Tumor-induced inflammation in mammary adipose tissue stimulates a vicious cycle of autotaxin expression and breast cancer progression

FASEB Journal

Volumn 29, Issue 9, 2015, Pages 3990-4000

  Benesch, Matthew G K ^a   Tang, Xiaoyun ^a   Dewald, Jay ^a   Dong, Wei Feng ^a   Mackey, John R ^a   Hemmings, Denise G ^a   McMullen, Todd P W ^a   Brindley, David N ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Chemokines; Cytokines; Lysophosphatidate; Syngeneic mouse model; Tumor stroma

Indexed keywords

AUTOTAXIN; CYTOKINE; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; LYSOPHOSPHATIDIC ACID; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR; ALKYLGLYCEROPHOSPHOETHANOLAMINE PHOSPHODIESTERASE; PHOSPHODIESTERASE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER GROWTH; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; LEUKOCYTE; MAMMARY GLAND FAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; ADIPOSE TISSUE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BREAST TUMOR; ENZYMOLOGY; EXPERIMENTAL MAMMARY NEOPLASM; GENE EXPRESSION REGULATION; GENETICS; MAMMARY GLAND; PATHOLOGY; UDDER;

ADIPOSE TISSUE; ANIMALS; BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; NEOPLASM PROTEINS; PHOSPHORIC DIESTER HYDROLASES;

EID: 84952719202     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-274480     Document Type: Article

References (66)

1. Siegel, R. L., Miller, K. D., and Jemal, A. (2015) Cancer statistics, 2015. CA Cancer J. Clin. 65,5-29
2. Kawalec, P., Lopuch, S., and Mikrut, A. (2015) Effectiveness of targeted therapy in patients with previously untreated metastatic breast cancer: a systematic review and meta-analysis. Clin. Breast Cancer 15, 90-100 PubMed
3. Benesch, M. G. K., Ko, Y. M., McMullen, T. P. W., and Brindley, D. N. (2014) Autotaxin in the crosshairs: taking aim at cancer and other inflammatory conditions. FEBS Lett. 588, 2712-2727
4. Brindley, D. N., Lin, F. T., and Tigyi, G. J. (2013) Role of the autotaxin-lysophosphatidate axis in cancer resistance to chemotherapy and radiotherapy. Biochim. Biophys. Acta 1831, 74-85
5. Nakanaga, K., Hama, K., and Aoki, J. (2010) Autotaxin: an LPA producing enzyme with diverse functions. J. Biochem. 148, 13-24
6. Tanaka, M., Okudaira, S., Kishi, Y., Ohkawa, R., Iseki, S., Ota, M., Noji, S., Yatomi, Y., Aoki, J., and Arai, H. (2006) Autotaxin stabilizes blood vessels and is required for embryonic vasculature by producing lysophosphatidic acid. J. Biol. Chem. 281, 25822-25830
7. Van Meeteren, L. A., Ruurs, P., Stortelers, C., Bouwman, P., van Rooijen, M. A., Pradère, J. P., Pettit, T. R., Wakelam, M. J., Saulnier-Blache, J. S., Mummery, C. L., Moolenaar, W. H., and Jonkers, J. (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 26, 5015-5022
8. Yuelling, L. W., Waggener, C. T., Afshari, F. S., Lister, J. A., and Fuss, B. (2012) Autotaxin/ENPP2 regulates oligodendrocyte differentiation in vivo in the developing zebrafish hindbrain. Glia 60, 1605-1618
9. Lai,S.L.,Yao,W.L.,Tsao,K.C.,Houben,A.J.,Albers,H.M.,Ovaa, H., Moolenaar, W. H., and Lee, S. J. (2012) Autotaxin/Lpar3 signaling regulates Kupffer's vesicle formation and left-right asymmetry in zebrafish. Development 139, 4439-4448
10. Teo, K., and Brunton, V. G. (2014) The role and therapeutic potential of the autotaxin-lysophosphatidate signalling axis in breast cancer. Biochem. J. 463,157-165
11. Yung, Y. C., Stoddard, N. C., and Chun, J. (2014) LPA receptor signaling: pharmacology, physiology, and pathophysiology. J. Lipid Res. 55, 1192-1214
12. Samadi, N., Bekele, R., Capatos, D., Venkatraman, G., Sariahmetoglu, M., and Brindley, D. N. (2011) Regulation of lysophosphatidate signaling by autotaxin and lipid phosphate phosphatases with respect to tumor progression, angiogenesis, metastasis and chemo-resistance. Biochimie 93,61-70
13. Liu, S., Umezu-Goto, M., Murph, M., Lu, Y., Liu, W., Zhang, F., Yu, S., Stephens,L.C.,Cui,X.,Murrow,G.,Coombes,K.,Muller,W.,Hung, M. C., Perou, C. M., Lee, A. V., Fang, X., and Mills, G. B. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15,539-550
14. Popnikolov, N. K., Dalwadi, B. H., Thomas, J. D., Johannes, G. J., and Imagawa, W. T. (2012) Association of autotaxin and lysophosphatidic acid receptor 3 with aggressiveness of human breast carcinoma. Tumour Biol. 33, 2237-2243
15. Gaetano, C. G., Samadi, N., Tomsig, J. L., Macdonald, T. L., Lynch, K. R., and Brindley, D. N. (2009) Inhibition of autotaxin production or activity blocks lysophosphatidylcholine-induced migration of human breast cancer and melanoma cells. Mol. Carcinog. 48,801-809
16. Euer, N., Schwirzke, M., Evtimova, V., Burtscher, H., Jarsch, M., Tarin, D., and Weidle, U. H. (2002) Identificationof genes associated with metastasis of mammary carcinoma in metastatic versus nonmetastatic cell lines. Anticancer Res. 22(2A), 733-740
17. Samadi, N., Gaetano, C., Goping, I. S., and Brindley, D. N. (2009) Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene 28, 1028-1039
18. Samadi, N., Bekele, R. T., Goping, I. S., Schang, L. M., and Brindley, D. N. (2011) Lysophosphatidate induces chemo-resistance by releasing breast cancer cells from taxol-induced mitotic arrest. PLoS ONE 6,e20608
19. Zhang, R., Wang, J., Ma, S., Huang, Z., and Zhang, G. (2011) Requirement of osteopontin in the migration and protection against taxol-induced apoptosis via the ATX-LPA axis in SGC7901 cells. BMC Cell Biol. 12,11
20. Vidot, S., Witham, J., Agarwal, R., Greenhough, S., Bamrah, H. S., Tigyi,G.J.,Kaye,S.B.,andRichardson,A.(2010)Autotaxindelays apoptosis induced by carboplatin in ovarian cancer cells. Cell. Signal. 22,926-935
21. Bekele, R., and Brindley, D. N. (2012) Role of autotaxin and lysophosphatidate in cancer progression and resistance to chemotherapy and radiotherapy. Clin. Lipidol. 7, 313-328
22. Deng, W., Shuyu, E., Tsukahara, R., Valentine, W. J., Durgam, G., Gududuru, V., Balazs, L., Manickam, V., Arsura, M., VanMiddlesworth, L., Johnson, L. R., Parrill, A. L., Miller, D. D., and Tigyi, G. (2007) The lysophosphatidic acid type 2 receptor is required for protection against radiation-induced intestinal injury. Gastroenterology 132, 1834-1851
23. Benesch,M.G.K.,Tang,X.,Maeda,T.,Ohhata,A.,Zhao,Y.Y.,Kok, B. P. C., Dewald, J., Hitt, M., Curtis, J. M., McMullen, T. P. W., and Brindley, D. N. (2014) Inhibition of autotaxin delays breast tumor growth and lung metastasis in mice. FASEB J. 28, 2655-2666
24. Venkatraman, G., Benesch, M. G., Tang, X., Dewald, J., McMullen, T. P., and Brindley, D. N. (2015) Lysophosphatidate signaling stabilizes Nrf2 and increases the expression of genes involved in drug resistance and oxidative stress responses: implications for cancer treatment. FASEB J. 29, 772-785
25. Hackett, A. J., Smith, H. S., Springer, E. L., Owens, R. B., Nelson-Rees, W.A.,Riggs,J.L.,andGardner,M.B.(1977)Twosyngeneiccelllines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J. Natl. Cancer Inst. 58, 1795-1806
26. Benesch, M. G. K., Zhao, Y. Y., Curtis, J. M., McMullen, T. P. W., and Brindley, D. N. (2015) Regulation of autotaxin expression and secretion by lysophosphatidate and sphingosine 1-phosphate J. Lipid Res. 56, 1134-1144
27. Carswell, K., Lee, M.-J., and Fried, S. (2012) Culture of isolated human adipocytes and isolated adipose tissue. Methods Mol. Biol. 806, 203-214
28. Germain, D. R., Graham, K., Glubrecht, D. D., Hugh, J. C., Mackey, J. R., and Godbout, R. (2011) DEAD box 1: a novel and independent prognostic marker for early recurrencein breastcancer. Breast Cancer Res. Treat. 127,53-63
29. Zhang, J., Wang, P., Dykstra, M., Gelebart, P., Williams, D., Ingham, R.,Adewuyi,E.E.,Lai,R.,andMcMullen,T.(2012)Platelet-derived growth factor receptor-a promotes lymphatic metastases in papillary thyroid cancer. J. Pathol. 228, 241-250
30. Murata, J., Lee, H. Y., Clair, T., Krutzsch, H. C., Arestad, A. A., Sobel, M. E., Liotta, L. A., and Stracke, M. L. (1994) cDNA cloning of the human tumor motility-stimulating protein, autotaxin, reveals a homology with phosphodiesterases. J. Biol. Chem. 269, 30479-30484
31. Turner, M. D., Nedjai, B., Hurst, T., and Pennington, D. J. (2014) Cytokines and chemokines: at the crossroads of cell signalling and inflammatory disease. Biochim. Biophys. Acta 1843,2563-2582
32. Houben, A. J., van Wijk, X. M., van Meeteren, L. A., van Zeijl, L., van de Westerlo, E. M., Hausmann, J., Fish, A., Perrakis, A., vanKuppevelt,T. H.,andMoolenaar,W.H.(2013)Thepolybasic insertion in autotaxin a confers specific binding to heparin and cell surface heparan sulfate proteoglycans. J. Biol. Chem. 288,510-519
33. Fulkerson, Z., Wu, T., Sunkara, M., Kooi, C. V., Morris, A. J., and Smyth, S. S. (2011) Binding of autotaxin to integrins localizes lysophosphatidic acid production to platelets and mammalian cells. J. Biol. Chem. 286, 34654-34663
34. Hausmann, J., Kamtekar, S., Christodoulou, E., Day, J. E., Wu, T., Fulkerson, Z., Albers, H. M., van Meeteren, L. A., Houben, A. J., van Zeijl, L., Jansen, S., Andries, M., Hall, T., Pegg, L. E., Benson, T. E., Kasiem, M., Harlos, K., Kooi, C. W., Smyth, S. S., Ovaa, H., Bollen, M., Morris, A. J., Moolenaar, W. H., and Perrakis, A. (2011) Structural basis of substrate discrimination and integrin binding by autotaxin. Nat.Struct.Mol.Biol.18,198-204
35. Boucher, J., Quilliot, D., Pradères, J. P., Simon, M. F., Grès, S., Guigné, C., Prévot, D., Ferry, G., Boutin, J. A., Carpéné, C., Valet, P., and Saulnier-Blache, J. S. (2005) Potential involvement of adipocyte insulin resistance in obesity-associated up-regulation of adipocyte lysophospholipase D/autotaxin expression. Diabetologia 48,569-577
36. Dusaulcy, R., Rancoule, C., Grès, S., Wanecq, E., Colom, A., Guigné, C., van Meeteren, L. A., Moolenaar, W. H., Valet, P., and Saulnier-Blache, J. S. (2011) Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. J. Lipid Res. 52, 1247-1255
37. Ferry, G., Tellier, E., Try, A., Grés, S., Naime, I., Simon, M. F., Rodriguez, M., Boucher, J., Tack, I., Gesta, S., Chomarat, P., Dieu, M., Raes, M., Galizzi, J. P., Valet, P., Boutin, J. A., and Saulnier-Blache, J. S. (2003) Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation: up-regulated expression with adipocyte differentiation and obesity. J. Biol. Chem. 278, 18162-18169
38. Federico, L., Ren, H., Mueller, P. A., Wu, T., Liu, S., Popovic, J., Blalock, E. M., Sunkara, M., Ovaa, H., Albers, H. M., Mills, G. B., Morris, A. J., and Smyth, S. S. (2012) Autotaxin and its product lysophosphatidic acid suppress brown adipose differentiation and promote diet-induced obesity in mice. Mol. Endocrinol. 26, 786-797
39. Sundaram, S., Johnson, A. R., and Makowski, L. (2013) Obesity, metabolism and the microenvironment: links to cancer. J. Carcinog. 12,19
40. De Pergola, G., and Silvestris, F. (2013) Obesity as a major risk factor for cancer. J. Obes. 2013, 291546
41. Brown, K. A. (2014) Impact of obesity on mammary gland inflammation and local estrogen production. J. Mammary Gland Biol. Neoplasia 19,183-189
42. Zhao, C., Sardella, A., Chun, J., Poubelle, P. E., Fernandes, M. J., and Bourgoin, S. G. (2011) TNF-alpha promotes LPA1- and LPA3-mediatedrecruitmentofleukocytesinvivothroughCXCR2ligand chemokines. J. Lipid Res. 52, 1307-1318
43. Lawlor, K. E., Campbell, I. K., Metcalf, D., O'Donnell, K., van Nieuwenhuijze, A., Roberts, A. W., and Wicks, I. P. (2004) Critical role for granulocyte colony-stimulating factor in inflammatory arthritis. Proc. Natl. Acad. Sci. USA 101, 11398-11403
44. Gutschalk,C.M.,Herold-Mende,C.C.,Fusenig,N.E.,andMueller, M. M. (2006) Granulocyte colony-stimulating factor and granulocytemacrophage colony-stimulating factor promote malignant growth of cells from head and neck squamous cell carcinomas in vivo. Cancer Res. 66, 8026-8036
45. Knowlden, S., and Georas, S. N. (2014) The autotaxin-LPA axis emerges as a novel regulator of lymphocyte homing and inflammation. J. Immunol. 192, 851-857
46. Okudaira, S., Yukiura, H., and Aoki, J. (2010) Biological roles of lysophosphatidic acid signaling through its production by autotaxin. Biochimie 92, 698-706
47. Ikeda, H., andYatomi, Y. (2012) Autotaxin in liver fibrosis. Clin. Chim. Acta 413, 1817-1821
48. Tang,N.,Zhao,Y.,Feng,R.,Liu,Y.,Wang,S.,Wei,W.,Ding,Q.,An, M. S., Wen, J., and Li, L. (2014) Lysophosphatidic acid accelerates lung fibrosis by inducing differentiation of mesenchymal stem cells into myofibroblasts. J. Cell. Mol. Med. 18, 156-169
49. Bourgoin, S. G., and Zhao, C. (2010) Autotaxin and lysophospholipids in rheumatoid arthritis. Curr. Opin. Investig. Drugs 11, 515-526
50. Nikitopoulou, I., Oikonomou, N., Karouzakis, E., Sevastou, I., Nikolaidou-Katsaridou, N., Zhao, Z., Mersinias, V., Armaka, M., Xu, Y., Masu, M., Mills, G. B., Gay, S., Kollias, G., and Aidinis, V. (2012) Autotaxin expression from synovial fibroblasts is essential for the pathogenesis of modeled arthritis. J. Exp. Med. 209,925-933
51. Hozumi, H., Hokari, R., Kurihara, C., Narimatsu, K., Sato, H., Sato, S., Ueda, T., Higashiyama, M., Okada, Y., Watanabe, C., Komoto, S., Tomita,K.,Kawaguchi,A.,Nagao,S.,andMiura,S.(2013)Involvement of autotaxin/lysophospholipase D expression in intestinal vessels in aggravation of intestinal damage through lymphocyte migration. Lab. Invest. 93,508-519
52. Dvorak, H. F. (1986) Tumors: wounds that do not heal-similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659
53. Schäfer, M., and Werner, S. (2008) Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628-638
54. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144,646-674
55. Colotta, F., Allavena, P., Sica, A., Garlanda, C., and Mantovani, A. (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30, 1073-1081
56. Kehlen, A., Englert, N., Seifert, A., Klonisch, T., Dralle, H., Langner, J., and Hoang-Vu, C. (2004) Expression, regulation and function of autotaxin in thyroid carcinomas. Int. J. Cancer 109,833-838
57. Brindley, D. N. (2004) Lipid phosphate phosphatases and related proteins: signaling functions in development, cell division, and cancer. J. Cell. Biochem. 92, 900-912
58. Barber, M. N., Risis, S., Yang, C., Meikle, P. J., Staples, M., Febbraio, M. A., and Bruce, C. R. (2012) Plasma lysophosphatidylcholine levels are reduced in obesity and type 2 diabetes. PLoS ONE 7,e41456
59. Bernardi, M., Ricci, C. S., and Zaccherini, G. (2014) Role of human albumin in the management of complications of liver cirrhosis. J. Clin. Exp. Hepatol. 4, 302-311
60. Britschgi, A., Andraos, R., Brinkhaus, H., Klebba, I., Romanet, V., Müller, U., Murakami, M., Radimerski, T., and Bentires-Alj, M. (2012) JAK2/STAT5 inhibition circumvents resistance to PI3K/ mTOR blockade: a rationale for cotargeting these pathways in metastatic breast cancer. Cancer Cell 22, 796-811
61. Chung, A. S., Wu, X., Zhuang, G., Ngu, H., Kasman, I., Zhang, J., Vernes, J.M., Jiang,Z., Meng, Y. G., Peale, F. V., Ouyang, W., and Ferrara, N. (2013) An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat. Med. 19, 1114-1123
62. Pylayeva-Gupta, Y., Lee, K. E., Hajdu, C. H., Miller, G., and Bar-Sagi, D. (2012) Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia. Cancer Cell 21, 836-847
63. Kishi, Y., Okudaira, S., Tanaka, M., Hama, K., Shida, D., Kitayama, J., Yamori, T., Aoki, J., Fujimaki, T., and Arai, H. (2006) Autotaxin is overexpressed in glioblastoma multiforme and contributes to cell motility of glioblastoma by converting lysophosphatidylcholine to lysophosphatidic acid. J. Biol. Chem. 281, 17492-17500
64. Jankowski, M. (2011) Autotaxin: its role in biology of melanoma cells and as a pharmacological target. Enzyme Res. 2011, 194857
65. Benesch, M. G. K., Ko, Y. M., Tang, X., Dewald, J., Lopez-Campistrous, A., Zhao, Y. Y., Lai, R., Curtis, J. M., Brindley, D. N., and McMullen, T. P. W. (2015) Autotaxin is an inflammatory mediator and therapeutic target in thyroid cancer. Endocr. Relat. Cancer, doi: 10.1530/ERC-15-0045, Epub June 2, 2015
66. Brindley, D. N., Benesch, M. G. K., Murph, M. M. (2015) Autotaxin: an enzymatic augmenter of malignant progression linked to inflammation. In Melanoma: Current Clinical Management and Future Therapeutics (Murph, M., ed.) pp. 297-324, InTech. doi: 10.5772/ 59013