Metabolic heterogeneity and immunocompetence of infiltrating immune cells in the breast cancer microenvironment (Review)
- Authors:
- Hongdan Chen
- Yizeng Sun
- Zeyu Yang
- Supeng Yin
- Yao Li
- Mi Tang
- Junping Zhu
- Fan Zhang
-
Affiliations: Department of Breast and Thyroid Surgery, Chongqing General Hospital, University of Chinese Academy of Sciences, Chongqing 401147, P.R. China - Published online on: January 22, 2021 https://doi.org/10.3892/or.2021.7946
- Pages: 846-856
-
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2019. CA Cancer J Clin. 69:7–34. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vranic S, Cyprian FS, Gatalica Z and Palazzo J: PD-L1 status in breast cancer: Current view and perspectives. Semin Cancer Biol. Dec 26–2019.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Engelhard VH, Rodriguez AB, Mauldin IS, Woods AN, Peske JD and Slingluff CL Jr: Immune Cell Infiltration and tertiary lymphoid structures as determinants of antitumor immunity. J Immunol. 200:432–442. 2018. View Article : Google Scholar : PubMed/NCBI | |
Savas P, Virassamy B, Ye C, Salim A, Mintoff CP, Caramia F, Salgado R, Byrne DJ, Teo ZL, Dushyanthen S, et al: Publisher correction: Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis. Nat Med. 24:19412018. View Article : Google Scholar : PubMed/NCBI | |
Zhang SC, Hu ZQ, Long JH, Zhu GM, Wang Y, Jia Y, Zhou J, Ouyang Y and Zeng Z: Clinical implications of tumor-infiltrating immune cells in breast cancer. J Cancer. 10:6175–6184. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wu D: Innate and adaptive immune cell metabolism in tumor microenvironment. Adv Exp Med Biol. 1011:211–223. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kishton RJ, Sukumar M and Restifo NP: Metabolic regulation of T cell longevity and function in tumor immunotherapy. Cell Metab. 26:94–109. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hobson-Gutierrez SA and Carmona-Fontaine C: The metabolic axis of macrophage and immune cell polarization. Dis Model Mech. 11:dmm0344622018. View Article : Google Scholar : PubMed/NCBI | |
Warburg O: Über den Stoffwechsel der Carcinomzelle. Naturwissenschaften. 12:1131–1137. 1924. View Article : Google Scholar | |
Lane AN, Higashi RM and Fan TW: Metabolic reprogramming in tumors: Contributions of the tumor microenvironment. Genes Dis. 7:185–198. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kim J and DeBerardinis RJ: Mechanisms and implications of metabolic heterogeneity in cancer. Cell Metab. 30:434–446. 2019. View Article : Google Scholar : PubMed/NCBI | |
Mehla K and Singh PK: Metabolic regulation of macrophage polarization in cancer. Trends Cancer. 5:822–834. 2019. View Article : Google Scholar : PubMed/NCBI | |
Basit F, Mathan T, Sancho D and de Vries IJM: Human dendritic cell subsets undergo distinct metabolic reprogramming for immune response. Front Immunol. 9:24892018. View Article : Google Scholar : PubMed/NCBI | |
Zhang L and Romero P: Metabolic control of CD8(+) T cell fate decisions and antitumor immunity. Trends Mol Med. 24:30–48. 2018. View Article : Google Scholar : PubMed/NCBI | |
Poznanski SM, Barra NG, Ashkar AA and Schertzer JD: Immunometabolism of T cells and NK cells: Metabolic control of effector and regulatory function. Inflamm Res. 67:813–828. 2018. View Article : Google Scholar : PubMed/NCBI | |
Norton KA, Jin K and Popel AS: Modeling triple-negative breast cancer heterogeneity: Effects of stromal macrophages, fibroblasts and tumor vasculature. J Theor Biol. 452:56–68. 2018. View Article : Google Scholar : PubMed/NCBI | |
Skala MC, Fontanella A, Lan L, Izatt JA and Dewhirst MW: Longitudinal optical imaging of tumor metabolism and hemodynamics. J Biomed Opt. 15:0111122010. View Article : Google Scholar : PubMed/NCBI | |
Roulot A, Héquet D, Guinebretière JM, Vincent-Salomon A, Lerebours F, Dubot C and Rouzier R: Tumoral heterogeneity of breast cancer. Ann Biol Clin (Paris). 74:653–660. 2016.PubMed/NCBI | |
Carmona-Fontaine C, Deforet M, Akkari L, Thompson CB, Joyce JA and Xavier JB: Metabolic origins of spatial organization in the tumor microenvironment. Proc Natl Acad Sci USA. 114:2934–2939. 2017. View Article : Google Scholar : PubMed/NCBI | |
Montcourrier P, Silver I, Farnoud R, Bird I and Rochefort H: Breast cancer cells have a high capacity to acidify extracellular milieu by a dual mechanism. Clin Exp Metastasis. 15:382–392. 1997. View Article : Google Scholar : PubMed/NCBI | |
Logozzi M, Spugnini E, Mizzoni D, Di Raimo R and Fais S: Extracellular acidity and increased exosome release as key phenotypes of malignant tumors. Cancer Metastasis Rev. 38:93–101. 2019. View Article : Google Scholar : PubMed/NCBI | |
Gao T, Li JZ, Lu Y, Zhang CY, Li Q, Mao J and Li LH: The mechanism between epithelial mesenchymal transition in breast cancer and hypoxia microenvironment. Biomed Pharmacother. 80:393–405. 2016. View Article : Google Scholar : PubMed/NCBI | |
Liu ZJ, Semenza GL and Zhang HF: Hypoxia-inducible factor 1 and breast cancer metastasis. J Zhejiang Univ Sci B. 16:32–43. 2015. View Article : Google Scholar : PubMed/NCBI | |
Daşu A, Toma-Daşu I and Karlsson M: Theoretical simulation of tumour oxygenation and results from acute and chronic hypoxia. Phys Med Biol. 48:2829–2842. 2003. View Article : Google Scholar : PubMed/NCBI | |
Mantovani A, Allavena P, Sica A and Balkwill F: Cancer-related inflammation. Nature. 454:436–444. 2008. View Article : Google Scholar : PubMed/NCBI | |
Byrne A, Savas P, Sant S, Li R, Virassamy B, Luen SJ, Beavis PA, Mackay LK, Neeson PJ and Loi S: Tissue-resident memory T cells in breast cancer control and immunotherapy responses. Nat Rev Clin Oncol. 17:341–348. 2020. View Article : Google Scholar : PubMed/NCBI | |
Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR, Elstrom RL, June CH and Thompson CB: The CD28 signaling pathway regulates glucose metabolism. Immunity. 16:769–777. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kamiński MM, Sauer SW, Kamiński M, Opp S, Ruppert T, Grigaravičius P, Grudnik P, Gröne HJ, Krammer PH and Gülow K: T cell activation is driven by an ADP-dependent glucokinase linking enhanced glycolysis with mitochondrial reactive oxygen species generation. Cell Rep. 2:1300–1315. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gentric G, Mieulet V and Mechta-Grigoriou F: Heterogeneity in cancer metabolism: New concepts in an old field. Antioxid Redox Signal. 26:462–485. 2017. View Article : Google Scholar : PubMed/NCBI | |
MacPherson S, Kilgour M and Lum JJ: Understanding lymphocyte metabolism for use in cancer immunotherapy. FEBS J. 285:2567–2578. 2018. View Article : Google Scholar : PubMed/NCBI | |
Michalek RD, Gerriets VA, Jacobs SR, Macintyre AN, MacIver NJ, Mason EF, Sullivan SA, Nichols AG and Rathmell JC: Cutting edge: Distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol. 186:3299–3303. 2011. View Article : Google Scholar : PubMed/NCBI | |
Berod L, Friedrich C, Nandan A, Freitag J, Hagemann S, Harmrolfs K, Sandouk A, Hesse C, Castro CN, Bähre H, et al: De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat Med. 20:1327–1333. 2014. View Article : Google Scholar : PubMed/NCBI | |
Phan AT and Goldrath AW: Hypoxia-inducible factors regulate T cell metabolism and function. Mol Immunol. 68:527–535. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim JW, Tchernyshyov I, Semenza GL and Dang CV: HIF-1-mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3:177–185. 2006. View Article : Google Scholar : PubMed/NCBI | |
Westendorf AM, Skibbe K, Adamczyk A, Buer J, Geffers R, Hansen W, Pastille E and Jendrossek V: Hypoxia enhances immunosuppression by inhibiting CD4+ effector T cell function and promoting treg activity. Cell Physiol Biochem. 41:1271–1284. 2017. View Article : Google Scholar : PubMed/NCBI | |
Molon B, Calì B and Viola A: T cells and cancer: How metabolism shapes immunity. Front Immunol. 7:202016. View Article : Google Scholar : PubMed/NCBI | |
Mack N, Mazzio EA, Bauer D, Flores-Rozas H and Soliman KF: Stable shRNA silencing of lactate dehydrogenase A (LDHA) in human MDA-MB-231 breast cancer cells fails to alter lactic acid production, glycolytic activity, ATP or survival. Anticancer Res. 37:1205–1212. 2017. View Article : Google Scholar : PubMed/NCBI | |
Siska PJ and Rathmell JC: T cell metabolic fitness in antitumor immunity. Trends Immunol. 36:257–264. 2015. View Article : Google Scholar : PubMed/NCBI | |
Peppicelli S, Toti A, Giannoni E, Bianchini F, Margheri F, Del Rosso M and Calorini L: Metformin is also effective on lactic acidosis-exposed melanoma cells switched to oxidative phosphorylation. Cell Cycle. 15:1908–1918. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, Gottfried E, Schwarz S, Rothe G, Hoves S, et al: Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood. 109:3812–3819. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ho PC, Bihuniak JD, Macintyre AN, Staron M, Liu X, Amezquita R, Tsui YC, Cui G, Micevic G, Perales JC, et al: Phosphoenolpyruvate Is a metabolic checkpoint of anti-tumor t cell responses. Cell. 162:1217–1228. 2015. View Article : Google Scholar : PubMed/NCBI | |
Beckermann KE, Dudzinski SO and Rathmell JC: Dysfunctional T cell metabolism in the tumor microenvironment. Cytokine Growth Factor Rev. 35:7–14. 2017. View Article : Google Scholar : PubMed/NCBI | |
Neugent ML, Goodwin J, Sankaranarayanan I, Yetkin CE, Hsieh MH and Kim JW: A new perspective on the heterogeneity of cancer glycolysis. Biomol Ther (Seoul). 26:10–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Angelin A, Gil-de-Gómez L, Dahiya S, Jiao J, Guo L, Levine MH, Wang Z, Quinn WJ III, Kopinski PK, Wang L, et al: Foxp3 reprograms T cell metabolism to function in low-glucose, high-lactate environments. Cell Metab. 25:1282–1293.e7. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hao Y, Li D, Xu Y, Ouyang J, Wang Y, Zhang Y, Li B, Xie L and Qin G: Investigation of lipid metabolism dysregulation and the effects on immune microenvironments in pan-cancer using multiple omics data. BMC Bioinformatics. 20 (Suppl 7):S1952019. View Article : Google Scholar | |
Saleh R and Elkord E: FoxP3+ T regulatory cells in cancer: Prognostic biomarkers and therapeutic targets. Cancer Lett. 490:174–185. 2020. View Article : Google Scholar : PubMed/NCBI | |
Iranparast S, Tayebi S, Ahmadpour F and Yousefi B: Tumor-Induced metabolism and T cells located in tumor environment. Curr Cancer Drug Targets. 20:741–756. 2020. View Article : Google Scholar : PubMed/NCBI | |
Shang W, Xu R, Xu T, Wu M, Xu J and Wang F: Ovarian cancer cells promote glycolysis metabolism and TLR8-mediated metabolic control of human CD4+ T cells. Front Oncol. 10:5708992020. View Article : Google Scholar : PubMed/NCBI | |
Vardhana SA, Hwee MA, Berisa M, Wells DK, Yost KE, King B, Smith M, Herrera PS, Chang HY, Satpathy AT, et al: Impaired mitochondrial oxidative phosphorylation limits the self-renewal of T cells exposed to persistent antigen. Nat Immunol. 21:1022–1033. 2020. View Article : Google Scholar : PubMed/NCBI | |
Beier UH, Angelin A, Akimova T, Wang L, Liu Y, Xiao H, Koike MA, Hancock SA, Bhatti TR, Han R, et al: Essential role of mitochondrial energy metabolism in Foxp3+ T-regulatory cell function and allograft survival. FASEB J. 29:2315–2326. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gerriets VA, Kishton RJ, Nichols AG, Macintyre AN, Inoue M, Ilkayeva O, Winter PS, Liu X, Priyadharshini B, Slawinska ME, et al: Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J Clin Invest. 125:194–207. 2015. View Article : Google Scholar : PubMed/NCBI | |
Duan W, Ding Y, Yu X, Ma D, Yang B, Li Y, Huang L, Chen Z, Zheng J and Yang C: Metformin mitigates autoimmune insulitis by inhibiting Th1 and Th17 responses while promoting Treg production. Am J Transl Res. 11:2393–2402. 2019.PubMed/NCBI | |
Lu L, Barbi J and Pan F: The regulation of immune tolerance by FOXP3. Nat Rev Immunol. 17:703–717. 2017. View Article : Google Scholar : PubMed/NCBI | |
Georgiev P, Charbonnier LM and Chatila TA: Regulatory T cells: The many faces of Foxp3. J Clin Immunol. 39:623–640. 2019. View Article : Google Scholar : PubMed/NCBI | |
Gerriets VA, Kishton RJ, Johnson MO, Cohen S, Siska PJ, Nichols AG, Warmoes MO, de Cubas AA, MacIver NJ, Locasale JW, et al: Foxp3 and Toll-like receptor signaling balance Treg cell anabolic metabolism for suppression. Nat Immunol. 17:1459–1466. 2016. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Feng L, Li S, Long D, Shan J and Li Y: TGF-β1 maintains Foxp3 expression and inhibits glycolysis in natural regulatory T cells via PP2A-mediated suppression of mTOR signaling. Immunol Lett. 226:31–37. 2020. View Article : Google Scholar : PubMed/NCBI | |
Choi J, Gyamfi J, Jang H and Koo JS: The role of tumor-associated macrophage in breast cancer biology. Histol Histopathol. 33:133–145. 2018.PubMed/NCBI | |
Su S, Liu Q, Chen J, Chen J, Chen F, He C, Huang D, Wu W, Lin L, Huang W, et al: A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell. 25:605–620. 2014. View Article : Google Scholar : PubMed/NCBI | |
Klingen TA, Chen Y, Aas H, Wik E and Akslen LA: Tumor-associated macrophages are strongly related to vascular invasion, non-luminal subtypes, and interval breast cancer. Hum Pathol. 69:72–80. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tarique AA, Logan J, Thomas E, Holt PG, Sly PD and Fantino E: Phenotypic, functional, and plasticity features of classical and alternatively activated human macrophages. Am J Respir Cell Mol Biol. 53:676–688. 2015. View Article : Google Scholar : PubMed/NCBI | |
Geeraerts X, Bolli E, Fendt SM and Van Ginderachter JA: Macrophage metabolism as therapeutic target for cancer, atherosclerosis, and obesity. Front Immunol. 8:2892017. View Article : Google Scholar : PubMed/NCBI | |
Mantovani A, Marchesi F, Malesci A, Laghi L and Allavena P: Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 14:399–416. 2017. View Article : Google Scholar : PubMed/NCBI | |
De Santa F, Vitiello L, Torcinaro A and Ferraro E: The role of metabolic remodeling in macrophage polarization and its effect on skeletal muscle regeneration. Antioxid Redox Signal. 30:1553–1598. 2019. View Article : Google Scholar : PubMed/NCBI | |
Van den Bossche J, Baardman J, Otto NA, van der Velden S, Neele AE, van den Berg SM, Luque-Martin R, Chen HJ, Boshuizen MC, Ahmed M, et al: Mitochondrial dysfunction prevents repolarization of inflammatory macrophages. Cell Rep. 17:684–696. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kim J: Regulation of immune cell functions by metabolic reprogramming. J Immuno Res. 2018:86054712018. | |
Rodríguez-Prados JC, Través PG, Cuenca J, Rico D, Aragonés J, Martín-Sanz P, Cascante M and Boscá L: Substrate fate in activated macrophages: A comparison between innate, classic, and alternative activation. J Immunol. 185:605–614. 2010. View Article : Google Scholar : PubMed/NCBI | |
Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, Wagner RA, Greaves DR, Murray PJ and Chawla A: Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 4:13–24. 2006. View Article : Google Scholar : PubMed/NCBI | |
Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, et al: Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 513:559–563. 2014. View Article : Google Scholar : PubMed/NCBI | |
Feng R, Morine Y, Ikemoto T, Imura S, Iwahashi S, Saito Y and Shimada M: Nrf2 activation drive macrophages polarization and cancer cell epithelial-mesenchymal transition during interaction. Cell Commun Signal. 16:542018. View Article : Google Scholar : PubMed/NCBI | |
Maftouh M, Avan A, Sciarrillo R, Granchi C, Leon LG, Rani R, Funel N, Smid K, Honeywell R, Boggi U, et al: Synergistic interaction of novel lactate dehydrogenase inhibitors with gemcitabine against pancreatic cancer cells in hypoxia. Br J Cancer. 110:172–182. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mediani L, Gibellini F, Bertacchini J, Frasson C, Bosco R, Accordi B, Basso G, Bonora M, Calabrò ML, Mattiolo A, et al: Reversal of the glycolytic phenotype of primary effusion lymphoma cells by combined targeting of cellular metabolism and PI3K/Akt/mTOR signaling. Oncotarget. 7:5521–5537. 2016. View Article : Google Scholar : PubMed/NCBI | |
Lin S, Sun L, Lyu X, Ai X, Du D, Su N, Li H, Zhang L, Yu J and Yuan S: Lactate-activated macrophages induced aerobic glycolysis and epithelial-mesenchymal transition in breast cancer by regulation of CCL5-CCR5 axis: A positive metabolic feedback loop. Oncotarget. 8:110426–110443. 2017. View Article : Google Scholar : PubMed/NCBI | |
Viola A, Munari F, Sánchez-Rodríguez R, Scolaro T and Castegna A: The metabolic signature of macrophage responses. Front Immunol. 10:14622019. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Wang H, Mao C, Sun M, Dominah G, Chen L and Zhuang Z: Fatty acid oxidation contributes to IL-1β secretion in M2 macrophages and promotes macrophage-mediated tumor cell migration. Mol Immunol. 94:27–35. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wu H, Han Y, Rodriguez Sillke Y, Deng H, Siddiqui S, Treese C, Schmidt F, Friedrich M, Keye J, Wan J, et al: Lipid droplet-dependent fatty acid metabolism controls the immune suppressive phenotype of tumor-associated macrophages. EMBO Mol Med. 11:e106982019. View Article : Google Scholar : PubMed/NCBI | |
Rombaldova M, Janovska P, Kopecky J and Kuda O: Omega-3 fatty acids promote fatty acid utilization and production of pro-resolving lipid mediators in alternatively activated adipose tissue macrophages. Biochem Biophys Res Commun. 490:1080–1085. 2017. View Article : Google Scholar : PubMed/NCBI | |
Huang SC, Everts B, Ivanova Y, O'Sullivan D, Nascimento M, Smith AM, Beatty W, Love-Gregory L, Lam WY, O'Neill CM, et al: Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat Immunol. 15:846–855. 2014. View Article : Google Scholar : PubMed/NCBI | |
Jin H, He Y, Zhao P, Hu Y, Tao J, Chen J and Huang Y: Targeting lipid metabolism to overcome EMT-associated drug resistance via integrin β3/FAK pathway and tumor-associated macrophage repolarization using legumain-activatable delivery. Theranostics. 9:265–278. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chiossone L, Dumas PY, Vienne M and Vivier E: Natural killer cells and other innate lymphoid cells in cancer. Nat Rev Immunol. 18:671–688. 2018. View Article : Google Scholar : PubMed/NCBI | |
Terrén I, Orrantia A, Vitallé J, Zenarruzabeitia O and Borrego F: NK cell metabolism and tumor microenvironment. Front Immunol. 10:22782019. View Article : Google Scholar : PubMed/NCBI | |
Gardiner CM: NK cell metabolism. J Leukoc Biol. 105:1235–1242. 2019. View Article : Google Scholar : PubMed/NCBI | |
Keating SE, Zaiatz-Bittencourt V, Loftus RM, Keane C, Brennan K, Finlay DK and Gardiner CM: Metabolic reprogramming supports IFN-γ production by CD56bright NK cells. J Immunol. 196:2552–2560. 2016. View Article : Google Scholar : PubMed/NCBI | |
Keppel MP, Saucier N, Mah AY, Vogel TP and Cooper MA: Activation-specific metabolic requirements for NK Cell IFN-γ production. J Immunol. 194:1954–1962. 2015. View Article : Google Scholar : PubMed/NCBI | |
Assmann N, O'Brien KL, Donnelly RP, Dyck L, Zaiatz-Bittencourt V, Loftus RM, Heinrich P, Oefner PJ, Lynch L, Gardiner CM, et al: Srebp-controlled glucose metabolism is essential for NK cell functional responses. Nat Immunol. 18:1197–1206. 2017. View Article : Google Scholar : PubMed/NCBI | |
Cooper MA, Fehniger TA and Caligiuri MA: The biology of human natural killer-cell subsets. Trends Immunol. 22:633–640. 2001. View Article : Google Scholar : PubMed/NCBI | |
Schafer JR, Salzillo TC, Chakravarti N, Kararoudi MN, Trikha P, Foltz JA, Wang R, Li S and Lee DA: Education-dependent activation of glycolysis promotes the cytolytic potency of licensed human natural killer cells. J Allergy Clin Immunol. 143:346–358.e6. 2019. View Article : Google Scholar : PubMed/NCBI | |
Parodi M, Raggi F, Cangelosi D, Manzini C, Balsamo M, Blengio F, Eva A, Varesio L, Pietra G, Moretta L, et al: Hypoxia modifies the transcriptome of human NK cells, modulates their immunoregulatory profile, and influences NK cell subset migration. Front Immunol. 9:23582018. View Article : Google Scholar : PubMed/NCBI | |
Balsamo M, Manzini C, Pietra G, Raggi F, Blengio F, Mingari MC, Varesio L, Moretta L, Bosco MC and Vitale M: Hypoxia downregulates the expression of activating receptors involved in NK-cell-mediated target cell killing without affecting ADCC. Eur J Immunol. 43:2756–2764. 2013. View Article : Google Scholar : PubMed/NCBI | |
Dengler VL, Galbraith M and Espinosa JM: Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol. 49:1–15. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yang C, Tsaih SW, Lemke A, Flister MJ, Thakar MS and Malarkannan S: mTORC1 and mTORC2 differentially promote natural killer cell development. Elife. 7:e356192018. View Article : Google Scholar : PubMed/NCBI | |
Chambers AM, Wang J, Lupo KB, Yu H, Atallah Lanman NM and Matosevic S: Adenosinergic signaling alters natural killer cell functional responses. Front Immunol. 9:25332018. View Article : Google Scholar : PubMed/NCBI | |
Brand A, Singer K, Koehl GE, Kolitzus M, Schoenhammer G, Thiel A, Matos C, Bruss C, Klobuch S, Peter K, et al: LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells. Cell Metab. 24:657–671. 2016. View Article : Google Scholar : PubMed/NCBI | |
Stiff A, Trikha P, Mundy-Bosse B, McMichael E, Mace TA, Benner B, Kendra K, Campbell A, Gautam S, Abood D, et al: Nitric oxide production by myeloid-derived suppressor cells plays a role in impairing Fc receptor-mediated natural killer cell function. Clin Cancer Res. 24:1891–1904. 2018. View Article : Google Scholar : PubMed/NCBI | |
Piñeiro Fernández J, Luddy KA, Harmon C and O'Farrelly C: Hepatic tumor microenvironments and effects on NK cell phenotype and function. Int J Mol Sci. 20:41312019. View Article : Google Scholar | |
Vitale M, Cantoni C, Pietra G, Mingari MC and Moretta L: Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol. 44:1582–1592. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Guan D, Wang S, Chai LYA, Xu S and Lam KP: Glycolysis and oxidative phosphorylation play critical roles in natural killer cell receptor-mediated natural killer cell functions. Front Immunol. 11:2022020. View Article : Google Scholar : PubMed/NCBI | |
Terrén I, Orrantia A, Vitallé J, Astarloa-Pando G, Zenarruzabeitia O and Borrego F: Modulating NK cell metabolism for cancer immunotherapy. Semin Hematol. 57:213–224. 2020. View Article : Google Scholar : PubMed/NCBI | |
Kobayashi T, Lam PY, Jiang H, Bednarska K, Gloury RE, Murigneux V, Tay J, Jacquelot N, Li R, Tuong ZK, et al: Increased lipid metabolism impairs NK cell function and mediates adaptation to the lymphoma environment. Blood. Aug 20–2020.(Epub ahead of print). View Article : Google Scholar | |
Inoue H, Miyaji M, Kosugi A, Nagafuku M, Okazaki T, Mimori T, Amakawa R, Fukuhara S, Domae N, Bloom ET and Umehara H: Lipid rafts as the signaling scaffold for NK cell activation: Tyrosine phosphorylation and association of LAT with phosphatidylinositol 3-kinase and phospholipase C-gamma following CD2 stimulation. Eur J Immunol. 32:2188–2198. 2002. View Article : Google Scholar : PubMed/NCBI | |
Niavarani SR, Lawson C, Bakos O, Boudaud M, Batenchuk C, Rouleau S and Tai LH: Lipid accumulation impairs natural killer cell cytotoxicity and tumor control in the postoperative period. BMC Cancer. 19:8232019. View Article : Google Scholar : PubMed/NCBI | |
Michelet X, Dyck L, Hogan A, Loftus RM, Duquette D, Wei K, Beyaz S, Tavakkoli A, Foley C, Donnelly R, et al: Metabolic reprogramming of natural killer cells in obesity limits antitumor responses. Nat Immunol. 19:1330–1340. 2018. View Article : Google Scholar : PubMed/NCBI | |
Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, Tyurin VA, Corzo A, Cho HI, Celis E, Lennox B, et al: Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med. 16:880–886. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gao F, Liu C, Guo J, Sun W, Xian L, Bai D, Liu H, Cheng Y, Li B, Cui J, et al: Radiation-driven lipid accumulation and dendritic cell dysfunction in cancer. Sci Rep. 5:96132015. View Article : Google Scholar : PubMed/NCBI | |
Dong H and Bullock TN: Metabolic influences that regulate dendritic cell function in tumors. Front Immunol. 5:242014. View Article : Google Scholar : PubMed/NCBI | |
Brown TP, Bhattacharjee P, Ramachandran S, Sivaprakasam S, Ristic B, Sikder MOF and Ganapathy V: The lactate receptor GPR81 promotes breast cancer growth via a paracrine mechanism involving antigen-presenting cells in the tumor microenvironment. Oncogene. 39:3292–3304. 2020. View Article : Google Scholar : PubMed/NCBI | |
Ibrahim J, Nguyen AH, Rehman A, Ochi A, Jamal M, Graffeo CS, Henning JR, Zambirinis CP, Fallon NC, Barilla R, et al: Dendritic cell populations with different concentrations of lipid regulate tolerance and immunity in mouse and human liver. Gastroenterology. 143:1061–1072. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mellor AL and Munn DH: Creating immune privilege: Active local suppression that benefits friends, but protects foes. Nat Rev Immunol. 8:74–80. 2008. View Article : Google Scholar : PubMed/NCBI | |
Everts B, Amiel E, Huang SC, Smith AM, Chang CH, Lam WY, Redmann V, Freitas TC, Blagih J, van der Windt GJ, et al: TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKε supports the anabolic demands of dendritic cell activation. Nat Immunol. 15:323–332. 2014. View Article : Google Scholar : PubMed/NCBI | |
Guak H, Al Habyan S, Ma EH, Aldossary H, Al-Masri M, Won SY, Ying T, Fixman ED, Jones RG, McCaffrey LM and Krawczyk CM: Glycolytic metabolism is essential for CCR7 oligomerization and dendritic cell migration. Nat Commun. 9:24632018. View Article : Google Scholar : PubMed/NCBI | |
Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ, Cross JR, Jung E, Thompson CB, Jones RG and Pearce EJ: Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood. 115:4742–4749. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nasi A, Fekete T, Krishnamurthy A, Snowden S, Rajnavölgyi E, Catrina AI, Wheelock CE, Vivar N and Rethi B: Dendritic cell reprogramming by endogenously produced lactic acid. J Immunol. 191:3090–3099. 2013. View Article : Google Scholar : PubMed/NCBI | |
Gottfried E, Kunz-Schughart LA, Ebner S, Mueller-Klieser W, Hoves S, Andreesen R, Mackensen A and Kreutz M: Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood. 107:2013–2021. 2006. View Article : Google Scholar : PubMed/NCBI | |
Naldini A, Morena E, Pucci A, Miglietta D, Riboldi E, Sozzani S and Carraro F: Hypoxia affects dendritic cell survival: Role of the hypoxia-inducible factor-1α and lipopolysaccharide. J Cell Physiol. 227:587–595. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lawless SJ, Kedia-Mehta N, Walls JF, McGarrigle R, Convery O, Sinclair LV, Navarro MN, Murray J and Finlay DK: Glucose represses dendritic cell-induced T cell responses. Nat Commun. 8:156202017. View Article : Google Scholar : PubMed/NCBI | |
Ramakrishnan R, Tyurin VA, Veglia F, Condamine T, Amoscato A, Mohammadyani D, Johnson JJ, Zhang LM, Klein-Seetharaman J, Celis E, et al: Oxidized lipids block antigen cross-presentation by dendritic cells in cancer. J Immunol. 192:2920–2931. 2014. View Article : Google Scholar : PubMed/NCBI | |
Menendez JA and Lupu R: Fatty acid synthase (FASN) as a therapeutic target in breast cancer. Expert Opin Thera Targets. 21:1001–1016. 2017. View Article : Google Scholar | |
Ventura R, Mordec K, Waszczuk J, Wang Z, Lai J, Fridlib M, Buckley D, Kemble G and Heuer TS: Inhibition of de novo palmitate synthesis by fatty acid synthase induces apoptosis in tumor cells by remodeling cell membranes, inhibiting signaling pathways, and reprogramming gene expression. EBioMedicine. 2:808–824. 2015. View Article : Google Scholar : PubMed/NCBI | |
Jiang L, Fang X, Wang H, Li D and Wang X: Ovarian cancer-intrinsic fatty acid synthase prevents anti-tumor immunity by disrupting tumor-infiltrating dendritic cells. Front Immunol. 9:29272018. View Article : Google Scholar : PubMed/NCBI | |
Cubillos-Ruiz JR, Silberman PC, Rutkowski MR, Chopra S, Perales-Puchalt A, Song M, Zhang S, Bettigole SE, Gupta D, Holcomb K, et al: ER Stress Sensor XBP1 controls Anti-tumor immunity by disrupting dendritic cell homeostasis. Cell. 161:1527–1538. 2015. View Article : Google Scholar : PubMed/NCBI | |
Xiong Y, Liu L, Xia Y, Qi Y, Chen Y, Chen L, Zhang P, Kong Y, Qu Y, Wang Z, et al: Tumor infiltrating mast cells determine oncogenic HIF-2α-conferred immune evasion in clear cell renal cell carcinoma. Cancer Immunol Immunother. 68:731–741. 2019. View Article : Google Scholar : PubMed/NCBI | |
Schwartz M, Zhang Y and Rosenblatt JD: B cell regulation of the anti-tumor response and role in carcinogenesis. J Immunother Cancer. 4:402016. View Article : Google Scholar : PubMed/NCBI | |
Aponte-López A, Fuentes-Pananá EM, Cortes-Muñoz D and Muñoz-Cruz S: Mast cell, the neglected member of the tumor microenvironment: Role in breast cancer. J Immunol Res. 2018:25842432018. View Article : Google Scholar : PubMed/NCBI | |
Okano M, Oshi M, Butash AL, Katsuta E, Tachibana K, Saito K, Okayama H, Peng X, Yan L, Kono K, Ohtake T and Takabe K: Triple-negative breast cancer with high levels of Annexin A1 expression is associated with mast cell infiltration, inflammation, and angiogenesis. Int J Mol Sci. 20:41972019. View Article : Google Scholar | |
Glajcar A, Szpor J, Pacek A, Tyrak KE, Chan F, Streb J, Hodorowicz-Zaniewska D and Okoń K: The relationship between breast cancer molecular subtypes and mast cell populations in tumor microenvironment. Virchows Arch. 470:505–515. 2017. View Article : Google Scholar : PubMed/NCBI | |
Spector AA: The importance of free fatty acid in tumor nutrition. Cancer Res. 27:1580–1586. 1967.PubMed/NCBI | |
Li Z and Zhang H: Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci. 73:377–392. 2016. View Article : Google Scholar : PubMed/NCBI | |
Al-Khami AA, Zheng L, Del Valle L, Hossain F, Wyczechowska D, Zabaleta J, Sanchez MD, Dean MJ, Rodriguez PC and Ochoa AC: Exogenous lipid uptake induces metabolic and functional reprogramming of tumor-associated myeloid-derived suppressor cells. Oncoimmunology. 6:e13448042017. View Article : Google Scholar : PubMed/NCBI | |
Cao W and Gabrilovich D: Abstract 3649: Contribution of fatty acid accumulation to myeloid-derived suppressor cell function in cancer. Cancer Res. 71:3649. 2011.PubMed/NCBI | |
Veglia F, Tyurin VA, Blasi M, De Leo A, Kossenkov AV, Donthireddy L, To TKJ, Schug Z, Basu S, Wang F, et al: Fatty acid transport protein 2 reprograms neutrophils in cancer. Nature. 569:73–78. 2019. View Article : Google Scholar : PubMed/NCBI |