EGFR signaling enhances aerobic glycolysis in triple-negative breast cancer cells to promote tumor growth and immune escape

Cancer Research

Volumn 76, Issue 5, 2016, Pages 1284-1296

  Lim, Seung Oe ^a   Li, Chia Wei ^a   Xia, Weiya ^a   Lee, Heng Huan ^a   Chang, Shih Shin ^a,b   Shen, Jia ^a   Hsu, Jennifer L ^a   Raftery, Daniel ^c,d   Djukovic, Danijel ^c   Gu, Haiwei ^c   Chang, Wei Chao ^e,f   Wang, Hung Ling ^e   Chen, Mong Liang ^e   Huo, Longfei ^a   Chen, Chung Hsuan ^f   Wu, Yun ^g   Sahin, Aysegul ^g   Hanash, Samir M ^d,g   Hortobagyi, Gabriel N ^g   Hung, Mien Chie ^a,b,e,h  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d USA   (United States)

^e CHINA MEDICAL UNIVERSITY   (Taiwan)

^f GENOMICS RESEARCH CENTER   (Taiwan)

^g UNIVERSITY OF TEXAS   (United States)

^h ASIA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYGLUCOSE; EPIDERMAL GROWTH FACTOR RECEPTOR; FRUCTOSE 1,6 BISPHOSPHATE; GEFITINIB; LACTIC ACID; PYRUVATE KINASE; EGFR PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER CELL LINE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL ACTIVITY; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; GLYCOLYSIS; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNE ESCAPE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; TUMOR ESCAPE; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; AEROBIC METABOLISM; ANIMAL; BAGG ALBINO MOUSE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

AEROBIOSIS; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GLYCOLYSIS; HUMANS; MICE; MICE, INBRED BALB C; PYRUVATE KINASE; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR ESCAPE;

EID: 84961825288     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2478     Document Type: Article

References (48)

1. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
2. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
3. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012;21:297-308.
4. Dang CV. Links between metabolism and cancer. Genes Dev 2012;26:877-90.
5. Fang R, Xiao T, Fang Z, Sun Y, Li F, Gao Y, et al. MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J Biol Chem 2012;287:23227-35.
6. Mathupala SP, Ko YH, Pedersen PL. Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper ofmalignancy when bound to mitochondria. Oncogene 2006;25:4777-86.
7. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008;452:230-3.
8. Dombrauckas JD, Santarsiero BD, Mesecar AD. Structural basis for tumor pyruvate kinase M2 allosteric regulation and catalysis. Biochemistry 2005;44:9417-29.
9. Mazurek S, Boschek CB, Hugo F, Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin Cancer Biol 2005;15:300-8.
10. Mazurek S. Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. Int J Biochem Cell Biol 2011;43:969-80.
11. Joyce JA, Fearon DT. T cell exclusion, immune privilege, and the tumor microenvironment. Science 2015;348:74-80.
12. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252-64.
13. Pollizzi KN, Powell JD. Integrating canonical and metabolic signalling programmes in the regulation of T cell responses. Nat Rev Immunol 2014;14:435-46.
14. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011;35:871-82.
15. Pearce EL, Poffenberger MC, Chang CH, Jones RG. Fueling immunity: insights into metabolism and lymphocyte function. Science 2013;342:1242454.
16. Doherty JR, Cleveland JL. Targeting lactate metabolism for cancer therapeutics. J Clin Invest 2013;123:3685-92.
17. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010;141:1117-34.
18. Carey L, Winer E, Viale G, Cameron D, Gianni L. Triple-negative breast cancer: disease entity or title of convenience? Nat Rev Clin Oncol 2010;7:683-92.
19. Gazinska P, Grigoriadis A, Brown JP, Millis RR, Mera A, Gillett CE, et al. Comparison of basal-like triple-negative breast cancer defined by morphology, immunohistochemistry and transcriptional profiles. Mod Pathol 2013;26:955-66.
20. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011;121:2750-67.
21. Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol 2008;26:2568-81.
22. Metzger-Filho O, Tutt A, De Azambuja E, Saini KS, Viale G, Loi S, et al. Dissecting the heterogeneity of triple-negative breast cancer. J Clin Oncol 2012;30:1879-87.
23. Dickler MN, Cobleigh MA, Miller KD, Klein PM, Winer EP. Efficacy and safety of erlotinib in patients with locally advanced or metastatic breast cancer. Breast Cancer Res Treat 2009;115:115-21.
24. Mueller KL, Yang ZQ, Haddad R, Ethier SP, Boerner JL. EGFR/Met association regulates EGFR TKI resistance in breast cancer. J Mol Signal 2010;5:8.
25. Carey LA, Rugo HS, Marcom PK, Mayer EL, Esteva FJ, Ma CX, et al. TBCRC 001: randomized phase II study of cetuximab in combination with carboplatin in stage IV triple-negative breast cancer. J Clin Oncol 2012;30:2615-23.
26. Scaltriti M, Baselga J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res 2006;12:5268-72.
27. Kaplan O, Jaroszewski JW, Faustino PJ, Zugmaier G, Ennis BW, Lippman M, et al. Toxicity and effectsof epidermal growth factor on glucose metabolism of MDA-468 human breast cancer cells. J Biol Chem 1990;265:13641-9.
28. Baulida J, Onetti R, Bassols A. Effects of epidermal growth factor on glycolysis in A431 cells. Biochem Biophys Res Commun 1992;183:1216-23.
29. Yang W, Xia Y, Ji H, Zheng Y, Liang J, Huang W, et al. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature 2011;480:118-22.
30. Yang W, Xia Y, Hawke D, Li X, Liang J, Xing D, et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 2012;150:685-96.
31. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008;135:2128-40.
32. Xia W, Wei Y, Du Y, Liu J, Chang B, Yu YL, et al. Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Mol Carcinog 2009;48:610-7.
33. Lang JY, Hsu JL, Meric-Bernstam F, Chang CJ, Wang Q, Bao Y, et al. BikDD eliminates breast cancer initiating cells and synergizes with lapatinib for breast cancer treatment. Cancer Cell 2011;20:341-56.
34. Sheppard KA, Fitz LJ, Lee JM, Benander C, George JA, Wooters J, et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 2004;574:37-41.
35. Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, et al. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013;497:383-7.
36. Huo L, Wang YN, Xia W, Hsu SC, Lai CC, Li LY, et al. RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc Natl Acad Sci U S A 2010;107:16125-30.
37. Anastasiou D, Poulogiannis G, Asara JM, Boxer MB, Jiang JK, Shen M, et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011;334:1278-83.
38. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2009;2:ra73.
39. Aghaee F, Pirayesh Islamian J, Baradaran B. Enhanced radiosensitivity and chemosensitivity of breast cancer cells by 2-deoxy-d-glucose in combination therapy. J Breast Cancer 2012;15:141-7.
40. Dwarakanath BS, Singh D, Banerji AK, Sarin R, Venkataramana NK, Jalali R, et al. Clinical studies for improving radiotherapy with 2-deoxy-D-glucose: present status and future prospects. J Cancer Res Ther 2009;5 Suppl 1:S21-6.
41. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 2011;10:671-84.
42. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 2007;109:3812-9.
43. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010;463:364-8.
44. Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H, et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperonemediated autophagy and promotes tumor growth. Mol Cell 2011;42:719-30.
45. Anastasiou D, Yu Y, Israelsen WJ, Jiang JK, Boxer MB, Hong BS, et al. Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis. Nat Chem Biol 2012;8:839-47.
46. Goldberg MS, Sharp PA. Pyruvate kinase M2-specific siRNA induces apoptosis and tumor regression. J Exp Med 2012;209:217-24.
47. Dong C, Yuan T, Wu Y, Wang Y, Fan TW, Miriyala S, et al. Loss of FBP1 by Snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell 2013;23:316-31.
48. Li B, Qiu B, Lee DS, Walton ZE, Ochocki JD, Mathew LK, et al. Fructose-1, 6-bisphosphatase opposes renal carcinoma progression. Nature 2014;513:251-5.