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Cancer and Metastasis Reviews

Erschienen in:

08.08.2022

The adipocyte microenvironment and cancer

verfasst von: Abir Mukherjee, Agnes J. Bilecz, Ernst Lengyel

Erschienen in: Cancer and Metastasis Reviews | Ausgabe 3/2022

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Abstract

Many epithelial tumors grow in the vicinity of or metastasize to adipose tissue. As tumors develop, crosstalk between adipose tissue and cancer cells leads to changes in adipocyte function and paracrine signaling, promoting a microenvironment that supports tumor growth. Over the last decade, it became clear that tumor cells co-opt adipocytes in the tumor microenvironment, converting them into cancer-associated adipocytes (CAA). As adipocytes and cancer cells engage, a metabolic symbiosis ensues that is driven by bi-directional signaling. Many cancers (colon, breast, prostate, lung, ovarian cancer, and hematologic malignancies) stimulate lipolysis in adipocytes, followed by the uptake of fatty acids (FA) from the surrounding adipose tissue. The FA enters the cancer cell through specific fatty acid receptors and binding proteins (e.g., CD36, FATP1) and are used for membrane synthesis, energy metabolism (β-oxidation), or lipid-derived cell signaling molecules (derivatives of arachidonic and linolenic acid). Therefore, blocking adipocyte-derived lipid uptake or lipid-associated metabolic pathways in cancer cells, either with a single agent or in combination with standard of care chemotherapy, might prove to be an effective strategy against cancers that grow in lipid-rich tumor microenvironments.

Lazar, I., Clement, E., Dauvillier, S., Milhas, D., Ducoux-Petit, M., LeGonidec, S., et al. (2016). Adipocyte exosomes promote melanoma aggressiveness through fatty acid oxidation: A novel mechanism linking obesity and cancer. Cancer Research, 76(14), 4051–4057. https://doi.org/10.1158/0008-5472.CAN-16-0651CrossRefPubMed

Nieman, K. M., Romero, I. L., Van Houten, B., & Lengyel, E. (2013). Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochimica et Biophysica Acta, 1831(10), 1533–1541. https://doi.org/10.1016/j.bbalip.2013.02.010CrossRefPubMedPubMedCentral

Lengyel, E., Makowski, L., DiGiovanni, J., & Kolonin, M. G. (2018). Cancer as a matter of fat: The crosstalk between adipose tissue and tumors. Trends Cancer, 4(5), 374–384. https://doi.org/10.1016/j.trecan.2018.03.004CrossRefPubMedPubMedCentral

Duman, C., Yaqubi, K., Hoffmann, A., Acikgoz, A. A., Korshunov, A., Bendszus, M., et al. (2019). Acyl-CoA-binding protein drives glioblastoma tumorigenesis by sustaining fatty acid oxidation. Cell Metabolism, 30(2), 274–289 e275. https://doi.org/10.1016/j.cmet.2019.04.004.

Reilly, S. M., Hung, C. W., Ahmadian, M., Zhao, P., Keinan, O., Gomez, A. V., et al. (2020). Catecholamines suppress fatty acid re-esterification and increase oxidation in white adipocytes via STAT3. Nature Metabolism, 2(7), 620–634. https://doi.org/10.1038/s42255-020-0217-6CrossRefPubMedPubMedCentral

Thomas, E. L., Saeed, N., Hajnal, J. V., Brynes, A., Goldstone, A. P., Frost, G., et al. (1998). Magnetic resonance imaging of total body fat. J Appl Physiol (1985), 85(5), 1778–1785. https://doi.org/10.1152/jappl.1998.85.5.1778.

Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., et al. (2009). High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes, 58(7), 1526–1531. https://doi.org/10.2337/db09-0530CrossRefPubMedPubMedCentral

Kahn, C. R., Wang, G., & Lee, K. Y. (2019). Altered adipose tissue and adipocyte function in the pathogenesis of metabolic syndrome. Journal of Clinical Investigation, 129(10), 3990–4000. https://doi.org/10.1172/JCI129187CrossRefPubMedPubMedCentral

Vijay, J., Gauthier, M. F., Biswell, R. L., Louiselle, D. A., Johnston, J. J., Cheung, W. A., et al. (2020). Single-cell analysis of human adipose tissue identifies depot and disease specific cell types. Nature Metabolism, 2(1), 97–109. https://doi.org/10.1038/s42255-019-0152-6CrossRefPubMed

10.

Crewe, C., An, Y. A., & Scherer, P. E. (2017). The ominous triad of adipose tissue dysfunction: Inflammation, fibrosis, and impaired angiogenesis. Journal of Clinical Investigation, 127(1), 74–82. https://doi.org/10.1172/JCI88883CrossRefPubMedPubMedCentral

11.

Lauby-Secretan, B., Scoccianti, C., Loomis, D., Grosse, Y., Bianchini, F., Straif, K., et al. (2016). Body fatness and cancer–Viewpoint of the IARC working group. New England Journal of Medicine, 375(8), 794–798. https://doi.org/10.1056/NEJMsr1606602CrossRefPubMed

12.

Ringel, A. E., Drijvers, J. M., Baker, G. J., Catozzi, A., Garcia-Canaveras, J. C., Gassaway, B. M., et al. (2020). Obesity shapes metabolism in the tumor microenvironment to suppress anti-tumor immunity. Cell, 183(7), 1848–1866 e1826. https://doi.org/10.1016/j.cell.2020.11.009.

13.

Maury, E., Ehala-Aleksejev, K., Guiot, Y., Detry, R., Vandenhooft, A., & Brichard, S. M. (2007). Adipokines oversecreted by omental adipose tissue in human obesity. American Journal of Physiology - Endocrinology and Metabolism, 293, E656–E665.CrossRef

14.

Dirat, B., Bochet, L., Dabek, M., Daviaud, D., Dauvillier, S., Majed, B., et al. (2011). Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Research, 71(7), 2455–2465. https://doi.org/10.1158/0008-5472.CAN-10-3323CrossRefPubMed

15.

Arner, P., & Kulyte, A. (2015). MicroRNA regulatory networks in human adipose tissue and obesity. Nature Reviews: Endocrinology, 11(5), 276–288. https://doi.org/10.1038/nrendo.2015.25CrossRefPubMed

16.

Maguire, O. A., Ackerman, S. E., Szwed, S. K., Maganti, A. V., Marchildon, F., Huang, X., et al. (2021). Creatine-mediated crosstalk between adipocytes and cancer cells regulates obesity-driven breast cancer. Cell Metabolism, 33(3), 499–512 e496. https://doi.org/10.1016/j.cmet.2021.01.018.

17.

Romero, I. L., McCormick, A., McEwen, K. A., Park, S., Karrison, T., Yamada, S. D., et al. (2012). Relationship of type II diabetes and metformin use to ovarian cancer progression, survival, and chemosensitivity. Obstetrics and Gynecology, 119(1), 61–67. https://doi.org/10.1097/AOG.0b013e3182393ab3CrossRefPubMed

18.

Sun, C., Li, X., Guo, E., Li, N., Zhou, B., Lu, H., et al. (2020). MCP-1/CCR-2 axis in adipocytes and cancer cell respectively facilitates ovarian cancer peritoneal metastasis. Oncogene, 39(8), 1681–1695. https://doi.org/10.1038/s41388-019-1090-1CrossRefPubMed

19.

Goodwin, P. J., Chen, B. E., Gelmon, K. A., Whelan, T. J., Ennis, M., Lemieux, J., et al. (2022). Effect of metformin vs placebo on invasive disease-free survival in patients with breast cancer: The MA.32 randomized clinical trial. JAMA, 327(20), 1963–1973. https://doi.org/10.1001/jama.2022.6147.

20.

Kazantzis, M., & Stahl, A. (2012). Fatty acid transport proteins, implications in physiology and disease. Biochimica et Biophysica Acta, 1821(5), 852–857. https://doi.org/10.1016/j.bbalip.2011.09.010CrossRefPubMed

21.

Nath, A., Li, I., Roberts, L. R., & Chan, C. (2015). Elevated free fatty acid uptake via CD36 promotes epithelial-mesenchymal transition in hepatocellular carcinoma. Scientific Reports, 5, 14752. https://doi.org/10.1038/srep14752CrossRefPubMedPubMedCentral

22.

Nath, A., & Chan, C. (2016). Genetic alterations in fatty acid transport and metabolism genes are associated with metastatic progression and poor prognosis of human cancers. Scientific Reports, 6, 18669. https://doi.org/10.1038/srep18669CrossRefPubMedPubMedCentral

23.

Hao, Y., Li, D., Xu, Y., Ouyang, J., Wang, Y., Zhang, Y., et al. (2019). Investigation of lipid metabolism dysregulation and the effects on immune microenvironments in pan-cancer using multiple omics data. BMC Bioinformatics, 20(Suppl 7), 195. https://doi.org/10.1186/s12859-019-2734-4CrossRefPubMedPubMedCentral

24.

Ladanyi, A., Mukherjee, A., Kenny, H. A., Johnson, A., Mitra, A. K., Sundaresan, S., et al. (2018). Adipocyte-induced CD36 expression drives ovarian cancer progression and metastasis. Oncogene, 37(17), 2285–2301. https://doi.org/10.1038/s41388-017-0093-zCrossRefPubMedPubMedCentral

25.

Pascual, G., Avgustinova, A., Mejetta, S., Martin, M., Castellanos, A., Attolini, C. S., et al. (2017). Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature, 541(7635), 41–45. https://doi.org/10.1038/nature20791CrossRefPubMed

26.

Pascual, G., Dominguez, D., Elosua-Bayes, M., Beckedorff, F., Laudanna, C., Bigas, C., et al. (2021). Dietary palmitic acid promotes a prometastatic memory via Schwann cells. Nature, 599(7885), 485–490. https://doi.org/10.1038/s41586-021-04075-0CrossRefPubMed

27.

Choi, C. H., Choi, J. J., Park, Y. A., Lee, Y. Y., Song, S. Y., Sung, C. O., et al. (2012). Identification of differentially expressed genes according to chemosensitivity in advanced ovarian serous adenocarcinomas: Expression of GRIA2 predicts better survival. British Journal of Cancer, 107(1), 91–99. https://doi.org/10.1038/bjc.2012.217CrossRefPubMedPubMedCentral

28.

Watt, M. J., Clark, A. K., Selth, L. A., Haynes, V. R., Lister, N., Rebello, R., et al. (2019). Suppressing fatty acid uptake has therapeutic effects in preclinical models of prostate cancer. Science Translational Medicine, 11(478). https://doi.org/10.1126/scitranslmed.aau5758.

29.

Zhang, M., Di Martino, J. S., Bowman, R. L., Campbell, N. R., Baksh, S. C., Simon-Vermot, T., et al. (2018). Adipocyte-derived lipids mediate melanoma progression via FATP proteins. Cancer Discovery, 8(8), 1006–1025. https://doi.org/10.1158/2159-8290.CD-17-1371CrossRefPubMedPubMedCentral

30.

Nomura, D. K., Long, J. Z., Niessen, S., Hoover, H. S., Ng, S. W., & Cravatt, B. F. (2010). Monoacylglycerol lipase regulates a fatty acid network that promotes cancer pathogenesis. Cell, 140, 49–61.CrossRef

31.

Nieman, K. M., Kenny, H. A., Penicka, C. V., Ladanyi, A., Buell-Gutbrod, R., Zillhardt, M. R., et al. (2011). Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nature Medicine, 17(11), 1498–1503. https://doi.org/10.1038/nm.2492CrossRefPubMedPubMedCentral

32.

Eckert, M. A., Coscia, F., Chryplewicz, A., Chang, J. W., Hernandez, K. M., Pan, S., et al. (2019). Proteomics reveals NNMT as a master metabolic regulator of cancer-associated fibroblasts. Nature, 569(7758), 723–728. https://doi.org/10.1038/s41586-019-1173-8CrossRefPubMedPubMedCentral

33.

Mukherjee, A., Chiang, C. Y., Daifotis, H. A., Nieman, K. M., Fahrmann, J. F., Lastra, R. R., et al. (2020). Adipocyte-induced FABP4 expression in ovarian cancer cells promotes metastasis and mediates carboplatin resistance. Cancer Research, 80(8), 1748–1761. https://doi.org/10.1158/0008-5472.CAN-19-1999CrossRefPubMed

34.

Xu, A., Wang, Y., Xu, J. Y., Stejskal, D., Tam, S., Zhang, J., et al. (2006). Adipocyte fatty acid-binding protein is a plasma biomarker closely associated with obesity and metabolic syndrome. Clinical Chemistry, 52(3), 405–413. https://doi.org/10.1373/clinchem.2005.062463CrossRefPubMed

35.

Cao, H., Sekiya, M., Ertunc, M. E., Burak, M. F., Mayers, J. R., White, A., et al. (2013). Adipocyte lipid chaperone AP2 is a secreted adipokine regulating hepatic glucose production. Cell Metabolism, 17(5), 768–778. https://doi.org/10.1016/j.cmet.2013.04.012CrossRefPubMedPubMedCentral

36.

Hao, J., Zhang, Y., Yan, X., Yan, F., Sun, Y., Zeng, J., et al. (2018). Circulating adipose fatty acid binding protein is a new link underlying obesity-associated breast/mammary tumor development. Cell Metabolism, 28(5), 689–705 e685. https://doi.org/10.1016/j.cmet.2018.07.006.

37.

Laurent, V., Guerard, A., Mazerolles, C., Le Gonidec, S., Toulet, A., Nieto, L., et al. (2016). Periprostatic adipocytes act as a driving force for prostate cancer progression in obesity. Nature Communications, 7, 10230. https://doi.org/10.1038/ncomms10230CrossRefPubMedPubMedCentral

38.

Louie, S. M., Roberts, L. S., Mulvihill, M. M., Luo, K., & Nomura, D. K. (2013). Cancer cells incorporate and remodel exogenous palmitate into structural and oncogenic signaling lipids. Biochimica et Biophysica Acta, 1831(10), 1566–1572. https://doi.org/10.1016/j.bbalip.2013.07.008CrossRefPubMed

39.

Fang, M., Shen, Z., Huang, S., Zhao, L., Chen, S., Mak, T. W., et al. (2010). The ER UDPase ENTPD5 promotes protein N-glycosylation, the Warburg effect, and proliferation in the PTEN pathway. Cell, 143(5), 711–724. https://doi.org/10.1016/j.cell.2010.10.010CrossRefPubMed

40.

Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., et al. (2012). Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 149(5), 1060–1072. https://doi.org/10.1016/j.cell.2012.03.042CrossRefPubMedPubMedCentral

41.

Kagan, V. E., Mao, G., Qu, F., Angeli, J. P., Doll, S., Croix, C. S., et al. (2017). Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nature Chemical Biology, 13(1), 81–90. https://doi.org/10.1038/nchembio.2238CrossRefPubMed

42.

Wang, T., Fahrmann, J. F., Lee, H., Li, Y. J., Tripathi, S. C., Yue, C., et al. (2018). JAK/STAT3-regulated fatty acid beta-oxidation is critical for breast cancer stem cell self-renewal and chemoresistance. Cell Metabolism, 27(6), 1357. https://doi.org/10.1016/j.cmet.2018.04.018CrossRefPubMedPubMedCentral

43.

Ye, H., Adane, B., Khan, N., Sullivan, T., Minhajuddin, M., Gasparetto, M., et al. (2016). Leukemic stem cells evade chemotherapy by metabolic adaptation to an adipose tissue niche. Cell Stem Cell, 19(1), 23–37. https://doi.org/10.1016/j.stem.2016.06.001CrossRefPubMedPubMedCentral

44.

Pike, L. S., Smift, A. L., Croteau, N. J., Ferrick, D. A., & Wu, M. (2011). Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochimica et Biophysica Acta, 1807(6), 726–734. https://doi.org/10.1016/j.bbabio.2010.10.022CrossRefPubMed

45.

Iwamoto, H., Abe, M., Yang, Y., Cui, D., Seki, T., Nakamura, M., et al. (2018). Cancer lipid metabolism confers antiangiogenic drug resistance. Cell Metabolism, 28(1), 104–117 e105. https://doi.org/10.1016/j.cmet.2018.05.005.

46.

Zhang, Y., Daquinag, A., Amaya-Manzanares, F., Sirin, O., Tseng, C., & Kolonin, M. G. (2012). Stromal progenitor cells from endogenous adipose tissue contribute to pericytes and adipocytes that populate the tumor microenvironment. Cancer Research, 72(20), 5198–5208.CrossRef

47.

Ackerman, D., Tumanov, S., Qiu, B., Michalopoulou, E., Spata, M., Azzam, A., et al. (2018). Triglycerides promote lipid homeostasis during hypoxic stress by balancing fatty acid saturation. Cell Rep, 24(10), 2596–2605 e2595. https://doi.org/10.1016/j.celrep.2018.08.015.

48.

Krist, L. F., Eestermans, I. L., Steenbergen, J. J., Hoefsmit, E. C., Cuesta, M. A., Meyer, S., et al. (1995). Cellular composition of milky spots in the human greater omentum: An immunochemical and ultrastructural study. Anatomical Record, 241(2), 163–174. https://doi.org/10.1002/ar.1092410204CrossRefPubMed

49.

Cui, L., Johkura, K., Liang, Y., Teng, R., Ogiwara, N., Okouchi, Y., et al. (2002). Biodefense function of omental milky spots through cell adhesion molecules and leukocyte proliferation. Cell and Tissue Research, 310(3), 321–330. https://doi.org/10.1007/s00441-002-0636-6CrossRefPubMed

50.

Morison, R. (1906). Remarks on some functions of the omentum. British Medical Journal, 1(2350), 76–78. https://doi.org/10.1136/bmj.1.2350.76CrossRefPubMedPubMedCentral

51.

Van Vugt, E., Van Rijthoven, E. A., Kamperdijk, E. W., & Beelen, R. H. (1996). Omental milky spots in the local immune response in the peritoneal cavity of rats. Anatomical Record, 244(2), 235–245. https://doi.org/10.1002/(SICI)1097-0185(199602)244:2%3c235::AID-AR11%3e3.0.CO;2-QCrossRefPubMed

52.

Benezech, C., Luu, N. T., Walker, J. A., Kruglov, A. A., Loo, Y., Nakamura, K., et al. (2015). Inflammation-induced formation of fat-associated lymphoid clusters. Nature Immunology, 16(8), 819–828. https://doi.org/10.1038/ni.3215CrossRefPubMedPubMedCentral

53.

Shimotsuma, M., Simpson-Morgan, M. W., Takahashi, T., & Hagiwara, A. (1992). Activation of omental milky spots and milky spot macrophages by intraperitoneal administration of a streptococcal preparation, OK-432. Cancer Research, 52(19), 5400–5402.PubMed

54.

Sorensen, E. W., Gerber, S. A., Sedlacek, A. L., Rybalko, V. Y., Chan, W. M., & Lord, E. M. (2009). Omental immune aggregates and tumor metastasis within the peritoneal cavity. Immunologic Research, 45(2–3), 185–194. https://doi.org/10.1007/s12026-009-8100-2CrossRefPubMed

55.

Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W., Jr. (2003). Obesity is associated with macrophage accumulation in adipose tissue. The Journal of Clinical Investigation, 112(12), 1796–1808. https://doi.org/10.1172/JCI19246CrossRefPubMedPubMedCentral

56.

Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., et al. (2003). Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. Journal of Clinical Investigation, 112(12), 1821–1830. https://doi.org/10.1172/JCI19451CrossRefPubMedPubMedCentral

57.

Martinez, O., de Victoria, E., Xu, X., Koska, J., Francisco, A. M., Scalise, M., Ferrante, A. W., Jr., et al. (2009). Macrophage content in subcutaneous adipose tissue: Associations with adiposity, age, inflammatory markers, and whole-body insulin action in healthy Pima Indians. Diabetes, 58(2), 385–393. https://doi.org/10.2337/db08-0536CrossRef

58.

Saberi, M., Woods, N. B., de Luca, C., Schenk, S., Lu, J. C., Bandyopadhyay, G., et al. (2009). Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metabolism, 10(5), 419–429. https://doi.org/10.1016/j.cmet.2009.09.006CrossRefPubMedPubMedCentral

59.

Arkan, M. C., Hevener, A. L., Greten, F. R., Maeda, S., Li, Z. W., Long, J. M., et al. (2005). IKK-beta links inflammation to obesity-induced insulin resistance. Nature Medicine, 11(2), 191–198. https://doi.org/10.1038/nm1185CrossRefPubMed

60.

Solinas, G., Vilcu, C., Neels, J. G., Bandyopadhyay, G. K., Luo, J. L., Naugler, W., et al. (2007). JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metabolism, 6(5), 386–397. https://doi.org/10.1016/j.cmet.2007.09.011CrossRefPubMed

61.

Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., & Locati, M. (2004). The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology, 25(12), 677–686. https://doi.org/10.1016/j.it.2004.09.015CrossRefPubMed

62.

Kelly, B., & O’Neill, L. A. (2015). Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Research, 25(7), 771–784. https://doi.org/10.1038/cr.2015.68CrossRefPubMedPubMedCentral

63.

Serbulea, V., Upchurch, C. M., Schappe, M. S., Voigt, P., DeWeese, D. E., Desai, B. N., et al. (2018). Macrophage phenotype and bioenergetics are controlled by oxidized phospholipids identified in lean and obese adipose tissue. Proceedings of the National Academy of Sciences of the United States of America, 115(27), E6254–E6263. https://doi.org/10.1073/pnas.1800544115CrossRefPubMedPubMedCentral

64.

Xu, X., Grijalva, A., Skowronski, A., van Eijk, M., Serlie, M. J., & Ferrante, A. W., Jr. (2013). Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metabolism, 18(6), 816–830. https://doi.org/10.1016/j.cmet.2013.11.001CrossRefPubMedPubMedCentral

65.

Kratz, M., Coats, B. R., Hisert, K. B., Hagman, D., Mutskov, V., Peris, E., et al. (2014). Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metabolism, 20(4), 614–625. https://doi.org/10.1016/j.cmet.2014.08.010CrossRefPubMedPubMedCentral

66.

Krishnan, V., Tallapragada, S., Schaar, B., Kamat, K., Chanana, A. M., Zhang, Y., et al. (2020). Omental macrophages secrete chemokine ligands that promote ovarian cancer colonization of the omentum via CCR1. Commun Biol, 3(1), 524. https://doi.org/10.1038/s42003-020-01246-zCrossRefPubMedPubMedCentral

67.

Etzerodt, A., Moulin, M., Doktor, T. K., Delfini, M., Mossadegh-Keller, N., Bajenoff, M., et al. (2020). Tissue-resident macrophages in omentum promote metastatic spread of ovarian cancer. Journal of Experimental Medicine, 217(4). https://doi.org/10.1084/jem.20191869.

68.

Tiwari, P., Blank, A., Cui, C., Schoenfelt, K. Q., Zhou, G., Xu, Y., et al. (2019). Metabolically activated adipose tissue macrophages link obesity to triple-negative breast cancer. Journal of Experimental Medicine, 216(6), 1345–1358. https://doi.org/10.1084/jem.20181616CrossRefPubMedPubMedCentral

69.

Linde, N., Casanova-Acebes, M., Sosa, M. S., Mortha, A., Rahman, A., Farias, E., et al. (2018). Macrophages orchestrate breast cancer early dissemination and metastasis. Nature Communications, 9(1), 21. https://doi.org/10.1038/s41467-017-02481-5CrossRefPubMedPubMedCentral

70.

Hao, J., Yan, F., Zhang, Y., Triplett, A., Zhang, Y., Schultz, D. A., et al. (2018). Expression of adipocyte/macrophage fatty acid-binding protein in tumor-associated macrophages promotes breast cancer progression. Cancer Research, 78(9), 2343–2355. https://doi.org/10.1158/0008-5472.CAN-17-2465CrossRefPubMedPubMedCentral

71.

Wensveen, F. M., Jelencic, V., Valentic, S., Sestan, M., Wensveen, T. T., Theurich, S., et al. (2015). NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nature Immunology, 16(4), 376–385. https://doi.org/10.1038/ni.3120CrossRefPubMed

72.

Geller, M. A., Knorr, D. A., Hermanson, D. A., Pribyl, L., Bendzick, L., McCullar, V., et al. (2013). Intraperitoneal delivery of human natural killer cells for treatment of ovarian cancer in a mouse xenograft model. Cytotherapy, 15(10), 1297–1306. https://doi.org/10.1016/j.jcyt.2013.05.022CrossRefPubMedPubMedCentral

73.

Hermanson, D. L., Bendzick, L., Pribyl, L., McCullar, V., Vogel, R. I., Miller, J. S., et al. (2016). Induced pluripotent stem cell-derived natural killer cells for treatment of ovarian cancer. Stem Cells, 34(1), 93–101. https://doi.org/10.1002/stem.2230CrossRefPubMed

74.

Nham, T., Poznanski, S. M., Fan, I. Y., Shenouda, M. M., Chew, M. V., Lee, A. J., et al. (2018). Ex vivo-expanded NK cells from blood and ascites of ovarian cancer patients are cytotoxic against autologous primary ovarian cancer cells. Cancer Immunology, Immunotherapy, 67(4), 575–587. https://doi.org/10.1007/s00262-017-2112-xCrossRefPubMed

75.

Sedlacek, A. L., Gerber, S. A., Randall, T. D., van Rooijen, N., Frelinger, J. G., & Lord, E. M. (2013). Generation of a dual-functioning antitumor immune response in the peritoneal cavity. American Journal of Pathology, 183(4), 1318–1328. https://doi.org/10.1016/j.ajpath.2013.06.030CrossRefPubMedPubMedCentral

76.

Castriconi, R., Cantoni, C., Della Chiesa, M., Vitale, M., Marcenaro, E., Conte, R., et al. (2003). Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: Consequences for the NK-mediated killing of dendritic cells. Proceedings of the National Academy of Sciences of the United States of America, 100(7), 4120–4125. https://doi.org/10.1073/pnas.0730640100CrossRefPubMedPubMedCentral

77.

Yu, J., Wei, M., Becknell, B., Trotta, R., Liu, S., Boyd, Z., et al. (2006). Pro- and antiinflammatory cytokine signaling: Reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity, 24(5), 575–590. https://doi.org/10.1016/j.immuni.2006.03.016CrossRefPubMed

78.

Yaqoob, P., Newsholme, E. A., & Calder, P. C. (1994). Inhibition of natural killer cell activity by dietary lipids. Immunology Letters, 41(2–3), 241–247. https://doi.org/10.1016/0165-2478(94)90140-6CrossRefPubMed

79.

Niavarani, S. R., Lawson, C., Bakos, O., Boudaud, M., Batenchuk, C., Rouleau, S., et al. (2019). Lipid accumulation impairs natural killer cell cytotoxicity and tumor control in the postoperative period. BMC Cancer, 19(1), 823. https://doi.org/10.1186/s12885-019-6045-yCrossRefPubMedPubMedCentral

80.

Michelet, X., Dyck, L., Hogan, A., Loftus, R. M., Duquette, D., Wei, K., et al. (2018). Metabolic reprogramming of natural killer cells in obesity limits antitumor responses. Nature Immunology, 19(12), 1330–1340. https://doi.org/10.1038/s41590-018-0251-7CrossRefPubMed

81.

Talukdar, S., Oh, D. Y., Bandyopadhyay, G., Li, D., Xu, J., McNelis, J., et al. (2012). Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nature Medicine, 18(9), 1407–1412. https://doi.org/10.1038/nm.2885CrossRefPubMedPubMedCentral

82.

Elgazar-Carmon, V., Rudich, A., Hadad, N., & Levy, R. (2008). Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. Journal of Lipid Research, 49(9), 1894–1903. https://doi.org/10.1194/jlr.M800132-JLR200CrossRefPubMed

83.

Nijhuis, J., Rensen, S. S., Slaats, Y., van Dielen, F. M., Buurman, W. A., & Greve, J. W. (2009). Neutrophil activation in morbid obesity, chronic activation of acute inflammation. Obesity (Silver Spring), 17(11), 2014–2018. https://doi.org/10.1038/oby.2009.113CrossRef

84.

Tkalcevic, J., Novelli, M., Phylactides, M., Iredale, J. P., Segal, A. W., & Roes, J. (2000). Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity, 12(2), 201–210. https://doi.org/10.1016/s1074-7613(00)80173-9CrossRefPubMed

85.

Adkison, A. M., Raptis, S. Z., Kelley, D. G., & Pham, C. T. (2002). Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. Journal of Clinical Investigation, 109(3), 363–371. https://doi.org/10.1172/JCI13462CrossRefPubMedPubMedCentral

86.

Liu, Z., Shapiro, S. D., Zhou, X., Twining, S. S., Senior, R. M., Giudice, G. J., et al. (2000). A critical role for neutrophil elastase in experimental bullous pemphigoid. Journal of Clinical Investigation, 105(1), 113–123. https://doi.org/10.1172/JCI3693CrossRefPubMedPubMedCentral

87.

Jackson-Jones, L. H., Smith, P., Portman, J. R., Magalhaes, M. S., Mylonas, K. J., Vermeren, M. M., et al. (2020). Stromal cells covering omental fat-associated lymphoid clusters trigger formation of neutrophil aggregates to capture peritoneal contaminants. Immunity, 52(4), 700–715 e706. https://doi.org/10.1016/j.immuni.2020.03.011.

88.

Lee, W., Ko, S. Y., Mohamed, M. S., Kenny, H. A., Lengyel, E., & Naora, H. (2019). Neutrophils facilitate ovarian cancer premetastatic niche formation in the omentum. Journal of Experimental Medicine, 216(1), 176–194. https://doi.org/10.1084/jem.20181170CrossRefPubMedPubMedCentral

89.

Cui, C., Chakraborty, K., Tang, X. A., Zhou, G., Schoenfelt, K. Q., Becker, K. M., et al. (2021). Neutrophil elastase selectively kills cancer cells and attenuates tumorigenesis. Cell, 184(12), 3163–3177 e3121. https://doi.org/10.1016/j.cell.2021.04.016.

90.

Nishimura, S., Manabe, I., Nagasaki, M., Eto, K., Yamashita, H., Ohsugi, M., et al. (2009). CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nature Medicine, 15(8), 914–920. https://doi.org/10.1038/nm.1964CrossRefPubMed

91.

Feuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., et al. (2009). Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nature Medicine, 15(8), 930–939. https://doi.org/10.1038/nm.2002CrossRefPubMedPubMedCentral

92.

Winer, S., Chan, Y., Paltser, G., Truong, D., Tsui, H., Bahrami, J., et al. (2009). Normalization of obesity-associated insulin resistance through immunotherapy. Nature Medicine, 15(8), 921–929. https://doi.org/10.1038/nm.2001CrossRefPubMedPubMedCentral

93.

Wang, Z., Aguilar, E. G., Luna, J. I., Dunai, C., Khuat, L. T., Le, C. T., et al. (2019). Paradoxical effects of obesity on T cell function during tumor progression and PD-1 checkpoint blockade. Nature Medicine, 25(1), 141–151. https://doi.org/10.1038/s41591-018-0221-5CrossRefPubMed

94.

Liu, Y., Metzinger, M. N., Lewellen, K. A., Cripps, S. N., Carey, K. D., Harper, E. I., et al. (2015). Obesity contributes to ovarian cancer metastatic success through increased lipogenesis, enhanced vascularity, and decreased infiltration of M1 macrophages. Cancer Research, 75(23), 5046–5057. https://doi.org/10.1158/0008-5472.CAN-15-0706CrossRefPubMedPubMedCentral

95.

Zhang, C., Yue, C., Herrmann, A., Song, J., Egelston, C., Wang, T., et al. (2020). STAT3 activation-induced fatty acid oxidation in CD8(+) T effector cells is critical for obesity-promoted breast tumor growth. Cell Metabolism, 31(1), 148–161 e145. https://doi.org/10.1016/j.cmet.2019.10.013.

96.

Ma, X., Xiao, L., Liu, L., Ye, L., Su, P., Bi, E., et al. (2021). CD36-mediated ferroptosis dampens intratumoral CD8(+) T cell effector function and impairs their antitumor ability. Cell Metabolism, 33(5), 1001–1012 e1005. https://doi.org/10.1016/j.cmet.2021.02.015.

Titel: The adipocyte microenvironment and cancer
verfasst von: Abir Mukherjee
Agnes J. Bilecz
Ernst Lengyel
Publikationsdatum: 08.08.2022
Verlag: Springer US
Erschienen in: Cancer and Metastasis Reviews / Ausgabe 3/2022
Print ISSN: 0167-7659
Elektronische ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-022-10059-x

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The adipocyte microenvironment and cancer

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