorder, but not tumorigenesis, in conditional knock-out mouse models. J Biol Chem. 2009 Feb;284(9):6004–6013. PubMed PMID: 19106106; PubMed Central PMCID: PMCPMC2645843. eng.
  • Bonnard C, Durand A, Peyrol S, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest. 2008 Feb;118(2):789–800. PubMed PMID: 18188455; PubMed Central PMCID: PMCPMC2176186. eng.
  • Wu M, Neilson A, Swift AL, et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol. 2007 Jan;292(1):C125–36. PubMed PMID: 16971499; eng.

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