Obesity-associated NLRC4 inflammasome activation drives breast cancer progression

Nature Communications

Volumn 7, Issue , 2016, Pages

  Kolb, Ryan ^a   Phan, Liem ^b,c   Borcherding, Nicholas ^a,d   Liu, Yinghong ^e   Yuan, Fang ^e   Janowski, Ann M ^a   Xie, Qing ^a   Markan, Kathleen R ^a   Li, Wei ^a   Potthoff, Matthew J ^a   Fuentes Mattei, Enrique ^c   Ellies, Lesley G ^f   Knudson, C Michael ^a   Lee, Mong Hong ^b,c   Yeung, Sai Ching J ^b,c   Cassel, Suzanne L ^a,h   Sutterwala, Fayyaz S ^a,h   Zhang, Weizhou ^a,d,g  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF TEXAS   (United States)

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

^d The University of Iowa   (United States)

^e CENTRAL SOUTH UNIVERSITY   (China)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^h CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD163 ANTIGEN; CD33 ANTIGEN; CD68 ANTIGEN; CRYOPYRIN; CXCL1 CHEMOKINE; GELATINASE B; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; METFORMIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR C4; UNCLASSIFIED DRUG; VASCULOTROPIN A; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; IPAF PROTEIN, MOUSE; NLRC4 PROTEIN, HUMAN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VEGFA PROTEIN, HUMAN;

CANCER; DISEASE TREATMENT; GENE EXPRESSION; GENETIC ANALYSIS; IMMUNE RESPONSE; OBESITY; SENSORY SYSTEM; TUMOR;

ADIPOCYTE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED MACROPHAGE; BREAST ADENOCARCINOMA; CANCER ASSOCIATED FIBROBLAST; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIET INDUCED OBESITY; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; EX VIVO STUDY; FEMALE; HUMAN; HUMAN TISSUE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION; ANIMAL; BREAST; BREAST TUMOR; C57BL MOUSE; CANCER TRANSPLANTATION; COMPLICATION; CYTOLOGY; DISEASE EXACERBATION; EXPERIMENTAL MAMMARY NEOPLASM; METABOLISM; OBESITY; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BREAST; BREAST NEOPLASMS; CALCIUM-BINDING PROTEINS; CARD SIGNALING ADAPTOR PROTEINS; CELL LINE, TUMOR; DISEASE PROGRESSION; FEMALE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; LYMPHOCYTES, TUMOR-INFILTRATING; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MYELOID CELLS; NEOPLASM TRANSPLANTATION; OBESITY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84990848498     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13007     Document Type: Article

References (57)

1. Flegal, K. M., Kit, B. K. & Graubard, B. I. Overweight, obesity, and all-cause mortality-reply. JAMA 309, 1681-1682 (2013).
2. Reeves, G. K. et al. Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. Br. Med. J. 335, 1134 (2007).
3. Rose, D. P. & Vona-Davis, L. Influence of obesity on breast cancer receptor status and prognosis. Expert Rev. Anticancer Ther. 9, 1091-1101 (2009).
4. Reeves, G. K., Pirie, K., Green, J., Bull, D. & Beral, V. Comparison of the effects of genetic and environmental risk factors on in situ and invasive ductal breast cancer. Int. J. Cancer 131, 930-937 (2012).
5. Gilbert, C. A. & Slingerland, J. M. Cytokines, obesity, and cancer: new insights on mechanisms linking obesity to cancer risk and progression. Annu. Rev. Med. 64, 45-57 (2013).
6. Donath, M. Y. Inflammation as a sensor of metabolic stress in obesity and type 2 diabetes. Endocrinology 152, 4005-4006 (2011).
7. Andersen, C. J., Murphy, K. E. & Fernandez, M. L. Impact of obesity and metabolic syndrome on immunity. Adv. Nutr. 7, 66-75 (2016).
8. Font-Burgada, J., Sun, B. & Karin, M. Obesity and cancer: the oil that feeds the flame. Cell Metab. 23, 48-62 (2016).
9. Verdile, G. et al. Inflammation and oxidative stress: the molecular connectivity between insulin resistance, obesity, and Alzheimer's disease. Mediators of inflammation 2015, 105828 (2015).
10. Vandanmagsar, B. et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179-188 (2011).
11. Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796-1808 (2003).
12. Sutterwala, F. S., Ogura, Y., Zamboni, D. S., Roy, C. R. & Flavell, R. A. NALP3: a key player in caspase-1 activation. J. Endotoxin Res. 12, 251-256 (2006).
13. Jin, L. et al. Expression of interleukin-1beta in human breast carcinoma. Cancer 80, 421-434 (1997).
14. Arendt, L. M. et al. Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis. Cancer Res. 73, 6080-6093 (2013).
15. Fuentes-Mattei, E. et al. Effects of obesity on transcriptomic changes and cancer hallmarks in estrogen receptor-positive breast cancer. J. Natl Cancer Inst. 106, dju158 (2014).
16. Biswas, T., Gu, X., Yang, J., Ellies, L. G. & Sun, L. Z. Attenuation of TGF-beta signaling supports tumor progression of a mesenchymal-like mammary tumor cell line in a syngeneic murine model. Cancer Lett. 346, 129-138 (2014).
17. Sugiura, K. & Stock, C. C. Studies in a tumor spectrum. I. Comparison of the action of methylbis (2-chloroethyl)amine and 3-bis(2-chloroethyl) aminomethyl-4-methoxymethyl-5-hydroxy-6-methylpyridine on the growth of a variety of mouse and rat tumors. Cancer 5, 382-402 (1952).
18. Ewens, A. et al. Doxorubicin plus interleukin-2 chemoimmunotherapy against breast cancer in mice. Cancer Res. 66, 5419-5426 (2006).
19. Rogers, H. W. et al. Interleukin 1 participates in the development of anti-Listeria responses in normal and SCID mice. Proc. Natl Acad. Sci. USA 89, 1011-1015 (1992).
20. Zhao, Y., Wang, Z., Jiang, Y. & Yang, C. Inactivation of Rac1 reduces Trastuzumab resistance in PTEN deficient and insulin-like growth factor I receptor overexpressing human breast cancer SKBR3 cells. Cancer Lett. 313, 54-63 (2011).
21. Lumeng, C. N., Bodzin, J. L. & Saltiel, A. R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117, 175-184 (2007).
22. Mariathasan, S. et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218 (2004).
23. Lara-Tejero, M. et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412 (2006).
24. Qu, Y. et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature 490, 539-542 (2012).
25. Barcelos, L. S. et al. Role of the chemokines CCL3/MIP-1 alpha and CCL5/ RANTES in sponge-induced inflammatory angiogenesis in mice. Microvasc. Res. 78, 148-154 (2009).
26. Wei, Z. W. et al. CXCL1 promotes tumor growth through VEGF pathway activation and is associated with inferior survival in gastric cancer. Cancer Lett. 359, 335-343 (2015).
27. Mehner, C. et al. Tumor cell-produced matrix metalloproteinase 9 (MMP-9) drives malignant progression and metastasis of basal-like triple negative breast cancer. Oncotarget 5, 2736-2749 (2014).
28. Pakradouni, J. et al. Plasma NOV/CCN3 levels are closely associated with obesity in patients with metabolic disorders. PLoS ONE 8, e66788 (2013).
29. Loebig, M. et al. Evidence for a relationship between VEGF and BMI independent of insulin sensitivity by glucose clamp procedure in a homogenous group healthy young men. PLoS ONE 5, e12610 (2010).
30. Gomez-Ambrosi, J. et al. Involvement of serum vascular endothelial growth factor family members in the development of obesity in mice and humans. J. Nutr. Biochem. 21, 774-780 (2010).
31. Sung, H. K. et al. Adipose vascular endothelial growth factor regulates metabolic homeostasis through angiogenesis. Cell Metab. 17, 61-72 (2013).
32. Tan, W. et al. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature 470, 548-553 (2011).
33. Lin, L. et al. CCL18 from tumor-associated macrophages promotes angiogenesis in breast cancer. Oncotarget 6, 34758-34773 (2015).
34. Lin, F. S., Lin, C. C., Chien, C. S., Luo, S. F. & Yang, C. M. Involvement of p42/ p44 MAPK, JNK, and NF-kappaB in IL-1beta-induced ICAM-1 expression in human pulmonary epithelial cells. J. Cell Physiol. 202, 464-473 (2005).
35. Evans, J. M., Donnelly, L. A., Emslie-Smith, A. M., Alessi, D. R. & Morris, A. D. Metformin and reduced risk of cancer in diabetic patients. Br. Med. J. 330, 1304-1305 (2005).
36. Kasznicki, J., Sliwinska, A. & Drzewoski, J. Metformin in cancer prevention and therapy. Ann. Transl. Med. 2, 57 (2014).
37. Monami, M., Lamanna, C., Balzi, D., Marchionni, N. & Mannucci, E. Sulphonylureas and cancer: a case-control study. Acta Diabetol. 46, 279-284 (2009).
38. Zhou, G. et al. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108, 1167-1174 (2001).
39. Zaafar, D. K., Zaitone, S. A. & Moustafa, Y. M. Role of metformin in suppressing 1,2-dimethylhydrazine-induced colon cancer in diabetic and nondiabetic mice: effect on tumor angiogenesis and cell proliferation. PLoS ONE 9, e100562 (2014).
40. Ersoy, C. et al. The effect of metformin treatment on VEGF and PAI-1 levels in obese type 2 diabetic patients. Diabet Res. Clin. Pract. 81, 56-60 (2008).
41. Gyorffy, B. et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treat. 123, 725-731 (2010).
42. Kitamura, T. et al. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J. Exp. Med. 212, 1043-1059 (2015).
43. Takemura, Y. et al. Metformin suppresses interleukin (IL)-1beta-induced IL-8 production, aromatase activation, and proliferation of endometriotic stromal cells. J. Clin. Endocrinol. Metab. 92, 3213-3218 (2007).
44. Kelly, B., Tannahill, G. M., Murphy, M. P. & O'Neill, L. A. Metformin inhibits the production of reactive oxygen species from NADH:ubiquinone oxidoreductase to limit induction of interleukin-1beta (IL-1beta) and boosts interleukin-10 (IL-10) in lipopolysaccharide (LPS)-activated macrophages. J. Biol. Chem. 290, 20348-20359 (2015).
45. Kolb, R., Liu, G. H., Janowski, A. M., Sutterwala, F. S. & Zhang, W. Inflammasomes in cancer: a double-edged sword. Protein Cell 5, 12-20 (2014).
46. Cani, P. D. et al. Changes in gut microbiota control metabolic endotoxemiainduced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 1470-1481 (2008).
47. Elinav, E. et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745-757 (2011).
48. Chae, Y. K. et al. Repurposing metformin for cancer treatment: current clinical studies. Oncotarget 7, 40767-40780 (2016).
49. Lopez-Castejon, G. & Pelegrin, P. Current status of inflammasome blockers as anti-inflammatory drugs. Expert. Opin. Investig. Drugs 21, 995-1007 (2012).
50. Tolaney, S. M. et al. Role of vascular density and normalization in response to neoadjuvant bevacizumab and chemotherapy in breast cancer patients. Proc. Natl Acad. Sci. USA 112, 14325-14330 (2015).
51. O'Connell, K. A. & Edidin, M. A mouse lymphoid endothelial cell line immortalized by simian virus 40 binds lymphocytes and retains functional characteristics of normal endothelial cells. J. Immunol. 144, 521-525 (1990).
52. Kuida, K. et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267, 2000-2003 (1995).
53. Sutterwala, F. S. et al. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327 (2006).
54. Horai, R. et al. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187, 1463-1475 (1998).
55. Shornick, L. P. et al. Mice deficient in IL-1beta manifest impaired contact hypersensitivity to trinitrochlorobenzone. J. Exp. Med. 183, 1427-1436 (1996).
56. Markan, K. R. et al. Circulating FGF21 is liver derived and enhances glucose uptake during refeeding and overfeeding. Diabetes 63, 4057-4063 (2014).
57. Borcherding, N. et al. Paracrine Wnt5a signaling inhibits the expansion of tumor-initiating cells. Cancer Res. 75, 1972-1982 (2015).